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33
Fish and Fisheries. 2019;1–33. wileyonlinelibrary.com/journal/faf | 1 Received: 25 January 2019 | Revised: 12 March 2019 | Accepted: 14 March 2019 DOI: 10.1111/faf.12367 ORIGINAL ARTICLE Population-level consequences of seismic surveys on fishes: An interdisciplinary challenge Hans Slabbekoorn 1 | John Dalen 2 | Dick de Haan 3 | Hendrik V. Winter 3 | Craig Radford 4 | Michael A. Ainslie 5 | Kevin D. Heaney 6 | Tobias van Kooten 3 | Len Thomas 7 | John Harwood 7 1 Institute of Biology (IBL), Leiden University, Leiden, The Netherlands 2 Soundmare, Bergen, Norway 3 Wageningen Marine Research (WMR), IJmuiden, The Netherlands 4 University of Auckland, Leigh, New Zealand 5 JASCO/TNO, Safety & Defence, The Hague, The Netherlands 6 OASIS Inc., Fairfax Station, Virginia 7 Centre for Research into Ecological and Environmental Modelling (CREEM), University of St. Andrews, St. Andrews, UK Correspondence Hans Slabbekoorn, Institute of Biology (IBL), Leiden University, Leiden, The Netherlands. Email: [email protected] Abstract Offshore activities elevate ambient sound levels at sea, which may affect marine fauna. We reviewed the literature about impact of airgun acoustic exposure on fish in terms of damage, disturbance and detection and explored the nature of impact as- sessment at population level. We provided a conceptual framework for how to ad- dress this interdisciplinary challenge, and we listed potential tools for investigation. We focused on limitations in data currently available, and we stressed the potential benefits from cross-species comparisons. Well-replicated and controlled studies do not exist for hearing thresholds and dose–response curves for airgun acoustic expo- sure. We especially lack insight into behavioural changes for free-ranging fish to ac- tual seismic surveys and on lasting effects of behavioural changes in terms of time and energy budgets, missed feeding or mating opportunities, decreased performance in predator-prey interactions, and chronic stress effects on growth, development and reproduction. We also lack insight into whether any of these effects could have population-level consequences. General “population consequences of acoustic dis- turbance” (PCAD) models have been developed for marine mammals, but there has been little progress so far in other taxa. The acoustic world of fishes is quite different from human perception and imagination as fish perceive particle motion and sound pressure. Progress is therefore also required in understanding the nature and extent to which fishes extract acoustic information from their environment. We addressed the challenges and opportunities for upscaling individual impact to the population, community and ecosystem level and provided a guide to critical gaps in our knowledge. KEYWORDS airgun, behavioural response, dynamic energy budget, fish hearing, population consequences of acoustic disturbance, stress physiology This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. © 2019 The Authors. Fish and Fisheries published by John Wiley & Sons Ltd.

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Page 1: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

Fish and Fisheries 20191ndash33 wileyonlinelibrarycomjournalfafemsp|emsp1

Received25January2019emsp |emsp Revised12March2019emsp |emsp Accepted14March2019DOI 101111faf12367

O R I G I N A L A R T I C L E

Population- level consequences of seismic surveys on fishes An interdisciplinary challenge

Hans Slabbekoorn1 emsp| John Dalen2emsp| Dick de Haan3emsp| Hendrik V Winter3emsp| Craig Radford4emsp| Michael A Ainslie5emsp| Kevin D Heaney6emsp| Tobias van Kooten3emsp| Len Thomas7emsp| John Harwood7

1InstituteofBiology(IBL)LeidenUniversityLeidenTheNetherlands2SoundmareBergenNorway3WageningenMarineResearch(WMR)IJmuidenTheNetherlands4UniversityofAucklandLeighNewZealand5JASCOTNOSafetyampDefenceTheHagueTheNetherlands6OASISIncFairfaxStationVirginia7CentreforResearchintoEcologicalandEnvironmentalModelling(CREEM)UniversityofStAndrewsStAndrewsUK

CorrespondenceHansSlabbekoornInstituteofBiology(IBL)LeidenUniversityLeidenTheNetherlandsEmailhwslabbekoornbiologyleidenunivnl

AbstractOffshore activities elevate ambient sound levels at seawhichmay affectmarinefaunaWereviewedtheliteratureaboutimpactofairgunacousticexposureonfishintermsofdamagedisturbanceanddetectionandexploredthenatureofimpactas-sessmentatpopulationlevelWeprovidedaconceptualframeworkforhowtoad-dressthisinterdisciplinarychallengeandwelistedpotentialtoolsforinvestigationWefocusedonlimitationsindatacurrentlyavailableandwestressedthepotentialbenefitsfromcross-speciescomparisonsWell-replicatedandcontrolledstudiesdonotexistforhearingthresholdsanddosendashresponsecurvesforairgunacousticexpo-sureWeespeciallylackinsightintobehaviouralchangesforfree-rangingfishtoac-tualseismicsurveysandonlastingeffectsofbehaviouralchangesintermsoftimeandenergybudgetsmissedfeedingormatingopportunitiesdecreasedperformanceinpredator-preyinteractionsandchronicstresseffectsongrowthdevelopmentandreproductionWe also lack insight into whether any of these effects could havepopulation-levelconsequencesGeneralldquopopulationconsequencesofacousticdis-turbancerdquo(PCAD)modelshavebeendevelopedformarinemammalsbuttherehasbeenlittleprogresssofarinothertaxaTheacousticworldoffishesisquitedifferentfromhumanperceptionandimaginationasfishperceiveparticlemotionandsoundpressureProgressisthereforealsorequiredinunderstandingthenatureandextenttowhichfishesextractacousticinformationfromtheirenvironmentWeaddressedthechallengesandopportunitiesforupscalingindividual impacttothepopulationcommunity and ecosystem level and provided a guide to critical gaps in ourknowledge

K E Y W O R D S

airgunbehaviouralresponsedynamicenergybudgetfishhearingpopulationconsequencesofacousticdisturbancestressphysiology

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttribution-NonCommercialLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedandisnotusedforcommercialpurposescopy2019TheAuthorsFish and FisheriespublishedbyJohnWileyampSonsLtd

2emsp |emsp emspensp SLABBEKOORN Et AL

1emsp |emspINTRODUC TION

Humanactivitiesatseaaddsoundtotheworldoffishesandhenceelevate natural levels of ambient noise (Frisk 2012 Hildebrand2009McDonaldHildebrandampWiggins2006)Thishaspotentialconsequencesforaquaticanimalsthatliveinadarkorlow-visibilityworldandheavilyrelyonsoundformanyaspectsoftheirlifethataf-fectsurvivalandreproduction(CarrollPrzeslawskiGunningBruceampDuncan2017CoxBrennanGerwingDudasamp Juanes2018HawkinsPembrokeampPopper2015PengZhaoampLiu2015)AllfishesarelikelytobesensitivetosoundtosomeextentManyspe-ciesalsouseacousticsignalsforcommunicationamongconspecificsand acoustic cues for detectionof predatorsor prey all ofwhichmay be affected by the presence of anthropogenic noise (Ladich2008 Popper amp Hastings 2009 Radford Kerridge amp Simpson2014 Slabbekoorn etal 2010) Furthermore the whole varietyof sounds in their surroundingscreatesa soundscape that isusedfor orientation and navigation (Fay 2009 SlabbekoornampBouton2008)Consequentlytheirauditorysensitivitymakesthemvulner-abletodamageincaseofover-exposureanddisturbanceincaseofanysoundintheaudiblerangethatisperceivedasathreatorcausingdistraction(ChanGiraldo-PerezSmithampBlumstein2010KightampSwaddle2011Shannonetal2016)Man-madesoundsthatover-lapintimeandfrequencycanalsomaskbiologicallyrelevantsoundsmaking them lessaudibleandunderminingdetectionandrecogni-tion(BrummampSlabbekoorn2005DoolingampLeek2018)

Noise pollution can affectwell-being and fitness of individualfishthroughdamagedisturbanceandmasking(Carrolletal2017Cox etal 2018)However the impact of sound is not often verydirect or obvious except for rare cases of over-exposure wheredeadorstunnedfishcomefloattothesurfaceduringorsoonafteran acoustic event such as underwater pile driving or explosions(Halvorsen Casper Matthews Carlson amp Popper 2012 Popperetal2014)Soundlevelsunderwatertypicallygounnoticedbyhu-mansthatareonornearthewaterandobservingfishbehaviourisevenchallengingtomarineinvestigatorsthatapplyspecialtools(egBruceetal2018Cookeetal2014MetcalfeWrightTudoracheampWilson 2016) Furthermore it is challenging to determine thelong-termimpactonwelfareorfitnessfromshort-termbehaviouralchanges inresponsetoanthropogenicnoise thechallenge isevengreaterifthereisaphysiologicalresponsebutnoapparentchangeinbehaviour(KightampSwaddle2011KuncMcLaughlinampSchmidt2016)Neverthelessscientificandpublicawarenesshas increasedoverthelastdecadesacrosstaxaandconcernsfromfisheriescon-servationists andpolicymakers have resulted in noise pollution tobe integrated inenvironmental legislation inagrowingpartof theworld (Farcas ThompsonampMerchant 2016 Popper etal 2014Southall etal 2007Weilgart 2007WillsteedGill BirchenoughampJude2017)

Theconcernsaboutpotentiallydetrimentaleffectsofman-madesounds on marine life has led to regulation in the United Statesvia theMarineMammal Protection Act (MMPA) the EndangeredSpeciesAct(ESA)andtheMagnusonndashStevensFisheryConservation

andManagementAct(MSA)bywhichindividualanimalsofspecificspeciesareprotectedagainstharmandharassment(DolmanampJasny2015Gordonetal 2003Merchant2019Williamsetal 2015)TheMarineStrategyFrameworkDirective(MSFD)oftheEuropeanUnionisdifferentandrequiresmemberstatestoachieveormaintainGoodEnvironmentalStatus(GES)by2020Descriptor11oftheGESrequiresthatldquoIntroductionofenergyincludingunderwaternoiseisatlevelsthatdonotadverselyaffectthemarineenvironmentrdquoforwhichtwoindicatorsarespecifieddistributionintimeandspaceofloudlow-andmid-frequencyimpulsivesound(Indicator1111)andcontinuouslow-frequencysoundaround125Hz(Indicator1121)

FortheUnitedStatesandtheEUregulatorsrequireinsightsthatarecurrentlylimitedormissing(Hawkinsetal2015Nowaceketal2015 Popper etal 2014 Southall etal 2007) Threshold soundconditionsforphysicaldamageofindividualanimalsorbehaviouralorphysiological effects that likely affect survivalorprobabilityofreproductionareonlyavailable forvery fewspecies (independentofwhethertheyfallundertheMMPAorESA)Furthermoredataonsoundimpactorindividualwelfareandfitnessarenotonlyrareornon-existingforfree-ranginganimals(Nedelecetal2017Simpsonetal 2016) but there is also still a large gap in knowledgewhenitcomestotranslatingsuchdatatoldquoadverse effects on the environ-mentrdquo which is required to assess whether ldquoGood Environmental Statusrdquohasbeenachieved(Kuncetal2016Newetal2014NRC

1 INTRODUCTION 1

2 IMPACT ASSESSMENT 3

21Riskevaluationmethods 3

22Productivitysusceptibilityassessment 4

23Populationconsequencesofdisturbancemodels 5

3 ACOUSTIC EXPLORATION OF THE SEAFLOOR 8

31Thenatureofseismicsurveys 8

32Airgunarraysizeandseasonality 9

4 THE AUDITORY WORLD OF FISHES 11

41Fundamentalsoffishhearing 11

42Soundfieldshearingandpotentialforimpact 13

5 OVERVIEW OF AIRGUN IMPACT STUDIES 15

51Historicalperspectiveandmethodologicalconsiderations

15

52Behaviouralresponsetoairgunexposure 15

53Airgunexposurestudieswithcagedfish 16

54Physiologicalstressresponsestoloudsounds 18

6 MODELLING CONSEQUENCES 20

61Modellingpopulation-leveleffects 20

62Individual-basedmodels 21

63Multitrophicstockmodels 22

7 CONCLUSIONS 23

ACKNOWLEDGEMENTS 24

REFERENCES 24

emspensp emsp | emsp3SLABBEKOORN Et AL

2005 Shannon etal 2016) Sufficient understanding of whethermeasuresofmitigationarenecessaryoradequateconsequentlyre-mainselusive

Airgunsused forseismicsurveysareoneofseveralprominentsourcesofnoisepollution(Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)Seismicsurveysinvolvelong seriesof intense soundpulses reflectionsofwhich from theseabedprovideinformationontheshapeandcompositionofoceanbottomlayersTheyareusedforexampletoobtaininsightintothesizeandlocationofoilandgasresourcesTheairgunsoundpulsescan make a significant contribution to the underwater ambientsoundprofileoverlargeareasastheycanbeaudibleoverthousandsofkilometres(Hildebrand2009Nieukirketal2012)Globaltrendsinacousticpresencesincehistoricalexplorationswithdynamiteinthe1920shaveseenchangesinsourcetypeandsurveyscalewhilespreadingofseismicexplorationactivitylargelyfollowedeconomicdevelopments(LandroslashampAmundsen2018)similartotherisingpat-ternsinvesselnoisesincethe1950s(Frisk2012McDonaldetal2006)

TheaimofthispaperistoreviewthecurrentstateofknowledgeonwhetherandhowseismicsurveyscanhaveadetrimentaleffectonfishesOurexplicittargetwastoevaluatetheevidenceforimpactfromairgun acoustic exposureon fish in termsofdamage distur-banceanddetectionofbiologicallyrelevantsoundsandtoaddressthepotential for extrapolationofdata and insights topopulation-levelconsequencesWethereforeexploredtheinterdisciplinaryna-tureofimpactassessment(cfRosaampKoper2018)focusedontheabundantlimitationsinthedatacurrentlyavailableandprovidedanoverviewofrelevantinformationandpotentialtoolssuitableforin-vestigationoncedatabecomeavailableCriticalfortheevaluationistounderstand(a)thateffectsonindividualanimalsshouldbetrans-latedtoconsequencesforstockspopulationsspeciescommunitiesorwholeecosystemsand(b)thatchoicesforspatial(localregionalglobal)andtemporalresolution(nowcomingyearsordecadesfor-ever)arelikelytohavealargeimpactontheoutcomewhilethesechoicescanberegardedaspoliticalorstrategicdecisions

Theorderinwhichweaddresstopicsandsubdisciplinesisasfol-lowsWestartwithabriefdescriptionofgeneralandmorespecificriskevaluationmethodsforenvironmentalhazardsSpecialattentionisallocatedtoso-calledproductivitysusceptibilityassessment(PSAMilton2001Patricketal20092010) asapplied to fish stocksandpopulationconsequencesofdisturbance(PCoD)models(Farmeretal2018NationalResearchCouncil2005Newetal2014)asappliedmainlytomarinemammalsWeaddressthepotentialrele-vanceforfishesexposedtosoundingeneralandseismicsurveysinparticularAsmarinebiologistsandpolicymakerstypicallyhavelittleknowledgeaboutseismicoperationswefurtheraddressthenatureofseismicsurveystoprovide insights intothesoundsourceof in-vestigationandthepotentialexposurecharacteristicsofmarinefish

Alsocriticalfortheevaluationisinsightintowhatweknow(andoftendonotknow)aboutwhatandhowfisheshearWethereforeprovideabriefreviewonfundamentalsoffishhearingfollowedbyaprimeronsoundpropagationmodelsthatrelatecharacteristicsof

thesoundsourcetothespreadandnatureoftheman-madesoundfieldWesubsequentlyreviewpublishedstudiesonbehaviouralandphysiologicalresponsedatarelatedtoairgunexposureandotherex-perimentalsoundexposurestudiesrelevanttopotentialeffectsofseismicsurveysWealsoaddresshowtointegratesuchavailableandnewdataintoaPCoD-typeframeworkusingdynamicenergybud-gets(DEBs)individual-basedmodels(IBMs)andmultitrophicstockmodels (MSMs) Finally we evaluate the feasibility of ecosystem-based assessments for sound impact assessmentwhich is an ap-proachthatcanbenefitfromexperienceandmodellinginfisheriesagainprovidedthatsufficientdatabecomeavailableaboutimpactofacousticdisturbanceonfishes

2emsp |emspIMPAC T A SSESSMENT

21emsp|emspRisk evaluation methods

Riskassessment isusedtoquantifytherisk (ieexpectedadversechangetotheenvironmentduetooneormorehazards)associatedwithdifferentalternativeactions(egHalpernetal2008HammarWikstroumlmampMolander2014Hobdayetal2007Newetal2014Weed 2005) There aremanyways to categorize risk assessmentmethodsforexample(a)rapidvsin-depth(b)top-downvsbottom-up (c) data-rich vs data-poor (d) qualitative semi-quantitativeorquantitativeand(e)empirical(iebasedondatawithlittleunderly-ing theory) vsmechanistic (basedon theoreticalmodels possiblyparameterizedwithdata)

Qualitative methods typically categorize different risks intoordinal (ie ordered) classes such as ldquolowrdquo ldquomediumrdquo and ldquohighrdquoalong two axes frequency (likelihood of occurrence) and severity(Figure1a)Theassignmentofriskleveltoeachelementoftheclas-sification(egsomethingthatishighfrequencybutlowseverityasnotbeingofconcernbutsomethingthatislowfrequencybuthighseverity as being ofmoderate concern) is essentially based on anunstatedalgorithm

Semi-quantitativemethods such as so-called productivity andsusceptibilityassessment(PSA)mayhavemultipleaxesandassignnumericalvaluestoeachaxisThesevaluesareordinalbutnotnom-inal(iethedifferencebetween1and2isnotnecessarilythesameas the difference between 2 and 3mdashnor do numbers on differentaxes necessarily have the same scale)Overall risk is obtained bysummingoraveragingthenumericalscoresmdashsomethingthatisofdu-biousutilitygiventheordinalnatureofthescoresImplicitorexplicitweightingandrescalingissometimesusedAsidefromPSAanotherexampleofsucharbitrarysummationisthecumulativeimpactanal-ysisofHalpernetal(2008)

Both qualitative and semi-quantitative methods suffer fromthesamefundamentalproblemcomparisonorcombinationofdif-ferent ordinal variables is essentially arbitrary Potential solutionsinclude groundtruthing where possible and simulation testingfor example throughmanagement strategy evaluation (Altenback1995)Anexampleofsimulationtestingisthatappliedtotheldquocatchlimit algorithmrdquo of the InternationalWhaling Commission Revised

4emsp |emsp emspensp SLABBEKOORN Et AL

ManagementProcedureNotethatsuchtestsareinherentlyquan-titativePossiblythebestsolutionistouseaquantitativemethodinthefirstplace

Quantitativemethodsrangefromin-depthbottom-updata-richmechanisticmethodssuchasafullPCoDmodel(Costaetal2015Newetal2014)tosemi-rapidtop-downdata-poorsemi-empiricalmethodssuchastheldquointerimPCoDrdquoapproachofKingetal(2015)whichusedexpertelicitation(describedlater)toparameterizeasim-plifiedfullPCoDmodelWearecurrentlyawareofonequalitativeandonemorequantitativeanalysisofpopulationconsequencesofacoustic disturbance on fishes Hammar etal (2014) conductedanecological riskassessment (ERA)onathreatenedpopulationofAtlanticcod(Gadus morhuaGadidae)inthecontextofawindfarmprojectTheyexploredthepotentialimpactofsixstressorsthreeofwhichweresoundrelatedmoderate-levelnoisefromworkingves-selsandoperatingturbinesandextremeover-exposureduetopile-drivingnoiseintheconstructionphaseTheanalysissuggestedthatpiledrivingwasthemosthazardousstressorthatcouldposeaseri-ousrisktothecodpopulationunderstudyAsignificantreductionofthisriskwasachievedinthemodelbyavoidingpile-drivingactivity

in themonths of cod recruitment Studies like this provide usefulinsights forurgentdecisionsandwhendataare lackingHowevertheydonotprovidesufficientquantificationanddonotexploitthedetailedinsightphysiologicalmodelsmayyield

SivleKvadsheimandAinslie(2014)modelledpopulationconse-quencesofsonarexposureforherring(Clupea harengusClupeidae)based on maximum reported sound levels of no behavioural re-sponse Their predictions for the potential risk to the populationofwhenthesemaximumlevelswereexceededvariedwithseasondependingonthedensityoffishTheriskofanypopulationconse-quencewaslowestduringspread-outfeedingbutincreasedinpe-riodsofpopulationaggregationHoweveringeneraltheresponseestimateswere lowandSivleetal (2014)concludedthat it isun-likely that todaysnaval sonaractivitywill lead toanypopulation-leveleffectforthisspecies

More sophisticated riskanalyses takeanexposureassessmentandadosendashresponseassessmentintoaccount(seeBoydetal2008)to characterize and evaluate whether the level of environmentalhazardisabovesomespecifiedthresholdformitigation(Figure1b)buttheserelyonavailabledataandarequantitativeinnatureThemain issuewithquantitativeapproaches isdeterminingwhere theinputcomesfromTheinputcomeseitherfromdatawhichareofteninshortsupplyorfromexpertelicitationwhichcanbeunreliableiftheanalysisisnotperformedwellandinverydata-poorsituationsTheobviousremedyhereistocollectsufficientandadequateinputdataoruseappropriatemethodologyforexpertelicitation incon-certwiththeriskevaluationeffortRobustnesstomodelmisspeci-ficationcanbeevaluatedthroughsimulationtestingAswebelievethat semi-quantitative PSA could (with development) be a usefulapproach in somecasesand thatPCoDmodelshavepotential formarinemammalsbutalsoforfishesweheregiveabriefdescriptionofthestateoftheartinboth

22emsp|emspProductivity susceptibility assessment

Productivity susceptibility assessment (PSA Milton 2001) canbe characterized as being rapid top-down data-poor semi-quantitativeandempiricalandwasoriginallydevelopedtoevaluatethe risk that fisheriespose to specific target species indata-poorsituations (Milton2001StobutzkiMillerampBrewer2001) Ithassubsequently been expanded to cover a wide range of fisheriesmanagementeffectsonfishstocks(habitatimpactecosystemcon-siderationsmanagementefficacymdashegHobdaySmithampStobutzki2004Hobdayetal2007Rosenbergetal2007)Itinvolvesscor-ingtheproductivityofasusceptiblespecies intermsofanumberof demographic parameters that affect population growth rate(survivalbirthrateetc)anditssusceptibilityintermsofexposureto risk from fisheries (areal and vertical distribution aggregationetc)andcurrentstatus(currentmanagementstrategyetc)(Patricketal20092010)TheproductivityscoresarethenaveragedandthesusceptibilityscoresmultipliedtogetherSpeciesthathavealowproductivityscoreandahighsusceptibilityscoreareconsideredtobeparticularlyvulnerable

F I G U R E 1emsp (a)Qualitativemethodofriskcategorizationintothequalitativeclassesldquolowrdquoldquomediumrdquoandldquohighrdquobasedonevaluationalongtwoaxesconsequenceseverityandaccidentfrequency(orprobability)Thecombinationsidentifysituationsofconcernormajorconcern(redrawnfromAltenback1995)(b)Generalmanagementframeworkforhazardidentificationandriskassessmenttoquantifytheriskandevaluatealternativeactions(mitigateoracceptrisk)(fromBoydetal2008)

High

Medium

Low

Low Medium High

Consequences of Severity

Acci

dent

freq

uenc

y

MajorConcern

MajorConcern

MajorConcernConcern

Concern

Identification of environmental hazard

Exposure assessment(number of animals location level)

Dosendash response assessment(toxicity and secondary effects)

Risk characterization (quotient)

Above thresholdfor action

Mitigation

YES

NO Risk acceptable

(a)

(b)

emspensp emsp | emsp5SLABBEKOORN Et AL

Themain productivity attributes of thePSA approachmaybeusefulinanyevaluationofdetrimentalimpactandconcernfactorsfor fish stocks The main attributes include maximum populationgrowth maximum individual size and age the ldquovon Bertalanffyrdquogrowthcoefficientforhowrapidlyafishreachesthismaximumsizeand theageatmaturitynaturalmortality and fecunditybreedingstrategy recruitmentpatternandmean trophic level (ahighscoreforpiscivoresintermediateforomnivoresandalowscoreforplank-tivores)Themainsusceptibilityattributesof thePSAapproach inthecontextoffisheriesconcerncatchabilityasdeterminedbygeo-graphicareaoverlapandverticaldistributionoverlapbetweenstockandfishingeffortsgeographicconcentrationseasonalmigrationsschooling aggregations and other behavioural and morphologicaltraitsinadditiontodesirabilityandmarketvalue(Patricketal20092010)Factorssuchastheeffectivenessofmanagementtocontrolcatch ratesand theeffectsof fishinggearonhabitatqualityhavealsobeenaddedto theseoriginalattributes inorder todeterminesusceptibilitytofisheries(Hobdayetal2007)

Additional susceptibility attributes that should be consideredif PSA were to be applied to seismic acoustic exposure includethegeographicandverticaldistributionoverlapofaparticularfishspecieswiththeacousticrangeofsoundsourcestodetermineex-posureprobability and level in termsof both soundpressure andparticlemotionAnyimpactofacousticexposureshouldbeconsid-eredontopofandinthecontextofseasonalvariationandspecificlifestagesizeandreproductiveconditionsandthefisheriesimpactifthetargetspeciesisalsoharvestedHoweverwebelievethatPSAcannotbeusedyetforevaluatingthepotentialvulnerabilityoffishstocks to anthropogenic noiseManyof the susceptibility scoringcategoriescurrentlyusedinPSAarenotparticularlyappropriateforassessingthepotentialeffectsofanthropogenicnoiseInadditionthe appropriateness of the essentially arbitraryway inwhich theindividual productivity and susceptibility scores are combined toprovideasinglemetricneedstobeevaluatedAnewsetofsuscep-tibilityscoringcategoriescouldbedevelopedforexampleusinganexpertelicitationprocess(SutherlandampBurgman2015)toidentifyfishspeciesandstocksthatarelikelytobeparticularlyvulnerabletotheeffects

23emsp|emspPopulation consequences of disturbance models

The population consequences of disturbance (PCoD) and popula-tion consequences of acoustic disturbance (PCAD) models (NRC2005Newetal2014)consistofaseriesoftransferfunctionsthatdescribehowexposure to stressors (such as anthropogenicnoise)affects individual behaviour how the resulting changes in behav-iourcanaffecthealth(definedasallinternalfactorsthataffectbodyconditionorhomoeostasis)andhowvariationsinhealthmayaffectvitalrates(survivalreproductionandgrowthageatfirstbreeding)Furthermorethetransferfunctionatthehighestleveloforganiza-tioninthemodeladdresseshowtheaccumulationofdataaboutthewayinwhichdifferentindividualsareexposedtoandaffectedbya

stressorcanbeusedtoscaleuptheanticipatedchangesinvitalratestopredictpopulation-leveleffects

PCADmodels have now been applied to a number of marinemammalspeciesforexamplenorthernandsouthernelephantseals(Mirounga angustirostris and M leoninaPhocidaeNewetal2014Costaetal2015)NorthAtlanticrightwhales (Eubalaena glacialisBalaenidae Schick Kraus etal 2013) beakedwhales (ZiphiidaeNew Moretti Hooker Costa amp Simmons 2013) harbour por-poise (Phocoena phocoena Phocoenidae Harwood King Schickamp Donovan 2014) and minke whale (Balaenoptera acutorostrataBalaenopteridaeChristiansenampLusseau2015)buttherearehardlyanyexamplessofarforfish(butseeSivleetal2014)

IdeallythepredictionsofPCADmodelsshouldbefittedtoap-propriatetimeseriesofempiricaldataobtainedoverarangeoflev-elsofdisturbanceTheresultsofsuchafittingprocesscanthenbeused to improve theparameter estimates andquantify theuncer-taintyassociatedwiththemodelpredictionsusingapproachessuchasBayesianhidden-processmodelling(NewmanBucklandLindleyThomasampFernandez 2006)However so far in no case has thisbeenpossibleandthereforeallmodelsappliedshouldstillbecon-sideredasldquoexploratoryrdquoExploratorymodelsareparticularlyusefulforcomparingthepossibleconsequencesofdifferentscenariosandforidentifyingpriorityareasforresearchHowever it is importantthat the uncertainties associatedwith their underlying parametervaluesaredocumentedandthattheeffectsoftheseuncertaintiesontheirpredictionsarequantified

Itisusefultoexploresomeofthedetailsofthemodelapplica-tionsinmarinemammalstoevaluatesomeoftheproblemsandsolu-tionsthatmayalsoapply insomewaytofishesNewetal (2014)forexampleusedthePCoDmodelstructuretoinvestigatethepo-tentialeffectsoflostforagingdivesonthehealth(measuredbytotallipidmassmdashseeSchickNewetal2013)ofadult femalesouthernelephant seals and the implications of variation in health for pupsurvivalandpopulationdynamicsTheyusedinformationobtainedfromdataloggersthatwereattachedtoanimalsimmediatelybeforetheyembarkedontheirpost-moultforagingtripsThedataloggersallowedareconstructionoftheirsurfacetransittimeandtheirforag-ingdivetimeDuringportionsofsomeforagingdiveselephantsealsdrift and the rateofverticalmovementduring thedrift is relatedtotheratiooflipidtoleanbodymassThedataloggerinformationwascalibratedagainstactuallipidgainduringtheforagingtripusingmeasurementsofbodycompositioncollectedbeforeandaftertheforagingtriptoenableestimationofdailylipidgain

FurthermoreNewetal (2014) linkedmaternalmassatbreed-ing to pupmass atweaning (Arnbom Fedak BoydampMcConnell1993)andpupmassatweaningtopupsurvival(McMahonBurtonampBester20002003)ThemodelwasthenusedtodeterminetheeffectofforagingdivedisturbanceonpupsurvivalItwasassumedthattherewerenoforagingdivesforthedurationofthedisturbanceandsurfacetransittimewassettotheobservedmaximumforthatindividual If animalswere disturbed for 50 of their time at seain1year thepredicteddecline inpopulationsizewassmall (lt1)However if thatdisturbancewouldcontinue indefinitely (eg asa

6emsp |emsp emspensp SLABBEKOORN Et AL

resultofvariationsintheextentoftheAntarcticicesheetcausedbyclimatechange)thepredictedeffectswouldbemuchgreater(a10declineinabundanceover30years)

TheanalysesinNewetal(2014)wereonlypossiblebecausede-tailedlongitudinaldatawereavailableonthemovementshealthandreproductivesuccessofalargenumberofadultfemalesealsSuchextensivedata sets requiredecadesof intensive research and areonly available for a fewmarinemammal populations ResearchershaveadoptedarangeoftechniquestobuildPCoDmodels insitu-ationswhereempiricaldataaremore limitedNabe-NielsenSiblyTougaardTeilmannandSveegaard(2014)usedanindividual-basedmodelofthemovementsofharbourporpoisestoestimatethepo-tentialeffectsofresponsestothesoundassociatedwithwindtur-bineoperationandshippingontheirenergyandreservesTheyuseda hypothetical relationship between energy reserves and survivalto calculate population-level consequences Villegas-AmtmannSchwarzSumichandCosta(2015)usedasimilarapproachtopre-dictthepotentialeffectsofreducedenergyintakeonreproductivesuccessandsurvivalforwesterngreywhales(Eschrichtius robustusEschrichtiidae)

Ifempiricaldataaresufficienttoestimatearelationbetweenbe-haviouralchangeandhealthbutnotbetweenhealthandvitalratesitmaybepossibletouseasurrogatemeasurefortherelevantvitalrate Christiansen and Lusseau (2015) used a bioenergetic modelandempiricalinformationonthebehaviouralresponseofadultfe-maleminkewhalestowhale-watchingboatsontheirsummerfeed-ing grounds in Iceland to estimate the effects of these responsesonthewhalesrsquohealth(asmeasuredbytheirblubbervolume)Theycalculated how different rates of encounter with whale-watchingboatswould affect an individualwhales health at the end of thesummerandthenusedanempiricallyderivedrelationbetweenfe-maleblubbervolumeandfoetallength(ChristiansenRasmussenampLusseau2014)asa surrogate for the relationshipbetweenhealthandtheprobabilityofgivingbirthAlthoughinteractionswithwhale-watchingboatsresultedina40reductioninfeedingactivitythepredictedeffectonafemalesbodyconditionoverthecourseofthesummerwasverysmall (0049reduction)becauseboatencoun-terswere actually rare This reduction in body conditionwas notpredictedtoaffectfoetalsurvivalHoweverevenifChristiansenandLusseau(2015)haddetectedasignificanteffectonfoetalsurvivaltheywould have been unable to forecast the population-level ef-fectsofexposuretowhale-watchingboatsbecausetheproportionoftheNorthAtlanticminkewhalepopulationthatfeedsinIcelandicwatersisnotknown

In situations where even surrogate measures are unavailableexpert elicitation (Runge Converse amp Lyons 2011 Sutherland ampBurgman2015)canbeusedtoparameterizesomeofthetransferfunctionsofthePCoDmodelExpertelicitationisaformalprocessinwhichanumberofexpertsonaparticulartopicareaskedtopre-dictwhatmay happen in a particular situation These predictionsare combined into calibrated quantitative statements with asso-ciated uncertainty which can be incorporated into mathematicalmodels(Martinetal2012)Kingetal(2015)usedthisapproachto

parameterize relationshipsbetween thenumberofdaysonwhichharbourporpoisesweredisturbedbynoiseassociatedwiththecon-structionofoffshorewindfarmsandtheirsurvivalandreproductivesuccessTheserelationshipswerethenusedtopredictthepotentialpopulationconsequencesofdifferentscenariosfortheconstructionofmultiplewindfarms

Thereare several studiesondifferentmarinemammal speciesthat have filled data gaps by asking experts Lusseau etal (2011)usedanexpertelicitationapproachtopredictthepotentialaggre-gate effect of noise associatedwithwind farm construction tourboat operation and harbour expansion on a bottlenose dolphin(Tursiops truncatusDelphinidae)populationThompsonetal(2013)usedittoassesspopulation-level impactsofdisturbancefrompiledrivingonharbourseals(Phoca vitulinaPhocidae)Spatialdistribu-tionpatternsandreceivednoiselevelswereintegratedwithdataonthepotentialfordisplacementandhearingdamageIngeneralun-certaintiesinecologicalmodelsarenotunusual(seeegClarketal2001HarwoodampStokes2003)andexpertelicitationisonewaytodealwiththemAcomplementaryapproachisecologicalriskassess-ment(ERA)possiblycombinedwithweightofevidence(WOE)(seeegHammaretal2014Hobdayetal2007Weed2005)

BasedontheexperienceandexamplesofPCADmodelsforma-rinemammalsaflowchart isdevelopedinFigure2whichappliesthe samemodel components transfer functions (Box1) and vitalratesinamodelforpopulationconsequencesofairgundisturbanceto fishesBeforeaddressing the literature inmoredetail the flowchartprovidesanoverviewofhowexposuretothesoundsofaseis-micsurveymaychangebehaviourinsuchawaythatitreducesin-dividualforagingefficiency(PurserampRadford2011ShafieiSabetNeoampSlabbekoorn2015)andincreasesvulnerabilitytopredation(Chanetal2010SimpsonPurserampRadford2015)Furthermoreswimmingmore or less efficientmay also detrimentally affect in-dividual energetics (Metcalfe etal 2016Villegas-Amtmannetal2015) while swimming less or in the wrong direction may resultin missed mating or spawning opportunities (Boussard 1981RossingtonBensonLepperampJones2013)Thesechanges inbe-haviourtogetherwithacuteorchronicstressphysiologicalchangesmayundermineindividualbodyconditionimmunocompetenceandphysiologicalinvestmentingrowthandreproduction(Barton2002Sierra-Flores Atack Migaud amp Davie 2015 Wendelaar-Bonga1997)The spectral and temporal structureof soundswill alsoaf-fect physiological stress levels as stronger responses have beenreportedtoboatnoiseandintermittentnoisethantomorehomog-enous white noise (Nichols Anderson amp Sirovic 2015WysockiDittamiampLadich2006respectively)

The translation from individual-level effects to the populationlevelinthePCADmodelforfishes(Figure2)isreflectedintheconse-quencesofthesebehaviouralandphysiologicalchangesforthevitalratesintermsofgrowthsurvivalandreproduction(cfCostaetal2015Harwoodetal2014Newetal2014)Thevitalratesdonotonlydetermineindividualfitnessimportanttounderstandselectionpressuresandevolutionarypotential(ChristiansenampLusseau2015HeinoPauliampDieckmann2015)butalsodeterminepopulationor

emspensp emsp | emsp7SLABBEKOORN Et AL

stockdevelopments(Hammaretal2014Newetal2014Patricketal2009)Directimpactsofseismicsurveyactivitiesonfisheriesare incorporatedthrough increasingor reducingcatchrateswhile

indirect impactsofseismicsurveyactivitiesonfisheriesarerepre-sented through potential impact on stock developments (McCullyPhillips Scottamp Ellis 2015 Patrick etal 2009) Behavioural and

F IGURE 2emspAflowchartofthepopulationconsequencesofacousticdisturbancemodeltailoredtofishes(asdevelopedinthecontextofairgunsoundandcodasamodelspecieshencetheacronymPCAD4Cod)DirectimpactonfisheriesindicatedinthetoprightisdeterminedbypositiveornegativechangesincatchrateduetofishmovementsduringandafteraseismicsurveyIndirectimpactonfisheriesunderneathisaffectedbybehavioural(green)andphysiological(pink)changesandtheirpotentiallynegativeeffectsforindividualfitnesspopulationhealthandstockdevelopmentTransferfunctionsthatrequirecriticalevaluationarenumbered1ndash12andareexplainedindetailinBox1Notethatindividualfitnessconcernslifetimereproductivesuccesswhichistheaccumulationofvitalratesattheindividuallevel(growthsurvivalandreproduction)Furthermorealthoughtransferfunctionsaredepictedunidirectionallythereversedpathwaycanalsoberelevantandimportantaspopulation-levelmetricssuchasabundanceandshiftsinpredator-preyorcompetitorrelationshipsmayfeedbackfrompopulationtoindividuallevel(iewarrantingbidirectionalarrows)

Airgun exposure

Behavioural change

Physiological change

Direct impact on fisheries

Indirect impact on fisheriesFeeding impact

Predation risk

Swimming energetics

Reproductive opportunities

Growth rate

survival

reproduction

Chronic stress

Immunocompetence

Developmental impact

Reproductive investment

Individual fitness

Population health amp stock development

1 2

4 5

7 8

9 10

11 12

113

6

Population consequences of acoustic disturbance model for fishes as applied to

airgun sound and cod (PCAD4Cod)

Box 1enspTransfer functions of the PCAD model for fishes (linked to Figure 2)1Behaviouralchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)2Physiologicalchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)3Interactionsbetweenbehaviouralresponsivenessandphysiologicalstate4Consequencesofbehaviouralchange(acuteandchronic)forvitalratesa ImpactonforagingefficiencyandopportunitiesbImpactonvulnerabilitytopredation(especiallyjuveniles)c EnergeticconsequencesofalteredswimmingpatternsdReproductiveconsequencesthroughmissedbreedingopportunities(adults)

5Consequencesofphysiologicalchange(acuteandchronic)forvitalratesa ImpactonchronicstressbeyondregulatoryfluctuationsbImpactonvulnerabilitytoinfectionsanddiseasecDevelopmentalconsequencesofphysiologicalimbalancedReproductiveconsequencesthroughfolliclematuration(adultsonly)

6Effectsonvitalratesofinteractionsbetweenbehaviouralandphysiologicalresponses7 Impactofbehaviouraleffectsongrowthratesurvivalandreproduction8Impactofphysiologicaleffectsongrowthratesurvivalandreproduction9 Impactofbehaviouralandphysiologicaleffectsonindividualfitness(lifetimereproductivesuccess)10enspConsequencesofchangesinindividualfitnessatthepopulationandstocklevel11enspEvaluationofdirectandindirecteffectsofseismicsurveysonfisheries12enspEvaluationofimpactfromseismicsurveysinthecontextof(sustainable)harvestingbyfisheries

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

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BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

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Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

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ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

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CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

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DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

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DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

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Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

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FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

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Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

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Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

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FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

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FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

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GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

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TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

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TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 2: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

2emsp |emsp emspensp SLABBEKOORN Et AL

1emsp |emspINTRODUC TION

Humanactivitiesatseaaddsoundtotheworldoffishesandhenceelevate natural levels of ambient noise (Frisk 2012 Hildebrand2009McDonaldHildebrandampWiggins2006)Thishaspotentialconsequencesforaquaticanimalsthatliveinadarkorlow-visibilityworldandheavilyrelyonsoundformanyaspectsoftheirlifethataf-fectsurvivalandreproduction(CarrollPrzeslawskiGunningBruceampDuncan2017CoxBrennanGerwingDudasamp Juanes2018HawkinsPembrokeampPopper2015PengZhaoampLiu2015)AllfishesarelikelytobesensitivetosoundtosomeextentManyspe-ciesalsouseacousticsignalsforcommunicationamongconspecificsand acoustic cues for detectionof predatorsor prey all ofwhichmay be affected by the presence of anthropogenic noise (Ladich2008 Popper amp Hastings 2009 Radford Kerridge amp Simpson2014 Slabbekoorn etal 2010) Furthermore the whole varietyof sounds in their surroundingscreatesa soundscape that isusedfor orientation and navigation (Fay 2009 SlabbekoornampBouton2008)Consequentlytheirauditorysensitivitymakesthemvulner-abletodamageincaseofover-exposureanddisturbanceincaseofanysoundintheaudiblerangethatisperceivedasathreatorcausingdistraction(ChanGiraldo-PerezSmithampBlumstein2010KightampSwaddle2011Shannonetal2016)Man-madesoundsthatover-lapintimeandfrequencycanalsomaskbiologicallyrelevantsoundsmaking them lessaudibleandunderminingdetectionandrecogni-tion(BrummampSlabbekoorn2005DoolingampLeek2018)

Noise pollution can affectwell-being and fitness of individualfishthroughdamagedisturbanceandmasking(Carrolletal2017Cox etal 2018)However the impact of sound is not often verydirect or obvious except for rare cases of over-exposure wheredeadorstunnedfishcomefloattothesurfaceduringorsoonafteran acoustic event such as underwater pile driving or explosions(Halvorsen Casper Matthews Carlson amp Popper 2012 Popperetal2014)Soundlevelsunderwatertypicallygounnoticedbyhu-mansthatareonornearthewaterandobservingfishbehaviourisevenchallengingtomarineinvestigatorsthatapplyspecialtools(egBruceetal2018Cookeetal2014MetcalfeWrightTudoracheampWilson 2016) Furthermore it is challenging to determine thelong-termimpactonwelfareorfitnessfromshort-termbehaviouralchanges inresponsetoanthropogenicnoise thechallenge isevengreaterifthereisaphysiologicalresponsebutnoapparentchangeinbehaviour(KightampSwaddle2011KuncMcLaughlinampSchmidt2016)Neverthelessscientificandpublicawarenesshas increasedoverthelastdecadesacrosstaxaandconcernsfromfisheriescon-servationists andpolicymakers have resulted in noise pollution tobe integrated inenvironmental legislation inagrowingpartof theworld (Farcas ThompsonampMerchant 2016 Popper etal 2014Southall etal 2007Weilgart 2007WillsteedGill BirchenoughampJude2017)

Theconcernsaboutpotentiallydetrimentaleffectsofman-madesounds on marine life has led to regulation in the United Statesvia theMarineMammal Protection Act (MMPA) the EndangeredSpeciesAct(ESA)andtheMagnusonndashStevensFisheryConservation

andManagementAct(MSA)bywhichindividualanimalsofspecificspeciesareprotectedagainstharmandharassment(DolmanampJasny2015Gordonetal 2003Merchant2019Williamsetal 2015)TheMarineStrategyFrameworkDirective(MSFD)oftheEuropeanUnionisdifferentandrequiresmemberstatestoachieveormaintainGoodEnvironmentalStatus(GES)by2020Descriptor11oftheGESrequiresthatldquoIntroductionofenergyincludingunderwaternoiseisatlevelsthatdonotadverselyaffectthemarineenvironmentrdquoforwhichtwoindicatorsarespecifieddistributionintimeandspaceofloudlow-andmid-frequencyimpulsivesound(Indicator1111)andcontinuouslow-frequencysoundaround125Hz(Indicator1121)

FortheUnitedStatesandtheEUregulatorsrequireinsightsthatarecurrentlylimitedormissing(Hawkinsetal2015Nowaceketal2015 Popper etal 2014 Southall etal 2007) Threshold soundconditionsforphysicaldamageofindividualanimalsorbehaviouralorphysiological effects that likely affect survivalorprobabilityofreproductionareonlyavailable forvery fewspecies (independentofwhethertheyfallundertheMMPAorESA)Furthermoredataonsoundimpactorindividualwelfareandfitnessarenotonlyrareornon-existingforfree-ranginganimals(Nedelecetal2017Simpsonetal 2016) but there is also still a large gap in knowledgewhenitcomestotranslatingsuchdatatoldquoadverse effects on the environ-mentrdquo which is required to assess whether ldquoGood Environmental Statusrdquohasbeenachieved(Kuncetal2016Newetal2014NRC

1 INTRODUCTION 1

2 IMPACT ASSESSMENT 3

21Riskevaluationmethods 3

22Productivitysusceptibilityassessment 4

23Populationconsequencesofdisturbancemodels 5

3 ACOUSTIC EXPLORATION OF THE SEAFLOOR 8

31Thenatureofseismicsurveys 8

32Airgunarraysizeandseasonality 9

4 THE AUDITORY WORLD OF FISHES 11

41Fundamentalsoffishhearing 11

42Soundfieldshearingandpotentialforimpact 13

5 OVERVIEW OF AIRGUN IMPACT STUDIES 15

51Historicalperspectiveandmethodologicalconsiderations

15

52Behaviouralresponsetoairgunexposure 15

53Airgunexposurestudieswithcagedfish 16

54Physiologicalstressresponsestoloudsounds 18

6 MODELLING CONSEQUENCES 20

61Modellingpopulation-leveleffects 20

62Individual-basedmodels 21

63Multitrophicstockmodels 22

7 CONCLUSIONS 23

ACKNOWLEDGEMENTS 24

REFERENCES 24

emspensp emsp | emsp3SLABBEKOORN Et AL

2005 Shannon etal 2016) Sufficient understanding of whethermeasuresofmitigationarenecessaryoradequateconsequentlyre-mainselusive

Airgunsused forseismicsurveysareoneofseveralprominentsourcesofnoisepollution(Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)Seismicsurveysinvolvelong seriesof intense soundpulses reflectionsofwhich from theseabedprovideinformationontheshapeandcompositionofoceanbottomlayersTheyareusedforexampletoobtaininsightintothesizeandlocationofoilandgasresourcesTheairgunsoundpulsescan make a significant contribution to the underwater ambientsoundprofileoverlargeareasastheycanbeaudibleoverthousandsofkilometres(Hildebrand2009Nieukirketal2012)Globaltrendsinacousticpresencesincehistoricalexplorationswithdynamiteinthe1920shaveseenchangesinsourcetypeandsurveyscalewhilespreadingofseismicexplorationactivitylargelyfollowedeconomicdevelopments(LandroslashampAmundsen2018)similartotherisingpat-ternsinvesselnoisesincethe1950s(Frisk2012McDonaldetal2006)

TheaimofthispaperistoreviewthecurrentstateofknowledgeonwhetherandhowseismicsurveyscanhaveadetrimentaleffectonfishesOurexplicittargetwastoevaluatetheevidenceforimpactfromairgun acoustic exposureon fish in termsofdamage distur-banceanddetectionofbiologicallyrelevantsoundsandtoaddressthepotential for extrapolationofdata and insights topopulation-levelconsequencesWethereforeexploredtheinterdisciplinaryna-tureofimpactassessment(cfRosaampKoper2018)focusedontheabundantlimitationsinthedatacurrentlyavailableandprovidedanoverviewofrelevantinformationandpotentialtoolssuitableforin-vestigationoncedatabecomeavailableCriticalfortheevaluationistounderstand(a)thateffectsonindividualanimalsshouldbetrans-latedtoconsequencesforstockspopulationsspeciescommunitiesorwholeecosystemsand(b)thatchoicesforspatial(localregionalglobal)andtemporalresolution(nowcomingyearsordecadesfor-ever)arelikelytohavealargeimpactontheoutcomewhilethesechoicescanberegardedaspoliticalorstrategicdecisions

Theorderinwhichweaddresstopicsandsubdisciplinesisasfol-lowsWestartwithabriefdescriptionofgeneralandmorespecificriskevaluationmethodsforenvironmentalhazardsSpecialattentionisallocatedtoso-calledproductivitysusceptibilityassessment(PSAMilton2001Patricketal20092010) asapplied to fish stocksandpopulationconsequencesofdisturbance(PCoD)models(Farmeretal2018NationalResearchCouncil2005Newetal2014)asappliedmainlytomarinemammalsWeaddressthepotentialrele-vanceforfishesexposedtosoundingeneralandseismicsurveysinparticularAsmarinebiologistsandpolicymakerstypicallyhavelittleknowledgeaboutseismicoperationswefurtheraddressthenatureofseismicsurveystoprovide insights intothesoundsourceof in-vestigationandthepotentialexposurecharacteristicsofmarinefish

Alsocriticalfortheevaluationisinsightintowhatweknow(andoftendonotknow)aboutwhatandhowfisheshearWethereforeprovideabriefreviewonfundamentalsoffishhearingfollowedbyaprimeronsoundpropagationmodelsthatrelatecharacteristicsof

thesoundsourcetothespreadandnatureoftheman-madesoundfieldWesubsequentlyreviewpublishedstudiesonbehaviouralandphysiologicalresponsedatarelatedtoairgunexposureandotherex-perimentalsoundexposurestudiesrelevanttopotentialeffectsofseismicsurveysWealsoaddresshowtointegratesuchavailableandnewdataintoaPCoD-typeframeworkusingdynamicenergybud-gets(DEBs)individual-basedmodels(IBMs)andmultitrophicstockmodels (MSMs) Finally we evaluate the feasibility of ecosystem-based assessments for sound impact assessmentwhich is an ap-proachthatcanbenefitfromexperienceandmodellinginfisheriesagainprovidedthatsufficientdatabecomeavailableaboutimpactofacousticdisturbanceonfishes

2emsp |emspIMPAC T A SSESSMENT

21emsp|emspRisk evaluation methods

Riskassessment isusedtoquantifytherisk (ieexpectedadversechangetotheenvironmentduetooneormorehazards)associatedwithdifferentalternativeactions(egHalpernetal2008HammarWikstroumlmampMolander2014Hobdayetal2007Newetal2014Weed 2005) There aremanyways to categorize risk assessmentmethodsforexample(a)rapidvsin-depth(b)top-downvsbottom-up (c) data-rich vs data-poor (d) qualitative semi-quantitativeorquantitativeand(e)empirical(iebasedondatawithlittleunderly-ing theory) vsmechanistic (basedon theoreticalmodels possiblyparameterizedwithdata)

Qualitative methods typically categorize different risks intoordinal (ie ordered) classes such as ldquolowrdquo ldquomediumrdquo and ldquohighrdquoalong two axes frequency (likelihood of occurrence) and severity(Figure1a)Theassignmentofriskleveltoeachelementoftheclas-sification(egsomethingthatishighfrequencybutlowseverityasnotbeingofconcernbutsomethingthatislowfrequencybuthighseverity as being ofmoderate concern) is essentially based on anunstatedalgorithm

Semi-quantitativemethods such as so-called productivity andsusceptibilityassessment(PSA)mayhavemultipleaxesandassignnumericalvaluestoeachaxisThesevaluesareordinalbutnotnom-inal(iethedifferencebetween1and2isnotnecessarilythesameas the difference between 2 and 3mdashnor do numbers on differentaxes necessarily have the same scale)Overall risk is obtained bysummingoraveragingthenumericalscoresmdashsomethingthatisofdu-biousutilitygiventheordinalnatureofthescoresImplicitorexplicitweightingandrescalingissometimesusedAsidefromPSAanotherexampleofsucharbitrarysummationisthecumulativeimpactanal-ysisofHalpernetal(2008)

Both qualitative and semi-quantitative methods suffer fromthesamefundamentalproblemcomparisonorcombinationofdif-ferent ordinal variables is essentially arbitrary Potential solutionsinclude groundtruthing where possible and simulation testingfor example throughmanagement strategy evaluation (Altenback1995)Anexampleofsimulationtestingisthatappliedtotheldquocatchlimit algorithmrdquo of the InternationalWhaling Commission Revised

4emsp |emsp emspensp SLABBEKOORN Et AL

ManagementProcedureNotethatsuchtestsareinherentlyquan-titativePossiblythebestsolutionistouseaquantitativemethodinthefirstplace

Quantitativemethodsrangefromin-depthbottom-updata-richmechanisticmethodssuchasafullPCoDmodel(Costaetal2015Newetal2014)tosemi-rapidtop-downdata-poorsemi-empiricalmethodssuchastheldquointerimPCoDrdquoapproachofKingetal(2015)whichusedexpertelicitation(describedlater)toparameterizeasim-plifiedfullPCoDmodelWearecurrentlyawareofonequalitativeandonemorequantitativeanalysisofpopulationconsequencesofacoustic disturbance on fishes Hammar etal (2014) conductedanecological riskassessment (ERA)onathreatenedpopulationofAtlanticcod(Gadus morhuaGadidae)inthecontextofawindfarmprojectTheyexploredthepotentialimpactofsixstressorsthreeofwhichweresoundrelatedmoderate-levelnoisefromworkingves-selsandoperatingturbinesandextremeover-exposureduetopile-drivingnoiseintheconstructionphaseTheanalysissuggestedthatpiledrivingwasthemosthazardousstressorthatcouldposeaseri-ousrisktothecodpopulationunderstudyAsignificantreductionofthisriskwasachievedinthemodelbyavoidingpile-drivingactivity

in themonths of cod recruitment Studies like this provide usefulinsights forurgentdecisionsandwhendataare lackingHowevertheydonotprovidesufficientquantificationanddonotexploitthedetailedinsightphysiologicalmodelsmayyield

SivleKvadsheimandAinslie(2014)modelledpopulationconse-quencesofsonarexposureforherring(Clupea harengusClupeidae)based on maximum reported sound levels of no behavioural re-sponse Their predictions for the potential risk to the populationofwhenthesemaximumlevelswereexceededvariedwithseasondependingonthedensityoffishTheriskofanypopulationconse-quencewaslowestduringspread-outfeedingbutincreasedinpe-riodsofpopulationaggregationHoweveringeneraltheresponseestimateswere lowandSivleetal (2014)concludedthat it isun-likely that todaysnaval sonaractivitywill lead toanypopulation-leveleffectforthisspecies

More sophisticated riskanalyses takeanexposureassessmentandadosendashresponseassessmentintoaccount(seeBoydetal2008)to characterize and evaluate whether the level of environmentalhazardisabovesomespecifiedthresholdformitigation(Figure1b)buttheserelyonavailabledataandarequantitativeinnatureThemain issuewithquantitativeapproaches isdeterminingwhere theinputcomesfromTheinputcomeseitherfromdatawhichareofteninshortsupplyorfromexpertelicitationwhichcanbeunreliableiftheanalysisisnotperformedwellandinverydata-poorsituationsTheobviousremedyhereistocollectsufficientandadequateinputdataoruseappropriatemethodologyforexpertelicitation incon-certwiththeriskevaluationeffortRobustnesstomodelmisspeci-ficationcanbeevaluatedthroughsimulationtestingAswebelievethat semi-quantitative PSA could (with development) be a usefulapproach in somecasesand thatPCoDmodelshavepotential formarinemammalsbutalsoforfishesweheregiveabriefdescriptionofthestateoftheartinboth

22emsp|emspProductivity susceptibility assessment

Productivity susceptibility assessment (PSA Milton 2001) canbe characterized as being rapid top-down data-poor semi-quantitativeandempiricalandwasoriginallydevelopedtoevaluatethe risk that fisheriespose to specific target species indata-poorsituations (Milton2001StobutzkiMillerampBrewer2001) Ithassubsequently been expanded to cover a wide range of fisheriesmanagementeffectsonfishstocks(habitatimpactecosystemcon-siderationsmanagementefficacymdashegHobdaySmithampStobutzki2004Hobdayetal2007Rosenbergetal2007)Itinvolvesscor-ingtheproductivityofasusceptiblespecies intermsofanumberof demographic parameters that affect population growth rate(survivalbirthrateetc)anditssusceptibilityintermsofexposureto risk from fisheries (areal and vertical distribution aggregationetc)andcurrentstatus(currentmanagementstrategyetc)(Patricketal20092010)TheproductivityscoresarethenaveragedandthesusceptibilityscoresmultipliedtogetherSpeciesthathavealowproductivityscoreandahighsusceptibilityscoreareconsideredtobeparticularlyvulnerable

F I G U R E 1emsp (a)Qualitativemethodofriskcategorizationintothequalitativeclassesldquolowrdquoldquomediumrdquoandldquohighrdquobasedonevaluationalongtwoaxesconsequenceseverityandaccidentfrequency(orprobability)Thecombinationsidentifysituationsofconcernormajorconcern(redrawnfromAltenback1995)(b)Generalmanagementframeworkforhazardidentificationandriskassessmenttoquantifytheriskandevaluatealternativeactions(mitigateoracceptrisk)(fromBoydetal2008)

High

Medium

Low

Low Medium High

Consequences of Severity

Acci

dent

freq

uenc

y

MajorConcern

MajorConcern

MajorConcernConcern

Concern

Identification of environmental hazard

Exposure assessment(number of animals location level)

Dosendash response assessment(toxicity and secondary effects)

Risk characterization (quotient)

Above thresholdfor action

Mitigation

YES

NO Risk acceptable

(a)

(b)

emspensp emsp | emsp5SLABBEKOORN Et AL

Themain productivity attributes of thePSA approachmaybeusefulinanyevaluationofdetrimentalimpactandconcernfactorsfor fish stocks The main attributes include maximum populationgrowth maximum individual size and age the ldquovon Bertalanffyrdquogrowthcoefficientforhowrapidlyafishreachesthismaximumsizeand theageatmaturitynaturalmortality and fecunditybreedingstrategy recruitmentpatternandmean trophic level (ahighscoreforpiscivoresintermediateforomnivoresandalowscoreforplank-tivores)Themainsusceptibilityattributesof thePSAapproach inthecontextoffisheriesconcerncatchabilityasdeterminedbygeo-graphicareaoverlapandverticaldistributionoverlapbetweenstockandfishingeffortsgeographicconcentrationseasonalmigrationsschooling aggregations and other behavioural and morphologicaltraitsinadditiontodesirabilityandmarketvalue(Patricketal20092010)Factorssuchastheeffectivenessofmanagementtocontrolcatch ratesand theeffectsof fishinggearonhabitatqualityhavealsobeenaddedto theseoriginalattributes inorder todeterminesusceptibilitytofisheries(Hobdayetal2007)

Additional susceptibility attributes that should be consideredif PSA were to be applied to seismic acoustic exposure includethegeographicandverticaldistributionoverlapofaparticularfishspecieswiththeacousticrangeofsoundsourcestodetermineex-posureprobability and level in termsof both soundpressure andparticlemotionAnyimpactofacousticexposureshouldbeconsid-eredontopofandinthecontextofseasonalvariationandspecificlifestagesizeandreproductiveconditionsandthefisheriesimpactifthetargetspeciesisalsoharvestedHoweverwebelievethatPSAcannotbeusedyetforevaluatingthepotentialvulnerabilityoffishstocks to anthropogenic noiseManyof the susceptibility scoringcategoriescurrentlyusedinPSAarenotparticularlyappropriateforassessingthepotentialeffectsofanthropogenicnoiseInadditionthe appropriateness of the essentially arbitraryway inwhich theindividual productivity and susceptibility scores are combined toprovideasinglemetricneedstobeevaluatedAnewsetofsuscep-tibilityscoringcategoriescouldbedevelopedforexampleusinganexpertelicitationprocess(SutherlandampBurgman2015)toidentifyfishspeciesandstocksthatarelikelytobeparticularlyvulnerabletotheeffects

23emsp|emspPopulation consequences of disturbance models

The population consequences of disturbance (PCoD) and popula-tion consequences of acoustic disturbance (PCAD) models (NRC2005Newetal2014)consistofaseriesoftransferfunctionsthatdescribehowexposure to stressors (such as anthropogenicnoise)affects individual behaviour how the resulting changes in behav-iourcanaffecthealth(definedasallinternalfactorsthataffectbodyconditionorhomoeostasis)andhowvariationsinhealthmayaffectvitalrates(survivalreproductionandgrowthageatfirstbreeding)Furthermorethetransferfunctionatthehighestleveloforganiza-tioninthemodeladdresseshowtheaccumulationofdataaboutthewayinwhichdifferentindividualsareexposedtoandaffectedbya

stressorcanbeusedtoscaleuptheanticipatedchangesinvitalratestopredictpopulation-leveleffects

PCADmodels have now been applied to a number of marinemammalspeciesforexamplenorthernandsouthernelephantseals(Mirounga angustirostris and M leoninaPhocidaeNewetal2014Costaetal2015)NorthAtlanticrightwhales (Eubalaena glacialisBalaenidae Schick Kraus etal 2013) beakedwhales (ZiphiidaeNew Moretti Hooker Costa amp Simmons 2013) harbour por-poise (Phocoena phocoena Phocoenidae Harwood King Schickamp Donovan 2014) and minke whale (Balaenoptera acutorostrataBalaenopteridaeChristiansenampLusseau2015)buttherearehardlyanyexamplessofarforfish(butseeSivleetal2014)

IdeallythepredictionsofPCADmodelsshouldbefittedtoap-propriatetimeseriesofempiricaldataobtainedoverarangeoflev-elsofdisturbanceTheresultsofsuchafittingprocesscanthenbeused to improve theparameter estimates andquantify theuncer-taintyassociatedwiththemodelpredictionsusingapproachessuchasBayesianhidden-processmodelling(NewmanBucklandLindleyThomasampFernandez 2006)However so far in no case has thisbeenpossibleandthereforeallmodelsappliedshouldstillbecon-sideredasldquoexploratoryrdquoExploratorymodelsareparticularlyusefulforcomparingthepossibleconsequencesofdifferentscenariosandforidentifyingpriorityareasforresearchHowever it is importantthat the uncertainties associatedwith their underlying parametervaluesaredocumentedandthattheeffectsoftheseuncertaintiesontheirpredictionsarequantified

Itisusefultoexploresomeofthedetailsofthemodelapplica-tionsinmarinemammalstoevaluatesomeoftheproblemsandsolu-tionsthatmayalsoapply insomewaytofishesNewetal (2014)forexampleusedthePCoDmodelstructuretoinvestigatethepo-tentialeffectsoflostforagingdivesonthehealth(measuredbytotallipidmassmdashseeSchickNewetal2013)ofadult femalesouthernelephant seals and the implications of variation in health for pupsurvivalandpopulationdynamicsTheyusedinformationobtainedfromdataloggersthatwereattachedtoanimalsimmediatelybeforetheyembarkedontheirpost-moultforagingtripsThedataloggersallowedareconstructionoftheirsurfacetransittimeandtheirforag-ingdivetimeDuringportionsofsomeforagingdiveselephantsealsdrift and the rateofverticalmovementduring thedrift is relatedtotheratiooflipidtoleanbodymassThedataloggerinformationwascalibratedagainstactuallipidgainduringtheforagingtripusingmeasurementsofbodycompositioncollectedbeforeandaftertheforagingtriptoenableestimationofdailylipidgain

FurthermoreNewetal (2014) linkedmaternalmassatbreed-ing to pupmass atweaning (Arnbom Fedak BoydampMcConnell1993)andpupmassatweaningtopupsurvival(McMahonBurtonampBester20002003)ThemodelwasthenusedtodeterminetheeffectofforagingdivedisturbanceonpupsurvivalItwasassumedthattherewerenoforagingdivesforthedurationofthedisturbanceandsurfacetransittimewassettotheobservedmaximumforthatindividual If animalswere disturbed for 50 of their time at seain1year thepredicteddecline inpopulationsizewassmall (lt1)However if thatdisturbancewouldcontinue indefinitely (eg asa

6emsp |emsp emspensp SLABBEKOORN Et AL

resultofvariationsintheextentoftheAntarcticicesheetcausedbyclimatechange)thepredictedeffectswouldbemuchgreater(a10declineinabundanceover30years)

TheanalysesinNewetal(2014)wereonlypossiblebecausede-tailedlongitudinaldatawereavailableonthemovementshealthandreproductivesuccessofalargenumberofadultfemalesealsSuchextensivedata sets requiredecadesof intensive research and areonly available for a fewmarinemammal populations ResearchershaveadoptedarangeoftechniquestobuildPCoDmodels insitu-ationswhereempiricaldataaremore limitedNabe-NielsenSiblyTougaardTeilmannandSveegaard(2014)usedanindividual-basedmodelofthemovementsofharbourporpoisestoestimatethepo-tentialeffectsofresponsestothesoundassociatedwithwindtur-bineoperationandshippingontheirenergyandreservesTheyuseda hypothetical relationship between energy reserves and survivalto calculate population-level consequences Villegas-AmtmannSchwarzSumichandCosta(2015)usedasimilarapproachtopre-dictthepotentialeffectsofreducedenergyintakeonreproductivesuccessandsurvivalforwesterngreywhales(Eschrichtius robustusEschrichtiidae)

Ifempiricaldataaresufficienttoestimatearelationbetweenbe-haviouralchangeandhealthbutnotbetweenhealthandvitalratesitmaybepossibletouseasurrogatemeasurefortherelevantvitalrate Christiansen and Lusseau (2015) used a bioenergetic modelandempiricalinformationonthebehaviouralresponseofadultfe-maleminkewhalestowhale-watchingboatsontheirsummerfeed-ing grounds in Iceland to estimate the effects of these responsesonthewhalesrsquohealth(asmeasuredbytheirblubbervolume)Theycalculated how different rates of encounter with whale-watchingboatswould affect an individualwhales health at the end of thesummerandthenusedanempiricallyderivedrelationbetweenfe-maleblubbervolumeandfoetallength(ChristiansenRasmussenampLusseau2014)asa surrogate for the relationshipbetweenhealthandtheprobabilityofgivingbirthAlthoughinteractionswithwhale-watchingboatsresultedina40reductioninfeedingactivitythepredictedeffectonafemalesbodyconditionoverthecourseofthesummerwasverysmall (0049reduction)becauseboatencoun-terswere actually rare This reduction in body conditionwas notpredictedtoaffectfoetalsurvivalHoweverevenifChristiansenandLusseau(2015)haddetectedasignificanteffectonfoetalsurvivaltheywould have been unable to forecast the population-level ef-fectsofexposuretowhale-watchingboatsbecausetheproportionoftheNorthAtlanticminkewhalepopulationthatfeedsinIcelandicwatersisnotknown

In situations where even surrogate measures are unavailableexpert elicitation (Runge Converse amp Lyons 2011 Sutherland ampBurgman2015)canbeusedtoparameterizesomeofthetransferfunctionsofthePCoDmodelExpertelicitationisaformalprocessinwhichanumberofexpertsonaparticulartopicareaskedtopre-dictwhatmay happen in a particular situation These predictionsare combined into calibrated quantitative statements with asso-ciated uncertainty which can be incorporated into mathematicalmodels(Martinetal2012)Kingetal(2015)usedthisapproachto

parameterize relationshipsbetween thenumberofdaysonwhichharbourporpoisesweredisturbedbynoiseassociatedwiththecon-structionofoffshorewindfarmsandtheirsurvivalandreproductivesuccessTheserelationshipswerethenusedtopredictthepotentialpopulationconsequencesofdifferentscenariosfortheconstructionofmultiplewindfarms

Thereare several studiesondifferentmarinemammal speciesthat have filled data gaps by asking experts Lusseau etal (2011)usedanexpertelicitationapproachtopredictthepotentialaggre-gate effect of noise associatedwithwind farm construction tourboat operation and harbour expansion on a bottlenose dolphin(Tursiops truncatusDelphinidae)populationThompsonetal(2013)usedittoassesspopulation-level impactsofdisturbancefrompiledrivingonharbourseals(Phoca vitulinaPhocidae)Spatialdistribu-tionpatternsandreceivednoiselevelswereintegratedwithdataonthepotentialfordisplacementandhearingdamageIngeneralun-certaintiesinecologicalmodelsarenotunusual(seeegClarketal2001HarwoodampStokes2003)andexpertelicitationisonewaytodealwiththemAcomplementaryapproachisecologicalriskassess-ment(ERA)possiblycombinedwithweightofevidence(WOE)(seeegHammaretal2014Hobdayetal2007Weed2005)

BasedontheexperienceandexamplesofPCADmodelsforma-rinemammalsaflowchart isdevelopedinFigure2whichappliesthe samemodel components transfer functions (Box1) and vitalratesinamodelforpopulationconsequencesofairgundisturbanceto fishesBeforeaddressing the literature inmoredetail the flowchartprovidesanoverviewofhowexposuretothesoundsofaseis-micsurveymaychangebehaviourinsuchawaythatitreducesin-dividualforagingefficiency(PurserampRadford2011ShafieiSabetNeoampSlabbekoorn2015)andincreasesvulnerabilitytopredation(Chanetal2010SimpsonPurserampRadford2015)Furthermoreswimmingmore or less efficientmay also detrimentally affect in-dividual energetics (Metcalfe etal 2016Villegas-Amtmannetal2015) while swimming less or in the wrong direction may resultin missed mating or spawning opportunities (Boussard 1981RossingtonBensonLepperampJones2013)Thesechanges inbe-haviourtogetherwithacuteorchronicstressphysiologicalchangesmayundermineindividualbodyconditionimmunocompetenceandphysiologicalinvestmentingrowthandreproduction(Barton2002Sierra-Flores Atack Migaud amp Davie 2015 Wendelaar-Bonga1997)The spectral and temporal structureof soundswill alsoaf-fect physiological stress levels as stronger responses have beenreportedtoboatnoiseandintermittentnoisethantomorehomog-enous white noise (Nichols Anderson amp Sirovic 2015WysockiDittamiampLadich2006respectively)

The translation from individual-level effects to the populationlevelinthePCADmodelforfishes(Figure2)isreflectedintheconse-quencesofthesebehaviouralandphysiologicalchangesforthevitalratesintermsofgrowthsurvivalandreproduction(cfCostaetal2015Harwoodetal2014Newetal2014)Thevitalratesdonotonlydetermineindividualfitnessimportanttounderstandselectionpressuresandevolutionarypotential(ChristiansenampLusseau2015HeinoPauliampDieckmann2015)butalsodeterminepopulationor

emspensp emsp | emsp7SLABBEKOORN Et AL

stockdevelopments(Hammaretal2014Newetal2014Patricketal2009)Directimpactsofseismicsurveyactivitiesonfisheriesare incorporatedthrough increasingor reducingcatchrateswhile

indirect impactsofseismicsurveyactivitiesonfisheriesarerepre-sented through potential impact on stock developments (McCullyPhillips Scottamp Ellis 2015 Patrick etal 2009) Behavioural and

F IGURE 2emspAflowchartofthepopulationconsequencesofacousticdisturbancemodeltailoredtofishes(asdevelopedinthecontextofairgunsoundandcodasamodelspecieshencetheacronymPCAD4Cod)DirectimpactonfisheriesindicatedinthetoprightisdeterminedbypositiveornegativechangesincatchrateduetofishmovementsduringandafteraseismicsurveyIndirectimpactonfisheriesunderneathisaffectedbybehavioural(green)andphysiological(pink)changesandtheirpotentiallynegativeeffectsforindividualfitnesspopulationhealthandstockdevelopmentTransferfunctionsthatrequirecriticalevaluationarenumbered1ndash12andareexplainedindetailinBox1Notethatindividualfitnessconcernslifetimereproductivesuccesswhichistheaccumulationofvitalratesattheindividuallevel(growthsurvivalandreproduction)Furthermorealthoughtransferfunctionsaredepictedunidirectionallythereversedpathwaycanalsoberelevantandimportantaspopulation-levelmetricssuchasabundanceandshiftsinpredator-preyorcompetitorrelationshipsmayfeedbackfrompopulationtoindividuallevel(iewarrantingbidirectionalarrows)

Airgun exposure

Behavioural change

Physiological change

Direct impact on fisheries

Indirect impact on fisheriesFeeding impact

Predation risk

Swimming energetics

Reproductive opportunities

Growth rate

survival

reproduction

Chronic stress

Immunocompetence

Developmental impact

Reproductive investment

Individual fitness

Population health amp stock development

1 2

4 5

7 8

9 10

11 12

113

6

Population consequences of acoustic disturbance model for fishes as applied to

airgun sound and cod (PCAD4Cod)

Box 1enspTransfer functions of the PCAD model for fishes (linked to Figure 2)1Behaviouralchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)2Physiologicalchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)3Interactionsbetweenbehaviouralresponsivenessandphysiologicalstate4Consequencesofbehaviouralchange(acuteandchronic)forvitalratesa ImpactonforagingefficiencyandopportunitiesbImpactonvulnerabilitytopredation(especiallyjuveniles)c EnergeticconsequencesofalteredswimmingpatternsdReproductiveconsequencesthroughmissedbreedingopportunities(adults)

5Consequencesofphysiologicalchange(acuteandchronic)forvitalratesa ImpactonchronicstressbeyondregulatoryfluctuationsbImpactonvulnerabilitytoinfectionsanddiseasecDevelopmentalconsequencesofphysiologicalimbalancedReproductiveconsequencesthroughfolliclematuration(adultsonly)

6Effectsonvitalratesofinteractionsbetweenbehaviouralandphysiologicalresponses7 Impactofbehaviouraleffectsongrowthratesurvivalandreproduction8Impactofphysiologicaleffectsongrowthratesurvivalandreproduction9 Impactofbehaviouralandphysiologicaleffectsonindividualfitness(lifetimereproductivesuccess)10enspConsequencesofchangesinindividualfitnessatthepopulationandstocklevel11enspEvaluationofdirectandindirecteffectsofseismicsurveysonfisheries12enspEvaluationofimpactfromseismicsurveysinthecontextof(sustainable)harvestingbyfisheries

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

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BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

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and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

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NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

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PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

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PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

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Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

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Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

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SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

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SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

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SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

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SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 3: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp3SLABBEKOORN Et AL

2005 Shannon etal 2016) Sufficient understanding of whethermeasuresofmitigationarenecessaryoradequateconsequentlyre-mainselusive

Airgunsused forseismicsurveysareoneofseveralprominentsourcesofnoisepollution(Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)Seismicsurveysinvolvelong seriesof intense soundpulses reflectionsofwhich from theseabedprovideinformationontheshapeandcompositionofoceanbottomlayersTheyareusedforexampletoobtaininsightintothesizeandlocationofoilandgasresourcesTheairgunsoundpulsescan make a significant contribution to the underwater ambientsoundprofileoverlargeareasastheycanbeaudibleoverthousandsofkilometres(Hildebrand2009Nieukirketal2012)Globaltrendsinacousticpresencesincehistoricalexplorationswithdynamiteinthe1920shaveseenchangesinsourcetypeandsurveyscalewhilespreadingofseismicexplorationactivitylargelyfollowedeconomicdevelopments(LandroslashampAmundsen2018)similartotherisingpat-ternsinvesselnoisesincethe1950s(Frisk2012McDonaldetal2006)

TheaimofthispaperistoreviewthecurrentstateofknowledgeonwhetherandhowseismicsurveyscanhaveadetrimentaleffectonfishesOurexplicittargetwastoevaluatetheevidenceforimpactfromairgun acoustic exposureon fish in termsofdamage distur-banceanddetectionofbiologicallyrelevantsoundsandtoaddressthepotential for extrapolationofdata and insights topopulation-levelconsequencesWethereforeexploredtheinterdisciplinaryna-tureofimpactassessment(cfRosaampKoper2018)focusedontheabundantlimitationsinthedatacurrentlyavailableandprovidedanoverviewofrelevantinformationandpotentialtoolssuitableforin-vestigationoncedatabecomeavailableCriticalfortheevaluationistounderstand(a)thateffectsonindividualanimalsshouldbetrans-latedtoconsequencesforstockspopulationsspeciescommunitiesorwholeecosystemsand(b)thatchoicesforspatial(localregionalglobal)andtemporalresolution(nowcomingyearsordecadesfor-ever)arelikelytohavealargeimpactontheoutcomewhilethesechoicescanberegardedaspoliticalorstrategicdecisions

Theorderinwhichweaddresstopicsandsubdisciplinesisasfol-lowsWestartwithabriefdescriptionofgeneralandmorespecificriskevaluationmethodsforenvironmentalhazardsSpecialattentionisallocatedtoso-calledproductivitysusceptibilityassessment(PSAMilton2001Patricketal20092010) asapplied to fish stocksandpopulationconsequencesofdisturbance(PCoD)models(Farmeretal2018NationalResearchCouncil2005Newetal2014)asappliedmainlytomarinemammalsWeaddressthepotentialrele-vanceforfishesexposedtosoundingeneralandseismicsurveysinparticularAsmarinebiologistsandpolicymakerstypicallyhavelittleknowledgeaboutseismicoperationswefurtheraddressthenatureofseismicsurveystoprovide insights intothesoundsourceof in-vestigationandthepotentialexposurecharacteristicsofmarinefish

Alsocriticalfortheevaluationisinsightintowhatweknow(andoftendonotknow)aboutwhatandhowfisheshearWethereforeprovideabriefreviewonfundamentalsoffishhearingfollowedbyaprimeronsoundpropagationmodelsthatrelatecharacteristicsof

thesoundsourcetothespreadandnatureoftheman-madesoundfieldWesubsequentlyreviewpublishedstudiesonbehaviouralandphysiologicalresponsedatarelatedtoairgunexposureandotherex-perimentalsoundexposurestudiesrelevanttopotentialeffectsofseismicsurveysWealsoaddresshowtointegratesuchavailableandnewdataintoaPCoD-typeframeworkusingdynamicenergybud-gets(DEBs)individual-basedmodels(IBMs)andmultitrophicstockmodels (MSMs) Finally we evaluate the feasibility of ecosystem-based assessments for sound impact assessmentwhich is an ap-proachthatcanbenefitfromexperienceandmodellinginfisheriesagainprovidedthatsufficientdatabecomeavailableaboutimpactofacousticdisturbanceonfishes

2emsp |emspIMPAC T A SSESSMENT

21emsp|emspRisk evaluation methods

Riskassessment isusedtoquantifytherisk (ieexpectedadversechangetotheenvironmentduetooneormorehazards)associatedwithdifferentalternativeactions(egHalpernetal2008HammarWikstroumlmampMolander2014Hobdayetal2007Newetal2014Weed 2005) There aremanyways to categorize risk assessmentmethodsforexample(a)rapidvsin-depth(b)top-downvsbottom-up (c) data-rich vs data-poor (d) qualitative semi-quantitativeorquantitativeand(e)empirical(iebasedondatawithlittleunderly-ing theory) vsmechanistic (basedon theoreticalmodels possiblyparameterizedwithdata)

Qualitative methods typically categorize different risks intoordinal (ie ordered) classes such as ldquolowrdquo ldquomediumrdquo and ldquohighrdquoalong two axes frequency (likelihood of occurrence) and severity(Figure1a)Theassignmentofriskleveltoeachelementoftheclas-sification(egsomethingthatishighfrequencybutlowseverityasnotbeingofconcernbutsomethingthatislowfrequencybuthighseverity as being ofmoderate concern) is essentially based on anunstatedalgorithm

Semi-quantitativemethods such as so-called productivity andsusceptibilityassessment(PSA)mayhavemultipleaxesandassignnumericalvaluestoeachaxisThesevaluesareordinalbutnotnom-inal(iethedifferencebetween1and2isnotnecessarilythesameas the difference between 2 and 3mdashnor do numbers on differentaxes necessarily have the same scale)Overall risk is obtained bysummingoraveragingthenumericalscoresmdashsomethingthatisofdu-biousutilitygiventheordinalnatureofthescoresImplicitorexplicitweightingandrescalingissometimesusedAsidefromPSAanotherexampleofsucharbitrarysummationisthecumulativeimpactanal-ysisofHalpernetal(2008)

Both qualitative and semi-quantitative methods suffer fromthesamefundamentalproblemcomparisonorcombinationofdif-ferent ordinal variables is essentially arbitrary Potential solutionsinclude groundtruthing where possible and simulation testingfor example throughmanagement strategy evaluation (Altenback1995)Anexampleofsimulationtestingisthatappliedtotheldquocatchlimit algorithmrdquo of the InternationalWhaling Commission Revised

4emsp |emsp emspensp SLABBEKOORN Et AL

ManagementProcedureNotethatsuchtestsareinherentlyquan-titativePossiblythebestsolutionistouseaquantitativemethodinthefirstplace

Quantitativemethodsrangefromin-depthbottom-updata-richmechanisticmethodssuchasafullPCoDmodel(Costaetal2015Newetal2014)tosemi-rapidtop-downdata-poorsemi-empiricalmethodssuchastheldquointerimPCoDrdquoapproachofKingetal(2015)whichusedexpertelicitation(describedlater)toparameterizeasim-plifiedfullPCoDmodelWearecurrentlyawareofonequalitativeandonemorequantitativeanalysisofpopulationconsequencesofacoustic disturbance on fishes Hammar etal (2014) conductedanecological riskassessment (ERA)onathreatenedpopulationofAtlanticcod(Gadus morhuaGadidae)inthecontextofawindfarmprojectTheyexploredthepotentialimpactofsixstressorsthreeofwhichweresoundrelatedmoderate-levelnoisefromworkingves-selsandoperatingturbinesandextremeover-exposureduetopile-drivingnoiseintheconstructionphaseTheanalysissuggestedthatpiledrivingwasthemosthazardousstressorthatcouldposeaseri-ousrisktothecodpopulationunderstudyAsignificantreductionofthisriskwasachievedinthemodelbyavoidingpile-drivingactivity

in themonths of cod recruitment Studies like this provide usefulinsights forurgentdecisionsandwhendataare lackingHowevertheydonotprovidesufficientquantificationanddonotexploitthedetailedinsightphysiologicalmodelsmayyield

SivleKvadsheimandAinslie(2014)modelledpopulationconse-quencesofsonarexposureforherring(Clupea harengusClupeidae)based on maximum reported sound levels of no behavioural re-sponse Their predictions for the potential risk to the populationofwhenthesemaximumlevelswereexceededvariedwithseasondependingonthedensityoffishTheriskofanypopulationconse-quencewaslowestduringspread-outfeedingbutincreasedinpe-riodsofpopulationaggregationHoweveringeneraltheresponseestimateswere lowandSivleetal (2014)concludedthat it isun-likely that todaysnaval sonaractivitywill lead toanypopulation-leveleffectforthisspecies

More sophisticated riskanalyses takeanexposureassessmentandadosendashresponseassessmentintoaccount(seeBoydetal2008)to characterize and evaluate whether the level of environmentalhazardisabovesomespecifiedthresholdformitigation(Figure1b)buttheserelyonavailabledataandarequantitativeinnatureThemain issuewithquantitativeapproaches isdeterminingwhere theinputcomesfromTheinputcomeseitherfromdatawhichareofteninshortsupplyorfromexpertelicitationwhichcanbeunreliableiftheanalysisisnotperformedwellandinverydata-poorsituationsTheobviousremedyhereistocollectsufficientandadequateinputdataoruseappropriatemethodologyforexpertelicitation incon-certwiththeriskevaluationeffortRobustnesstomodelmisspeci-ficationcanbeevaluatedthroughsimulationtestingAswebelievethat semi-quantitative PSA could (with development) be a usefulapproach in somecasesand thatPCoDmodelshavepotential formarinemammalsbutalsoforfishesweheregiveabriefdescriptionofthestateoftheartinboth

22emsp|emspProductivity susceptibility assessment

Productivity susceptibility assessment (PSA Milton 2001) canbe characterized as being rapid top-down data-poor semi-quantitativeandempiricalandwasoriginallydevelopedtoevaluatethe risk that fisheriespose to specific target species indata-poorsituations (Milton2001StobutzkiMillerampBrewer2001) Ithassubsequently been expanded to cover a wide range of fisheriesmanagementeffectsonfishstocks(habitatimpactecosystemcon-siderationsmanagementefficacymdashegHobdaySmithampStobutzki2004Hobdayetal2007Rosenbergetal2007)Itinvolvesscor-ingtheproductivityofasusceptiblespecies intermsofanumberof demographic parameters that affect population growth rate(survivalbirthrateetc)anditssusceptibilityintermsofexposureto risk from fisheries (areal and vertical distribution aggregationetc)andcurrentstatus(currentmanagementstrategyetc)(Patricketal20092010)TheproductivityscoresarethenaveragedandthesusceptibilityscoresmultipliedtogetherSpeciesthathavealowproductivityscoreandahighsusceptibilityscoreareconsideredtobeparticularlyvulnerable

F I G U R E 1emsp (a)Qualitativemethodofriskcategorizationintothequalitativeclassesldquolowrdquoldquomediumrdquoandldquohighrdquobasedonevaluationalongtwoaxesconsequenceseverityandaccidentfrequency(orprobability)Thecombinationsidentifysituationsofconcernormajorconcern(redrawnfromAltenback1995)(b)Generalmanagementframeworkforhazardidentificationandriskassessmenttoquantifytheriskandevaluatealternativeactions(mitigateoracceptrisk)(fromBoydetal2008)

High

Medium

Low

Low Medium High

Consequences of Severity

Acci

dent

freq

uenc

y

MajorConcern

MajorConcern

MajorConcernConcern

Concern

Identification of environmental hazard

Exposure assessment(number of animals location level)

Dosendash response assessment(toxicity and secondary effects)

Risk characterization (quotient)

Above thresholdfor action

Mitigation

YES

NO Risk acceptable

(a)

(b)

emspensp emsp | emsp5SLABBEKOORN Et AL

Themain productivity attributes of thePSA approachmaybeusefulinanyevaluationofdetrimentalimpactandconcernfactorsfor fish stocks The main attributes include maximum populationgrowth maximum individual size and age the ldquovon Bertalanffyrdquogrowthcoefficientforhowrapidlyafishreachesthismaximumsizeand theageatmaturitynaturalmortality and fecunditybreedingstrategy recruitmentpatternandmean trophic level (ahighscoreforpiscivoresintermediateforomnivoresandalowscoreforplank-tivores)Themainsusceptibilityattributesof thePSAapproach inthecontextoffisheriesconcerncatchabilityasdeterminedbygeo-graphicareaoverlapandverticaldistributionoverlapbetweenstockandfishingeffortsgeographicconcentrationseasonalmigrationsschooling aggregations and other behavioural and morphologicaltraitsinadditiontodesirabilityandmarketvalue(Patricketal20092010)Factorssuchastheeffectivenessofmanagementtocontrolcatch ratesand theeffectsof fishinggearonhabitatqualityhavealsobeenaddedto theseoriginalattributes inorder todeterminesusceptibilitytofisheries(Hobdayetal2007)

Additional susceptibility attributes that should be consideredif PSA were to be applied to seismic acoustic exposure includethegeographicandverticaldistributionoverlapofaparticularfishspecieswiththeacousticrangeofsoundsourcestodetermineex-posureprobability and level in termsof both soundpressure andparticlemotionAnyimpactofacousticexposureshouldbeconsid-eredontopofandinthecontextofseasonalvariationandspecificlifestagesizeandreproductiveconditionsandthefisheriesimpactifthetargetspeciesisalsoharvestedHoweverwebelievethatPSAcannotbeusedyetforevaluatingthepotentialvulnerabilityoffishstocks to anthropogenic noiseManyof the susceptibility scoringcategoriescurrentlyusedinPSAarenotparticularlyappropriateforassessingthepotentialeffectsofanthropogenicnoiseInadditionthe appropriateness of the essentially arbitraryway inwhich theindividual productivity and susceptibility scores are combined toprovideasinglemetricneedstobeevaluatedAnewsetofsuscep-tibilityscoringcategoriescouldbedevelopedforexampleusinganexpertelicitationprocess(SutherlandampBurgman2015)toidentifyfishspeciesandstocksthatarelikelytobeparticularlyvulnerabletotheeffects

23emsp|emspPopulation consequences of disturbance models

The population consequences of disturbance (PCoD) and popula-tion consequences of acoustic disturbance (PCAD) models (NRC2005Newetal2014)consistofaseriesoftransferfunctionsthatdescribehowexposure to stressors (such as anthropogenicnoise)affects individual behaviour how the resulting changes in behav-iourcanaffecthealth(definedasallinternalfactorsthataffectbodyconditionorhomoeostasis)andhowvariationsinhealthmayaffectvitalrates(survivalreproductionandgrowthageatfirstbreeding)Furthermorethetransferfunctionatthehighestleveloforganiza-tioninthemodeladdresseshowtheaccumulationofdataaboutthewayinwhichdifferentindividualsareexposedtoandaffectedbya

stressorcanbeusedtoscaleuptheanticipatedchangesinvitalratestopredictpopulation-leveleffects

PCADmodels have now been applied to a number of marinemammalspeciesforexamplenorthernandsouthernelephantseals(Mirounga angustirostris and M leoninaPhocidaeNewetal2014Costaetal2015)NorthAtlanticrightwhales (Eubalaena glacialisBalaenidae Schick Kraus etal 2013) beakedwhales (ZiphiidaeNew Moretti Hooker Costa amp Simmons 2013) harbour por-poise (Phocoena phocoena Phocoenidae Harwood King Schickamp Donovan 2014) and minke whale (Balaenoptera acutorostrataBalaenopteridaeChristiansenampLusseau2015)buttherearehardlyanyexamplessofarforfish(butseeSivleetal2014)

IdeallythepredictionsofPCADmodelsshouldbefittedtoap-propriatetimeseriesofempiricaldataobtainedoverarangeoflev-elsofdisturbanceTheresultsofsuchafittingprocesscanthenbeused to improve theparameter estimates andquantify theuncer-taintyassociatedwiththemodelpredictionsusingapproachessuchasBayesianhidden-processmodelling(NewmanBucklandLindleyThomasampFernandez 2006)However so far in no case has thisbeenpossibleandthereforeallmodelsappliedshouldstillbecon-sideredasldquoexploratoryrdquoExploratorymodelsareparticularlyusefulforcomparingthepossibleconsequencesofdifferentscenariosandforidentifyingpriorityareasforresearchHowever it is importantthat the uncertainties associatedwith their underlying parametervaluesaredocumentedandthattheeffectsoftheseuncertaintiesontheirpredictionsarequantified

Itisusefultoexploresomeofthedetailsofthemodelapplica-tionsinmarinemammalstoevaluatesomeoftheproblemsandsolu-tionsthatmayalsoapply insomewaytofishesNewetal (2014)forexampleusedthePCoDmodelstructuretoinvestigatethepo-tentialeffectsoflostforagingdivesonthehealth(measuredbytotallipidmassmdashseeSchickNewetal2013)ofadult femalesouthernelephant seals and the implications of variation in health for pupsurvivalandpopulationdynamicsTheyusedinformationobtainedfromdataloggersthatwereattachedtoanimalsimmediatelybeforetheyembarkedontheirpost-moultforagingtripsThedataloggersallowedareconstructionoftheirsurfacetransittimeandtheirforag-ingdivetimeDuringportionsofsomeforagingdiveselephantsealsdrift and the rateofverticalmovementduring thedrift is relatedtotheratiooflipidtoleanbodymassThedataloggerinformationwascalibratedagainstactuallipidgainduringtheforagingtripusingmeasurementsofbodycompositioncollectedbeforeandaftertheforagingtriptoenableestimationofdailylipidgain

FurthermoreNewetal (2014) linkedmaternalmassatbreed-ing to pupmass atweaning (Arnbom Fedak BoydampMcConnell1993)andpupmassatweaningtopupsurvival(McMahonBurtonampBester20002003)ThemodelwasthenusedtodeterminetheeffectofforagingdivedisturbanceonpupsurvivalItwasassumedthattherewerenoforagingdivesforthedurationofthedisturbanceandsurfacetransittimewassettotheobservedmaximumforthatindividual If animalswere disturbed for 50 of their time at seain1year thepredicteddecline inpopulationsizewassmall (lt1)However if thatdisturbancewouldcontinue indefinitely (eg asa

6emsp |emsp emspensp SLABBEKOORN Et AL

resultofvariationsintheextentoftheAntarcticicesheetcausedbyclimatechange)thepredictedeffectswouldbemuchgreater(a10declineinabundanceover30years)

TheanalysesinNewetal(2014)wereonlypossiblebecausede-tailedlongitudinaldatawereavailableonthemovementshealthandreproductivesuccessofalargenumberofadultfemalesealsSuchextensivedata sets requiredecadesof intensive research and areonly available for a fewmarinemammal populations ResearchershaveadoptedarangeoftechniquestobuildPCoDmodels insitu-ationswhereempiricaldataaremore limitedNabe-NielsenSiblyTougaardTeilmannandSveegaard(2014)usedanindividual-basedmodelofthemovementsofharbourporpoisestoestimatethepo-tentialeffectsofresponsestothesoundassociatedwithwindtur-bineoperationandshippingontheirenergyandreservesTheyuseda hypothetical relationship between energy reserves and survivalto calculate population-level consequences Villegas-AmtmannSchwarzSumichandCosta(2015)usedasimilarapproachtopre-dictthepotentialeffectsofreducedenergyintakeonreproductivesuccessandsurvivalforwesterngreywhales(Eschrichtius robustusEschrichtiidae)

Ifempiricaldataaresufficienttoestimatearelationbetweenbe-haviouralchangeandhealthbutnotbetweenhealthandvitalratesitmaybepossibletouseasurrogatemeasurefortherelevantvitalrate Christiansen and Lusseau (2015) used a bioenergetic modelandempiricalinformationonthebehaviouralresponseofadultfe-maleminkewhalestowhale-watchingboatsontheirsummerfeed-ing grounds in Iceland to estimate the effects of these responsesonthewhalesrsquohealth(asmeasuredbytheirblubbervolume)Theycalculated how different rates of encounter with whale-watchingboatswould affect an individualwhales health at the end of thesummerandthenusedanempiricallyderivedrelationbetweenfe-maleblubbervolumeandfoetallength(ChristiansenRasmussenampLusseau2014)asa surrogate for the relationshipbetweenhealthandtheprobabilityofgivingbirthAlthoughinteractionswithwhale-watchingboatsresultedina40reductioninfeedingactivitythepredictedeffectonafemalesbodyconditionoverthecourseofthesummerwasverysmall (0049reduction)becauseboatencoun-terswere actually rare This reduction in body conditionwas notpredictedtoaffectfoetalsurvivalHoweverevenifChristiansenandLusseau(2015)haddetectedasignificanteffectonfoetalsurvivaltheywould have been unable to forecast the population-level ef-fectsofexposuretowhale-watchingboatsbecausetheproportionoftheNorthAtlanticminkewhalepopulationthatfeedsinIcelandicwatersisnotknown

In situations where even surrogate measures are unavailableexpert elicitation (Runge Converse amp Lyons 2011 Sutherland ampBurgman2015)canbeusedtoparameterizesomeofthetransferfunctionsofthePCoDmodelExpertelicitationisaformalprocessinwhichanumberofexpertsonaparticulartopicareaskedtopre-dictwhatmay happen in a particular situation These predictionsare combined into calibrated quantitative statements with asso-ciated uncertainty which can be incorporated into mathematicalmodels(Martinetal2012)Kingetal(2015)usedthisapproachto

parameterize relationshipsbetween thenumberofdaysonwhichharbourporpoisesweredisturbedbynoiseassociatedwiththecon-structionofoffshorewindfarmsandtheirsurvivalandreproductivesuccessTheserelationshipswerethenusedtopredictthepotentialpopulationconsequencesofdifferentscenariosfortheconstructionofmultiplewindfarms

Thereare several studiesondifferentmarinemammal speciesthat have filled data gaps by asking experts Lusseau etal (2011)usedanexpertelicitationapproachtopredictthepotentialaggre-gate effect of noise associatedwithwind farm construction tourboat operation and harbour expansion on a bottlenose dolphin(Tursiops truncatusDelphinidae)populationThompsonetal(2013)usedittoassesspopulation-level impactsofdisturbancefrompiledrivingonharbourseals(Phoca vitulinaPhocidae)Spatialdistribu-tionpatternsandreceivednoiselevelswereintegratedwithdataonthepotentialfordisplacementandhearingdamageIngeneralun-certaintiesinecologicalmodelsarenotunusual(seeegClarketal2001HarwoodampStokes2003)andexpertelicitationisonewaytodealwiththemAcomplementaryapproachisecologicalriskassess-ment(ERA)possiblycombinedwithweightofevidence(WOE)(seeegHammaretal2014Hobdayetal2007Weed2005)

BasedontheexperienceandexamplesofPCADmodelsforma-rinemammalsaflowchart isdevelopedinFigure2whichappliesthe samemodel components transfer functions (Box1) and vitalratesinamodelforpopulationconsequencesofairgundisturbanceto fishesBeforeaddressing the literature inmoredetail the flowchartprovidesanoverviewofhowexposuretothesoundsofaseis-micsurveymaychangebehaviourinsuchawaythatitreducesin-dividualforagingefficiency(PurserampRadford2011ShafieiSabetNeoampSlabbekoorn2015)andincreasesvulnerabilitytopredation(Chanetal2010SimpsonPurserampRadford2015)Furthermoreswimmingmore or less efficientmay also detrimentally affect in-dividual energetics (Metcalfe etal 2016Villegas-Amtmannetal2015) while swimming less or in the wrong direction may resultin missed mating or spawning opportunities (Boussard 1981RossingtonBensonLepperampJones2013)Thesechanges inbe-haviourtogetherwithacuteorchronicstressphysiologicalchangesmayundermineindividualbodyconditionimmunocompetenceandphysiologicalinvestmentingrowthandreproduction(Barton2002Sierra-Flores Atack Migaud amp Davie 2015 Wendelaar-Bonga1997)The spectral and temporal structureof soundswill alsoaf-fect physiological stress levels as stronger responses have beenreportedtoboatnoiseandintermittentnoisethantomorehomog-enous white noise (Nichols Anderson amp Sirovic 2015WysockiDittamiampLadich2006respectively)

The translation from individual-level effects to the populationlevelinthePCADmodelforfishes(Figure2)isreflectedintheconse-quencesofthesebehaviouralandphysiologicalchangesforthevitalratesintermsofgrowthsurvivalandreproduction(cfCostaetal2015Harwoodetal2014Newetal2014)Thevitalratesdonotonlydetermineindividualfitnessimportanttounderstandselectionpressuresandevolutionarypotential(ChristiansenampLusseau2015HeinoPauliampDieckmann2015)butalsodeterminepopulationor

emspensp emsp | emsp7SLABBEKOORN Et AL

stockdevelopments(Hammaretal2014Newetal2014Patricketal2009)Directimpactsofseismicsurveyactivitiesonfisheriesare incorporatedthrough increasingor reducingcatchrateswhile

indirect impactsofseismicsurveyactivitiesonfisheriesarerepre-sented through potential impact on stock developments (McCullyPhillips Scottamp Ellis 2015 Patrick etal 2009) Behavioural and

F IGURE 2emspAflowchartofthepopulationconsequencesofacousticdisturbancemodeltailoredtofishes(asdevelopedinthecontextofairgunsoundandcodasamodelspecieshencetheacronymPCAD4Cod)DirectimpactonfisheriesindicatedinthetoprightisdeterminedbypositiveornegativechangesincatchrateduetofishmovementsduringandafteraseismicsurveyIndirectimpactonfisheriesunderneathisaffectedbybehavioural(green)andphysiological(pink)changesandtheirpotentiallynegativeeffectsforindividualfitnesspopulationhealthandstockdevelopmentTransferfunctionsthatrequirecriticalevaluationarenumbered1ndash12andareexplainedindetailinBox1Notethatindividualfitnessconcernslifetimereproductivesuccesswhichistheaccumulationofvitalratesattheindividuallevel(growthsurvivalandreproduction)Furthermorealthoughtransferfunctionsaredepictedunidirectionallythereversedpathwaycanalsoberelevantandimportantaspopulation-levelmetricssuchasabundanceandshiftsinpredator-preyorcompetitorrelationshipsmayfeedbackfrompopulationtoindividuallevel(iewarrantingbidirectionalarrows)

Airgun exposure

Behavioural change

Physiological change

Direct impact on fisheries

Indirect impact on fisheriesFeeding impact

Predation risk

Swimming energetics

Reproductive opportunities

Growth rate

survival

reproduction

Chronic stress

Immunocompetence

Developmental impact

Reproductive investment

Individual fitness

Population health amp stock development

1 2

4 5

7 8

9 10

11 12

113

6

Population consequences of acoustic disturbance model for fishes as applied to

airgun sound and cod (PCAD4Cod)

Box 1enspTransfer functions of the PCAD model for fishes (linked to Figure 2)1Behaviouralchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)2Physiologicalchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)3Interactionsbetweenbehaviouralresponsivenessandphysiologicalstate4Consequencesofbehaviouralchange(acuteandchronic)forvitalratesa ImpactonforagingefficiencyandopportunitiesbImpactonvulnerabilitytopredation(especiallyjuveniles)c EnergeticconsequencesofalteredswimmingpatternsdReproductiveconsequencesthroughmissedbreedingopportunities(adults)

5Consequencesofphysiologicalchange(acuteandchronic)forvitalratesa ImpactonchronicstressbeyondregulatoryfluctuationsbImpactonvulnerabilitytoinfectionsanddiseasecDevelopmentalconsequencesofphysiologicalimbalancedReproductiveconsequencesthroughfolliclematuration(adultsonly)

6Effectsonvitalratesofinteractionsbetweenbehaviouralandphysiologicalresponses7 Impactofbehaviouraleffectsongrowthratesurvivalandreproduction8Impactofphysiologicaleffectsongrowthratesurvivalandreproduction9 Impactofbehaviouralandphysiologicaleffectsonindividualfitness(lifetimereproductivesuccess)10enspConsequencesofchangesinindividualfitnessatthepopulationandstocklevel11enspEvaluationofdirectandindirecteffectsofseismicsurveysonfisheries12enspEvaluationofimpactfromseismicsurveysinthecontextof(sustainable)harvestingbyfisheries

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

AartsGMvonBenda-BeckmannAMvonLuckeKSertlekHOumlvanBemmelenRGeelhoedSCVhellipKirkwoodR (2016)Movement strategy of harbour porpoise affects the number ofanimals acoustically exposed to underwater explosions Marine Ecology Progress Series 557 261ndash275 httpsdoiorg103354meps11829

AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 4: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

4emsp |emsp emspensp SLABBEKOORN Et AL

ManagementProcedureNotethatsuchtestsareinherentlyquan-titativePossiblythebestsolutionistouseaquantitativemethodinthefirstplace

Quantitativemethodsrangefromin-depthbottom-updata-richmechanisticmethodssuchasafullPCoDmodel(Costaetal2015Newetal2014)tosemi-rapidtop-downdata-poorsemi-empiricalmethodssuchastheldquointerimPCoDrdquoapproachofKingetal(2015)whichusedexpertelicitation(describedlater)toparameterizeasim-plifiedfullPCoDmodelWearecurrentlyawareofonequalitativeandonemorequantitativeanalysisofpopulationconsequencesofacoustic disturbance on fishes Hammar etal (2014) conductedanecological riskassessment (ERA)onathreatenedpopulationofAtlanticcod(Gadus morhuaGadidae)inthecontextofawindfarmprojectTheyexploredthepotentialimpactofsixstressorsthreeofwhichweresoundrelatedmoderate-levelnoisefromworkingves-selsandoperatingturbinesandextremeover-exposureduetopile-drivingnoiseintheconstructionphaseTheanalysissuggestedthatpiledrivingwasthemosthazardousstressorthatcouldposeaseri-ousrisktothecodpopulationunderstudyAsignificantreductionofthisriskwasachievedinthemodelbyavoidingpile-drivingactivity

in themonths of cod recruitment Studies like this provide usefulinsights forurgentdecisionsandwhendataare lackingHowevertheydonotprovidesufficientquantificationanddonotexploitthedetailedinsightphysiologicalmodelsmayyield

SivleKvadsheimandAinslie(2014)modelledpopulationconse-quencesofsonarexposureforherring(Clupea harengusClupeidae)based on maximum reported sound levels of no behavioural re-sponse Their predictions for the potential risk to the populationofwhenthesemaximumlevelswereexceededvariedwithseasondependingonthedensityoffishTheriskofanypopulationconse-quencewaslowestduringspread-outfeedingbutincreasedinpe-riodsofpopulationaggregationHoweveringeneraltheresponseestimateswere lowandSivleetal (2014)concludedthat it isun-likely that todaysnaval sonaractivitywill lead toanypopulation-leveleffectforthisspecies

More sophisticated riskanalyses takeanexposureassessmentandadosendashresponseassessmentintoaccount(seeBoydetal2008)to characterize and evaluate whether the level of environmentalhazardisabovesomespecifiedthresholdformitigation(Figure1b)buttheserelyonavailabledataandarequantitativeinnatureThemain issuewithquantitativeapproaches isdeterminingwhere theinputcomesfromTheinputcomeseitherfromdatawhichareofteninshortsupplyorfromexpertelicitationwhichcanbeunreliableiftheanalysisisnotperformedwellandinverydata-poorsituationsTheobviousremedyhereistocollectsufficientandadequateinputdataoruseappropriatemethodologyforexpertelicitation incon-certwiththeriskevaluationeffortRobustnesstomodelmisspeci-ficationcanbeevaluatedthroughsimulationtestingAswebelievethat semi-quantitative PSA could (with development) be a usefulapproach in somecasesand thatPCoDmodelshavepotential formarinemammalsbutalsoforfishesweheregiveabriefdescriptionofthestateoftheartinboth

22emsp|emspProductivity susceptibility assessment

Productivity susceptibility assessment (PSA Milton 2001) canbe characterized as being rapid top-down data-poor semi-quantitativeandempiricalandwasoriginallydevelopedtoevaluatethe risk that fisheriespose to specific target species indata-poorsituations (Milton2001StobutzkiMillerampBrewer2001) Ithassubsequently been expanded to cover a wide range of fisheriesmanagementeffectsonfishstocks(habitatimpactecosystemcon-siderationsmanagementefficacymdashegHobdaySmithampStobutzki2004Hobdayetal2007Rosenbergetal2007)Itinvolvesscor-ingtheproductivityofasusceptiblespecies intermsofanumberof demographic parameters that affect population growth rate(survivalbirthrateetc)anditssusceptibilityintermsofexposureto risk from fisheries (areal and vertical distribution aggregationetc)andcurrentstatus(currentmanagementstrategyetc)(Patricketal20092010)TheproductivityscoresarethenaveragedandthesusceptibilityscoresmultipliedtogetherSpeciesthathavealowproductivityscoreandahighsusceptibilityscoreareconsideredtobeparticularlyvulnerable

F I G U R E 1emsp (a)Qualitativemethodofriskcategorizationintothequalitativeclassesldquolowrdquoldquomediumrdquoandldquohighrdquobasedonevaluationalongtwoaxesconsequenceseverityandaccidentfrequency(orprobability)Thecombinationsidentifysituationsofconcernormajorconcern(redrawnfromAltenback1995)(b)Generalmanagementframeworkforhazardidentificationandriskassessmenttoquantifytheriskandevaluatealternativeactions(mitigateoracceptrisk)(fromBoydetal2008)

High

Medium

Low

Low Medium High

Consequences of Severity

Acci

dent

freq

uenc

y

MajorConcern

MajorConcern

MajorConcernConcern

Concern

Identification of environmental hazard

Exposure assessment(number of animals location level)

Dosendash response assessment(toxicity and secondary effects)

Risk characterization (quotient)

Above thresholdfor action

Mitigation

YES

NO Risk acceptable

(a)

(b)

emspensp emsp | emsp5SLABBEKOORN Et AL

Themain productivity attributes of thePSA approachmaybeusefulinanyevaluationofdetrimentalimpactandconcernfactorsfor fish stocks The main attributes include maximum populationgrowth maximum individual size and age the ldquovon Bertalanffyrdquogrowthcoefficientforhowrapidlyafishreachesthismaximumsizeand theageatmaturitynaturalmortality and fecunditybreedingstrategy recruitmentpatternandmean trophic level (ahighscoreforpiscivoresintermediateforomnivoresandalowscoreforplank-tivores)Themainsusceptibilityattributesof thePSAapproach inthecontextoffisheriesconcerncatchabilityasdeterminedbygeo-graphicareaoverlapandverticaldistributionoverlapbetweenstockandfishingeffortsgeographicconcentrationseasonalmigrationsschooling aggregations and other behavioural and morphologicaltraitsinadditiontodesirabilityandmarketvalue(Patricketal20092010)Factorssuchastheeffectivenessofmanagementtocontrolcatch ratesand theeffectsof fishinggearonhabitatqualityhavealsobeenaddedto theseoriginalattributes inorder todeterminesusceptibilitytofisheries(Hobdayetal2007)

Additional susceptibility attributes that should be consideredif PSA were to be applied to seismic acoustic exposure includethegeographicandverticaldistributionoverlapofaparticularfishspecieswiththeacousticrangeofsoundsourcestodetermineex-posureprobability and level in termsof both soundpressure andparticlemotionAnyimpactofacousticexposureshouldbeconsid-eredontopofandinthecontextofseasonalvariationandspecificlifestagesizeandreproductiveconditionsandthefisheriesimpactifthetargetspeciesisalsoharvestedHoweverwebelievethatPSAcannotbeusedyetforevaluatingthepotentialvulnerabilityoffishstocks to anthropogenic noiseManyof the susceptibility scoringcategoriescurrentlyusedinPSAarenotparticularlyappropriateforassessingthepotentialeffectsofanthropogenicnoiseInadditionthe appropriateness of the essentially arbitraryway inwhich theindividual productivity and susceptibility scores are combined toprovideasinglemetricneedstobeevaluatedAnewsetofsuscep-tibilityscoringcategoriescouldbedevelopedforexampleusinganexpertelicitationprocess(SutherlandampBurgman2015)toidentifyfishspeciesandstocksthatarelikelytobeparticularlyvulnerabletotheeffects

23emsp|emspPopulation consequences of disturbance models

The population consequences of disturbance (PCoD) and popula-tion consequences of acoustic disturbance (PCAD) models (NRC2005Newetal2014)consistofaseriesoftransferfunctionsthatdescribehowexposure to stressors (such as anthropogenicnoise)affects individual behaviour how the resulting changes in behav-iourcanaffecthealth(definedasallinternalfactorsthataffectbodyconditionorhomoeostasis)andhowvariationsinhealthmayaffectvitalrates(survivalreproductionandgrowthageatfirstbreeding)Furthermorethetransferfunctionatthehighestleveloforganiza-tioninthemodeladdresseshowtheaccumulationofdataaboutthewayinwhichdifferentindividualsareexposedtoandaffectedbya

stressorcanbeusedtoscaleuptheanticipatedchangesinvitalratestopredictpopulation-leveleffects

PCADmodels have now been applied to a number of marinemammalspeciesforexamplenorthernandsouthernelephantseals(Mirounga angustirostris and M leoninaPhocidaeNewetal2014Costaetal2015)NorthAtlanticrightwhales (Eubalaena glacialisBalaenidae Schick Kraus etal 2013) beakedwhales (ZiphiidaeNew Moretti Hooker Costa amp Simmons 2013) harbour por-poise (Phocoena phocoena Phocoenidae Harwood King Schickamp Donovan 2014) and minke whale (Balaenoptera acutorostrataBalaenopteridaeChristiansenampLusseau2015)buttherearehardlyanyexamplessofarforfish(butseeSivleetal2014)

IdeallythepredictionsofPCADmodelsshouldbefittedtoap-propriatetimeseriesofempiricaldataobtainedoverarangeoflev-elsofdisturbanceTheresultsofsuchafittingprocesscanthenbeused to improve theparameter estimates andquantify theuncer-taintyassociatedwiththemodelpredictionsusingapproachessuchasBayesianhidden-processmodelling(NewmanBucklandLindleyThomasampFernandez 2006)However so far in no case has thisbeenpossibleandthereforeallmodelsappliedshouldstillbecon-sideredasldquoexploratoryrdquoExploratorymodelsareparticularlyusefulforcomparingthepossibleconsequencesofdifferentscenariosandforidentifyingpriorityareasforresearchHowever it is importantthat the uncertainties associatedwith their underlying parametervaluesaredocumentedandthattheeffectsoftheseuncertaintiesontheirpredictionsarequantified

Itisusefultoexploresomeofthedetailsofthemodelapplica-tionsinmarinemammalstoevaluatesomeoftheproblemsandsolu-tionsthatmayalsoapply insomewaytofishesNewetal (2014)forexampleusedthePCoDmodelstructuretoinvestigatethepo-tentialeffectsoflostforagingdivesonthehealth(measuredbytotallipidmassmdashseeSchickNewetal2013)ofadult femalesouthernelephant seals and the implications of variation in health for pupsurvivalandpopulationdynamicsTheyusedinformationobtainedfromdataloggersthatwereattachedtoanimalsimmediatelybeforetheyembarkedontheirpost-moultforagingtripsThedataloggersallowedareconstructionoftheirsurfacetransittimeandtheirforag-ingdivetimeDuringportionsofsomeforagingdiveselephantsealsdrift and the rateofverticalmovementduring thedrift is relatedtotheratiooflipidtoleanbodymassThedataloggerinformationwascalibratedagainstactuallipidgainduringtheforagingtripusingmeasurementsofbodycompositioncollectedbeforeandaftertheforagingtriptoenableestimationofdailylipidgain

FurthermoreNewetal (2014) linkedmaternalmassatbreed-ing to pupmass atweaning (Arnbom Fedak BoydampMcConnell1993)andpupmassatweaningtopupsurvival(McMahonBurtonampBester20002003)ThemodelwasthenusedtodeterminetheeffectofforagingdivedisturbanceonpupsurvivalItwasassumedthattherewerenoforagingdivesforthedurationofthedisturbanceandsurfacetransittimewassettotheobservedmaximumforthatindividual If animalswere disturbed for 50 of their time at seain1year thepredicteddecline inpopulationsizewassmall (lt1)However if thatdisturbancewouldcontinue indefinitely (eg asa

6emsp |emsp emspensp SLABBEKOORN Et AL

resultofvariationsintheextentoftheAntarcticicesheetcausedbyclimatechange)thepredictedeffectswouldbemuchgreater(a10declineinabundanceover30years)

TheanalysesinNewetal(2014)wereonlypossiblebecausede-tailedlongitudinaldatawereavailableonthemovementshealthandreproductivesuccessofalargenumberofadultfemalesealsSuchextensivedata sets requiredecadesof intensive research and areonly available for a fewmarinemammal populations ResearchershaveadoptedarangeoftechniquestobuildPCoDmodels insitu-ationswhereempiricaldataaremore limitedNabe-NielsenSiblyTougaardTeilmannandSveegaard(2014)usedanindividual-basedmodelofthemovementsofharbourporpoisestoestimatethepo-tentialeffectsofresponsestothesoundassociatedwithwindtur-bineoperationandshippingontheirenergyandreservesTheyuseda hypothetical relationship between energy reserves and survivalto calculate population-level consequences Villegas-AmtmannSchwarzSumichandCosta(2015)usedasimilarapproachtopre-dictthepotentialeffectsofreducedenergyintakeonreproductivesuccessandsurvivalforwesterngreywhales(Eschrichtius robustusEschrichtiidae)

Ifempiricaldataaresufficienttoestimatearelationbetweenbe-haviouralchangeandhealthbutnotbetweenhealthandvitalratesitmaybepossibletouseasurrogatemeasurefortherelevantvitalrate Christiansen and Lusseau (2015) used a bioenergetic modelandempiricalinformationonthebehaviouralresponseofadultfe-maleminkewhalestowhale-watchingboatsontheirsummerfeed-ing grounds in Iceland to estimate the effects of these responsesonthewhalesrsquohealth(asmeasuredbytheirblubbervolume)Theycalculated how different rates of encounter with whale-watchingboatswould affect an individualwhales health at the end of thesummerandthenusedanempiricallyderivedrelationbetweenfe-maleblubbervolumeandfoetallength(ChristiansenRasmussenampLusseau2014)asa surrogate for the relationshipbetweenhealthandtheprobabilityofgivingbirthAlthoughinteractionswithwhale-watchingboatsresultedina40reductioninfeedingactivitythepredictedeffectonafemalesbodyconditionoverthecourseofthesummerwasverysmall (0049reduction)becauseboatencoun-terswere actually rare This reduction in body conditionwas notpredictedtoaffectfoetalsurvivalHoweverevenifChristiansenandLusseau(2015)haddetectedasignificanteffectonfoetalsurvivaltheywould have been unable to forecast the population-level ef-fectsofexposuretowhale-watchingboatsbecausetheproportionoftheNorthAtlanticminkewhalepopulationthatfeedsinIcelandicwatersisnotknown

In situations where even surrogate measures are unavailableexpert elicitation (Runge Converse amp Lyons 2011 Sutherland ampBurgman2015)canbeusedtoparameterizesomeofthetransferfunctionsofthePCoDmodelExpertelicitationisaformalprocessinwhichanumberofexpertsonaparticulartopicareaskedtopre-dictwhatmay happen in a particular situation These predictionsare combined into calibrated quantitative statements with asso-ciated uncertainty which can be incorporated into mathematicalmodels(Martinetal2012)Kingetal(2015)usedthisapproachto

parameterize relationshipsbetween thenumberofdaysonwhichharbourporpoisesweredisturbedbynoiseassociatedwiththecon-structionofoffshorewindfarmsandtheirsurvivalandreproductivesuccessTheserelationshipswerethenusedtopredictthepotentialpopulationconsequencesofdifferentscenariosfortheconstructionofmultiplewindfarms

Thereare several studiesondifferentmarinemammal speciesthat have filled data gaps by asking experts Lusseau etal (2011)usedanexpertelicitationapproachtopredictthepotentialaggre-gate effect of noise associatedwithwind farm construction tourboat operation and harbour expansion on a bottlenose dolphin(Tursiops truncatusDelphinidae)populationThompsonetal(2013)usedittoassesspopulation-level impactsofdisturbancefrompiledrivingonharbourseals(Phoca vitulinaPhocidae)Spatialdistribu-tionpatternsandreceivednoiselevelswereintegratedwithdataonthepotentialfordisplacementandhearingdamageIngeneralun-certaintiesinecologicalmodelsarenotunusual(seeegClarketal2001HarwoodampStokes2003)andexpertelicitationisonewaytodealwiththemAcomplementaryapproachisecologicalriskassess-ment(ERA)possiblycombinedwithweightofevidence(WOE)(seeegHammaretal2014Hobdayetal2007Weed2005)

BasedontheexperienceandexamplesofPCADmodelsforma-rinemammalsaflowchart isdevelopedinFigure2whichappliesthe samemodel components transfer functions (Box1) and vitalratesinamodelforpopulationconsequencesofairgundisturbanceto fishesBeforeaddressing the literature inmoredetail the flowchartprovidesanoverviewofhowexposuretothesoundsofaseis-micsurveymaychangebehaviourinsuchawaythatitreducesin-dividualforagingefficiency(PurserampRadford2011ShafieiSabetNeoampSlabbekoorn2015)andincreasesvulnerabilitytopredation(Chanetal2010SimpsonPurserampRadford2015)Furthermoreswimmingmore or less efficientmay also detrimentally affect in-dividual energetics (Metcalfe etal 2016Villegas-Amtmannetal2015) while swimming less or in the wrong direction may resultin missed mating or spawning opportunities (Boussard 1981RossingtonBensonLepperampJones2013)Thesechanges inbe-haviourtogetherwithacuteorchronicstressphysiologicalchangesmayundermineindividualbodyconditionimmunocompetenceandphysiologicalinvestmentingrowthandreproduction(Barton2002Sierra-Flores Atack Migaud amp Davie 2015 Wendelaar-Bonga1997)The spectral and temporal structureof soundswill alsoaf-fect physiological stress levels as stronger responses have beenreportedtoboatnoiseandintermittentnoisethantomorehomog-enous white noise (Nichols Anderson amp Sirovic 2015WysockiDittamiampLadich2006respectively)

The translation from individual-level effects to the populationlevelinthePCADmodelforfishes(Figure2)isreflectedintheconse-quencesofthesebehaviouralandphysiologicalchangesforthevitalratesintermsofgrowthsurvivalandreproduction(cfCostaetal2015Harwoodetal2014Newetal2014)Thevitalratesdonotonlydetermineindividualfitnessimportanttounderstandselectionpressuresandevolutionarypotential(ChristiansenampLusseau2015HeinoPauliampDieckmann2015)butalsodeterminepopulationor

emspensp emsp | emsp7SLABBEKOORN Et AL

stockdevelopments(Hammaretal2014Newetal2014Patricketal2009)Directimpactsofseismicsurveyactivitiesonfisheriesare incorporatedthrough increasingor reducingcatchrateswhile

indirect impactsofseismicsurveyactivitiesonfisheriesarerepre-sented through potential impact on stock developments (McCullyPhillips Scottamp Ellis 2015 Patrick etal 2009) Behavioural and

F IGURE 2emspAflowchartofthepopulationconsequencesofacousticdisturbancemodeltailoredtofishes(asdevelopedinthecontextofairgunsoundandcodasamodelspecieshencetheacronymPCAD4Cod)DirectimpactonfisheriesindicatedinthetoprightisdeterminedbypositiveornegativechangesincatchrateduetofishmovementsduringandafteraseismicsurveyIndirectimpactonfisheriesunderneathisaffectedbybehavioural(green)andphysiological(pink)changesandtheirpotentiallynegativeeffectsforindividualfitnesspopulationhealthandstockdevelopmentTransferfunctionsthatrequirecriticalevaluationarenumbered1ndash12andareexplainedindetailinBox1Notethatindividualfitnessconcernslifetimereproductivesuccesswhichistheaccumulationofvitalratesattheindividuallevel(growthsurvivalandreproduction)Furthermorealthoughtransferfunctionsaredepictedunidirectionallythereversedpathwaycanalsoberelevantandimportantaspopulation-levelmetricssuchasabundanceandshiftsinpredator-preyorcompetitorrelationshipsmayfeedbackfrompopulationtoindividuallevel(iewarrantingbidirectionalarrows)

Airgun exposure

Behavioural change

Physiological change

Direct impact on fisheries

Indirect impact on fisheriesFeeding impact

Predation risk

Swimming energetics

Reproductive opportunities

Growth rate

survival

reproduction

Chronic stress

Immunocompetence

Developmental impact

Reproductive investment

Individual fitness

Population health amp stock development

1 2

4 5

7 8

9 10

11 12

113

6

Population consequences of acoustic disturbance model for fishes as applied to

airgun sound and cod (PCAD4Cod)

Box 1enspTransfer functions of the PCAD model for fishes (linked to Figure 2)1Behaviouralchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)2Physiologicalchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)3Interactionsbetweenbehaviouralresponsivenessandphysiologicalstate4Consequencesofbehaviouralchange(acuteandchronic)forvitalratesa ImpactonforagingefficiencyandopportunitiesbImpactonvulnerabilitytopredation(especiallyjuveniles)c EnergeticconsequencesofalteredswimmingpatternsdReproductiveconsequencesthroughmissedbreedingopportunities(adults)

5Consequencesofphysiologicalchange(acuteandchronic)forvitalratesa ImpactonchronicstressbeyondregulatoryfluctuationsbImpactonvulnerabilitytoinfectionsanddiseasecDevelopmentalconsequencesofphysiologicalimbalancedReproductiveconsequencesthroughfolliclematuration(adultsonly)

6Effectsonvitalratesofinteractionsbetweenbehaviouralandphysiologicalresponses7 Impactofbehaviouraleffectsongrowthratesurvivalandreproduction8Impactofphysiologicaleffectsongrowthratesurvivalandreproduction9 Impactofbehaviouralandphysiologicaleffectsonindividualfitness(lifetimereproductivesuccess)10enspConsequencesofchangesinindividualfitnessatthepopulationandstocklevel11enspEvaluationofdirectandindirecteffectsofseismicsurveysonfisheries12enspEvaluationofimpactfromseismicsurveysinthecontextof(sustainable)harvestingbyfisheries

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

AartsGMvonBenda-BeckmannAMvonLuckeKSertlekHOumlvanBemmelenRGeelhoedSCVhellipKirkwoodR (2016)Movement strategy of harbour porpoise affects the number ofanimals acoustically exposed to underwater explosions Marine Ecology Progress Series 557 261ndash275 httpsdoiorg103354meps11829

AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

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WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

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Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

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WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 5: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp5SLABBEKOORN Et AL

Themain productivity attributes of thePSA approachmaybeusefulinanyevaluationofdetrimentalimpactandconcernfactorsfor fish stocks The main attributes include maximum populationgrowth maximum individual size and age the ldquovon Bertalanffyrdquogrowthcoefficientforhowrapidlyafishreachesthismaximumsizeand theageatmaturitynaturalmortality and fecunditybreedingstrategy recruitmentpatternandmean trophic level (ahighscoreforpiscivoresintermediateforomnivoresandalowscoreforplank-tivores)Themainsusceptibilityattributesof thePSAapproach inthecontextoffisheriesconcerncatchabilityasdeterminedbygeo-graphicareaoverlapandverticaldistributionoverlapbetweenstockandfishingeffortsgeographicconcentrationseasonalmigrationsschooling aggregations and other behavioural and morphologicaltraitsinadditiontodesirabilityandmarketvalue(Patricketal20092010)Factorssuchastheeffectivenessofmanagementtocontrolcatch ratesand theeffectsof fishinggearonhabitatqualityhavealsobeenaddedto theseoriginalattributes inorder todeterminesusceptibilitytofisheries(Hobdayetal2007)

Additional susceptibility attributes that should be consideredif PSA were to be applied to seismic acoustic exposure includethegeographicandverticaldistributionoverlapofaparticularfishspecieswiththeacousticrangeofsoundsourcestodetermineex-posureprobability and level in termsof both soundpressure andparticlemotionAnyimpactofacousticexposureshouldbeconsid-eredontopofandinthecontextofseasonalvariationandspecificlifestagesizeandreproductiveconditionsandthefisheriesimpactifthetargetspeciesisalsoharvestedHoweverwebelievethatPSAcannotbeusedyetforevaluatingthepotentialvulnerabilityoffishstocks to anthropogenic noiseManyof the susceptibility scoringcategoriescurrentlyusedinPSAarenotparticularlyappropriateforassessingthepotentialeffectsofanthropogenicnoiseInadditionthe appropriateness of the essentially arbitraryway inwhich theindividual productivity and susceptibility scores are combined toprovideasinglemetricneedstobeevaluatedAnewsetofsuscep-tibilityscoringcategoriescouldbedevelopedforexampleusinganexpertelicitationprocess(SutherlandampBurgman2015)toidentifyfishspeciesandstocksthatarelikelytobeparticularlyvulnerabletotheeffects

23emsp|emspPopulation consequences of disturbance models

The population consequences of disturbance (PCoD) and popula-tion consequences of acoustic disturbance (PCAD) models (NRC2005Newetal2014)consistofaseriesoftransferfunctionsthatdescribehowexposure to stressors (such as anthropogenicnoise)affects individual behaviour how the resulting changes in behav-iourcanaffecthealth(definedasallinternalfactorsthataffectbodyconditionorhomoeostasis)andhowvariationsinhealthmayaffectvitalrates(survivalreproductionandgrowthageatfirstbreeding)Furthermorethetransferfunctionatthehighestleveloforganiza-tioninthemodeladdresseshowtheaccumulationofdataaboutthewayinwhichdifferentindividualsareexposedtoandaffectedbya

stressorcanbeusedtoscaleuptheanticipatedchangesinvitalratestopredictpopulation-leveleffects

PCADmodels have now been applied to a number of marinemammalspeciesforexamplenorthernandsouthernelephantseals(Mirounga angustirostris and M leoninaPhocidaeNewetal2014Costaetal2015)NorthAtlanticrightwhales (Eubalaena glacialisBalaenidae Schick Kraus etal 2013) beakedwhales (ZiphiidaeNew Moretti Hooker Costa amp Simmons 2013) harbour por-poise (Phocoena phocoena Phocoenidae Harwood King Schickamp Donovan 2014) and minke whale (Balaenoptera acutorostrataBalaenopteridaeChristiansenampLusseau2015)buttherearehardlyanyexamplessofarforfish(butseeSivleetal2014)

IdeallythepredictionsofPCADmodelsshouldbefittedtoap-propriatetimeseriesofempiricaldataobtainedoverarangeoflev-elsofdisturbanceTheresultsofsuchafittingprocesscanthenbeused to improve theparameter estimates andquantify theuncer-taintyassociatedwiththemodelpredictionsusingapproachessuchasBayesianhidden-processmodelling(NewmanBucklandLindleyThomasampFernandez 2006)However so far in no case has thisbeenpossibleandthereforeallmodelsappliedshouldstillbecon-sideredasldquoexploratoryrdquoExploratorymodelsareparticularlyusefulforcomparingthepossibleconsequencesofdifferentscenariosandforidentifyingpriorityareasforresearchHowever it is importantthat the uncertainties associatedwith their underlying parametervaluesaredocumentedandthattheeffectsoftheseuncertaintiesontheirpredictionsarequantified

Itisusefultoexploresomeofthedetailsofthemodelapplica-tionsinmarinemammalstoevaluatesomeoftheproblemsandsolu-tionsthatmayalsoapply insomewaytofishesNewetal (2014)forexampleusedthePCoDmodelstructuretoinvestigatethepo-tentialeffectsoflostforagingdivesonthehealth(measuredbytotallipidmassmdashseeSchickNewetal2013)ofadult femalesouthernelephant seals and the implications of variation in health for pupsurvivalandpopulationdynamicsTheyusedinformationobtainedfromdataloggersthatwereattachedtoanimalsimmediatelybeforetheyembarkedontheirpost-moultforagingtripsThedataloggersallowedareconstructionoftheirsurfacetransittimeandtheirforag-ingdivetimeDuringportionsofsomeforagingdiveselephantsealsdrift and the rateofverticalmovementduring thedrift is relatedtotheratiooflipidtoleanbodymassThedataloggerinformationwascalibratedagainstactuallipidgainduringtheforagingtripusingmeasurementsofbodycompositioncollectedbeforeandaftertheforagingtriptoenableestimationofdailylipidgain

FurthermoreNewetal (2014) linkedmaternalmassatbreed-ing to pupmass atweaning (Arnbom Fedak BoydampMcConnell1993)andpupmassatweaningtopupsurvival(McMahonBurtonampBester20002003)ThemodelwasthenusedtodeterminetheeffectofforagingdivedisturbanceonpupsurvivalItwasassumedthattherewerenoforagingdivesforthedurationofthedisturbanceandsurfacetransittimewassettotheobservedmaximumforthatindividual If animalswere disturbed for 50 of their time at seain1year thepredicteddecline inpopulationsizewassmall (lt1)However if thatdisturbancewouldcontinue indefinitely (eg asa

6emsp |emsp emspensp SLABBEKOORN Et AL

resultofvariationsintheextentoftheAntarcticicesheetcausedbyclimatechange)thepredictedeffectswouldbemuchgreater(a10declineinabundanceover30years)

TheanalysesinNewetal(2014)wereonlypossiblebecausede-tailedlongitudinaldatawereavailableonthemovementshealthandreproductivesuccessofalargenumberofadultfemalesealsSuchextensivedata sets requiredecadesof intensive research and areonly available for a fewmarinemammal populations ResearchershaveadoptedarangeoftechniquestobuildPCoDmodels insitu-ationswhereempiricaldataaremore limitedNabe-NielsenSiblyTougaardTeilmannandSveegaard(2014)usedanindividual-basedmodelofthemovementsofharbourporpoisestoestimatethepo-tentialeffectsofresponsestothesoundassociatedwithwindtur-bineoperationandshippingontheirenergyandreservesTheyuseda hypothetical relationship between energy reserves and survivalto calculate population-level consequences Villegas-AmtmannSchwarzSumichandCosta(2015)usedasimilarapproachtopre-dictthepotentialeffectsofreducedenergyintakeonreproductivesuccessandsurvivalforwesterngreywhales(Eschrichtius robustusEschrichtiidae)

Ifempiricaldataaresufficienttoestimatearelationbetweenbe-haviouralchangeandhealthbutnotbetweenhealthandvitalratesitmaybepossibletouseasurrogatemeasurefortherelevantvitalrate Christiansen and Lusseau (2015) used a bioenergetic modelandempiricalinformationonthebehaviouralresponseofadultfe-maleminkewhalestowhale-watchingboatsontheirsummerfeed-ing grounds in Iceland to estimate the effects of these responsesonthewhalesrsquohealth(asmeasuredbytheirblubbervolume)Theycalculated how different rates of encounter with whale-watchingboatswould affect an individualwhales health at the end of thesummerandthenusedanempiricallyderivedrelationbetweenfe-maleblubbervolumeandfoetallength(ChristiansenRasmussenampLusseau2014)asa surrogate for the relationshipbetweenhealthandtheprobabilityofgivingbirthAlthoughinteractionswithwhale-watchingboatsresultedina40reductioninfeedingactivitythepredictedeffectonafemalesbodyconditionoverthecourseofthesummerwasverysmall (0049reduction)becauseboatencoun-terswere actually rare This reduction in body conditionwas notpredictedtoaffectfoetalsurvivalHoweverevenifChristiansenandLusseau(2015)haddetectedasignificanteffectonfoetalsurvivaltheywould have been unable to forecast the population-level ef-fectsofexposuretowhale-watchingboatsbecausetheproportionoftheNorthAtlanticminkewhalepopulationthatfeedsinIcelandicwatersisnotknown

In situations where even surrogate measures are unavailableexpert elicitation (Runge Converse amp Lyons 2011 Sutherland ampBurgman2015)canbeusedtoparameterizesomeofthetransferfunctionsofthePCoDmodelExpertelicitationisaformalprocessinwhichanumberofexpertsonaparticulartopicareaskedtopre-dictwhatmay happen in a particular situation These predictionsare combined into calibrated quantitative statements with asso-ciated uncertainty which can be incorporated into mathematicalmodels(Martinetal2012)Kingetal(2015)usedthisapproachto

parameterize relationshipsbetween thenumberofdaysonwhichharbourporpoisesweredisturbedbynoiseassociatedwiththecon-structionofoffshorewindfarmsandtheirsurvivalandreproductivesuccessTheserelationshipswerethenusedtopredictthepotentialpopulationconsequencesofdifferentscenariosfortheconstructionofmultiplewindfarms

Thereare several studiesondifferentmarinemammal speciesthat have filled data gaps by asking experts Lusseau etal (2011)usedanexpertelicitationapproachtopredictthepotentialaggre-gate effect of noise associatedwithwind farm construction tourboat operation and harbour expansion on a bottlenose dolphin(Tursiops truncatusDelphinidae)populationThompsonetal(2013)usedittoassesspopulation-level impactsofdisturbancefrompiledrivingonharbourseals(Phoca vitulinaPhocidae)Spatialdistribu-tionpatternsandreceivednoiselevelswereintegratedwithdataonthepotentialfordisplacementandhearingdamageIngeneralun-certaintiesinecologicalmodelsarenotunusual(seeegClarketal2001HarwoodampStokes2003)andexpertelicitationisonewaytodealwiththemAcomplementaryapproachisecologicalriskassess-ment(ERA)possiblycombinedwithweightofevidence(WOE)(seeegHammaretal2014Hobdayetal2007Weed2005)

BasedontheexperienceandexamplesofPCADmodelsforma-rinemammalsaflowchart isdevelopedinFigure2whichappliesthe samemodel components transfer functions (Box1) and vitalratesinamodelforpopulationconsequencesofairgundisturbanceto fishesBeforeaddressing the literature inmoredetail the flowchartprovidesanoverviewofhowexposuretothesoundsofaseis-micsurveymaychangebehaviourinsuchawaythatitreducesin-dividualforagingefficiency(PurserampRadford2011ShafieiSabetNeoampSlabbekoorn2015)andincreasesvulnerabilitytopredation(Chanetal2010SimpsonPurserampRadford2015)Furthermoreswimmingmore or less efficientmay also detrimentally affect in-dividual energetics (Metcalfe etal 2016Villegas-Amtmannetal2015) while swimming less or in the wrong direction may resultin missed mating or spawning opportunities (Boussard 1981RossingtonBensonLepperampJones2013)Thesechanges inbe-haviourtogetherwithacuteorchronicstressphysiologicalchangesmayundermineindividualbodyconditionimmunocompetenceandphysiologicalinvestmentingrowthandreproduction(Barton2002Sierra-Flores Atack Migaud amp Davie 2015 Wendelaar-Bonga1997)The spectral and temporal structureof soundswill alsoaf-fect physiological stress levels as stronger responses have beenreportedtoboatnoiseandintermittentnoisethantomorehomog-enous white noise (Nichols Anderson amp Sirovic 2015WysockiDittamiampLadich2006respectively)

The translation from individual-level effects to the populationlevelinthePCADmodelforfishes(Figure2)isreflectedintheconse-quencesofthesebehaviouralandphysiologicalchangesforthevitalratesintermsofgrowthsurvivalandreproduction(cfCostaetal2015Harwoodetal2014Newetal2014)Thevitalratesdonotonlydetermineindividualfitnessimportanttounderstandselectionpressuresandevolutionarypotential(ChristiansenampLusseau2015HeinoPauliampDieckmann2015)butalsodeterminepopulationor

emspensp emsp | emsp7SLABBEKOORN Et AL

stockdevelopments(Hammaretal2014Newetal2014Patricketal2009)Directimpactsofseismicsurveyactivitiesonfisheriesare incorporatedthrough increasingor reducingcatchrateswhile

indirect impactsofseismicsurveyactivitiesonfisheriesarerepre-sented through potential impact on stock developments (McCullyPhillips Scottamp Ellis 2015 Patrick etal 2009) Behavioural and

F IGURE 2emspAflowchartofthepopulationconsequencesofacousticdisturbancemodeltailoredtofishes(asdevelopedinthecontextofairgunsoundandcodasamodelspecieshencetheacronymPCAD4Cod)DirectimpactonfisheriesindicatedinthetoprightisdeterminedbypositiveornegativechangesincatchrateduetofishmovementsduringandafteraseismicsurveyIndirectimpactonfisheriesunderneathisaffectedbybehavioural(green)andphysiological(pink)changesandtheirpotentiallynegativeeffectsforindividualfitnesspopulationhealthandstockdevelopmentTransferfunctionsthatrequirecriticalevaluationarenumbered1ndash12andareexplainedindetailinBox1Notethatindividualfitnessconcernslifetimereproductivesuccesswhichistheaccumulationofvitalratesattheindividuallevel(growthsurvivalandreproduction)Furthermorealthoughtransferfunctionsaredepictedunidirectionallythereversedpathwaycanalsoberelevantandimportantaspopulation-levelmetricssuchasabundanceandshiftsinpredator-preyorcompetitorrelationshipsmayfeedbackfrompopulationtoindividuallevel(iewarrantingbidirectionalarrows)

Airgun exposure

Behavioural change

Physiological change

Direct impact on fisheries

Indirect impact on fisheriesFeeding impact

Predation risk

Swimming energetics

Reproductive opportunities

Growth rate

survival

reproduction

Chronic stress

Immunocompetence

Developmental impact

Reproductive investment

Individual fitness

Population health amp stock development

1 2

4 5

7 8

9 10

11 12

113

6

Population consequences of acoustic disturbance model for fishes as applied to

airgun sound and cod (PCAD4Cod)

Box 1enspTransfer functions of the PCAD model for fishes (linked to Figure 2)1Behaviouralchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)2Physiologicalchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)3Interactionsbetweenbehaviouralresponsivenessandphysiologicalstate4Consequencesofbehaviouralchange(acuteandchronic)forvitalratesa ImpactonforagingefficiencyandopportunitiesbImpactonvulnerabilitytopredation(especiallyjuveniles)c EnergeticconsequencesofalteredswimmingpatternsdReproductiveconsequencesthroughmissedbreedingopportunities(adults)

5Consequencesofphysiologicalchange(acuteandchronic)forvitalratesa ImpactonchronicstressbeyondregulatoryfluctuationsbImpactonvulnerabilitytoinfectionsanddiseasecDevelopmentalconsequencesofphysiologicalimbalancedReproductiveconsequencesthroughfolliclematuration(adultsonly)

6Effectsonvitalratesofinteractionsbetweenbehaviouralandphysiologicalresponses7 Impactofbehaviouraleffectsongrowthratesurvivalandreproduction8Impactofphysiologicaleffectsongrowthratesurvivalandreproduction9 Impactofbehaviouralandphysiologicaleffectsonindividualfitness(lifetimereproductivesuccess)10enspConsequencesofchangesinindividualfitnessatthepopulationandstocklevel11enspEvaluationofdirectandindirecteffectsofseismicsurveysonfisheries12enspEvaluationofimpactfromseismicsurveysinthecontextof(sustainable)harvestingbyfisheries

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

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AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

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Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

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and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

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NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

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PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

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PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

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PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

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PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

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Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

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SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

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SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

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SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

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SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 6: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

6emsp |emsp emspensp SLABBEKOORN Et AL

resultofvariationsintheextentoftheAntarcticicesheetcausedbyclimatechange)thepredictedeffectswouldbemuchgreater(a10declineinabundanceover30years)

TheanalysesinNewetal(2014)wereonlypossiblebecausede-tailedlongitudinaldatawereavailableonthemovementshealthandreproductivesuccessofalargenumberofadultfemalesealsSuchextensivedata sets requiredecadesof intensive research and areonly available for a fewmarinemammal populations ResearchershaveadoptedarangeoftechniquestobuildPCoDmodels insitu-ationswhereempiricaldataaremore limitedNabe-NielsenSiblyTougaardTeilmannandSveegaard(2014)usedanindividual-basedmodelofthemovementsofharbourporpoisestoestimatethepo-tentialeffectsofresponsestothesoundassociatedwithwindtur-bineoperationandshippingontheirenergyandreservesTheyuseda hypothetical relationship between energy reserves and survivalto calculate population-level consequences Villegas-AmtmannSchwarzSumichandCosta(2015)usedasimilarapproachtopre-dictthepotentialeffectsofreducedenergyintakeonreproductivesuccessandsurvivalforwesterngreywhales(Eschrichtius robustusEschrichtiidae)

Ifempiricaldataaresufficienttoestimatearelationbetweenbe-haviouralchangeandhealthbutnotbetweenhealthandvitalratesitmaybepossibletouseasurrogatemeasurefortherelevantvitalrate Christiansen and Lusseau (2015) used a bioenergetic modelandempiricalinformationonthebehaviouralresponseofadultfe-maleminkewhalestowhale-watchingboatsontheirsummerfeed-ing grounds in Iceland to estimate the effects of these responsesonthewhalesrsquohealth(asmeasuredbytheirblubbervolume)Theycalculated how different rates of encounter with whale-watchingboatswould affect an individualwhales health at the end of thesummerandthenusedanempiricallyderivedrelationbetweenfe-maleblubbervolumeandfoetallength(ChristiansenRasmussenampLusseau2014)asa surrogate for the relationshipbetweenhealthandtheprobabilityofgivingbirthAlthoughinteractionswithwhale-watchingboatsresultedina40reductioninfeedingactivitythepredictedeffectonafemalesbodyconditionoverthecourseofthesummerwasverysmall (0049reduction)becauseboatencoun-terswere actually rare This reduction in body conditionwas notpredictedtoaffectfoetalsurvivalHoweverevenifChristiansenandLusseau(2015)haddetectedasignificanteffectonfoetalsurvivaltheywould have been unable to forecast the population-level ef-fectsofexposuretowhale-watchingboatsbecausetheproportionoftheNorthAtlanticminkewhalepopulationthatfeedsinIcelandicwatersisnotknown

In situations where even surrogate measures are unavailableexpert elicitation (Runge Converse amp Lyons 2011 Sutherland ampBurgman2015)canbeusedtoparameterizesomeofthetransferfunctionsofthePCoDmodelExpertelicitationisaformalprocessinwhichanumberofexpertsonaparticulartopicareaskedtopre-dictwhatmay happen in a particular situation These predictionsare combined into calibrated quantitative statements with asso-ciated uncertainty which can be incorporated into mathematicalmodels(Martinetal2012)Kingetal(2015)usedthisapproachto

parameterize relationshipsbetween thenumberofdaysonwhichharbourporpoisesweredisturbedbynoiseassociatedwiththecon-structionofoffshorewindfarmsandtheirsurvivalandreproductivesuccessTheserelationshipswerethenusedtopredictthepotentialpopulationconsequencesofdifferentscenariosfortheconstructionofmultiplewindfarms

Thereare several studiesondifferentmarinemammal speciesthat have filled data gaps by asking experts Lusseau etal (2011)usedanexpertelicitationapproachtopredictthepotentialaggre-gate effect of noise associatedwithwind farm construction tourboat operation and harbour expansion on a bottlenose dolphin(Tursiops truncatusDelphinidae)populationThompsonetal(2013)usedittoassesspopulation-level impactsofdisturbancefrompiledrivingonharbourseals(Phoca vitulinaPhocidae)Spatialdistribu-tionpatternsandreceivednoiselevelswereintegratedwithdataonthepotentialfordisplacementandhearingdamageIngeneralun-certaintiesinecologicalmodelsarenotunusual(seeegClarketal2001HarwoodampStokes2003)andexpertelicitationisonewaytodealwiththemAcomplementaryapproachisecologicalriskassess-ment(ERA)possiblycombinedwithweightofevidence(WOE)(seeegHammaretal2014Hobdayetal2007Weed2005)

BasedontheexperienceandexamplesofPCADmodelsforma-rinemammalsaflowchart isdevelopedinFigure2whichappliesthe samemodel components transfer functions (Box1) and vitalratesinamodelforpopulationconsequencesofairgundisturbanceto fishesBeforeaddressing the literature inmoredetail the flowchartprovidesanoverviewofhowexposuretothesoundsofaseis-micsurveymaychangebehaviourinsuchawaythatitreducesin-dividualforagingefficiency(PurserampRadford2011ShafieiSabetNeoampSlabbekoorn2015)andincreasesvulnerabilitytopredation(Chanetal2010SimpsonPurserampRadford2015)Furthermoreswimmingmore or less efficientmay also detrimentally affect in-dividual energetics (Metcalfe etal 2016Villegas-Amtmannetal2015) while swimming less or in the wrong direction may resultin missed mating or spawning opportunities (Boussard 1981RossingtonBensonLepperampJones2013)Thesechanges inbe-haviourtogetherwithacuteorchronicstressphysiologicalchangesmayundermineindividualbodyconditionimmunocompetenceandphysiologicalinvestmentingrowthandreproduction(Barton2002Sierra-Flores Atack Migaud amp Davie 2015 Wendelaar-Bonga1997)The spectral and temporal structureof soundswill alsoaf-fect physiological stress levels as stronger responses have beenreportedtoboatnoiseandintermittentnoisethantomorehomog-enous white noise (Nichols Anderson amp Sirovic 2015WysockiDittamiampLadich2006respectively)

The translation from individual-level effects to the populationlevelinthePCADmodelforfishes(Figure2)isreflectedintheconse-quencesofthesebehaviouralandphysiologicalchangesforthevitalratesintermsofgrowthsurvivalandreproduction(cfCostaetal2015Harwoodetal2014Newetal2014)Thevitalratesdonotonlydetermineindividualfitnessimportanttounderstandselectionpressuresandevolutionarypotential(ChristiansenampLusseau2015HeinoPauliampDieckmann2015)butalsodeterminepopulationor

emspensp emsp | emsp7SLABBEKOORN Et AL

stockdevelopments(Hammaretal2014Newetal2014Patricketal2009)Directimpactsofseismicsurveyactivitiesonfisheriesare incorporatedthrough increasingor reducingcatchrateswhile

indirect impactsofseismicsurveyactivitiesonfisheriesarerepre-sented through potential impact on stock developments (McCullyPhillips Scottamp Ellis 2015 Patrick etal 2009) Behavioural and

F IGURE 2emspAflowchartofthepopulationconsequencesofacousticdisturbancemodeltailoredtofishes(asdevelopedinthecontextofairgunsoundandcodasamodelspecieshencetheacronymPCAD4Cod)DirectimpactonfisheriesindicatedinthetoprightisdeterminedbypositiveornegativechangesincatchrateduetofishmovementsduringandafteraseismicsurveyIndirectimpactonfisheriesunderneathisaffectedbybehavioural(green)andphysiological(pink)changesandtheirpotentiallynegativeeffectsforindividualfitnesspopulationhealthandstockdevelopmentTransferfunctionsthatrequirecriticalevaluationarenumbered1ndash12andareexplainedindetailinBox1Notethatindividualfitnessconcernslifetimereproductivesuccesswhichistheaccumulationofvitalratesattheindividuallevel(growthsurvivalandreproduction)Furthermorealthoughtransferfunctionsaredepictedunidirectionallythereversedpathwaycanalsoberelevantandimportantaspopulation-levelmetricssuchasabundanceandshiftsinpredator-preyorcompetitorrelationshipsmayfeedbackfrompopulationtoindividuallevel(iewarrantingbidirectionalarrows)

Airgun exposure

Behavioural change

Physiological change

Direct impact on fisheries

Indirect impact on fisheriesFeeding impact

Predation risk

Swimming energetics

Reproductive opportunities

Growth rate

survival

reproduction

Chronic stress

Immunocompetence

Developmental impact

Reproductive investment

Individual fitness

Population health amp stock development

1 2

4 5

7 8

9 10

11 12

113

6

Population consequences of acoustic disturbance model for fishes as applied to

airgun sound and cod (PCAD4Cod)

Box 1enspTransfer functions of the PCAD model for fishes (linked to Figure 2)1Behaviouralchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)2Physiologicalchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)3Interactionsbetweenbehaviouralresponsivenessandphysiologicalstate4Consequencesofbehaviouralchange(acuteandchronic)forvitalratesa ImpactonforagingefficiencyandopportunitiesbImpactonvulnerabilitytopredation(especiallyjuveniles)c EnergeticconsequencesofalteredswimmingpatternsdReproductiveconsequencesthroughmissedbreedingopportunities(adults)

5Consequencesofphysiologicalchange(acuteandchronic)forvitalratesa ImpactonchronicstressbeyondregulatoryfluctuationsbImpactonvulnerabilitytoinfectionsanddiseasecDevelopmentalconsequencesofphysiologicalimbalancedReproductiveconsequencesthroughfolliclematuration(adultsonly)

6Effectsonvitalratesofinteractionsbetweenbehaviouralandphysiologicalresponses7 Impactofbehaviouraleffectsongrowthratesurvivalandreproduction8Impactofphysiologicaleffectsongrowthratesurvivalandreproduction9 Impactofbehaviouralandphysiologicaleffectsonindividualfitness(lifetimereproductivesuccess)10enspConsequencesofchangesinindividualfitnessatthepopulationandstocklevel11enspEvaluationofdirectandindirecteffectsofseismicsurveysonfisheries12enspEvaluationofimpactfromseismicsurveysinthecontextof(sustainable)harvestingbyfisheries

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

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AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

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AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

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Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

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OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

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PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

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inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

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32emsp |emsp emspensp SLABBEKOORN Et AL

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SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

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Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

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SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

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SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

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TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 7: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp7SLABBEKOORN Et AL

stockdevelopments(Hammaretal2014Newetal2014Patricketal2009)Directimpactsofseismicsurveyactivitiesonfisheriesare incorporatedthrough increasingor reducingcatchrateswhile

indirect impactsofseismicsurveyactivitiesonfisheriesarerepre-sented through potential impact on stock developments (McCullyPhillips Scottamp Ellis 2015 Patrick etal 2009) Behavioural and

F IGURE 2emspAflowchartofthepopulationconsequencesofacousticdisturbancemodeltailoredtofishes(asdevelopedinthecontextofairgunsoundandcodasamodelspecieshencetheacronymPCAD4Cod)DirectimpactonfisheriesindicatedinthetoprightisdeterminedbypositiveornegativechangesincatchrateduetofishmovementsduringandafteraseismicsurveyIndirectimpactonfisheriesunderneathisaffectedbybehavioural(green)andphysiological(pink)changesandtheirpotentiallynegativeeffectsforindividualfitnesspopulationhealthandstockdevelopmentTransferfunctionsthatrequirecriticalevaluationarenumbered1ndash12andareexplainedindetailinBox1Notethatindividualfitnessconcernslifetimereproductivesuccesswhichistheaccumulationofvitalratesattheindividuallevel(growthsurvivalandreproduction)Furthermorealthoughtransferfunctionsaredepictedunidirectionallythereversedpathwaycanalsoberelevantandimportantaspopulation-levelmetricssuchasabundanceandshiftsinpredator-preyorcompetitorrelationshipsmayfeedbackfrompopulationtoindividuallevel(iewarrantingbidirectionalarrows)

Airgun exposure

Behavioural change

Physiological change

Direct impact on fisheries

Indirect impact on fisheriesFeeding impact

Predation risk

Swimming energetics

Reproductive opportunities

Growth rate

survival

reproduction

Chronic stress

Immunocompetence

Developmental impact

Reproductive investment

Individual fitness

Population health amp stock development

1 2

4 5

7 8

9 10

11 12

113

6

Population consequences of acoustic disturbance model for fishes as applied to

airgun sound and cod (PCAD4Cod)

Box 1enspTransfer functions of the PCAD model for fishes (linked to Figure 2)1Behaviouralchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)2Physiologicalchangesfollowingexposuretorealairgunnoiseundernaturalconditions(larvaejuvenilesandadults)3Interactionsbetweenbehaviouralresponsivenessandphysiologicalstate4Consequencesofbehaviouralchange(acuteandchronic)forvitalratesa ImpactonforagingefficiencyandopportunitiesbImpactonvulnerabilitytopredation(especiallyjuveniles)c EnergeticconsequencesofalteredswimmingpatternsdReproductiveconsequencesthroughmissedbreedingopportunities(adults)

5Consequencesofphysiologicalchange(acuteandchronic)forvitalratesa ImpactonchronicstressbeyondregulatoryfluctuationsbImpactonvulnerabilitytoinfectionsanddiseasecDevelopmentalconsequencesofphysiologicalimbalancedReproductiveconsequencesthroughfolliclematuration(adultsonly)

6Effectsonvitalratesofinteractionsbetweenbehaviouralandphysiologicalresponses7 Impactofbehaviouraleffectsongrowthratesurvivalandreproduction8Impactofphysiologicaleffectsongrowthratesurvivalandreproduction9 Impactofbehaviouralandphysiologicaleffectsonindividualfitness(lifetimereproductivesuccess)10enspConsequencesofchangesinindividualfitnessatthepopulationandstocklevel11enspEvaluationofdirectandindirecteffectsofseismicsurveysonfisheries12enspEvaluationofimpactfromseismicsurveysinthecontextof(sustainable)harvestingbyfisheries

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

AartsGMvonBenda-BeckmannAMvonLuckeKSertlekHOumlvanBemmelenRGeelhoedSCVhellipKirkwoodR (2016)Movement strategy of harbour porpoise affects the number ofanimals acoustically exposed to underwater explosions Marine Ecology Progress Series 557 261ndash275 httpsdoiorg103354meps11829

AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

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TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

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Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

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WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 8: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

8emsp |emsp emspensp SLABBEKOORN Et AL

physiological stress responsesmay affect fisheries directly by ef-fects on catch rate (eg LoslashkkeborgOna Vold amp Salthaug 2012ParryampGason 2006 Skalski Pearson ampMalme 1992 StreeverRabornKimHawkinsampPopper2016)andthroughthesuggestedroute of stock impact The nature and intensity of fisheries itselfwill obviously also feed back to population health and stock de-velopment (Lillyetal2008Savenkoffetal2006) Itshouldalsoberealizedthatsizeandcompositionoffishstocksmayalsocausefeedbackeffectsagainstthedirectionofarrowsonthevital ratelevelofgrowthratesurvivalandreproduction(ClaessenDeRoosamp Persson 2000 Persson Leonardsson de Roos Gyllenberg ampChristensen1998)

3emsp |emspACOUSTIC E XPLOR ATION OF THE SE AFLOOR

31emsp|emspThe nature of seismic surveys

It is important to know the nature of seismic surveys (Dragoset2005Gisiner2016LandroslashampAmundsen2018LawsampHedgeland2008)tounderstandwhattheimpactonfishescouldbeWethere-fore review aspects of operational procedures mostly based onsurveystrategies intheNorthAtlantic (seeegParkesampHatton1986Evans1997andalsoMalmeSmithampMiles1986DalenampKnudsen1987Loslashkkeborg1991LoslashkkeborgampSoldal1993EngaringsLoslashkkeborgOnaampSoldal1996Loslashkkeborgetal2012)whichwillaffect exposure conditions through shooting rate and variation indistancebetweenfishesandsoundsource(Figure3a)Itisimportanttorealizethatthereareseveraldifferenttypesofseismicsurveyswhichvary in shootingdensity that is thereare two-dimensional(2D) and three-dimensional (3D) surveys bothwith towed hydro-phone streamers 3D surveys can also have hydrophones at theoceanfloorincludingso-calledfour-dimensional(4D)andmulticom-ponent(4C)surveysandsitesurveysThesetypedifferencesrelatetovariationinthewaysofoperationforexampledistancesbetweenvesselcourselineswithinthesurveyareaandtherebytimebetweenvisiting and revisiting locations in the survey area Theymay alsovaryinqualityrequirementswithrespecttotheseismicdatawhichmay lead to restrictions on acceptablewind and sea surface con-ditionsWhen theweather is too rough the seismic vessel oftenmovesslowlyatsteeragewaywithnoothersoundenergyemissionsthanfromthevesselitself

2Dsurveysareoftenusedinlargeregionalsurveysinearlyex-plorationphasesforoilandgas inanareaThevessel followssin-glecourse linesor lines inagridwhereneighbouring linesmayberelativelyfarapart(1kmandmore)andlinesmaycrosseachotherTypicallyasinglesoundsourceisusedcomposedofseveralairgunstoformanairgunarraytowedat4ndash10munderthewatersurfaceAirguns generate sound by releasing a bubble of compressed airgenerating a high-pressure spherical pulse that travels away fromthesourcewithacomplexinterferencepatternsduetosurfacere-flectionandbathymetry-dependentpropagationTheairgunarrayusually generates a soundpulse (ldquoshotrdquo) every10swhichyields a

shotevery25mwhenthevesselspeedisabout5knots(26ms)HoweverseismicpulseratemayalsovaryUsuallyonehydrophonecable of 3000ndash12000m length called a streamer is towed at6ndash8mdepth

3D surveys are carried outwithin parts of the previously 2D-surveyed area that the oil and seismic companies evaluate as in-teresting and ldquopromisingrdquo From the mid-1980s 3D surveys havebeen increasingly used by the oil industry because they providemuchmore information about the seabedandpotential hydrocar-bonreservoirsthan2Dsurveys3Dsurveystypicallyuseoneortwosoundsources (in so-called flip-flopoperation) eachcomposedofmanyairgunsina largeairgunarraytowed250ndash400mbehindthe

F IGURE 3emsp (a)Artisticimpressionofaseismicsurveypresentedwiththeverticaldirectivitypatternoftheenergysourcespectraldensitylevel(dBre1μPa2 m2sHz)fortheairgunarrayatdifferentazimuthangles(courtesyŐzkanSertlek)Wedevelopedanalgorithmforthecalculationofairgunsignatures(AGORA)basedonvariousbranchesofphysicssuchasbubblemotiongaspressurelawsthermodynamicsandmasstransfer(SertlekampAinslie2015)whichisnowfreelyavailablefromLeidenUniversityathttpoalibhlsresearchcom(b)Schematicrepresentationofa3DsurveyvesselcoursepatternEachlinerepresentsavesselsail-lineThearrowsindicatevesseldirectionandpathwaystartinginbluechangingtoredandgrey-bluewithtimeinsubsequenttrackingcourses(courtesyJCaldwellOYOGeospaceandCWalkerSeabedGeosolutions)

(a)

(b)

(a)

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

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BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

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Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

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ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

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CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

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DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

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DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

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Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

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FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

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Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

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Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

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FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

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FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

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GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

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SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

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SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

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Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

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SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

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SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 9: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp9SLABBEKOORN Et AL

vesselatabout6mdepth(similarto2Dsurveys)Incontrasttothe2Dsurveythereareseveralhydrophonecables(6ndash16)withaninter-cabledistanceof25ndash150mThedistancebetweenthecourselinescoveringthe3Dseismicareamayvarybetween50and200mTheweatherrequirementsarestricterfor3Dthanfor2DsurveystheBeaufortwindforcemustbeequaltoorlt5correspondingtowindspeedsupto21knots(11ms)andthesignificantwaveheightmustbeequaltoorlt20m

Theairgunpulseratedoesnotneedtodifferbetween2Dor3DsurveysbutbesidespulserateitisalsorelevanttorealizethattheseismicsurveyoftenstopsWhenthevesselhasfinishedonesail-line thegenerationofseismicpulses typicallystopsupto2ndash4hrwhilethevesselturnstostartonthenextsail-lineFigure3bshowshowa3DsurveytypicallymaybeperformedThevesseltakesonelinethenturnswithallthestreamersondragintothenextselectedlineandsailsbackintotheoppositedirectionThemorestreamersthe larger the radiusof the turnwillhave tobeMorecablesalsomeansthattheshiphastorunfewercourselinestocoverthesameareaHoweveralthoughthismayreduceemissiontimeatthevesselduringmany3Dsurveysthefishwithinthesurveyareamayheartheemittedsoundduringthewholeactiveperiodofsurveywhiletheyarelikelytoexperienceperiodsofrelativesilenceduring2Dsurveysthatcoverlargerareas

4D surveys are used for reservoir monitoring and they areequivalenttorepeated3Dsurveysovertimethatisthe4thdimen-sion is time Ithasseveralnamesaspermanent reservoirmonitor-ing (PRM) life-of-field surveys (LoFS) or time-lapse surveys (TLS)(CaldwellKoudelkaNesteroffPriceampZhang2015Walker2014)Thetimeintervalbetweensurveysmaybevariableanddependsonthespecificsofthereservoirbeingmonitored4Dsurveysarepre-ciserepetitionsof3Dsurveysasdescribedaboveintermsofcourselines source capacity and hydrophone streamersOne alternativeoperationstrategycanbethatthehydrophonecablesarenottowedclosetothesurfacebutplacedatthebottomForthelattercasethesurveyisnamedoceanbottomseismic(4DOBS)oroceanbot-tomcableseismic(4DOBC)Cablesareeitherplacedatthebottompriortothesurveysandbroughtupagainafterthesurveysorburiedattheseabedpriortothefirst4DOBCsurveyuntiltheexploitationendoftheoilgasfield

Avariantofthe4DOBCwiththesameshootingprocedurebutdifferentsensortypes isthemulticomponentOBCwhichiscalled4COBCInthiscasethebottommountedcablesorsensorswithoutconnectingcablescontainseveralorthogonallyorientedgeophones(orequivalentparticlemotionsensors)inadditiontopressurehydro-phonesyieldingthepossibilityofmeasuringacousticshearwavesaswellaspressurewaves(Caldwelletal1999)Thistechniqueallowsdeterminationofboththetypeofwaveanditsdirectionofpropaga-tionThedistancesbetweencourselinesof4Dand4Csurveysarerathersmallandthetimebetweenvisitingandrevisitingaparticularpositionisrathershort(1hrtoafewhours)dependingonthesizeoftheseismicareaConsequentlyduringthe4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

Finally so-calledwell sitesurveysarea thorough investigationoftheseabedandsub-seabedfeatureswithsufficientpenetrationandresolutiontogatherdatathatareessentialfortheemplacementor anchoringof structuresdedicated tohydrocarbonexploitationThedataacquisitionmainlyaimsatimprovingtheinformationqual-ityofthebathy-morphologicalseabedfeaturesoftheupperlayersofthebottomforexampleprovidinghigherresolutiondatathantheseismicdata acquired for explorationpurposes This is usually formappingstratigraphyofshallowformationsandtodetectpotentialgaspocketsinshallowlayerstopreventblowoutsorotherdanger-ous events during drilling These activities are performedprior todecidingonwheretoplaceariginthedesiredpositionfortestdrill-ing and they are an integral part of theHealth Environment andSafety(HES)proceduresTheacquiredinformationshallensuresafeanchoringandhandlingoftherig

For thewell site surveys typically 1ndash4 small airguns on oneortwoairgunstringstowedat2ndash3mdepthandsparkers(seismicsoundsourcesbasedonhighvoltagedischarge)areusedwithasin-glehydrophonecableofusually600ndash1200m longFurthermoregeotechnicalsedimentsamplesmaybegatheredbymeansofpis-tonndashgravityorvibrocoresystemsinordertodeterminemechanicalcharacteristics of the seabed The topographical mapping of theseaflooristypicallydonewithamultibeamechosounderside-scansonar and sub-bottom profiler (the latter in case of very shallowsubsurface layers) while a single-beam echosounder is used fornavigationpurposesThe surveyareas are always relatively small(15ndash25km2or4ndash7nmi2)Thereareevenfurtherrestrictionsforasitesurveythanforthe3DsurveysThewindforcemustbeequalto or less thanBeaufort force 3 (up to 10 knots 5ms) and thesignificantwave heightmust be equal to or less than 02m Thedistances between vessel course lines are small for site surveysand the time of line-change is short (half an hour to a couple ofhours)dependingonthesizeandwaterdepthoftheseismicareaConsequentlysimilarlytothe3D4Dand4Csurveysthefishareagainlikelytobeexposedtoairgunsoundduringtheactiveperiodsofthewholesurvey

32emsp|emspAirgun array size and seasonality

Thesizeoftheairgunarrayisanothercriticalparameterforthepo-tential impactofseismicsurveysonfishesAlthoughvesselmove-mentpreventspeaksoundlevelsatthesamespotforlongperiodsthe contribution of seismic surveys to the overall ambient noiselevelsaveragedovertimecanbeconsiderablecomparedtoothersound sources (see Figure4a) The acoustic energy output froman airgun array is determined by the number of airguns and theirchambervolumesthesupplypressuretotheairgunsandtheairgunconfiguration within the arrays (Anonymous 2006 2014ab)Wepresentaselectionoftechnicalandoperationalfeaturesofdifferenttypesof seismic surveys inTable1For thegeometricdimensionsof airgunarrayswehave seena reductionof the size (length (in-line)bywidth(cross-line))ofthearraysfor2Dand3Dsurveysfromthebeginningofthe1980suntiltodayTypicallydimensionranges

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

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AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

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AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

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Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

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SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

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SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

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SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

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SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

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Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

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Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

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Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 10: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

10emsp |emsp emspensp SLABBEKOORN Et AL

todayare15ndash30m(in-line)by15ndash20m(cross-line)Meanvaluesandvariationsofthelengthandwidthofmostusedairgunarraysduring2010ndash2015are15(plusmn1)mby19(plusmn2)mfor2D3Dand4Dset-ups(Gisiner2016LandroslashampAmundsen2018)

Asimplebutreasonablypreciseindirectmeasureforthegener-atedsoundpressurepisthetotalchambervolumeVcoftheairgunarray(s)asaproxyfortheemittedenergyasthemajorityoftheair-gunset-upsworkwiththesamesupplypressureThisisbasedonthefactthatthere isacorrelationbetweenchambervolumeandgen-eratedsoundpressure(althoughchamberandopeningdesignalsoaffectpressurelevel)intheacousticfarfield(ISO2017)Forasingleairgunthepeaksoundpressurep0-pk~Vc

033 (VaageHauglandampUtheim1983)andforanairgunarraythepressurep0-pk~Vc

0385 (Malmeetal1986)When theairgunsareconfigured inanarraythe arraywill act as an acoustic transducerwith its vibrating sur-faceamplifyingtheverticallydown-goingwavefield inthecentralvolumebeneaththearraythusproducingadirectionalsoundfield(Caldwell ampDragoset 2000 Khodabandeloo Landroslash ampHanssen2017ParkesHattonampHaugland1984Tashmukhambetov IoupIoup SidorovskaiaampNewcomb2008)Theacoustic energy fromairgunsismorebiasedtolowerfrequenciesthanforotheranthro-pogenicsoundsourcessuchasvesselsandexplosivesandalsocon-trastingwiththewiderandhigherfrequencyrangecoveredbywind

The totalnumberofdays reported fora surveyof any type isoftennotequaltothenumberofdaysinwhichthereisactualseis-mic sound pulse emission The reason for this is that part of theoverallsurveyperiodalmostalwaysconcernsoperationaldowntimedue to bad weather conditions or technical problems Especiallylargeweatherimpactisreportedforsitesurveysasthesesurveysare very sensitive to wind and rough sea surface conditions Forinstance a survey that requires5daysof seismic data acquisitionmaytake1ndash2monthsAmoreprecisemeasureoftheeffectivetimeofseismicpulseexposureforasurveyisthereforethevesselkilo-metres duringwhich there is seismic survey activity Estimates ofeffectivesurveydurationindays(asinTable1)canbecalculatedbyassumingarealisticaveragevesselspeedof5knots(26ms)

As the quality requirements for the airgun recording data arefairlystrongseismicsurveysaretypicallyrestrictedtoseasonalpe-riodswithbeneficialwindandseasurfaceconditions(andseasonalwindowsof legalpermission)Theweatherconditionsmayforex-ample be rather rough in theNorthAtlantic and adjacentwatersduring lateautumnandwinterwhich results in rather lowactivityforseismicdataacquisitionduringthisperiodThisleavestheperiodfrommid-Apriltomid-Octobertobethehighseasonforseismicsur-veysinthesewatersWhilerelativelycalmseasmaystillallowsomeactivitiesinthewintermonthsuntilDecemberintheNorthSea(see

F IGURE 4emsp (a)Contributionofseismicsurveys(solidblueline)tothetotalacousticenergy(2yearaverage)intheDutchpartoftheNorthSea(DEEZ)indecidecadebandsrelativetotwootheranthropogenicnoisesources(shippingandexplosions)andnaturalwindnoise(Sertlek2016Sertleketal2019)Shippingismakingthelargestcontributionupto10kHzWindisaprominentcontributorabove5kHzSeismicsurveysareprominentatthelowfrequencies(between01and10kHz)The125-HzbandisexplicitlymentionedintheMarineStrategyFrameworkDirectiveoftheEuropeanlegislation(b)Seismicvesselactivitiesduring2012ndash2015expressedbytotalvesselkilometresintheNorwegianpartoftheNorthSeaMostsurveystakeplacefromApriluntilOctoberwithpeakactivitiesinJuneandJuly(courtesyTheNorwegianPetroleumDirectorateJStenloslashkk)

0

10000

20000

30000

40000

50000

Jan Feb March April May June July Aug Sep Oct Nov Dec

Seismic vessel activities in the North Sea 2012-2015

Vess

el k

ilom

etre

s

Month

(a)

(b)

Comparison of total acousc energyfor various sound sources

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

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AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

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AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

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Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

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Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

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SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

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SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

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Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

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StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 11: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp11SLABBEKOORN Et AL

Figure4b)otherroughseasfurthernorthmayremainlargelyunex-ploredbyseismicsurveysbetweenOctoberandMarchTheseason-alityofsurveyscanalsobeimportantrelativetofishecologyastheymay be differently sensitive and vulnerable to acoustic stressorsovertheyearDisturbanceanddeterrencepatternsmayforexam-ple vary amongperiodsofpre-spawningmigration pre-mating atthespawningfieldsandduringspawning (Carrolletal2017Coxetal2018Hawkinsetal2015Pengetal2015)

4emsp |emspTHE AUDITORY WORLD OF FISHES

41emsp|emspFundamentals of fish hearing

There are more than 30000 fish species which have evolvedsubstantial variation in the physical structures associated withhearing (Figure5a) However all fishes detect particle motion(PM)andshareanaccelerometer-likesystemforhearing(Ladich2014PopperampFay2011RadfordMontgomeryCaigerampHiggs2012)PMisdetectedbythreepairsofotolithorganswhichcon-sistofamass(theotolithitself)andthesensoryhaircellsThehaircellsactastransducersconvertingthemechanicalstimulusofPMintoanelectricalsignalthatcanbeprocessedbythecentralnerv-oussystemFishandthesensoryepitheliahaveapproximatelythesame density aswater andmove in conjunctionwith the soundfieldatlowfrequencyThecalcareousotolithisapproximately3ndash4

timesdenserandmoveswithadifferentialamplitudeandphasetothatofthefishbodyAsaconsequencethehaircellsthatareincontactwiththeotolithundergoashearingdisplacementwhichtheyldquotranslaterdquointotheneurologicalresponsesthatfeedauditoryperception

Manyfishspeciescanalsodetectsoundpressure(SP)inadditiontotheirmotionsensitivityviathegas-filledswimbladder(ahydro-staticorgan)orothergasbubble(Fay1969SandampEnger1973)Theswimbladdercanbeconnectedtothe intestinebythepneumaticduct (physostome fishes eg salmon)or canbeclosed (physoclistspeciesegcod) Inphysostomefishes thequantityofgas in theswimbladdercanberegulatedviagulpsofairatthesurfacewhileinphysoclistfishesthisgoesviagasabsorptionorreleasefromtheblood The lattermay bemore susceptible to damage at extremeacousticexposuresbutbothdetectsoundpressurethroughvolumeoscillationswhicharetransferredtotheinnerearThisisoftenfacil-itatedbyaphysicalconnectionforexamplethroughpairedbladderextensionsadditionalaircavitiesoraseriesofbones(Weberianos-sicles)(reviewedinPopperampFay2011)

Thelaterallinesystemcanalsodetectsoundbutthisistypicallynotlabelledashearing(BleckmannampZelick2009BraunCoombsampFay2002HiggsampRadford2013)Theunderlyingmechanismofsensitivityhoweverissimilarbetweenthelaterallineandtheinnereartheyarebothbasedonsensitivitytoparticlemotionviatrigger-ingofhaircells(Cofinetal2014PopperampFay2011)Anindirect

TABLE 1emspTechnicalandoperationalcharacteristicsofdifferenttypesofseismicsurveysduring2005ndash2014Weindicatedtherangebyprovidingtheminimumandmaximumforthetotalchambervolume(incubicinches1cubicinchequals00164L)andthelengthofhydrophonecablesandmeanaswellasrangeforthesurveyareasizeanddurationDescriptionsofseismicsurveytypescanbefoundinthetext3DPDSreferstoldquo3DProprietaryDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareproprietarytothelicenseecompanyand3DADSreferstoldquo3DAvailableDataSurveysrdquowhichare3Dsurveysofwhichtheseismicdataareavailabletoothercompanies(sharingaproductionlicenceofanoilgasfieldoravailabletootheroilindustryactorsforacertaincost)NAnotapplicableDataaremainlybasedonsurveysintheNorwegianExclusiveEconomicZone(NEEZtheNorthSeatheNorwegianSeatheBarentsSea)andtheBritishExclusiveEconomicZone(theNorthSea)

Survey typeNumber of airguns in arrays

Total chamber volume in litres (cubic inches)

Number of cables and length range [m]

Survey area size [km2]mdashmean and range

Survey duration [days]mdashmean and range

2Dsurveys

18ndash48 213(1300)1003(6300)

13000ndash12000

NA NA

3Dsurveys

3DPDS 12ndash48 328(2000)866(5280)

6ndash162400ndash10000

480132ndash681

4911ndash105

3DADS 12ndash38 328(2000)677(4130)

6ndash142400ndash6000

1238436ndash2355

15758ndash326

4DOBSsurveys

12ndash38 328(2000)834(5085)

6ndash122400ndash5000

22947ndash438

4718ndash124

4D4COBCsurveys

12ndash38 328(2000)654(3990)

Cablesatburiedintotheseabed

22947ndash438

4718ndash124

Sitesurveys

1ndash4 07(40)34(210)

1ndash2600ndash1200

22 NA

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

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BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

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Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

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ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

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CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

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DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

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DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

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Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

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FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

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Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

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Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

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FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

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FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

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GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

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Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

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Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

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SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 12: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

12emsp |emsp emspensp SLABBEKOORN Et AL

contributionofsoundpressurevia theswimbladder isalsopossi-bleThemostlikelyfunctionofthesensitivityofthelaterallinesys-temisfine-tuningresponsestostimuliatclosedistanceasitmostlyprovidessensitivitytomotioninthewaterflowdirectlyaroundthefish body As this nearbywater flow is affected by swimming ac-tivitycurrentandflowdisturbancebyother fishorobjects in the

watersensorymonitoringviathelaterallinesystemislikelyplayingacriticalroleinschoolingrheotaxisanddetectionofbothpredatorsandprey (Dijkgraaf1962SchwalbeBassettampWebb2012) It isunclear towhat extent interference ormasking by low-frequencysoundcouldunderminethesensoryfunctionofthelaterallinenoris it clear towhat extent the lateral lineplays a role in sensitivity

F IGURE 5emsp (a)SchematicoverviewofthecapabilityoffishtoperceivesoundsintermsofrelativeamplitudeandspectrumThethreethinlinesreflectthefollowingthreeauditorypathways(1)thegeneralsensitivityofallfishestoparticlemotionthroughinnervationofhaircellsclosetotheotolithsoftheinnerear(indarkblue)(2)thesensitivitytoparticlemotionoriginatingfromsoundpressurethroughpressure-to-motiontransductionforfishspecieswithaswimbladder(ingreen)whichtypicallyresultsinaloweroverallthresholdandanextensionofsensitivitytowardshigherfrequencies(greenarrows)and(3)thesensitivitytoparticlemotionviathelateralline(inlilac)Thisconcernsrelativelylowfrequenciesintheflowofwaterdirectlysurroundingthefish(throughmovementsofthefishitselfwaterflowcurrentsorturbulencebyotherfishorobjects)andwhichisnotlikelytooutcompetetheinnerearinsensitivityTheboldbluelinerepresentsthecumulativeshapeoftheaudiogramthesensitivitytosoundacrossfrequenciesattributabletoavariableandunquantifiedcombinationofsensitivitythroughthethreepathways(b)Hearingthresholdsofthreedifferentspeciesforindependentassessmentsofsoundpressurelevel(left)andsoundparticleaccelerationlevel(right)Thecommontriplefin(Forsterygion lapillumTripterygiidae)hasnoswimbladder(blacklines)TheNewZealandbigeye(Pempheris adspersusPempheridae)hasaswimbladderbutnoWeberianossicles(greenlines)Thegoldfish(Carassius auratusCyprinidae)hasaswimbladderandspecializedconductiontotheinnerearviaWeberianossicles(redlines)Intermsofparticlemotionallthreefishspecieshavesimilarhearingthresholdsbutwhenexpressedaspressurethresholdsthegoldfishisthemostsensitivefollowedbythebigeyeandthetriplefinbeingtheleastsensitive(Radfordetal2012)

Inner earLateral line

Frequency

Rela

tive

ampl

itude

Swim bladder

Frequency (Hz)

100 200 400 600 800

Hea

ring

thre

shol

d (d

B re

1 m

sndash2

)

ndash70

ndash60

ndash50

ndash40

ndash30

ndash20

ndash10

0

100 200 400 600 80070

80

90

100

110

120

130

140

150

Frequency (Hz)

Hea

ring

thre

shol

d (d

B re

1 u

Pa)

(a)

(b)

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

AartsGMvonBenda-BeckmannAMvonLuckeKSertlekHOumlvanBemmelenRGeelhoedSCVhellipKirkwoodR (2016)Movement strategy of harbour porpoise affects the number ofanimals acoustically exposed to underwater explosions Marine Ecology Progress Series 557 261ndash275 httpsdoiorg103354meps11829

AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 13: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp13SLABBEKOORN Et AL

todisturbancebyorcopingwithanthropogenicnoise(Braunetal2002HiggsampRadford2013)

Fishhearingdependsonbothhowintensethesoundisanditsfre-quencyandistypicallydepictedinspecies-specifichearingcurvesoraudiogramshearingthresholdsacrossfrequencies(KenyonLadichampYan1998LadichampFay2013)Withintheaudiblerangefishex-hibit auditory capabilities that gobeyondmeredetection suchasdiscriminationabilityamongsoundsofdifferentfrequencyandam-plitude(auditoryscenesegregation)oramongsoundsfromdiffer-entdirections (directionalhearingazimuthdetection)ordistances(ranging) Furthermore fish also exhibit relevant perceptual phe-nomenasuchashabituationandsensitization(NeoHubertBolleWinterampSlabbekoorn2018RadfordLefegravebreLecaillonNedelecampSimpson2016Rankinetal2009)whichmayplayacriticalrolein impact assessment (Bejder SamuelsWhitehead Finn ampAllen2009Hardingetal2018)andwhichapplyacrossmarinetaxa(egGoumltzampJanik2011SamsonMooneyGusseklooampHanlon2014)Howeverwestillknowverylittleabouttheseparateorintegratedrolesofsoundpressureandparticlemotionsensitivityintheseper-ceptualabilitiesoffishandmoststudieshavejustfocusedonhear-ingthresholdsandfrequencyranges

There are two different approaches to obtaining hearingthresholds behaviouralmethods and electrophysiologicalmeth-ods(LadichampFay2013)Behaviouralmethodsprovokeanactiveresponseofthefishtoasoundaftersomeformofconditioning(ei-therrewardorshockavoidance)Oncearesponsehasbeenestab-lishedthesoundlevelisthenprogressivelylowereduntilthefishnolongerrespondsThismethodprovidesthebestevidencethatafishisnotonlyabletohearbutalsoabletoprocessandrespondtothespecifictypeandintensitylevelofsoundElectrophysiologicalmethods register auditory evoked potentials (AEP) or auditorybrainstem responses (ABR) (Kenyon etal 1998) To apply themethodthefishistypicallymildlyanaesthetizedandheldinatankeitherat thesurfaceormid-waterandcutaneouselectrodesareplacedabove thebrainstem to recordelectrical signals from theauditory system Thresholds are determined through decreasingthe sound leveluntil theexperimenter canno longerdetect theAEPorABRsignal(LadichampFay2013)Howeververyfewstud-iesprovideadequateinsightsforunderstandingfishhearingundernaturalcircumstancesandarethereforelimitedforevaluatingpo-tential effects of sound exposure from anthropogenic sourcesBehavioural studies in captivity and electrophysiological mea-suresarebothusefulfordeterminingcrudespectralrange limitsanddamageafterexposuretoloudsounds(egHalvorsenCasperWoodleyCarlsonampPopper2012Popperetal2005)Theyaremuchlessusefulfordeterminingabsolutehearingsensitivityandoneshouldbeespeciallycautiousincomparingaudiogramsofdif-ferentspeciesgeneratedbydifferentlaboratories

Thereareveryfewstudiesthatprovideinsightintobothsen-sitivitytoPMandSP(Figure5b)ItisdifficulttopresentPMandSP signals independently andusually requires specializedequip-mentsuchasshakertablesordiametricallyopposedspeakersys-temsForexamplethecodhasbeenshowntodetectPMsignals

atfrequenciesbelow100HzbutdetectSPathigherfrequencies(ChapmanampHawkins1973SandampHawkins1973)Theyarealsoreportedtobesensitivetoinfrasound(soundatfrequenciesbelowthelowerlimitofthehumanhearingrangeat20Hz)throughlinearaccelerations(SandampKarlsen19862000)andithasbeensug-gestedthatthisparticularcomponentofthesoundfieldmaytrig-gertheavoidanceresponsetoanthropogenicsounds(SandEngerKarlsenKnudsenampKvernstuen2000)Forthelargemajorityofliteratureonlysoundpressurelevels(expressedindBre1μPa2)arepresentedwhileallfisharealsoprominentlysensitivetopar-ticleaccelerationlevel(dBre1(μms2)2)

Furthermore the majority of studies have been performedin small tanks in noisy laboratories where the sound fields arehighly complex as a result of pressure-release surfaces (Hawkinsetal2015Parvulescu19641967)Thelow-frequencycut-offat30ndash100Hz shown inmany audiograms often represents the low-frequency limitationsoftheequipmentormayreflectbackgroundnoise that is masking the test stimuli Consequently audiogramsprovideabasicmeansforcomparingthesensitivityandfrequencyrangeofdifferentfishesbuttheabsolutethresholdsshouldgener-allybe consideredunreliable For example reviewsbyLadich andFay (2013)andMaruskaandSisneros (2016)pointoutdifferencesof40ndash60dB in reportedhearing thresholds for the same specieslargely attributed to differences in measurement methodologyratherthanhearingabilityHarmonizationinmeasurementmethod-ologyisessentialifprogressistobemadetowardsimprovedquan-titativeunderstandingofcomparativehearingsensitivityinfishes

42emsp|emspSound fields hearing and potential for impact

Onlyanaudiblesoundcantriggerabehaviouralorphysiologicalre-sponseandhavepotentiallydetrimentalimpactAnauditorydosendashresponsecurvetoabroadbandsoundcouldbeusedtoassessthenumberoffisheshearinghumanactivitiesHoweverthereisacon-siderablegapinourunderstandingofthenaturalvariationinsoundpressureandparticlemotioninthesoundfieldaroundthefishjustbefore and during the seismic survey The following informationwouldberequiredforaplausibleestimate(a)densityanddistribu-tionoffishes(geographicallyandwithinthewatercolumn)(b)levelandspectralenergydistributionofthesoundsourceinsoundpres-sure and particle motion (c) propagation conditions between thesoundsourceandthefishforbothsoundcomponents(d)ambientnoiselevelsatthefishforbothsoundcomponentsand(e)auditorysensitivityacrossthespectrumofpotentiallyexposedfishes

AnimportantsourceofconfusionintheimplicationofauditorysensitivityisthehearingcurveoraudiogramThiscurvereflectsthethresholds for single-frequency tone pulses across the spectrumabovewhichsoundisperceivedbytheearHoweverthethresholdateachfrequencyisdeterminedbydetectionofeithertheparticlemotionorsoundpressurecomponentofthesoundoracombinationof bothAnother reason forwhy the current insights intohearingabilitiesoffishesarelimitedforapplicationstoimpactassessmentsis thatmostnatural (conspecificpredator-preyhabitatsignatures)

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

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AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

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AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

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BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

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Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

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Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

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Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

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OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

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emspensp emsp | emsp31SLABBEKOORN Et AL

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inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

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mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

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Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

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SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

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SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

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TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

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Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

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Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

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Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 14: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

14emsp |emsp emspensp SLABBEKOORN Et AL

andanthropogenicsounds (transientor long-lasting) includingair-gunsoundsarebroadbandThismeansthathearingthresholdsandmaskingwilldependontheaccumulationofenergyoverfrequency-dependent filter bandwidths Critical bandwidths are known forhardlyanyspeciesbutcod theyhavesymmetrical filter functionsthat increase with frequency (eg 59Hz at 40Hz and 165Hz at380Hz) (Hawkins amp Chapman 1975) Actual field data with be-haviouralresponsetendenciesforfree-rangingfishcombinedwithadequateassessmentsofthesoundfieldarerequiredtogetanyfur-therintermsofimpactassessments

Asmentionedaboveacousticexposureprobabilityandextentdepend not only on auditory capacities of the fish but also onsound source properties the distance between the fish and thesource and the propagation through thewater Acoustic propa-gation in theoceandependson the localenvironment includingphysicaloceanography(temperatureandsalinity)bathymetryseasurfaceroughnessbubblesandsedimentfeatures(BrekhovskikhLysanovampLysanov2003JensenKupermanPorterampSchmidt2011) Significant advancements have been made in the past20years in computational ocean acoustics (eg Harrison 2013Khodabandelooetal2017Sertlek2016)Fivemainbranchesofnumericalmodels are routinely applied to compute the acousticfield in ocean acoustics parabolic equation (PE)models (Collins1993TappertampNghiem-Phu1985)ray-basedmodels(WeinburgampBurridge1974)wavenumberintegrationtheorymodels(DiNapoliampDeavenport1980Schmidt1987)modetheory-basedmodels(Porter1995)andfluxmodels(Weston1959)Hybridmodelsarealsousedapplyingcombinationsoftheabove(egHarrison2015Hovem Tronstad Karlsen amp Loslashkkeborg 2012 Sertlek 2016SertlekSlabbekoorntenCateampAinslie2019)

Amajority of effort in ocean acoustics has been focusedonacoustic pressure (driven by the desire to quantify the perfor-manceofman-made sonar systems) andnot onparticlemotionParticlemotion the kinetic components of sound can be char-acterized in terms of sound particle displacement sound parti-clevelocitysoundparticleaccelerationoranyhigherderivativeOnce the velocity field is known in the frequency domain it isstraightforwardtoconverttodisplacementoraccelerationGivena reasonable understanding of bathymetry sediment type andlocal oceanography the numerical computation of the acousticfield(soundpressureandsoundparticlevelocity)isasolvedprob-lem for apoint sourceComputation in the frequencydomain iseffectedusing

whereS(f)isthesourcespectrum(ISO2017)andH(f)isthetrans-ferfunction(Greensfunction)(Jensenetal2011)ThePEmethodhasbeenappliedtothewaveequationforvelocitypotential(Smith2010)butthisisnotnecessaryiftheacousticpressurefieldisavail-ableonthecomputationalgridInthiscasetheparticlemotioncanbecomputedusingtherangeanddepthdiscretizedfinitedifferencederivative to compute the particle acceleration vector from thesoundpressurefield(inthefarfield)

Thepredictionof the soundpressure or particle velocity fieldassociatedwithaseismicsurveytransmissionisacomplexprobleminvolvinganunderstandingofacousticpropagationsourcephysicsand local oceanography Approaches to date have applied simpli-fiedmodelstoeachpartoftheproblemandusedtheminseriestopredict the acoustic field The parameters that describe the envi-ronmentareoftensuppliedfromlocalorworlddatabasesofocean-ography(Baranova2010)bathymetry(AmanteampEakins2009)andsedimenttype

Sourcemodelsexistforsingleairgunsandforarraysofairgunswhich typicallyprovide thesourcewaveform (timedomainsourcesignatures(t)(ISO2017))andsourcespectrum(frequencydomainsource signature S(f)) (ISO 2017) Acoustic propagation modelsarewelldeveloped(Jensenetal2011)andcanbeusedtohandlebroadband signals in arbitrary range-dependent environments Topredictthereceivedsoundfieldamodel isrunatasubsetoffre-quenciesandthecoherenttransferfunctionH(f)calculatedateachfrequencyThesoundpressureinthetimedomainp(t)istheinverseFouriertransformofthefrequencydomainquantityP(f)

Theuseofacousticcues formakingdecisionsoften requiresthe fishnotonly todetect a soundbut also tobe able to local-ize the sound source (Schuijf 1975 Schuijf amp Hawkins 1983)Perceptuallocalizationmechanismsforfishremainpoorlyknownlargelybecauseof thedifficulty in resolving the180degambiguityassociatedwiththedominantaxisofparticlemotionwhichpointstowardsandawayfromasoundsource(RogersampZeddies2009)Althoughseveralmodelshavebeenproposedtoaddressthisissue(Kalmijn1997RogersPopperHastingsampSaidel1988SchellartampMunck1987SchuijfampBuwalda1975)itisstillnotcompletelyclear how fish localize sound Nevertheless there is good be-havioural evidence that they can Zeddies etal (2012) studiedthe plainfinmidshipman (Porichthys notatus Batrachoididae) andshowed that female fish directed their swimming towards maleadvertisementcallsUsingadipolesourceinaconcretetanktheyshowedthatwhenfemaleswerereleasedalongthedipolevibra-toryaxistheytookstraightpathstothesoundsourcewhilewhenreleasedapproximately90degtothevibratoryaxistheytookmuchmore curvedpaths insteadThis indicates that the fish localizedthesoundsourcebyfollowingthedirectionofprominentaxesofPMinthelocalsoundfield(Zeddiesetal2012)Afollow-upex-perimentshowedthatsoundpressuredetectionislikelytoaidinthelocalizationtaskandthatthelaterallineisprobablynotcon-tributingsignificantly(Cofinetal2014)

Followingfromtheaboveafullunderstandingofpotential im-pactofanthropogenicnoisepollutionlikeincaseofaseismicsur-veywillrequiremoreinsightintotheambientsoundpressurelevelsin combinationwith the local directionality of theparticlemotionsoundfieldFurthermoreweneedtoknowwhetherwhenandhowtheacousticinformationisextractedbyfishesfordecision-making

(1)P(f)=S(f) sdotH(f)

p(t)=int+∾

minus∾

P(f) exp (+2ift) df

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

AartsGMvonBenda-BeckmannAMvonLuckeKSertlekHOumlvanBemmelenRGeelhoedSCVhellipKirkwoodR (2016)Movement strategy of harbour porpoise affects the number ofanimals acoustically exposed to underwater explosions Marine Ecology Progress Series 557 261ndash275 httpsdoiorg103354meps11829

AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

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Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

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Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 15: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp15SLABBEKOORN Et AL

andwhetherwhenandhowthisisnegativelyaffectedbythepres-ence of anthropogenic noise The nature of anthropogenic soundfeatures such as rise time reverberative temporal patterns andspectralcompositionandfluctuationarelikelycriticalandneedfur-ther investigation from a fish perspectiveModification by soundpropagationthroughthewaterhastobetakenintoaccountaswellaspropagation through theseabed includingshearwavesAt lowfrequencyinshallowwatersomeoftheenergyfromanairgunpulsemightpropagatealong thewaterndashseabedboundary in the formofso-calledScholtewaveswhichcouldincreasetheriskofdisturbancetobenthicfaunabutverylittleisknown

Fillingthegapsofknowledgeaddressedaboveisrequiredforabetterunderstandingofpotentialdisturbanceandmaskinginfishesbutwilllikelyalsorevealpotentialforperceptualresistanceforex-ampledue tosignal redundancyor thepossibility thatmorenoisyconditionsmakesurroundingsbetteraudiblethroughldquoacousticillu-minationrdquoAbetterunderstandingofthenaturalandhuman-alteredacoustic world would also allow future studies on the inherentlymultimodalnatureof theperceptualworldofanimals (HalfwerkampSlabbekoorn2015MunozampBlumstein2012VanderSluijsetal2011) Studies on perception and pollution taking a combinationof sound light chemical or temperature conditions into accountto study responsiveness (eg Heuschele Mannerla Gienapp ampCandolin 2009 Kunc Lyons Sigwart McLaughlin amp Houghton2014ShafieiSabetvanDoorenampSlabbekoorn2016)orexposuretoacombinationsofstressorsofdifferentmodalityarecriticalforaproperunderstandingofacousticecologyandnoisepollution inthe realworld (Carroll etal2017Hawkinsetal2015Nowaceketal2015)

5emsp |emspOVERVIE W OF AIRGUN IMPAC T STUDIES

51emsp|emspHistorical perspective and methodological considerations

Studiesonimpactfromairgunexposureonfishesstartedinthebe-ginningofthe1970safterthedevelopmentandtestinginthelate1960softhefirstcommercialairgunassemblybyBoltAssociatesIncUSAThefirsttwostudieswereoncagedcohosalmonsmolts(Oncorhynchus kisutch Salmonidae Weinhold amp Weaver 1972)and eggs and larvae of a variety of fish species (Kostyuchenko1973)whilethethirdonewasonfree-swimmingherring(Dalen1973)Most follow-upstudieshavebeenonconfinedandcagedfish and only some studies focused on behavioural impact onfree-swimming fish (Bruce etal 2018 Carroll etal 2017 Coxetal2018)Sometimesconsequencesofalteredfishbehaviourfor different typesof fisherieswere targetof the investigations(egDalenampKnudsen1987Skalski etal 1992Streeveretal2016)

Although the variety in methodology and approaches hasyielded considerable insight most fish studies were either lim-itedinbiologicalrelevanceorsufferedfromlimitedreplicationor

lacking controls (which should also be replicated)Note thatwedonot argue that all studieswith limited replicationor controlsare useless or wrong we just call for caution in evaluating thestateof theart andwrongoftenonlyapplies to the interpreta-tionofsuchstudiesbeingtoobroadorconclusiveBeyondfishesthere are several reports typically alsoof anecdotal nature andinvestigating a single seismic survey event in variousotherma-rine taxa (Andreacute et al 2011 Andriguetto-FilhoOstrensky PieSilva amp Boeger 2005DayMcCauley FitzgibbonHartmannampSemmens2017Gordonetal2003GuerraGonzaacutelezampRocha2004McCauley etal 2017 Parry ampGason 2006 Przeslawskietal2018)withcurrentlythemostadvancedexperimentalstud-iesonmarinemammals in theirnaturalenvironment (Catoetal2013Dunlopetal2016)

Despite methodological challenges it has become clear thatairgun sounds can potentially affect fishes in multiple ways (re-views eg in Dalen amp Knudsen 1987 Hirst amp Rodhouse 2000Handegard Tronstad amp Hovem 2013) At close range extremeover-exposure may induce physical injury potentially leading todeath (egMcCauleyFewtrellampPopper2003) for thevery fewnearbyindividuals(Popperetal2005)Beyondthiscloserangebutwithintheaudiblerangetheremaybebehaviouralandphysiologicaleffectsthataremoresubtlebutthatapplytomanymore individ-ualfish (generalreviews inSlabbekoornetal2010Normandeau2012Radfordetal2014Popperetal2014Hawkinsetal2015)Consequentlytheeffectsthatmayoccurbeyondtherangeofphys-icaldamagebutwithintheaudiblerangearethemainfocusofthefollowingreviewofbehaviouralandphysiologicalresponses

52emsp|emspBehavioural response to airgun exposure

There are few good case-studies in the peer-reviewed literaturethatreportontheimpactofaseismicsurveyonthebehaviouralre-sponse of free-ranging fish or the direct impact on local fisheries(Bruceetal2018Engaringsetal1996Hasseletal2004Loslashkkeborgetal 2012 Skalski etal 1992 Streever etal 2016) There arealsostudiesthatjustfocusedonthefishbehaviourofmoreorlessresident (egJorgensenampGyselman2009MillerampCripps2013Wardle etal 2001) and exclusively pelagic fish populations (egPentildeaHandegardampOna2013SlotteKansenDalenampOna2004)Thesestudiesdonotyieldcompletelycoherentresultsbutsuggestthat fishesexposed toairgun soundcould stop foragingand startswimmingdownthewatercolumnTheimpactoncatchratescanbepositiveornegativedependingonthetypeoffisheriescatchratescangoupforgillnetswhichdependonswimmingactivityorcangodownforlonglineswhichdependonactiveforaging

However these studies provide little insight into the fish per-spective(beyondtheseismicsurvey-relatedchangesinprobabilitytobecaught immediatelybyfisheries)Severalstudiesontemporalortropicalreefsystems(BoegerPieOstrenskyampCardoso2006MillerampCripps2013Wardleetal2001)haveshownthatairgunsoundburstscancausestartleresponsesinrelativelystationaryfishwhiletheyalsosuggest thatstartlesdonotnecessarily lead to long-term

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

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BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

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Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

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ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

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ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

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ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

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CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

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26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

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De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

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DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

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Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

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DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

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Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

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Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

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Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

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GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

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Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

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Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

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Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

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HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

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Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

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SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

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UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

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VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

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Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 16: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

16emsp |emsp emspensp SLABBEKOORN Et AL

changesinbehaviouralpatternsorspatialdeterrenceHoweverthisisratherprematureasageneralconclusionandweneedmorewell-designedstudies(cfSlabbekoornampBouton2008)fortheimpactas-sessmentonnatural patterns that can alreadybequite variablebythemselvesArecenttemperatereefstudybyPaxtonetal(2017)stilllimitedinreplicationanddurationoftheobservationsandnottakingothernearbyvesseltrafficintoaccountindicatedthatquitesubstan-tialspatialeffectsarealsopossibleMultispeciespresenceshoweda78declineduringeveningswithseismicsoundexposurecomparedtothesametimeperiodonthreepreviousobservationdays

Bruceetal(2018)conductedalargetelemetrystudyonthreefishspeciesinthewesternGippslandBasinbetweenthecoastofSouthernAustraliaandTasmaniabeforea2DseismicsurveywasundertakeninApril2015TheMVDukevesseltowedasingle41-L(2530-cubicinch)airgunarray(BOLTLongLifeArray)with16airgunstowedat6plusmn1mdepthfora10-daysurveyperiodThisstudyisfirstofallanillustrationofhowchallengingitistoobservefree-rangingfishinopenwateratseaForthetwoelasmobranchspecies76individualsweretaggedandreleasedattheanticipatedtreatmentsiteanda10-km-awaycontrolsitebutnoneoftheseyieldedapresenceinthetargetareasduringthesurveyThethirdspecieswithtelemetricdatawasaray-finnedte-leostandconcerned11tiger flatheads (Neoplatycephalus richardsoniPlatycephalidae) which were all released at the treatment site (sowithoutspatialcontrol)Nineindividuals(81)werereportedbythereceiversbeyond the first2daysafter taggingofwhicheightweredetectedinthetargetareaduringtheseismicsurvey

ThelargetaggingeffortofBruceetal(2018)endedupwithuse-fuldataoneighttigerflatheadfishwhichdonotallowstatisticsbutdotell somethingaboutdisplacementandmovementpatternsbe-foreduringandafteraseismicsurvey(eachindividualbeingitsowntemporal control) Fourof theeight informative fishwerepresentduringtheentiresurveyperiodandfourlefttheareaduringthesur-veyOftheselatterfourindividualsonehadbeenpresenton5dayspriorand6daysintothesurveyperiodandanotherhadbeenpres-ent4dayspriorand4daysintothesurveyTheothertwofishthatleftduringtheseismicsurveyarrivedonthefirstdayofthesurveytostayfor5daysorarrivedontheseconddaytoleaveagainbeforethenextdayThesefourwerenotrecordedtoreturninthefollow-ing4monthsofcontinuedmonitoringTheanalysesofdisplacementandmovementrevealedthatthetimeofdayatwhichthefishweremostactivevariedbeforeduringandafterthesurveyThereweregenerally twopeaks in activity over the daywhich turnedout tobe laterduring theseismic survey thanbefore theseismic surveyThefishalsomovedmorefrequentlyafterthanbeforeorduringthesurveyperiodandhadahigheraverage speedduring thanbeforeorafterThelatterwasattributedtopossibledisturbanceeffectsinstartleresponsesoreventsoferraticswimming

Thestudyon the tiger flatheads (Bruceetal2018)concernsasinglesurveyeventatonelocationatonemomentintimebutiscon-sistentwithapossibleresponsetotheseismicsurveyoperationsTheresponseisnotoneoflargespatialdisplacement(fourevenremain-ing inthetargetareaforthefullseismicsurveyperiod)butoneofmoderatechangesinlocalactivityasevidentfromvariationindiurnal

patternsandswimmingspeedSuchchangesinactivitypatternscouldhave detrimental energetic consequences due to increased invest-ment inmovement or decreased opportunity to feed andwarrantfurtherquantificationPhysiologicalstresswasnotinvestigatedbutanypotentialimpactcannotbeexcludedInadditiontothetelemetricdataon three fish species fisheries catchdataon15 specieswereextracted fromadatabaseof theAustralianFisheriesManagementAuthorityfortwogeartypes(Danishseineandgillnets)Avariableandinconsistentpatternofincreasedanddecreasedcatchratesperspeciescameoutofthisanalysis(Bruceetal2018)

Weareawareofonlyasinglestudythatfollowedindividualfree-rangingfishinthecontextofexperimentalairgunexposurecombin-ingvideowithanindividualtaggingeffort(Wardleetal2001)Thestudywasconductedaroundanunderwaterreef(ldquofishrockrdquo)offthecoastofwesternScotland(lt20mdepth)in1997Theyconducted8sessionsduringwhichtheygenerated8ndash74shots(oneperminute)onfiveconsecutivedaysVideoimagesrevealedtypicalc-startstartlere-sponses(stereotypicreflexinwhichthewholefishbodyiscurvedintoac-shapefollowedbyrapidacceleration)atthesoundburstwithoutany obvious directionality and rapid recovery of pre-exposure be-haviouralpatternsNosound-inducedchangesinfishabundanceandswimmingpatternswereobservedtotherepeatedseriesofsingleair-gunshotsTwooutoffivetaggedfishyieldedsomeinterestingdata

Oneindividualpollack(Pollachius pollachiusGadidae)showedniceandconsistentdiurnaltravelsfor10daysbeforethearrivalofthere-searchvesselbetweenthereefandaspotabout250mtothenorth-eastuptothedaythattheresearchvesselarrivedattheeastsideoftherockandthefishswamtothewestsideofittostaythererelativelyinactiveforthedurationoftheexposureSothisindividualrevealedasuddenshiftinbehaviourbutbeforethefirstairgunexposureThecoincidencewiththearrivaloftheresearchvesselmayindicatethatthe fish associated thatmoderate soundwith the previous experi-encewiththevesselontheeventofbeingcaughtAsecondindividualshowedabitmorevariableswimmingpatternandstayedclosertotherockbeforeduringandafterthe5dayswitheightairgunexposuresOnlyduringoneoftheexposuresmovementpathtracingrevealedaclear increaseinswimmingspeedandatrackfromtheexposureontheeastsidetotheshelteredsideonthewestOtherclearbehaviouralswitchesforthisindividualcouldberelatedtothearrivalofagreyseal(Halichoerus grypusPhocidae)andthepresenceofanactiveboat

Together these data provide anecdotal results (Wardle etal2001)indicatingthattaggingcanworkbutthatindividualscanvarysignificantlyintheirbehaviourFurthermoretheyalsoclearlyshowthatthereareotherfactorsthantheairgunexposureduringsuchanexperimentwhichcanleadtoconfoundedresults(taggingimpactpresenceofvesselcoincidencewitharrivalofpredator)Anycon-clusive statements awaitnewexperimental studieswith adequatereplicationandcontrols

53emsp|emspAirgun exposure studies with caged fish

The studies on airgun responses from free-ranging fish reviewedabove were suitable to obtain a general qualitative idea of what

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

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BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

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Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

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ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

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Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

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ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

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CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

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26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

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De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

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DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

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Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

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DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

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Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

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Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

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GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

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Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

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Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

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HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

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Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

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Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

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SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

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TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

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the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 17: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp17SLABBEKOORN Et AL

naturalresponsebehavioursmaylooklikeandtoanalysedirectim-pacton fisheriesbutnot for theassessmentofspecific thresholdvalues or understanding underlying mechanisms Alternative re-search strategies have resulted in complementary insights Thereare forexample somestudies thathaveaimedatobtainingsomesortofbehaviouralthresholdlevelforacousticexposuretoairguntocagedfishinoutsideconditions(FewtrellampMcCauley2012Hasseletal2004PearsonSkalskiampMalme1992)Thesestudiesprovideinsightintotheoccurrenceandnatureofbehaviouralresponsesal-thoughfishbehaviourmaybeaffectedbytheenclosureandbytheanimalsrsquorecentexperienceofbeingcaughtorbytheirbackgroundin aquaculture These studies do not yield sufficient quantitativedatayetforanydosendashresponsecurvebutsuggestatleastthatseis-mic surveys typically do not lead to immediatemortality but caninducebehaviouralchanges(iestartleanderraticflightresponsesdivingdownspeedingupandformingtightschoolswhichmayallvarywithspecies)andatextremelevelscanleadtohearingdamage(McCauleyetal20002003)

Sadlythisisallthatcanbeconcludedfromtheseoftenexpen-siveexperimentswithethicallydifficultexposureconditionsforthe

fishThestudiesreportonbehaviouralthresholdsforresponsestoairgunexposureinvolvingsoundpressurelevel (SPL)between130and180dBre1μPa2(seeBox2)butallsufferdramaticallyfromlackofreplication(typicallyn = 1ndash3)lackofadequatecontrols(noneorconfounded)anduseofvariablemixturesoffishspeciesofvariablebackground (variable refershere to trialvariabilitywithinstudies)Futurestudiesshouldaimatexperimentaldesignswithproperpe-riodsofobservationbeforeduringandaftertheseismicexposure(seeSmith2002Underwood1991SmokorowskiampRandall2017)withtreatmentandcontrolsitesinnearbyecologicallysimilarsites(controlbeyondacousticandbehaviouralimpactofthetreatment)Togainthemostrobustinsightsitisrequiredtoobtainreplicationofpairsoftreatmentndashcontrolsitesoverarangeofecologicallydiversehabitatsandwithdiversespeciescommunities

As full-scale seismic surveys are quite expensive and labour-intensivealternativemethodshavebeenusedtostudyexperimen-tallyhowbehaviouralresponsetendenciesdependonsoundlevelsandacoustic features (Figure6)HawkinsRobertsandCheesman(2014) used for example an approachwith underwater playbackofimpulsivesoundssimulatingthestrikesfromapiledriver(which

Box 2enspSound terminology

Basic concepts and physical quantitiesTheeffectsofseismicsurveysconsideredarethoseofunderwatersoundEffectivecommunicationaboutunderwatersoundrequiresaclearandconciselanguageofunderwateracousticsUnlikeforairborneacousticstheterminologyofwhichhasbeenstandardizedfordecadesunderwateracousticalterminologyisinitsinfancyWhenreportingsoundpressureandparticlemotionitisofprimeimpor-tancetouseclearandconsistentmetricsInordertominimizeconfusioncausedbypoorlydefinedterminologythroughoutthispaperwefollowISO184052017UnderwaterAcousticsmdashTerminology(ISO2017)ISO(2017)definesvariousquantitiesthatareusedtoquantifythesoundpressurefieldincludingmean-squaresoundpressure(p2)time-integratedsquaredsoundpressure(alsoknownassoundpres-sureexposureEpT)andzero-to-peaksoundpressure(p0ndashpk)Alsodefinedaremean-squaresoundparticlevelocity(u2)time-integratedsquared sound pressure (also known as sound particle velocity exposure EuT) and corresponding statistics of the sound particleacceleration

Levels in decibelsAlevelisalogarithmicmeasureofapowerquantityP(egsoundexposureormean-squaresoundpressure)andinacousticsisusuallyexpressedindecibels(Ainslie2015)SpecificallythelevelofapowerquantityPindecibelsistentimesthebase10logarithmofPP0whereP0isthereferencevalueofPForexamplesoundpressurelevel(abbreviatedSPL)isthelevelofthemean-squaresoundpressure(symbolLprms)soundpressureexposurelevel(abbreviatedSELorSELp)isthelevelofthetime-integratedsquaredsoundpressure(LEp)andzero-to-peaksoundpressurelevel(Lp0ndashpk)isthelevelofthezero-to-peaksoundpressureCounterpartsofthefirsttwolevelsfortheparticlevelocityfieldarethemean-squaresoundparticlevelocitylevel(Lurms)andtime-integratedsquaredsoundparticlevelocitylevel(or sound particle velocity exposure level (abbreviated SELu) symbol LEu) and corresponding levels are defined for sound particleacceleration

Reference valuesLevelsindecibelsaremeaninglessunlessaccompaniedbythecorrespondingreferencevalueInternationalstandardreferencevaluesofsoundpressuresoundparticlevelocityandsoundparticleaccelerationare1μPa1nmsand1μms2respectivelyThesereferencevaluesmaybesquaredtoreflectthedefinitionoflevelasapropertyofapowerquantity(egthereferencevaluesofmean-squaresoundpressuremean-squaresoundparticlevelocityandmean-squaresoundparticleaccelerationallproportionaltosoundpowerare1μPa21(nms)2and1(μms2)2andthereferencevaluesofthecorrespondingtime-integratedquantities(exposures)are1μPa2s1(nms)2sand1(μms2)2s)

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

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and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

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NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

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PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

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SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 18: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

18emsp |emsp emspensp SLABBEKOORN Et AL

typically occur at a higher rate than airgun sound bursts eg 30strikesinsteadof6perminute)inalough(lake)atthesouth-easterncoast of Ireland The behaviour of pelagic fish in response to thesound playback was observed with an echosounder and replica-tionwasachievedbyrepeatedtrialsaimingpresumablyatdifferentschools of relatively small sprat (Sprattus sprattus Clupeidae) andlargermackerel (Scomber scombrus Scombridae)bychanging loca-tionsatthesurfaceoftheloughfordifferentruns(butallwithinafewhundredmetres)

Responsepatternswereshowntobedependentonsoundlevelbutalsovariedqualitativelyforthedifferentspecies(Hawkinsetal2014)Spratschoolsreactedto50ofthepresentationsatsoundpressureexposurelevel(SELp)ofLEpss=135dBre1μPa

2sandweremore likely to spread laterally while mackerel schools reacted atLEpss=142dBre1μPa

2sbutweremorelikelytogodownthewatercolumn(LEpisthesymbolforSELpandthesubscriptldquossrdquoisanabbre-viationforldquosinglestrikerdquo(pulse))Theechosounderwasalsoabletotraceathirdtrophiclevelofzooplanktonwhichrevealedexposure-relateddownwardmovementsThisisaddingcredibilitytothestudybyMcCauley etal (2017) reporting zooplankton mortality up to1200mfromanairgunarrayHowever inferringacausalrelation-shipfromasingleobservationisatbestprematureespeciallywith-out amechanistic explanation for a possible ldquodeathby soundrdquo forcreaturesofplanktonsizeNeverthelessthestudybyHawkinsetal(2014)showedthateachofthethreetrophicgroupsmayresponddirectlytothesoundor indirectlybyrespondingtomovementsoftheothergroupImportantlythisstudyshowedthatpulsedacousticexposurecanhaveeffectsthatgobeyondasinglespeciesandmaycause changes in foodweb interactions (Francis Ortega amp Cruz2009Hubertetal2018SlabbekoornampHalfwerk2009)

Another approach that has been taken to assess behaviouralresponse tendencies concerns playback of anthropogenic soundsto fishes incaptivityThomsenetal (2012) forexampleexposedamixtureoffishspecies inafloatingpentoplaybackof impulsive

sounds (recordings of pile-driving strikes) and reported thresholdsoundlevelsatwhichfishmoved(eg140ndash161dBre1μPa2zero-to-peaksoundpressure level forcod) InanotherstudyKasteleinJenningsKommerenHelder-HoekandSchop(2017)usedasinglepile-driving recording to assess response tendencies of hatchery-raised seabass Dicentrarchus labrax Moronidae to intermittentsoundpulsesGroupsof four fish ina175times4m (2mdeep)basinwere scored for behavioural response thresholds (defined in thisstudyas2ormoreofthe4individualsshowingastartleorsuddenswimmingburstresponse)Twoindependenttestseries(with8and9groupsoffourfishrespectively)showedresponsethresholdsatLEpss=131dBand141dBre1μPa

2sandLEuss=67and77dBre1(nms)2srespectively(LEuisthesymbolforsoundparticlevelocityexposurelevel(SELu))Thedifferencebetweenthetwotestseriescould be due to size-dependent response tendencies variation intestorweatherconditionsbetween2yearsorvariationincaptivehistoryandacousticexperienceTheshort-termswimmingresponse(up to few seconds) was not reflected in longer-term changes ingroupcohesionwhichwasonlyinoneofthetwotestseriessignifi-cantlyaffectedbysoundlevel

Itisstressedthatstudiesincaptivityonaspecificmixtureoraselectedsubsetoffishraisedinahatcheryareoflimitedornovaluefor predicting absolute response levels forwild fishes respondingin free-rangingconditions (Slabbekoorn2016)Thiskindof studywithproperreplicationismostsuitabletogainfundamentalinsightinto response triggering potential of stimulus variation and expo-sure conditions Behavioural observations in floating pens havefor example confirmed that vessel noise shouldbe taken into ac-countwhen investigating impact of airgun exposure (De Robertisamp Handegard 2013 Doksaeligter Handegard Godoslash Kvadsheim ampNordlund 2012)Neo etal (2014 2015 2016 2018) determinedthe impactof temporalvariation in soundexposurewith replicatesetsof16groupsof4seabassandreportedconsistent (inabasinand floating pen set-up) relatively long-term (~10ndash30min) sound-inducedbehaviouralresponsessuchasdivingdownthewatercol-umnandincreasedgroupcohesionSomeimportantinsightsgainedwerethatintermittentsoundmayleadtolowersoundexposurelev-els(SEL)thancontinuoussoundbutstillcanyieldlonger-lastingbe-haviouraleffects(Neoetal2014)thatamplitudefluctuationsandpulserateintervalmayhavesubtleeffectsonthekindandintensityofaresponse(Neoetal20142015)andthatramp-upproceduresdonotnecessarilyleadtomitigationtargets(Neoetal2016)InthemostrecentstudyinthisseriesNeoetal(2018)reportedstrongerresponsivenessatnightthanduringdaytimeandhabituationinfad-ingresponsepatternsovereightrepeatedexposuresduring2days

54emsp|emspPhysiological stress responses to loud sounds

Physiological changes may or may not occur in parallel with thebehaviouralchangesbutaretypically investigatedseparatelyThestressresponseinfishcanbedividedintoaprimarysecondaryandtertiaryresponse(SapolskyRomeroampMunck2000Schreck1990)Theprimaryresponseconcernsthedetectionoftheenvironmental

F IGURE 6emspExampleofhowexposuretoanacousticstressor(ofparticularSoundPressureLevel)canaffectthetendencytomodifybaselinebehaviour(BehaviouralResponse)inatypicaldosendashresponsecurve(basedonkillerwhale(Orcinus orcaDelphinidae)datafromabehaviouralresponsestudyintoacousticexposurewithnavalsonar(Milleretal2014alsoseeHarrisetal2018))

60 80 100 120 140 160 180 200

Sound Pressure Level

Beha

viou

ral r

espo

nse

10

08

06

04

02

00

Mean50th percentile95th percentile99th percentile

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

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Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

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AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

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Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

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SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

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SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

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SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

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SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

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Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

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Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 19: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp19SLABBEKOORN Et AL

stressorbythecentralnervoussystemandtheassociatedneuroen-docrineresponseThesecondaryresponseisaconsequenceoftheprimaryandconcernsalterationofmetabolicpathwaysThetertiaryresponseconcernschangesinwhole-bodyactivityandperformanceTheprimaryresponseisapreconditionforapotentiallydetrimentaleffectbutisalsojustapartofthenaturalfluctuationsinahealthyfishtoregulatedailyactivitiesThesecondaryandtertiaryresponsesmayimplychronicstressandcanbedetrimentaltogrowthsurvivalandreproductivesuccessImportantlyindividualfishmaynotonlyshowvariationinbehaviouralresponsetoenvironmentalstressorsbutalsovaryconsiderablyandconsistentlyinphysiologicalresponsepatternsassociatedwithindividualcopingstyleswhichmayplayacriticalroleinthetranslationofanystressintofitnessconsequences(ConradWeinersmith Brodin Saltz amp Sih 2011 Koolhaas etal1999Oslashverlietal2007MacKenzieetal2009)

Cortisolconcentrationsincirculatingbloodplasmaareregardedasavaluableindicatorofacutestressaspartoftheprimaryresponseaswellaschronicstressofthesecondaryresponsethataffectsthe

energyregulationinthebodyandmayunderminedigestiveandre-productiveactivityimmunocompetenceandgeneralhomoeostasisofthebody(Barton2002Wendelaar-Bonga1997)Severalrecentstudies(Midwoodetal2014OConnoretal20102011)havealsoaddressed the tertiary response directly using exogenous cortisolimplants(whichisnotacompletebutelegantexperimentalmimicofthestressor-inducedactivationofthehypothalamicndashpituitaryndashinter-renalaxis)Theelevatedcortisollevels(for3ndash5days)weretypicallyassociatedwithanexpectedincreaseinmetabolicrateandoverallactivitybutalsocausedgrowthratedepressionandearlierwintermortality(comparedtocontrolsandsham-treatedfish)Populationmodelsconfirmthatsuchconsequencesfortheindividualofsingleshort-termstressorscantranslatetodetrimentaleffectsatthepop-ulationlevel(Edelineetal2009OConnoretal2011)

Currently there is still very little insight into physiological re-sponse patterns with respect to airgun exposure or any otherloudsoundArtificialand loudsoundscan inducearise incortisolinfish (andsurroundingwater)ashasbeenshowninhighlyartifi-cialconditionsinabucketinalaboratory(Wysockietal2006)Aslightlymore natural experiment but still in captive conditions ofanaquarium reportedalso strongercortisol rises ingiantkelpfish(Heterostichus rostratusClinidae) inresponsetorandomlyfluctuat-ingpresenceofboatnoisecomparedtocontinuousabsenceorpres-enceofthesamenoise(Nicholsetal2015)Howeverthecurrentstateoftheartonsound-inducedphysiologicalstressresponsesisbynomeans such thatqualitativeorquantitative translations canbemadetopopulation-levelconsequencesWearealsoonlyawareof one study directly investigating the physiological response infishexposedtoairgunsSantullietal (1999)conductedastudyonbiochemicalresponsestoairgunexposureinseabassalongtheeastcoastofItalyintheAdriaticSeaAlthoughthisstudysufferedfrommethodologicalissuessuchaspseudoreplicationofmultipleindivid-ualsperexposurecageandexposureconditionsbeingconfoundedbytimeinthewatertheirdatastillsuggestthatseveralbiochemicalparameterswereupregulated from6hrbefore to6hrafterexpo-sureandthattheelevatedlevelsweremostlygoneafter72hr

Another recentaquacultural studyconfirmed thepotential im-pactofacousticexposureontheacutephysiologicalstressresponsein cod (Sierra-Floresetal 2015) In this study codwereexposedto linear frequencysweeps (100ndash1000Hz)of10s foraperiodof10mininroundfishtanksof2mdiameterand1mdepth(314m3)atmoderatelyhighlevelsthatwereaimedatcommonsoundlevelsinaquaculturalfacilities(causedegbytalkingfeedingnettingorknocking)Theywereable toshowabriefbut significant increasein plasma cortisol concentrations peaked 20min after the onsetof the acoustic exposure Behavioural observations were limitedbutfreezingandldquotypicalswimmingresponsesrdquowerereportedThephysiologicalresponse incortisolelevationreturnedbacktobase-linelevelsinabout20min

Sierra-Floresetal (2015)alsoconductedasecondexperimentin which they explored the potentially negative effect of long-termacousticexposureonspawning throughchronic stressTheyusedtwolargertanksof53mdiameterand2mdepth(44m3)and

F IGURE 7emsp (a)Structureofthedynamicenergybudget(DEB)frameworkFoodisassimilatedintoanenergyreservepoolfromwhichafixedproportion(Ƙ)isspentongrowthimmunesystemandsomaticmaintenanceanddeductedfromthetotal(1-Ƙ)togettheenergyavailableformaturationandreproduction(modifiedfromMartinetal2013)(b)Exampleofhowvariationinbodycondition(Energyreserveswhichmayrelatetoanthropogenicnoise-dependentbehaviouraldecisionsreducedperformanceorphysiologicalstress)canaffectvitalrates(SurvivalinthiscasebasedonharbourporpoisedataonimpactfromoperationalnoisefromwindfarmsNabe-Nielsenetal2014)MoreenergyreservesyieldhighersurvivalratesMoreinvestmentinmaturationorreproduction(lowerK)requiresmoreenergytokeepsurvivalupandleadstoashiftinthecurvestotheright

Food

UptakeAssimilation

Defecation

Growth

Somatic maintenanceMaturation

Reproduction

Immune systemƘ

1-Ƙ

Surv

ival

Energy reserves

K = 08

K = 04

K = 02

0 5 10 15 20

10

08

06

04

02

0

(a)

(b)

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

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AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

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Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

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and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

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NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

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PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

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Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

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Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

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SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 20: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

20emsp |emsp emspensp SLABBEKOORN Et AL

exposedthefishinonetanksixtimes1hratrandomtimestothesamefrequencysweepasmentionedaboveandkepttheothertankatambient levelsThebroodstockconsistedof10femalesandsixmalesineachtank(whichwerereadyforspawningatabout60cmlengthandabout34kgmass)Thetwotanksdifferedintheperiodlength inwhicheggswereproducedwith thenoisy tankstopping3weeksearlierthanthequiettankbutoveralleggproductionwasnotdifferentHoweverthereweresignificantlyhighercortisollev-elsmeasuredineggsfromthenoisytankcomparedtothequiettankwhichwerecorrelatedwithsignificantlylowerfertilizationrateandlowerviability

Althoughthesepatternsofapparentreproductiveconsequencesofacousticexposurecorrespondtoreportedeffectsoneggcortisolconcentrationsfertilizationrateandviabilityfromcodstressedbyconfinement(MorganWilsonampCrim1999)theexperimentalde-signisunreplicatedAnytwobatchesofbroodstockmayshowvari-ationinstresslevelsandeggproductionhencetestingthecausalrelationshipwithacousticexposurerequiresappropriatereplicationExtrapolationtooutdoorconditionsisfurtherrestrictedbytheuseofspecificandartificialsoundstimulisoundfieldconditionsinthefishtanksthataredifferentfromnaturalwaterbodiesthebehaviouralspaceavailableforresponsepatternsandthehatchery-raisedback-ground of the test fish (Neo etal 2016 Slabbekoorn 2016)Weshould therefore be very careful with drawing conclusions fromstudieslikeSantullietal(1999)andSierra-Floresetal(2015)Theyshouldbeconsideredaspilots for future studiesofproperdesign(Catoetal2013SlabbekoornampBouton2008Underwood1991)withnaturalsoundfields inopenwaterandsoundstimuli thatre-sembleairgunsoundfeatures(takingdistance-dependentmodifica-tionwithpropagationintoaccount)

6emsp |emspMODELLING CONSEQUENCES

61emsp|emspModelling population- level effects

Twogeneralstrategiescanbedistinguishedforgainingunderstand-inginthepopulation-leveleffectsofseismicsurveysonfishthroughmodellingOnecouldbedescribedasldquobottom-uprdquowhereonebuildsafullydetailedmechanisticspecies-specificmodelincludingallef-fectsofunderwateracousticexposureonindividualsandarealisticacousticexposurescenarioThisisthenusedtoassesswhattheef-fectsareofsucharealisticexposurescenarioatthepopulationlevelThisstrategy isprobably themostdirectwayto findoutwhetherandtowhatextentthereisaproblemwithairgunacousticexposureconditionsofcurrentseismicsurveyingprocedures

The opposite route is also possible and starts by asking thequestion ldquowhatwouldwe consider a problematic population-leveleffectrdquoThisallowsforanldquoupfrontrdquodiscussionaboutwhatisanac-ceptableeffect(egacertainpercentagedecreaseinthenumberofadultindividuals)Themodellingapproachnowworksldquotop-downrdquointhatfirstanassessmentisdonetowhatextenttherelevantmodelparameterscanbechangedbeforethethresholdeffectisreachedThisresultcanbecomparedtotheknownpathwaysofsoundeffects

onindividualswhichrevealsthemostlikelypathwaysthatcanyieldpopulation-leveleffectsabovethethresholdIdeallythisalsoelim-inatesoneormorepathwaysforwhichthemodelshowsthatthepopulationdynamicsarerelativelyinsensitive

Theadvantageofthesecondapproachisthatpotentialeffectscanbeprioritizedintermsoftheirlikelihoodtogeneratepopulation-leveleffectsThiswayresourcesforexpensivefieldandlaboratorystudies can be directed towards the ldquomost promisingrdquo individual-level effects of exposureOn the other hand the prioritization isbasedontheassumptionsunderlying themodelsand if theseareinappropriate the approach could miss the most crucial effectsConsequentlyitappearslogicaltoalwaysincludethecost-effectivesecondstrategyand investwisely incollectionofspecificandpo-tentiallycrucialfielddatatoenterasparameterstoconfirmfindingswiththefirststrategyThetypesofmodelsarethesameforbothbottom-upandtop-downstrategies(egDeRoosampPersson2013MartinJagerNisbetPreussampGrimm2013)

Onesuitablemodellingframeworkfortheindividuallevelisthatof dynamic energy budget models (DEB Kooijman 2000 2010NisbetMullerLikaampKooijman2010)Inthisframeworkindivid-ualsaredescribedintermsoftheirsizeandenergeticstateandthemodelspecifieshowingestedenergyisusedforgrowthmaturationandreproductiongiventhestateoftheindividual (Figure7a)TheDEBframeworkincludeshighlymechanisticdescriptionsofhowen-ergyflowsthroughanorganism(TealvanHalvanKootenRuardijampRijnsdorp2012Metcalfeetal2016)Itcanthereforereadilyin-corporatethevariousindividual-leveleffectsofunderwatersoundwhichaffectindividualenergetics(eghigherstresslevelsleadingtohighermetabolicrates)andortimebudgets(egmoretimespentonavoidancebehaviouryieldinglesstimeleftforfeeding)

It is straightforward to use theDEBmodel as a basis for sim-ulating population dynamics by assuming that individuals shareacommonsourceof foodandkeeping trackofbirthsanddeaths(Figure7b) Thepopulation-levelmodel simply consistsof abook-keepingsystemtoaccountforallindividuals(Martinetal2013)allcohorts(DeRoosDiekmannampMetz1992)oradistributionoverin-dividualstates(AndersenampBeyer2006)Becauseallassumptionsinthisframeworkaremadeattheindividuallevelallpopulation-leveleffects are emergent properties of the individual-level effects onthemodelpopulationThisstrictseparationbetweenassumptionswhicharemadeononeleveloforganization(individual)andresultswhichareonanother leveloforganization (population) isamajoradvantageofthistypeofmodellingframework

An example DEB study on anchovy (Engraulis encrasicolusEngraulidae) reliably predicted temperature and age-class-specificgrowth and reproductive performance (Pecquerie Petitgasa ampKooijman2009)Alternativemodellingapproachesuseslightlydif-ferent conversion routeswith for example availableenergyallo-catedtothreestructurepoolssomalipidsandeggsThealternativeapproaches allow sensitivity analyses for variation in external en-vironmentalconditionsand internalallocationstrategies (egFrisketal 2015Megrey etal 2007) It is arbitrarywhether oneusesDEBoranyothersimilarframeworkastheyshouldallgiveresults

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

AartsGMvonBenda-BeckmannAMvonLuckeKSertlekHOumlvanBemmelenRGeelhoedSCVhellipKirkwoodR (2016)Movement strategy of harbour porpoise affects the number ofanimals acoustically exposed to underwater explosions Marine Ecology Progress Series 557 261ndash275 httpsdoiorg103354meps11829

AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 21: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp21SLABBEKOORN Et AL

pointing in thesamedirection (AndersenampBeyer2006DeRoosetal1992Martinetal2013)

BecauseDEBishighlymechanisticitdoesrequireconsiderableknowledgeaboutthespeciestobemodelledinparticularabouttheindividual-level parameters that specify energy expenditure Thiscanbeaproblem if theaim is tostudyspecies forwhichsuch in-depthknowledge isunavailableFurthermoresomeof theparam-eterstoDEBaredifficulttoobtainfromexperimentsForthis lastproblem a set of statistical routines have been developed whichcanestimateDEBparametersfromcommonexperimentaloutputssuch as growth curves and population time series (Lika Kearneyamp Kooijman 2011) Still this procedure requires experimental re-sultswhicharenotalwaysavailableinwhichcaseestimatescanbebasedonrelatedspecieswithknownparameters(egVanderVeerKooijmanampvanderMeer2001)Physiologicalmodels alsoallowimpactanalysesfordeviatingparametersthatenterthemodelandapparentlysubtlevariationmayaccumulatetosignificantchangesinindividualfitnessthatmayalterpopulationforecastsToxiceffectsonindividualshavebeentranslatedinthiswaytopopulation-leveleffects(JagerampKlok2010)whichshouldthereforealsobepossibleforsoundimpact

What is needed is accurate field data for sound-exposure-induced changes inbehavioural andphysiological parameters thatcanenterthemodelsThesedatashouldbecollectedunderavarietyofecologicalconditionstoalsoallowthesetoplayaroleinthemodelandenablefurtherexplorationofthepotentialforinteractionsandconsequences across the feasible parameter range For examplegrowthratetimeofmetamorphosisandmortalityofcodlarvaeareallaffectedbytemperatureandfoodavailability(egCookKunzlikHislopampPoulding1999HawkinsSoofianiampSmith1985MorganRideoutampColbourne2010Olsenetal2011)Increasingtempera-tures have therefore a strong effect on recruitment and availablehabitat in general (Kell Pilling ampOBrien 2005 Rindorf amp Lewy2006) Consequently impact analysis of anthropogenic factors islikelytogainbiologicalrelevancebytakingtheclimaticandmacro-ecologicalcontext intoaccountthatmaybecriticalbythemselvesfor collapse recovery or outburst (Beaugrand Brander LindleySouissiampReid2003CookSinclairampStefansson1997Cushing1984)ForexampletheNorthSeacodstockisclosetothesouthernedgeofthespeciesdistributionandclimatechangemayaffectstockdevelopmentsdirectlythroughtemperatureandindirectlythroughtheabundanceof zooplankton (BeaugrandampKirby2010Poumlrtneretal2001)

Vulnerability to disturbance by sound will also vary with ageandsizeAlthoughsoundimpactonlarvalstagesmaybelimitedina physical sensewehave little knowledgeof behavioural effectsEventhoughexperimentalexposuretopile-drivingsoundsdidnotaffectmortality in captivity (seeBolle etal 2012 for sole larvaeSolea soleaSoleidae)fishlarvaemaystillbephysically injured(DeSotoetal2013LoesBollepersonalcommunication)andmaynotsurviveorperformwell intheirnaturalenvironmentWedoknowthat larval stages of fishes andothermarine taxa are sensitive tosound(MontgomeryJeffsSimpsonMeekanampTindle2006)and

anecdotalcase-studiesonseismicsurveyeffectsonsimilarlysmallmarineanimalshavereportedmixedresults(andneedreplication)noeffectonthreeshrimpspecies(smalldecapodcrustaceans)tar-geted by fisheries (Andriguetto-Filho etal 2005) detrimental ef-fects on mortality behaviour and physiology for scallops (Pecten fumatusPectinidaeDayetal2017)andpotentiallyfataleffectonzooplankton(cfMcCauleyetal2017butseeFieldsetal2019)

Acousticexposuremayalsoaffectlarvalfeedingratesforwhichconsequencescouldbemodelledinasimilarwayastheeffectsoflight-dependentdetectabilityandturbulence-dependentefficiency(seeFiksenetal1998forherringandcodlarvae)Whenjuvenilesget older and larger theymove to another position in themarinefoodweb Size compositionof stocks and theirmainprey speciesare critical for understanding recruitment and stock development(Hjermannetal2007)andage-specificharvestinghasconsiderableimpactonstockdepletionandrecruitment(Diekert2013)Similarlythepotentialimpactofacousticdisturbanceonlocalpredator-preyinteractionswilllikelyheavilydependonsize-classes

WecanstartthinkingaboutfitnessconsequencesoncewehaveassessedbehaviouralandphysiologicaleffectsChangesinfoodup-takeorswimmingactivitycanbeconvertedtogainsand losses inenergy(egDaan1973DutilampLambert2000)Changesinpreda-tionrisk(egHammillampStenson2002KoumlsterampMoumlllmann2000Savenkoffetal2006)orreproductiveopportunity(Folkvordetal2014)mayyieldmorediscreteeventsthatmayhavestrongeffectson individual fitness It should be realized here that not only thetarget speciesmaybeaffectedby theacousticexposurebutalsopredatorandpreyspeciesmaybeaffected(cfHawkinsetal2014)Consequentlydetailedknowledgeabouttheecologyofthetargetspeciesandstock-specificconditionsisrequiredtogetafullpictureonfactors thatmaycontribute to thepotential impactofacousticover-exposureinaparticularareaforaparticulartime

62emsp|emspIndividual- based models

Individual-based models (IBMs) may also be a useful tool to ex-ploretheeffectsofenvironmentalstressorsonfishbehaviourandvital rates (Grimm etal 2005Willis 2011 and see eg SibertHamptonFournierampBills1999Daeweletal2008) IBMsareaclassofcomputationalmodelsforsimulatingtheactionsandinter-actions of autonomous agents the individual animals to exploreconsequences for the local population as awhole Theymay alsoincludeenergybudgetfeaturesbutincontrasttotheDEBmodelstheyincludespatialrealismIBMscanincludetheimpactofphysi-calpropertiesof fishhabitat suchas currents temperature tidesor turbulenceonmigrationor spatial distribution If thesemodelsare coupledwith3Dhydrodynamicmodels theycan include sub-routinesforenergybudgets(gainthroughforagingandlossthroughmetabolism)andprovideinsightintoenvironmentalimpactonvitalratesdependentonforexampleageclassandspecificfoodabun-danceIBMsoftenuseLagrangianmodellingofindividualfishlinkedto spatially resolved hydrodynamicmodels bywhich they can ac-countforfactorssuchasthevariabilityinexposuretoenvironmental

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

AartsGMvonBenda-BeckmannAMvonLuckeKSertlekHOumlvanBemmelenRGeelhoedSCVhellipKirkwoodR (2016)Movement strategy of harbour porpoise affects the number ofanimals acoustically exposed to underwater explosions Marine Ecology Progress Series 557 261ndash275 httpsdoiorg103354meps11829

AinslieMA (2015)AcenturyofsonarPlanetaryoceanographyun-derwater noise monitoring and the terminology of underwatersoundAcoustics Today1112ndash19

Altenback T (1995) A comparison of risk assessment techniques from qualitative to quantitativePaperpresentedatASMEpressurevesselsandpipingconferenceRetrievedfromhttpwwwostigovscitechservletspurl67753

AmanteCampEakinsBW (2009) ldquoETOPO1 1 Arc-minute global relief model Procedures data sources and analysisrdquo in NOAA Technical Memorandum NESDIS NGDC-24 (NationalGeophysicalDataCenterNOAA)

AndersenKHampBeyerJE(2006)Asymptoticsizedeterminesspe-ciesabundanceinthemarinesizespectrumThe American Naturalist16854ndash61httpsdoiorg101086504849

Andreacute M Soleacute M Lenoir M Durfort M Quero C Mas A hellipHoueacutegnigan L (2011) Low-frequency sounds induce acoustictrauma in cephalopodsFrontiers in Ecology and the Environment9489ndash493httpsdoiorg101890100124

Andriguetto-FilhoJMOstrenskyAPieMRSilvaUAampBoegerW A (2005) Evaluating the impact of seismic prospecting on ar-tisanal shrimp fisheriesContinental Shelf Research25 1720ndash1727httpsdoiorg101016jcsr200505003

Anonymous (2006)Marine sources Sercel - ToulonFranceUSAwwwsercelcomRetrievedfromhttpwwwoceandatacokrGroupWareHomeproductbrochureSercelMarine20Sourcespdf

Anonymous (2014a) Bolt technology corp Products Retrieved fromhttpwwwbolt-technologycompagesproductshtm

Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

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StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

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TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

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TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

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VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

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Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

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WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

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WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 22: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

22emsp |emsp emspensp SLABBEKOORN Et AL

stressorsandtherebyforindividualvariabilityindispersalthroughapatchyenvironment(HeathampGallego1997Hernandezetal2013LoughBuckleyWernerQuinlanampEdwards2005)

IBMs can be applied in combination with sound propagationmodels using species-specific data on typical swimming depthshearingsensitivityandspectralrangetoassessexposureprobabilityandconsequencesforover-exposureandbehaviouralresponsesoffishforanyparticularsoundevent(ErbeampKing2009Hovemetal2012 Southall etal 2007) An example of this approach can befoundinharbourporpoisesandtheirexposuretotheloudsoundsofunderwaterdetonationsofexplosives(Aartsetal2016VonBenda-Beckmannetal2015)Inthisworktheauthorsestimatedthatdet-onationsintheDutchpartoftheNorthSea(WWIIexplosives)causepermanenthearingdamagefor800ndash8000porpoisesperyearandmanymoreanimalswithsometemporaryimpactontheirhearing

Rossingtonetal (2013)usedan IBMapproach inwhich theycombinedahydrodynamicmodelandanunderwatersoundprop-agation model to assess the behavioural impact of an explicitpile-driving event for an offshore wind farm on movement pat-terns of cod off the coast from Liverpool and the Dee EstuaryRossington etal (2013) used realisticmean swimming speed forcodandlocallyobservedsizedistributionsandtestedtheimpactof being sensitive to sound disturbance (adjusting swimming di-rection and speed freezing or doubling) or not (continuation onthesametrajectorydeterminedbycorrelatedrandomwalk)Theyfoundout thatsensitive fishexperiencedsignificantdelayscom-paredtosimulatedcounterpartsthatwere insensitive (ldquodeafrdquo)ontheirmigration from the feeding grounds to their coastal targetwhichconcernsaknownspawningandnursinggroundforcodInthecontextofsoundpollutionasanenvironmentalstressoritmayalsobepossibletoapplyacombinationofenergyflowmodelsandindividual-basedmodels

63emsp|emspMultitrophic stock models

Insights intomultitrophic relationships and the human impact offisheriesarealsolikelytoplayanimportantroleintheevaluationofpotentialforsoundimpactonfishesTrophiclayersofpredatorandpreyfishandvariousgroupsofzooplanktonandzoobenthosplayasignificantroleinnaturalfoodwebsandfisheriesatanytrophiclayerinherentlyaffectinteractions(LindegrenMoumlllmannNielsenamp Stenseth 2009 Lindegren etal 2010 Neuenfeldt amp Koumlster2000 Persson etal 1998 Van Leeuwen De Roos amp Persson2008)Largepiscivorous fishare typically themostprofitable forfisheriesbutalsoforagefishcompose30ofglobalfisheriesland-ingsSimilarlysoundimpactwillnotberestrictedtosinglespeciesatasinglelifestageSoundmayaffecteveryspeciesinadifferentwaytherebyaffectinginteractionsindirectlywhilesoundmayalsoaffectinteractionsdirectlybyanimpactonpredator-preyrelation-ships(egPurserampRadford2011ShafieiSabetetal2015)

Modellingtheinteractionsbetweentrophiclayersisalsoimport-antfortheunderstandingoftheeffectofstressorsondynamicalfeed-backs between trophic layers (Claessen etal 2000 Persson etal

1998)Feedinginteractionsamonggroupsaresize-specificandhaveconsequencesforbothgroupspredationresultsinfoodforpredatorsandmortalityforpreyDuetodynamicalfeedbacksbetweentrophiclayersanimpactoffisheriesoradditionalstressorsmayhavecounter-intuitiveeffectsForexamplefishingonclupeidswhicharedominantpreyspeciesforcodintheBalticmaypreventafisheries-inducedcol-lapseofthecodpopulationThefishermenmayappeartocompetewithcodbutinsteadtheiractivitiescanreducecompetitionforfoodwithinthepreypopulationandtherebycauseashiftinthesizedistri-butionofclupeidsthatactuallyimprovesthefoodavailabilityforcod(DeRoosampPersson2013VanLeeuwenetal2008)

Mortalitythroughfisheriesisrecognizedasamajorfactorthathas tobe taken intoaccount forany typeofpopulationmodelasitistheconfirmedcauseofhistoricaldeclines(FrankPetrieChoiamp Leggett 2005 Hutchings Bishop amp McGregor-Shaw 1999)Acousticimpactanalysesofseismicsurveysonspecificpopulationsshouldthereforeintegratenotonlyexpectedprojectionsofclimatechange but also current harvesting regimes (Drinkwater 2005MacKenzieGislasonMoumlllmannampKoumlster2007)Modellingeffortstoassessimpactofanthropogenicsoundwillalsobenefitfromthe

F IGURE 8emspManybiologicalorganizationlevelsplayaroleinunderstandingthemechanismsunderlyingthepotentialimpactofapollutantsuchasairgunsoundonfishpopulationsItistheindividualthatisincontactwithitslocalenvironmentandenvironmentalstressorsUpscalingtopopulationscommunitiesandecosystemsrequiresinvestigatingprocessesatvariouslevelsandtakingdifferentkindsofabioticandanthropogenicfactorsintoaccount(modifiedfromCookeetal2014)Anthropogenicnoisecanaffectupscalingfromtheindividualtothepopulationlevel(Coxetal2018Kuncetal2016Slabbekoornetal2010)throughadirectimpactonvitalratessuchassurvivalandreproductionbutalsothroughanindirectimpactviagrowth(egalteringcohortbodyconditionandsizeatmaturation)orbehaviour(egdisplacementfromanareaorloweredfeedingefficiency)Upscalingfrompopulationtocommunityleveloccursthroughdisturbingeffectsonpredator-preyinteractions(ShafieiSabetetal2015)andotherinter-specificeffectssuchascompetitiverelease(Hubertetal2018SlabbekoornampHalfwerk2009)orthroughnoise-inducedhabitatalterations(Solanetal2016)Habitat-relatedstressorsandcumulativeeffectsfromotherfactorsthansoundpollutionarethelinkbetweencommunitiesandecosystems(Carrolletal2017Hawkinsetal2015Jones2016)

Individual

Population

Community

EcosystemHydrodynamicsclimate change

Seasonalityfisheries

Connectivitypollution fisheries

Reproduction growth behaviour

Competition multitrophic interactions

Habitat coupling species invasions

Processes affectingupscaling

Abiotic and anthropogenic

factors

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

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BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

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BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

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BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

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NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

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PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

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Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

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Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

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SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

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Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

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Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

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WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

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org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 23: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp23SLABBEKOORN Et AL

lessons learnedwithmodellingefforts in fisheries (Fogarty2014HilbornampLiermann1998Mace2001)Forexampleasmentionedbefore including environmental influences would make a modelsignificantlymoredynamicandrealisticwhichisalsotrueandim-plementedforpredictingimpactfromfisheries(Koumlsteretal2005)Anotheraspectofsimilarityconcernsconnectivityamongpopula-tionsorstocksandvariation in impactAcousticexposureon fishpopulations through seismic surveyswill inherently vary spatiallyAlso fisheries impact isneverhomogenousacross largeareas re-latedtothetypicalheterogeneityinfishingpressuredeterminedbysocioeconomicandregulatoryfactorsCouncilandDie (2015)ap-pliedahybridtypeofmodeltoinvestigatethisspatialvarietyinfish-ingpressureandrevealedrelevanteffectsontheagedistributionofmortalitywhichhadinturnagaineffectsonthestockspawningattributes

Finally although matters become increasingly complex withscaling up to population community and even ecosystem level(Figure8) we believe these steps are essential Not only has itbecome clear that the evaluation of sound impact should lookbeyondsingle-specieseffects (Francisetal2009)but therearealsoalreadyterrestrialandmarinereportsonnoise-inducedhab-itatmodificationthroughtheeffectsonthe localanimalcommu-nity(FrancisKleistOrtegaampCruz2012Solanetal2016)TheMarineStrategyFrameworkDirectiveoftheEUalreadytalksaboutldquoGoodEnvironmentalStatusrdquowhichobviouslyconcernsecosystemlevelAlsoinfisheriesmanagementstrategieslessonswerelearnedwithsingle-speciesorsingle-stockapproachesbeforemorecom-plexintegratedorecosystem-basedmodelsbecamemorepopular(Mace2001Pauly1996)Maximumsustainableyield(MSY)wasformerlyacommonmanagementtargetwhichmeantthatitwasatargettofishasmuchaspossiblewithoutcausingareductionthatwould involve a serious risk of stock extinctionHowever it has

becomeclearthat individualmanagementplansforseparatespe-cies inevitably yield conflicts and ignore interactions amonghar-vestedspeciesTheMSYhasthereforebecomemoreofanupperlimitandmanagementstrategiesarebeingupgradedwithecolog-icalcomplexity

Currentmanagementstrategiesmovetowardsecosystem-basedfisheriesmanagement(EBFM)(Fogarty2014)EBFMaimsatsustain-ableharvestingoffishestoretaintheimportantecosystemservicesof the marine environment EBFM is therefore a relevant conceptfor future developments in modelling sound impact beyond thesingle-specieslevelasitconcernsamorelocation-basedratherthana species-based approach and takes ecological regions as theman-agementtarget(seeegFogartyampMurawski1998LiuLiangChenChenampShen2012Liuetal2012)EBFMsolvesthechallengeofincorporatingtoomanyfactorsandplayersintoamodelforacomplexecosystemasthemarineenvironmentbynotusingspecificspeciesbutsize-classesorguildswhiletakingbothenvironmentalinfluencesandhumanimpactasintegralpartoftheecosystem(ArkemaAbramsonampDewsbury2006Ashleyetal2003DeJongePintoampTurner2012DolanPatrickampLink2016Fogarty2014Tamisetal2016)

7emsp |emspCONCLUSIONS

Our review reflects the interdisciplinary challenge of assessingpopulation-level consequences of seismic surveys on fishes Theinformation data and insights treated crossedmanydifferentdis-ciplinesandsubdisciplinesTheoverviewyieldsa fewkey insightsforthecurrentstateoftheartandmaingapsinourknowledge(seeBox3)Dataonthebehaviouralandphysiologicalresponsesoffishto seismic surveys are currently limited there are no species forwhichtherearewell-replicatedandadequatelycontrolleddatasets

Box 3enspSummary overview of current insightsbull Themosteffectivewaytomakeprogressinimpactassessmentisthroughcomplementaryeffortsindatacollection(behaviourphysi-ologyacoustics)andmodelling(individualbasedandenergybudget)withfeedbacktooneanotherateachstageandwitheverynewinsight

bull Wecurrentlylack(a)dosendashresponsedataforanybehaviouralorstressphysiologicaleffect(b)translationintovitalratesforpotentialbehaviouralorphysiologicalresponsesgivenfluctuatingecologicalconditionswithseasonlifestageandlocalityand(c)insightintopopulation-levelconsequencesofanypotentialeffectsonvitalrates

bull Behaviouralandstressphysiologicaleffectsarelikelytobemostrelevantforpopulation-levelconsequencesandshouldbeprioritizedover injuryanddeathforfurtherexplorationsincethepotential forbehaviouraleffects intermsofanimals involved isordersofmagnitudelarger

bull Datacollectedduringasingleseismicsurveycanprovidestatisticalevidenceforsound-relatedfishactivityordistributionatthiseventbutcannotserveasevidenceforsuchapatterningeneralReplicationatthelevelofthequestioniscriticalforthevalidityofanypracticaldatacollectioneffort

bull AccurateassessmentsofthesoundfieldatthefishintermsofbothpressureandparticlemotionarecriticalforanybehaviouralorphysiologicaleffectstudyIngeneralthereisastrongneedfordataonnaturalpatternsofvariationinparticlemotioninfishhabitat

bull Harmonizationinaudiogrammeasurementmethodologyisaprerequisiteforadvancesinquantitativeunderstandingofhearingsensi-tivityinfishes

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

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ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

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CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

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DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

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Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

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inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

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32emsp |emsp emspensp SLABBEKOORN Et AL

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Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 24: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

24emsp |emsp emspensp SLABBEKOORN Et AL

to start quantifying the population consequences of airgun expo-sureHoweverunlikeformarinemammalsthereexistsawealthofdataonphysiologyandenergeticsformanyfishspeciesthatcouldbeusefulintranslatingchangesinbehaviourintochangesinenergybudgetsandwhichcouldsubsequentlybeusedtoinferimpactongrowthmaturationreproductionandsurvival

Withrespecttopotentialformodellingimpactthemostsuit-ablecandidateapproachforriskassessmentdependsontheob-jectives ofmanagement the amount of available data and levelofexpertknowledgeandresourcesHowever there isperhapsbetter potential for data-intensive approaches for fish than fortherelativelyharder-to-studymarinemammalsforwhichPCADmodelsweredevelopedinthefirstplaceProperuseofqualitativeandsemi-quantitativemethodsbecomesinherentlyquantitativeandwe therefore believe that it is better to focus on quantita-tivemethodsExpertelicitationisausefulmethodtosynthesizeknowledge potentially extending the reach of explicitly quan-titative methods to data-poor situations Whatever method ischosen it is unlikely to be correct in every case This providesamotivationformonitoringoutcomesinasensitivewayandforadaptive management strategies (see eg Nichols amp Williams2006) Furthermore there are many stock monitoring studiesandpredictivemodelsforfishstockthattakebioticabioticandanthropogenicinfluencesintoaccount(egCardinaleampSvedaumlng2004Heathetal2013)

ConsequentlyfishseemanexcellenttaxonomicgrouptofurtherexplorethevalidityofPCAD-typemodelsandtopotentiallyexpandtheapplicationItwillbeimpossibletodevelopasinglemodelthatapplies to all fish species However the same problem applies tofisheriesimpactforwhichadvancedtheoriesandmethodologyhavebeendeveloped(egMcCullyPhillipsetal2015reviewinPatricketal2009)SeismicsurveysoundpulsesarejustoneanthropogenicpollutantwhichisnotlikelytobecomelessabundantinthefutureMany impulsive sound sources caused by human activities likelyhavesimilarpotentialforimpactsuchaspiledrivingforwindfarmconstructionandexplosionsrelatedtodetonationofwarfareammu-nitionWethereforebelievethatmarineconservationconcernsarelikelytogrowandmorestudiesarewarrantedthatintegratediffer-entdisciplinesandalsoconsidertheaccumulationofdifferentsoundsources

ACKNOWLEDG EMENTS

TheEampPSoundandMarineLifeJoint IndustryProgramme (JIP) isacollaborationamongoilandgasindustrycompaniestojoinforcesin gaining insights that are relevant in the context of sustainableexploration for and exploitation of natural resources at sea Theyalsosupportresearchontheeffectsofsoundonmarinelifetohelpgovernmentsmakeregulatorydecisionsbasedonthebestscienceandifnecessarytheindustrytodevelopeffectivemitigationstrat-egiesThecurrentreviewisadirectresultfromacallforproposalsbytheJIPandhasbenefitedfromtechnicalfeedbackfromseveral

JIPreviewerswithoutlosingtheindependencerequiredforanaca-demic review

ORCID

Hans Slabbekoorn httpsorcidorg0000-0003-2309-0048

R E FE R E N C E S

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Anonymous (2014b) The seamap sleeve gun Product sheet Seamap(UK) Ltd Retrieved from httpwwwseamapcompdfSeamap_Sleeve_Gunpdf

Arkema K K Abramson S C amp Dewsbury B M (2006) Marineecosystem-basedmanagement fromcharacterizationto implemen-tationFrontiers in Ecology and the Environment4525ndash532httpsdoiorg1018901540-9295(2006)4[525MEMFCT]20CO2

ArnbomTFedakMABoydILampMcConnellBJ(1993)Variationin weaningmass of pups in relation tomaternal mass postwean-ing fastdurationandweanedpupbehaviour insouthernelephantsealsatSouthGeorgiaCanadian Journal of Zoology711772ndash1781httpsdoiorg101139z93-252

AshleyMVWillsonMFPergamsORWODowdDJGendeSMampBrownJS(2003)EvolutionarilyenlightenedmanagementBiological Conservation 111 115ndash123 httpsdoiorg101016S0006-3207(02)00279-3

Baranova O (2010) World ocean atlas 2005US Department ofCommerceNationalOceanicandAtmosphericAdministration

BartonBA(2002)StressinfishAdiversityofresponseswithpartic-ularreferencestochanges incirculatingcorticosteroids Integrative

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

Beaugrand G Brander KM Lindley J A Souissi S amp Reid P C(2003)PlanktoneffectoncodrecruitmentintheNorthSeaNature426661ndash664httpsdoiorg101038nature02164

Beaugrand G amp Kirby R R (2010) Climate plankton andcod Global Change Biology 16 1268ndash1280 httpsdoiorg101111j1365-2486200902063x

BejderLSamuelsAWhiteheadHFinnHampAllenS(2009)Impactassessment research Use andmisuse of habituation sensitisationand tolerance in describing wildlife responses to anthropogenicstimuli Marine Ecology Progress Series 395 177ndash185 httpsdoiorg103354meps07979

BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

Cofin A B Zeddies D G Fay R R Brown A D Alderks P WBhandiwadAAhellipSisnerosJA(2014)Useoftheswimbladderandlaterallineinnear-fieldsoundsourcelocalizationbyfishJournal of Experimental Biology 217 2078ndash2088 httpsdoiorg101242jeb093831

CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

CookRMKunzlikJRHislopJRGampPouldingD(1999)Modelsof growth and maturity for North Sea cod Journal of Northwest Fisheries Science2591ndash99httpsdoiorg102960Jv25a8

Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

Costa D P Schwarz L Robinson P Schick R S Morris P ACondit R hellip Kilpatrick AM (2015) A bioenergetics approachto understanding the population consequences of disturbanceElephant seals as a model system In A N Popper A Hawkins(Eds)The effects of noise on aquatic life II(pp161ndash169)NewYorkNYSpringer

CouncilELampDieDJ(2015)Therelativeimportanceofsubpopula-tionconnectivityandtheagedistributionofmortality inexploitedmarinefishpopulationsEcological Modelling312247ndash255httpsdoiorg101016jecolmodel201505004

CoxKBrennanLPGerwingTGDudasSEampJuanesF(2018)SoundthealarmAmeta-analysisontheeffectofaquaticnoiseonfishbehaviorandphysiologyGlobal Change Biology243105ndash3116httpsdoiorg101111gcb14106

Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

Dalen J (1973) Stimulating herring shoals with sound Experiments in Hopavaringgen and ImsterfjordenVerrafjorden (In Norwegian) Report to the Norwegian Research Council of Technology and Natural Sciences 73-143-T

DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

DeSotoNADelormeNAtkinsJHowardSWilliamsJampJohnsonM(2013)Anthropogenicnoisecausesbodymalformationsandde-laysdevelopmentinmarinelarvaeScientific Reports32831httpsdoiorg101038srep02831

Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

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ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

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emspensp emsp | emsp33SLABBEKOORN Et AL

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VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

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org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 25: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp25SLABBEKOORN Et AL

and Comparative Biology 42 517ndash525 httpsdoiorg101093icb423517

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BleckmannHampZelickR(2009)LaterallinesystemoffishIntegrative Zoology413ndash25httpsdoiorg101111j1749-4877200800131x

BoegerWAPieMROstrenskyAampCardosoMF(2006)Theef-fectofexposuretoseismicprospectingoncoralreeffishesBrazilian Journal of Oceanography 54 235ndash239 httpsdoiorg101590S1679-87592006000300007

BolleLJdeJongCAFBiermanSMvanBeekPJGvanKeekenOAWesselsPWhellipDekelingRPA(2012)Commonsolelar-vaesurvivehighlevelsofpile-drivingsoundincontrolledexposureexperimentsPLoS ONE7e33052httpsdoiorg101371journalpone0033052

Boussard A (1981) The reactions of roach (Rutilus rutilus) and rudd (Scardinius erythrophthalmus) to noises produced by high speed boat-ingProceedingsof2ndBritishFreshwaterFisheriesConference(pp188ndash200)LiverpoolUKUniversityofLiverpool

BoydIBrownellBCatoDClarkCCostaDEvansPhellipZimmerW(2008)The effects of anthropogenic sound on marine mammals-AdraftresearchstrategyEuropeanScienceFoundationndashMarineBoardpo-sitionpaper13archivesesforgfileadminPublic_documents

BraunCBCoombsSampFayRR(2002)Whatisthenatureofmultisen-soryinteractionbetweenoctavolateralissub-systemsBrain Behavior and Evolution59162ndash176httpsdoiorg101159000064904

BrekhovskikhLMLysanovYPampLysanovJP(2003)Fundamentals of ocean acousticsNewYorkNYSpringerScienceampBusinessMedia

Bruce B Bradford R Foster S Lee K Lansdell M Cooper Samp Przeslawski R (2018) Quantifying fish behaviour and com-mercial catch rates in relation to a marine seismic surveyMarine Environmental Research 140 18ndash30 httpsdoiorg101016jmarenvres201805005

Brumm H amp Slabbekoorn H (2005) Acoustic communication innoise Advances in the Study of Behavior 35 151ndash209 httpsdoiorg101016S0065-3454(05)35004-2

Caldwell J Christie P Engelmark F McHugo S Oumlzdemir HKristiansen P amp MacLeod M (1999) Shear waves shine brightly Oilfield Review Spring14p

Caldwell J amp Dragoset W (2000) A brief overview of seis-mic air-gun arrays The Leading Edge 19 898ndash902 httpsdoiorg10119011438744

Caldwell J Koudelka E Nesteroff K Price R amp Zhang P (2015)Seismicpermanentreservoirmonitoring(PRM)ndashAgrowingmarketEAGE First Break3365ndash73

CardinaleMampSvedaumlngH (2004)Modelling recruitmentandabun-dance of Atlantic cod Gadus morhua in the eastern Skagerrak-Kattegat (North Sea) Evidence of severe depletion due to a pro-longed period of high fishing pressure Fisheries Research 69263ndash282httpsdoiorg101016jfishres200404001

Carroll A Przeslawski RGunningM-E Bruce BampDuncanA J(2017)Acritical reviewofthepotential impactsofmarineseismicsurveysonfishampinvertebratesMarine Pollution Bulletin1149ndash24httpsdoiorg101016jmarpolbul201611038

CatoDHNoadM JDunlop R AMcCauley RD GalesN JSalgadoKentCampDuncanA (2013)Astudyof thebehavioural

responseofwhalestothenoiseofseismicairgunsDesignmethodsandprogressAcoustics Australia4188ndash97

ChanAAYHGiraldo-PerezPSmithSampBlumsteinDT(2010)Anthropogenic noise affects risk assessment and attention ThedistractedpreyhypothesisBiology Letters6458ndash461httpsdoiorg101098rsbl20091081

ChapmanCJampHawkinsAD(1973)AfieldstudyofhearinginthecodGadus morhuaLJournal of Comparative Physiology85147ndash167httpsdoiorg101007BF00696473

Christiansen F amp LusseauD (2015) Linking behaviour to vital ratesto measure the effects of non-lethal disturbance on wildlifeConservation Letters8424ndash431httpsdoiorg101111conl12166

ChristiansenFRasmussenMHampLusseauD(2014)InferringenergyexpenditurefromrespirationratesinminkewhalestomeasuretheeffectsofwhalewatchingboatinteractionsJournal of Experimental Marine Biology and Ecology45996ndash104

ClaessenDDeRoosAMampPerssonL (2000)DwarfsandgiantsCannibalism and competition in size-structured populations The American Naturalist155219ndash237

Clark J S Carpenter S R Barber M Collins S Dobson AFoley J A hellip Wear D (2001) Ecological forecasts An emerg-ing imperative Science 293 657ndash660 httpsdoiorg101126science2935530657

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CollinsM(1993)Asplit-stepPadesolutionfortheparabolicequationmethodJournal of the Acoustical Society of America931736ndash1742httpsdoiorg1011211406739

ConradJLWeinersmithKLBrodinTSaltzJBampSihA(2011)BehaviouralsyndromesinfishesAreviewwithimplicationsforecol-ogyandfisheriesmanagementJournal of Fish Biology78395ndash435httpsdoiorg101111j1095-8649201002874x

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Cook R M Sinclair A amp Stefansson G (1997) Potential collapseof North Sea cod stocks Nature 385 521ndash522 httpsdoiorg101038385521a0

CookeS JKillenSSMetcalfe JDMcKenzieD JMouillotDJoslashrgensenCampPeckMA(2014)Conservationphysiologyacrossscales Insights from the marine realmConservation Physiology 2cou024httpsdoiorg101093conphyscou024

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Cushing D H (1984) The gadoid outburst in the North Sea Journal Conseil International pour lExploration de la Mer41159ndash166httpsdoiorg101093icesjms412159

DaanN(1973)AquantitativeanalysisofthefoodintakeofNorthSeacodGadus morhua Netherlands Journal for Sea Research6479ndash517httpsdoiorg1010160077-7579(73)90002-1

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

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DalenJampKnudsenGM(1987)Scaringeffectsinfishandharmfulef-fectsoneggslarvaeandfrybyoffshoreseismicexplorationsInHMMerklinger(Ed)Progress in underwater acoustics(pp93ndash102)LondonUKPlenumPresshttpsdoiorg101007978-1-4613-1871-2

DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

DeRoosAMDiekmannOampMetzJAJ(1992)Studyingthedy-namicsofstructuredpopulationmodelsAversatiletechniqueanditsapplicationtoDaphniapopulationdynamicsThe American Naturalist139123ndash147httpsdoiorg101086285316

DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

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Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

DijkgraafS (1962)Thefunctioningandsignificanceofthe lateral-lineorgansBiological Reviews3851ndash105

DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

ErbeCampKingA(2009)ModelingcumulativesoundexposurearoundmarineseismicsurveysJournal of the Acoustical Society of America1252443ndash2451httpsdoiorg10112113089588

EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

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RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

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org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 26: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

26emsp |emsp emspensp SLABBEKOORN Et AL

Daewel U Peck M A Kuumlhn W St John M A Alekseeva I ampSchrumC (2008)Couplingecosystemand individual-basedmod-els to simulate the influence of environmental variability on po-tential growth and survival of larval sprat (Sprattus sprattus L) inthe North Sea Fisheries Oceanography 17 333ndash351 httpsdoiorg101111j1365-2419200800482x

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DayRDMcCauleyRDFitzgibbonQPHartmannKampSemmensJM(2017)ExposuretoseismicairgunsignalscausesphysiologicalharmandaltersbehaviorinthescallopPecten fumatus Proceedings of the National Academy of Sciences of the United States of America114E8537ndashE8546httpsdoiorg101073pnas1700564114

De Jonge VN Pinto R amp Turner R K (2012) Integrating ecologi-cal economic and social aspects to generate useful managementinformationunder theEUDirectivesrsquo lsquoecosystemapproachrsquoOcean amp Coastal Management 68 169ndash188 httpsdoiorg101016jocecoaman201205017

DeRobertisAampHandegardNO(2013)Fishavoidanceofresearchvessels and the efficacy of noise-reduced vessels A review ICES Journal of Marine Science 70 34ndash45 httpsdoiorg101093icesjmsfss155

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DeRoosAMampPerssonL(2013)Population and community ecology of ontogenetic developmentPrincetonNJPrincetonUniversityPress

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Diekert F K (2013) The growing value of age Exploring economicgains fromage-specificharvesting in theNorthArcticcod fisheryCanadian Journal of Fisheries and Aquatic Sciences70 1346ndash1358httpsdoiorg101139cjfas-2012-0471

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DiNapoli F R amp Deavenport R L (1980) Theoretical and numeri-calGreens function fieldsolution inaplanemultilayeredmediumJournal of the Acoustical Society of America6792ndash105httpsdoiorg1011211383794

Doksaeligter L Handegard N O Godoslash O R Kvadsheim P H ampNordlund N (2012) Behavioural responses of captive herring tonaval sonar signals (1ndash16 kHz) throughout a yearly cycle Journal of the Acoustical Society of America 131 1632ndash1642 httpsdoiorg10112113675944

DolanTEPatrickWSampLinkJS(2016)Delineatingthecontinuumofmarineecosystem-basedmanagementAUSfisheries referencepoint perspective ICES Journal of Marine Science 73 1042ndash1050httpsdoiorg101093icesjmsfsv242

DolmanSJampJasnyM(2015)Evolutionofmarinenoisepollutionman-agementAquatic Mammals 41 357ndash374 httpsdoiorg101578AM4142015357

DoolingR JampLeekMR (2018)Communicationmaskingbyman-madenoiseInHSlabbekoornRJDoolingANPopperampRRFay(Eds)Effects of anthropogenic noise on animals Springer handbook of auditory research 66(pp23ndash46)NewYorkSpringerhttpsdoiorg101007978-1-4939-8574-6

Dragoset B (2005)A historical reflection on reflectionsThe Leading Edge2446ndash70httpsdoiorg10119012112392

DrinkwaterKF(2005)TheresponseofAtlanticcod(Gadus morhua)tofutureclimatechangeICES Journal of Marine Science621327ndash1337httpsdoiorg101016jicesjms200505015

DunlopRANoadMJMcCauleyRDKniestESladeRPatonDampCatoDH(2016)Responseofhumpbackwhales(Megaptera novaeangliae) to ramp-up of a small experimental airgun arrayMarine Pollution Bulletin 103 72ndash83 httpsdoiorg101016jmarpolbul201512044

Dutil J-D amp Lambert Y (2000) Naturalmortality from poor condi-tioninAtlanticcod(Gadus morhua)Canadian Journal of Fisheries and Aquatic Sciences57826ndash836httpsdoiorg101139f00-023

Edeline EHaugenTOWeltzien F-AClaessenDWinfield I JStensethNCampVoslashllestadLA(2009)Bodydownsizingcausedbynon-consumptivesocialstressseverelydepressespopulationgrowthrateProceedings of the Royal Society B277843ndash851

EngaringsALoslashkkeborgSOnaEampSoldalAV(1996)Effectsofseis-mic shooting on local abundance and catch rates of cod (Gadus morhua)andhaddock (Melanogrammus aeglefinus)Canadian Journal of Fisheries and Aquatic Sciences 53 2238ndash2249 httpsdoiorg101139f96-177

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EvansBJ(1997)A handbook for seismic data acquisition in exploration GeophysicalMonographSeriesNumber7(318p)DVFittermanampWHDragoset(Eds)SocietyofExplorationGeophysicists

Farcas A Thompson P M amp Merchant N D (2016) UnderwaternoisemodellingforenvironmentalimpactassessmentEnvironmental Impact Assessment Review 57 114ndash122 httpsdoiorg101016jeiar201511012

FarmerNABakerKZeddiesDADenesSLNorenDPGarrisonLPhellipZykovM(2018)Populationconsequencesofdisturbancebyoffshoreoilandgasactivityforendangeredspermwhales(Physeter macrocephalus) Biological Conservation 227 189ndash204 httpsdoiorg101016jbiocon201809006

Fay R R (1969) Behavioural audiogram for the goldfish Journal of Auditory Research9112ndash121

Fay R R (2009) Soundscapes and the sense of hear-ing of fishes Integrative Zoology 4 26ndash32 httpsdoiorg101111j1749-4877200800132x

FewtrellJLampMcCauleyRD(2012)ImpactofairgunnoiseonthebehaviourofmarinefishandsquidMarine Pollution Bulletin64984ndash993httpsdoiorg101016jmarpolbul201202009

FieldsDHandegardNODalenJEichnerCMaldeKKarlsenOslashhellipBrowmanH I (2019)Airgunblastsused inmarineseismicsurveyshaveaminoreffectonsurvivalatdistanceslessthan10mandnosublethaleffectsonbehaviourorgeneexpressionintheco-pepodCalanus finmarchicus ICES Journal of Marine Science(inpress)

FiksenOslashUtneACWAksnesDLEianeKHelvikJVampSundbyS(1998)ModellingtheinfluenceoflightturbulenceandontogenyoningestionratesinlarvalcodandherringFisheries Oceanography7355ndash363httpsdoiorg101046j1365-2419199800068x

FogartyMJ(2014)Theartofecosystem-basedfisherymanagementCanadian Journal of Fisheries and Aquatic Sciences 71 479ndash490httpsdoiorg101139cjfas-2013-0203

FogartyM J ampMurawski S A (1998) Large-scale disturbance andthestructureofmarinesystemsFisheryimpactsonGeorgesBankEcological Applications86ndash22httpsdoiorg1023072641359

Folkvord A Joslashrgensen C Korsbrekke K Nash R DM NilsenT amp Skjaeligraasen J E (2014) Trade-offs between growth andreproduction in wild Atlantic cod Canadian Journal of Fisheries and Aquatic Sciences 71 1106ndash1112 httpsdoiorg101139cjfas-2013-0600

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

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RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

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RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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32emsp |emsp emspensp SLABBEKOORN Et AL

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Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

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WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

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WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 27: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp27SLABBEKOORN Et AL

FrancisCDKleistNJOrtegaCPampCruzA(2012)Noisepollu-tion alters ecological services Enhanced pollination and disruptedseeddispersalProceedings of the Royal Society B Biological Sciences2792727ndash2735httpsdoiorg101098rspb20120230

FrancisCDOrtegaCPampCruzA(2009)CumulativeconsequencesofnoisepollutionNoisechangesaviancommunitiesandspeciesin-teractionsCurrent Biology191415ndash1419httpsdoiorg101016jcub200906052

FrankKTPetrieBChoiJSampLeggettWC(2005)Trophiccas-cadesinaformerlycod-dominatedecosystemScience3081621ndash1623httpsdoiorg101126science1113075

Frisk G V (2012) Noiseonomics The relationship between ambientnoiselevelsintheseaandglobaleconomictrendsScientific Reports2437httpsdoiorg101038srep00437

FriskCAndersenKHTemmingAHerrmanJPMadsenKSampKrausG (2015)Environmentaleffectsonsprat (Sprattus sprattus)physiology and growth at the distribution frontier A bioenergeticmodellingapproachEcological Modelling299130ndash139httpsdoiorg101016jecolmodel201411026

GisinerRC(2016)SoundandmarineseismicsurveysAcoustics Today1210ndash18

GordonJGillespieDPotterJFrantzisASimmondsMPSwiftRampThompsonD(2003)AreviewoftheeffectsofseismicsurveysonmarinemammalsMarine Technology Society Journal37 16ndash34httpsdoiorg104031002533203787536998

GoumltzTampJanikVM(2011)Repeatedelicitationoftheacousticstar-tle reflex leads tosensitisation insubsequentavoidancebehaviourandinducesfearconditioningBMC Neuroscience1230httpsdoiorg1011861471-2202-12-30

GrimmVRevillaEBergerUJeltschFMooijWMRailsbackSFhellipDeAngelisDL(2005)Patternorientedmodellingofagent-basedcomplex systems Lessons from ecology Science 310 987ndash991httpsdoiorg101126science1116681

GuerraAacuteGonzaacutelezAacuteFampRochaF(2004)Areviewoftherecordsof giant squid in the north-eastern Atlantic and severe injuries inArchiteuthis duxstrandedafteracousticexplorationsICES Journal of Marine Science20029

Halfwerk W amp Slabbekoorn H (2015) Pollution going multimodalThecompleximpactofthehuman-alteredsensoryenvironmentonanimalperceptionandperformanceBiology Letters11e20141051httpsdoiorg101098rsbl20141051

Halpern B SWalbridge S Selkoe K A Kappel C V Micheli FDAgrosaChellipWatsonR(2008)AglobalmapofhumanimpactonmarineecosystemsScience319948ndash952httpsdoiorg101126science1149345

HalvorsenMBCasperBMMatthewsFCarlsonTJampPopperAN(2012)Effectsofexposuretopile-drivingsoundsonthelakesturgeonNiletilapiaandhogchokerProceedings of the Royal Society B2794705ndash4714httpsdoiorg101098rspb20121544

HalvorsenMBCasperBMWoodleyCMCarlsonTJampPopperAN(2012)ThresholdforonsetofinjuryinChinooksalmonfromexposure to impulsive pile driving sounds PLoS ONE 7 e38968httpsdoiorg101371journalpone0038968

HammarLWikstroumlmAampMolanderS (2014)AssessingecologicalrisksofoffshorewindpoweronKattegatcodRenewable Energy66414ndash424httpsdoiorg101016jrenene201312024

HammillMOampStensonGB(2002)Estimated consumption of Atlantic cod (Gadus morhua) and some other prey by grey seals (Halichoerus grypus) and harp seals (Phoca groenlandica) in the southern Gulf of St Lawrence (NAFO Division 4T) Canadian Stock Assessment Secretariat Research Document2002054

Handegard N O Tronstad T V amp Hovem J M (2013) Evaluatingtheeffectof seismicsurveyson fishmdashTheefficacyofdifferentex-posuremetricstoexplaindisturbancerdquoCanadian Journal of Fisheries

and Aquatic Sciences 70 1271ndash1277 httpsdoiorg101139cjfas-2012-0465

HardingHRGordonTACHsuanREMackanessACERadfordANampSimpsonAD(2018)Fishinhabitatswithhighermotorboatdisturbance show reduced sensitivity to motorboat noise Biology Letters1420180441httpsdoiorg101098rsbl20180441

Harris C M Thomas L Falcone E A Hildebrand J Houser DKvadsheimPHhellipJanikVM(2018)MarinemammalsandsonarDose-responsestudiestherisk-disturbancehypothesisandtheroleofexposurecontextJournal of Applied Ecology20171ndash9

HarrisonCH (2013)Rayconvergence ina flux-likepropagation for-mulationThe Journal of the Acoustical Society of America1333777ndash3789httpsdoiorg10112114802642

HarrisonCH(2015)Efficientmodelingofrange-dependentraycon-vergence effects in propagation and reverberation The Journal of the Acoustical Society of America 137 2982ndash2985 httpsdoiorg10112114919335

Harwood JKing S SchickR SampDonovanC (2014)A draft pro-tocol for implementing the interim population consequences of distur-bance (PCOD) approach Assessing the effects of UK offshore renewable energy developments on marine mammal populations SMRUMarineReporttotheCrownEstateSMRULndashTCE-2013-014Scottish Marine and Freshwater Science 5

HarwoodJampStokesK(2003)Copingwithuncertaintyinecologicaladvice Lessons from fisheriesTrends in Ecology and Evolution18617ndash622httpsdoiorg101016jtree200308001

Hassel A Knutsen T Dalen J Skaar K Loslashkkeborg SMisundOAhellipHauglandEK (2004) Influenceof seismic shootingon thelessersandeel (Ammodytes marinus) ICES Journal of Marine Science611165ndash1173httpsdoiorg101016jicesjms200407008

HawkinsADampChapmanCJ(1975)MaskedauditorythresholdsinthecodGadus morhua L Journal of Comparative Physiology A103209ndash226httpsdoiorg101007BF00617122

Hawkins A D Pembroke A E amp Popper A N (2015) Informationgaps in understanding the effects of noise on fishes and inverte-bratesReviews in Fish Biology and Fisheries25 39ndash64httpsdoiorg101007s11160-014-9369-3

Hawkins A D Roberts L amp Cheesman S (2014) Responses offreeliving coastal pelagic fish to impulsive sounds Journal of the Acoustical Society of America 135 3101ndash3116 httpsdoiorg10112114870697

HawkinsADSoofianiNMampSmithGW(1985)Growthandfeed-ingofjuvenilecod(Gadus morhuaL)ICES Journal of Marine Science4211ndash32httpsdoiorg101093icesjms42111

HeathMRCullingMACrozierWWFoxCJGurneyWSCHutchinsonWFhellipCarvalhoGR(2013)Combinationofgeneticsandspatialmodellinghighlightsthesensitivityofcod(Gadus morhua)populationdiversityintheNorthSeatodistributionsoffishingICES Journal of Marine Science 71 794ndash807 httpsdoiorg101093icesjmsfst185

HeathMampGallegoA (1997) From thebiologyof the individual tothe dynamics of the population Bridging the gap in fish earlylife studies Journal of Fish Biology 51(Suppl A) 1ndash29 httpsdoiorg101111j1095-86491997tb06090x

HeinoMPauliBDampDieckmannU(2015)Fisheries-inducedevo-lutionAnnual Reviews of Ecology Evolution and Systematics46461ndash480httpsdoiorg101146annurev-ecolsys-112414-054339

HernandezKMRischDCholewiakDMDeanMJHatchLTHoffmanWShellipvanParijs SM (2013)AcousticmonitoringofAtlanticcod(Gadus morhua) inMassachusettsBayImplicationsformanagement and conservation ICES Journal of Marine Science70628ndash635httpsdoiorg101093icesjmsfst003

Heuschele J Mannerla M Gienapp P amp Candolin U (2009)Environment-dependent use of mate choice cues in sticklebacks

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

HilbornRampLiermannM(1998)StandingontheshouldersofgiantsLearning from experience in fisheries Reviews in Fish Biology and Fisheries8273ndash283httpsdoiorg101023A1008877912528

HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

HobdayAJSmithAWebbHDaleyRWayteSBulmanChellipWalkerT (2007)Ecological risk assessment for the effects of fishing methodology 174 p Report R041072 for the Australian FisheriesManagementAuthorityCanberraAustralia

Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

Parvulescu A (1964) Problems of propagation and processing InWN Tavolga (Ed) Marine bio-acoustics (pp 87ndash100) Oxford UKPergamonPress

ParvulescuA(1967)TheacousticsofsmalltanksInWNTavolga(Ed)Marine bio-acousticsVol2(pp7ndash13)OxfordUKPergamonPress

PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

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org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 28: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

28emsp |emsp emspensp SLABBEKOORN Et AL

Behavioral Ecology201223ndash1227httpsdoiorg101093behecoarp123

HiggsDMampRadfordCA(2013)ThecontributionofthelaterallinetohearinginfishJournal of Experimental Biology2161484ndash1490

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HildebrandJA(2009)AnthropogenicandnaturalsourcesofambientnoiseintheoceanMarine Ecology Progress Series3955ndash20httpsdoiorg103354meps08353

Hirst A amp Rodhouse P (2000) Impacts of geophysical seismic sur-veying on fishing successReviews in Fish Biology and Fisheries10113ndash118httpsdoiorg101023A1008987014736

HjermannDOslashBogstadBEikesetAMOttersenGGjoslashsaeligterHampStensethNC(2007)FoodwebdynamicsaffectNortheastArcticcodrecruitmentProceedings of the Royal Society London B274661ndash669httpsdoiorg101098rspb20060069

HobdayAJSmithAampStobutzkiI(2004)Ecological risk assessment for Australian Commonwealth fisheriesfinalreportReportR010934to the Australian Fisheries Management Authority CanberraAustralia72p

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Hovem JM Tronstad T V Karlsen H E amp Loslashkkeborg S (2012)Modelingpropagationofseismicairgunsoundsandtheeffectsonfish behaviour IEEE Journal of Oceanic Engineering 37 576ndash588httpsdoiorg101109JOE20122206189

HubertJCampbellJvanderBeekJGdenHaanMFVerhaveRVerkadeLSampSlabbekoornH(2018)EffectsofbroadbandsoundexposureontheinteractionbetweenforagingcrabandshrimpndashAfield study Environmental Pollution 243 1923ndash1929 httpsdoiorg101016jenvpol201809076

HutchingsJABishopTDampMcGregor-ShawCR(1999)SpawningbehaviourofAtlanticcodGadus morhuaEvidenceofmatecompetitionandmatechoiceinabroadcastspawnerCanadian Journal of Fisheries and Aquatic Sciences5697ndash104httpsdoiorg101139f98-216

ISO 2017 ISO 18405 underwater acoustics mdash Terminology April (2017)Retrievedfromhttpswwwisoorgstandard62406html

Jager T amp Klok C (2010) Extrapolating toxic effects on individu-als to the population level The role of dynamic energy budgetsPhilosophical Transaction of the royal Society B 265 3531ndash3540httpsdoiorg101098rstb20100137

Jensen F B Kuperman W A Porter M B amp Schmidt H (2011)Computational ocean acoustics New York NY Springer Science ampBusinessMedia

JonesFC (2016)CumulativeeffectsassessmentTheoreticalunder-pinnings and big problems Environmental Reviews 24 187ndash204httpsdoiorg101139er-2015-0073

JorgensenJKampGyselmanEC(2009)Hydroacousticmeasurementsof thebehavioural responseofarctic riverine fishes toseismicair-guns Journal of the Acoustical Society of America126 1598ndash1606httpsdoiorg10112113177276

KalmijnAJ(1997)Electricandnear-fieldacousticdetectionacompar-ativestudyActa Physiologica Scandinavica16125ndash38

KasteleinRAJenningsNKommerenAHelder-HoekLampSchopJ (2017) Acoustic dose-behavioural response relationship in seabass (Dicentrarchus labrax) exposed to playbacks of pile drivingsoundsMarine Environmental Research 130 315ndash324 httpsdoiorg101016jmarenvres201708010

KellLTPillingGMampOBrienCA(2005)ImplicationsofclimatechangeforthemanagementofNorthSeacod(Gadus morhua)ICES Journal of Marine Science621483ndash1491httpsdoiorg101016jicesjms200505006

Kenyon TN Ladich F amp YanH Y (1998) A comparative study ofhearing abilities in fishes The auditory brainstem response ap-proachJournal of Comparative Physiology A182307ndash318httpsdoiorg101007s003590050181

KhodabandelooBLandroslashMampHanssenA (2017)Acousticgener-ation of underwater cavitiesmdashComparing modeled and measuredacoustic signals generated by seismic air gun arrays The Journal of the Acoustical Society of America 141 2661ndash2672 httpsdoiorg10112114979939

KightCRampSwaddleJP(2011)HowandwhyenvironmentalnoiseimpactsanimalsAnintegrativemechanisticreviewEcology Letters141052ndash1061httpsdoiorg101111j1461-0248201101664x

King S L Schick R S Donovan C Booth C G BurgmanM Thomas L amp Harwood J (2015) An interim frameworkfor assessing the population consequences of disturbanceMethods in Ecology and Evolution 6 1150ndash1158 httpsdoiorg1011112041-210X12411

KooijmanSALM (2000)Dynamic energy mass budgets in biological systemsCambridgeUKUniversityPresshttpsdoiorg101017CBO9780511565403

KooijmanSALM(2010)Dynamic energy budget theory for metabolic organisation3rdednCambridgeUKUniversityPress

Koolhaas JM Korte SM De Boer S F vanDer Vegt B J vanReenenCGHopsterHhellipBlokhuisH J (1999)Coping stylesin animals Current status in behaviour and stress-physiologyNeuroscience amp Biobehavioural Reviews 23 925ndash935 httpsdoiorg101016S0149-7634(99)00026-3

KoumlsterFWampMoumlllmannC(2000)TrophodynamiccontrolbyclupeidpredatorsonrecruitmentsuccessinBalticcodICES Journal of Marine Science57310ndash323httpsdoiorg101006jmsc19990528

KoumlsterFWMoumlllmannCHinrichsenHHWielandKTomkiewiczJ Kraus G hellip Beyer J E (2005) Baltic cod recruitment Theimpact of climate variability on key processes ICES Journal of Marine Science 62 1408ndash1425 httpsdoiorg101016jicesjms200505004

Kostyuchenko L P (1973) Effects of elasticwaves generated inma-rineseismicprospectingonfisheggsintheBlackSeaHydrobiology Journal945ndash48

KuncHPLyonsGNSigwartJDMcLaughlinKEampHoughtonJ (2014) Anthropogenic noise affects behavior across sen-sory modalities American Naturalist 184 E93ndashE100 httpsdoiorg101086677545

KuncHPMcLaughlinKEampSchmidtR(2016)Aquaticnoisepol-lution Implications for individuals populations and ecosystemsProceedings of the Royal Society B Biological Sciences28320160839httpsdoiorg101098rspb20160839

LadichF (2008)Soundcommunication in fishesand the influenceofambientandanthropogenicnoiseBioacoustics1735ndash37

LadichF(2014)FishbioacousticsCurrent Opinions in Neurobiology28121ndash127httpsdoiorg101016jconb201406013

LadichFampFayRR(2013)AuditoryevokedpotentialaudiometryinfishReviews in Fish Biology and Fisheries23 317ndash364 httpsdoiorg101007s11160-012-9297-z

LandroslashMampAmundsenL(2018)Introduction to exploration geophysics with recent advancesRigaLatviaBivrost

Laws R M amp Hedgeland D (2008) The marine seismic airgunBioacoustics17124ndash127httpsdoiorg1010800952462220089753788

Lika K KearneyM R ampKooijman S A LM (2011) The lsquocovaria-tionmethodrsquoforestimatingtheparametersofthestandardDynamicEnergy Budget model II Properties and preliminary patternsJournal of Sea Research 66 278ndash288 httpsdoiorg101016jseares201109004

LillyGRWielandKRothschildB JSundbySDrinkwaterKFBranderKhellipVaacutezquezA(2008)DeclineandrecoveryofAtlantic

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cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

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emspensp emsp | emsp31SLABBEKOORN Et AL

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Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

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RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

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RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

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32emsp |emsp emspensp SLABBEKOORN Et AL

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the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

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VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

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Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

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Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

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WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 29: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp29SLABBEKOORN Et AL

cod(Gadus morhua)stocksthroughouttheNorthAtlanticInSGHKruseKDrinkwaterJNIanelliJSLinkDLStramVWespestadampDWoodby (Eds)Resiliency of gadid stocks to fishing and climate change(pp39ndash66)FairbanksALAlaskaSeaGrantProgramhttpsdoiorg104027rgsfcc2008

Lindegren M Moumlllmann C Nielsen A Brander K MacKenzie BR amp Stenseth N C (2010) Ecological forecasting under climatechangeThecaseofBalticcodProceedings of the Royal Society B2772121ndash2130

Lindegren M Moumlllmann C Nielsen A amp Stenseth N C (2009)PreventingthecollapseoftheBalticcodstockthroughanecosystem-basedmanagementapproachProceedings of the National Academy of Sciences of the United States of America10614722ndash14727httpsdoiorg101073pnas0906620106

LiuHFogartyMJGlaserSMAltmanIKaufmanLRosenbergA A amp Sugihara G (2012) Nonlinear dynamic features and co-predictabilityof theGeorgesBank fishcommunityMarine Ecology Progress Series464195ndash207httpsdoiorg103354meps09868

LiuKFRLiangHHChenCWChenJSampShenYS(2012b)Combining scientific facts and significance criteria to predict theresult of an environmental impact assessment review Journal of Environmental Informatics1993ndash107

LoslashkkeborgS(1991)Effects of a geophysical survey on catching success in longline fishing ICES CM 1991B 40 9 p

LoslashkkeborgSOnaEVoldAampSalthaugA(2012)Soundsfromseis-mic airgunsGear- and species-specific effects on catch rates andfish Canadian Journal of Fisheries and Aquatic Sciences 69 1278ndash1291httpsdoiorg101139f2012-059

LoslashkkeborgSampSoldalAV(1993)Theinfluenceofseismicexplorationwithairgunsoncod(Gadus morhua)behaviourandcatchratesICES Marine Science Symposium19662ndash67

LoughRGBuckleyLJWernerFEQuinlanJAampEdwardsKP(2005)Ageneralbiophysicalmodeloflarvalcod(Gadus morhua)growthappliedtopopulationsonGeorgesBankFisheries Oceanography14241ndash262httpsdoiorg101111j1365-2419200500330x

LusseauDNewLDonovanCCheneyBHastieGampHarwood J(2011)The development of a framework to understand and predict the pop-ulation consequences of disturbances for the Moray Firth bottlenose dolphin population Scottish Natural Heritage Commissioned Report No 468

Mace P (2001) A new role forMSY in single-species and ecosystemapproachestofisheriesstockassessmentandmanagementFish and Fisheries22ndash32httpsdoiorg101046j1467-2979200100033x

MacKenzie B R Gislason HMoumlllmann C amp Koumlster FW (2007)Impactof21stcenturyclimatechangeontheBalticSeafishcommu-nityandfisheriesGlobal Change Biology131348ndash1367httpsdoiorg101111j1365-2486200701369x

MacKenzie S Ribas L Pilarczyk M Capdevila D M Kadri S ampHuntingfordFA (2009)Screening forcopingstyle increases thepowerofgeneexpressionstudiesPLoS ONE4e5314httpsdoiorg101371journalpone0005314

MalmeC I SmithPWampMiles PR (1986)Study of the effects of offshore geophysical acoustic survey operations on important com-mercial fisheries in California Technical Report No 1 Report No6125 Contract No MMS 14-12-0001-30273 Prepared by BBNLaboratories Inc Cambridge Mass for Battelle Ventura OfficeCAUSA92p

MartinTGBurgmanMAFidlerFKuhnertPM Low-ChoySMcBrideMampMengersenK(2012)Elicitingexpertknowledgeinconservation science Conservation Biology 26 29ndash38 httpsdoiorg101111j1523-1739201101806x

MartinBTJagerTNisbetRMPreussTGampGrimmV(2013)Predictingpopulationdynamics from thepropertiesof individualsAcross-level testofDynamicEnergyBudget theoryThe American Naturalist181506ndash519httpsdoiorg101086669904

MaruskaKPampSisnerosJA(2016)Comparisonofelectrophysiolog-icalauditorymeasures in fishes InJASisneros (Ed)Fish hearing and bioacoustics An anthology in honor of Arthur N Popper and Richard R Fay Advances in experimental medicine and biology (pp227ndash254)NewYorkNYSpringer

McCauleyRDDayRDSwadlingKMFitzgibbonQPWatsonREampSemmensJM(2017)Widelyusedmarineseismicsurveyairgunoperationsnegatively impactzooplanktonNature Ecology amp Evolution10195httpsdoiorg101038s41559-017-0195

McCauley RD Fewtrell J Duncan A J Jenner C JennerM-NPenrose J D hellipMcCabe K (2000) Marine seismic surveys ndash astudy of environmental implications The APPEA Journal 40 692ndash706httpsdoiorg101071AJ99048

McCauleyRDFewtrellJampPopperAN(2003)Highintensityan-thropogenicsounddamagesfishearsJournal of the Acoustical Society of America113638ndash642httpsdoiorg10112111527962

McCullyPhillipsSRScottFampEllisJR(2015)Havingconfidencein productivity susceptibility analysesAmethod for underpinningscientific advice on skate stocks Fisheries Research 171 87ndash100httpsdoiorg101016jfishres201501005

McDonaldMAHildebrandJAampWigginsSM (2006) Increasesindeepoceanambientnoise in theNortheastPacificwestof SanNicolasIslandCaliforniaJournal of the Acoustical Society of America120711ndash718httpsdoiorg10112112216565

McMahonCRBurtonHRampBesterMN (2000)WeaningmassandthefuturesurvivalofjuvenilesouthernelephantsealsMirounga leoninaatMacquarieIslandAntarctic Science12149ndash153

McMahonCRBurtonHRampBesterMN(2003)Ademographiccom-parisonoftwoelephantsealpopulationsJournal of Animal Ecology7261ndash74httpsdoiorg101046j1365-2656200300685x

Megrey B A Rose K A Klumb R A Hay D E Werner F EEslingerDLampSmithS L (2007)Abioenergetics-basedpop-ulationdynamicsmodelofPacificherring(Clupea harengus pallasi)coupled to a lower trophic level nutrientndashphytoplanktonndashzoo-planktonmodelDescriptioncalibrationandsensitivityanalysisEcological Modelling 202 144ndash164 httpsdoiorg101016jecolmodel200608020

Merchant N D (2019) Underwater noise abatement Economic fac-torsandpolicyoptionsEnvironmental Science amp Policy92116ndash123httpsdoiorg101016jenvsci201811014

MetcalfeJDWrightSTudoracheCampWilsonRP(2016)RecentadvancesintelemetryforestimatingtheenergymetabolismofwildfishesJournal of Fish Biology88284ndash297httpsdoiorg101111jfb12804

Midwood J D LarsenM H BoelM Jepsen N Aarestrup K ampCookeSJ (2014)Doescortisolmanipulationinfluenceoutmigra-tionbehavioursurvivalandgrowthofseatroutAfieldtestofcarry-overeffectsinwildfishMarine Ecology Progress Series496135ndash144httpsdoiorg103354meps10524

MillerPJOAntunesRNWensveenPJSamarraF IPAlvesACTyackPLhellipThomasL(2014)Dose-responserelationshipsfor the onset of avoidance of sonar by free-ranging killer whalesJournal of the Acoustical Society of America135975ndash993httpsdoiorg10112114861346

Miller IampCrippsE (2013)ThreedimensionalmarineseismicsurveyhasnomeasurableeffectonspeciesrichnessorabundanceofacoralreefassociatedfishcommunityMarine Pollution Bulletin7763ndash70httpsdoiorg101016jmarpolbul201310031

MiltonDA (2001)Assessing the susceptibility to fishingof popula-tionsofraretrawlbycatchSeasnakescaughtbyAustraliasnorth-ernprawnfisheryBiological Conservation101281ndash290httpsdoiorg101016S0006-3207(00)00232-9

Montgomery JC JeffsA Simpson SDMeekanMampTindleC(2006) Sound as an orientation cue for the pelagic larvae of reef

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

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NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

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PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

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PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

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PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

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Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

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Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

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SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

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SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

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SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 30: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

30emsp |emsp emspensp SLABBEKOORN Et AL

fishesanddecapodcrustaceansAdvances in Marine Biology51143ndash196httpsdoiorg101016S0065-2881(06)51003-X

MorganMJRideoutRMampColbourneEB(2010)Impactofenvi-ronmentaltemperatureonAtlanticcodGadus morhuaenergyalloca-tiontogrowthconditionandreproductionMarine Ecology Progress Series404185ndash195httpsdoiorg103354meps08502

MorganMJWilsonCEampCrimLW(1999)TheeffectsofstressonreproductioninAtlanticcodJournal of Fish Biology54477ndash488httpsdoiorg101111j1095-86491999tb00629x

MunozNEampBlumsteinDT(2012)Multisensoryperceptioninun-certainenvironmentsBehavioral Ecology23 457ndash462httpsdoiorg101093behecoarr220

Nabe-Nielsen J Sibly RM Tougaard J Teilmann J amp SveegaardS (2014) Effects of noise and by-catch on aDanish harbour por-poise population Ecological Modelling 272 242ndash251 httpsdoiorg101016jecolmodel201309025

NationalResearchCouncil(2005)Marine mammal populations and ocean noise determining when noise causes biologically significant effects WashingtonDCNationalAcademicPress126ppRetrieved fromhttpwwwnapeducatalog11147html

NedelecSLRadfordANPearlLMcCormickMIMeekanMGampSimpsonSD(2017)MotorboatnoiseimpactsparentalbehaviourandoffspringsurvivalinareeffishProceedings of the Royal Society B28420170143httpsdoiorg101098rspb20170143

Neo Y Y Hubert J Bolle L Winter H V amp Slabbekoorn H(2018) European seabass respond more strongly to noise expo-sureatnightandhabituateoverrepeatedtrialsofsoundexposureEnvironmental Pollution 239 367ndash374 httpsdoiorg101016jenvpol201804018

NeoYYHubertJBolleLWinterHVtenCateCampSlabbekoornH(2016)SoundexposurechangesEuropeanseabassbehaviourina large outdoor floating pen Effects of temporal structure and aramp-upprocedureEnvironmental Pollution21426ndash34httpsdoiorg101016jenvpol201603075

Neo Y Y Seitz J Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2014) Temporal structure of sound affectsbehavioural recovery from noise impact in European seabassBiological Conservation 178 65ndash73 httpsdoiorg101016jbiocon201407012

Neo Y Y Ufkes E Kastelein R A Winter H V ten Cate C ampSlabbekoorn H (2015) Impulsive sounds change European sea-bass swimming patterns Influence of pulse repetition intervalMarine Pollution Bulletin 97 111ndash117 httpsdoiorg101016jmarpolbul201506027

Neuenfeldt S amp Koumlster FW (2000) Trophodynamic control on re-cruitmentsuccess inBalticcodThe influenceofcannibalism ICES Journal of Marine Science 57 300ndash309 httpsdoiorg101006jmsc20000647

NewLFClarkJSCostaDPFleishmanEHindellMAKlanjščekThellipHarwoodJ(2014)Usingshort-termmeasuresofbehaviourtoestimatelong-termfitnessofsouthernelephantsealsMarine Ecology Progress Series49699ndash108httpsdoiorg103354meps10547

NewLFMorettiD JHookerSKCostaDPampSimmonsSE(2013)Usingenergeticmodelstoinvestigatethesurvivalandrepro-ductionofbeakedwhales (familyZiphiidae)PLoS ONE8 e68725httpsdoiorg101371journalpone0068725

NewmanKBBucklandSTLindleySTThomasLampFernandezC (2006)Hiddenprocessmodels foranimalpopulationdynamicsEcological Applications1674ndash86httpsdoiorg10189004-0592

NicholsTAAndersonTWampSirovicA (2015) Intermittentnoiseinducesphysiologicalstress inacoastalmarinefishPLoS ONE10e0139157httpsdoiorg101371journalpone0139157

Nichols J D amp Williams B K (2006) Monitoring for conserva-tion Trends in Ecology and Evolution 21 668ndash673 httpsdoiorg101016jtree200608007

NieukirkSLMellingerDKMooreSEKlinckKDziakRPampGoslinJ(2012)Soundsfromairgunsandfinwhalesrecordedinthemid-AtlanticOcean1999ndash2009Journal of the Acoustical Society of America1311102ndash1112httpsdoiorg10112113672648

Nisbet R M Muller E B Lika K amp Kooijman S A L M (2000)From molecules to ecosystems through dynamic energy bud-get models Journal of Animal Ecology 69 913ndash926 httpsdoiorg101046j1365-2656200000448x

Normandeau Associates (2012) Effects of noise on fish fisheries and invertebrates in the US atlantic and arctic from energy industry sound-generating activitiesALiteratureSynthesisfortheUSDeptof the Interior Bureau of Ocean Energy Management Retrievedfromhttpmhkpnnlgovwikiimages880

Nowacek D P Clark C W Mann D Miller P J O RosenbaumH C Golden J S hellip Southall B L (2015) Marine seismic sur-veysandoceannoiseTime forcoordinatedandprudentplanningFrontiers in Ecology and the Environment 13 378ndash386 httpsdoiorg101890130286

OConnor C M Gilmour K M Arlinghaus R Hasler C TPhilipp D P amp Cooke S J (2010) Seasonal carryover effectsfollowing the administration of cortisol to a wild teleost fishPhysiological and Biochemical Zoology 83 950ndash957 httpsdoiorg101086656286

OConnorCMGilmourKMArlinghausRMatsumuraSSuskiCDPhilippDPampCookeSJ(2011)Theconsequencesofshort-termcortisolelevationonindividualphysiologyandgrowthrate inwild largemouth bass (Micropterus salmoides) Canadian Journal of Fisheries and Aquatic Sciences68693ndash705httpsdoiorg101139f2011-009

Olsen E M Ottersen G Llope M Chan K-S Beaugrand G ampStensethNC(2011)SpawningstockandrecruitmentinNorthSeacodshapedbyfoodandclimateProceedings of the Royal Society B278504ndash510httpsdoiorg101098rspb20101465

OslashverliOslashSorensenCPulmanKGTPottingerTGKorzanWJSummers CHampNilssonG E (2007) Evolutionary backgroundfor stress-coping styles Relationships between physiological be-havioural and cognitive traits in non-mammalian vertebratesNeuroscience amp Biobehavioural Reviews 31 396ndash412 httpsdoiorg101016jneubiorev200610006

Parkes G E amp Hatton L (1986) The marine seismic source (p 114)DordrechtNetherlandsDReidelPublishingCompanyhttpsdoiorg101007978-94-017-3385-4

ParkesGEHattonLampHauglandT(1984)Marinesourcearraydi-rectivityAnewwideairgunarraysystemFirst Break29ndash15

ParryGDampGasonA(2006)TheeffectofseismicsurveysoncatchratesofrocklobstersinwesternVictoriaAustraliaFisheries Research79272ndash284httpsdoiorg101016jfishres200603023

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PatrickW S Spencer P Link JCope J Field JKobayashiDhellipOverholtzW (2010)Usingproductivity and susceptibility indicestoassessthevulnerabilityofUnitedStatesfishstockstooverfishingFisheries Bulletin108305ndash322

PatrickWSSpencerPOrmsethOCopeJFieldJKobayashiDhellipLawsonP(2009)Use of productivity and susceptibility indices to de-termine stock vulnerability with example applications to six US fisher-iesUSDepCommerNOAATechMemoNMFS-FSPO-10190p

Pauly D (1996) One hundred million tonnes of fish and fish-eries research Fisheries Research 25 25ndash38 httpsdoiorg1010160165-7836(95)00436-X

PaxtonABTaylorJCNowacekDCDaleJColeEVossCMampPetersonCH(2017)Seismicsurveynoisedisruptedfishuseof

emspensp emsp | emsp31SLABBEKOORN Et AL

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PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

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Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

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Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

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RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

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Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

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Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

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mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

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SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

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SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

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SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

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ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

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Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 31: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp31SLABBEKOORN Et AL

atemperatereefMarine Policy7868ndash73httpsdoiorg101016jmarpol201612017

PearsonWHSkalski JRampMalmeC I (1992)Effectsof soundsfromageophysical surveydeviceonbehaviourofcaptive rockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences491343ndash1356httpsdoiorg101139f92-150

Pecquerie L Petitgasa P amp Kooijman S A LM (2009)Modelingfish growth and reproduction in the context of the DynamicEnergyBudgettheorytopredictenvironmentalimpactonanchovyspawningdurationJournal of Sea Research6293ndash105httpsdoiorg101016jseares200906002

PentildeaHHandegardNOampOnaE(2013)Feedingherringschoolsdonot react to seismicairgunsurveys ICES Journal of Marine Science701174ndash1180

PengCZhaoXampLiuG(2015)Noiseintheseaanditsimpactsonmarine organisms International Journal of Environmental Research and Public Health 12 12304ndash12323 httpsdoiorg103390ijerph121012304

Persson L Leonardsson K de Roos A M Gyllenberg M ampChristensen B (1998) Ontogenetic scaling of foraging rates andthe dynamics of a size-structured consumer-resource modelTheoretical Population Biology54270ndash293httpsdoiorg101006tpbi19981380

Popper A N amp Fay R R (2011) Rethinking sound detection byfishes Hearing Research 273 25ndash36 httpsdoiorg101016jheares200912023

PopperANampHastingsMC (2009)Theeffectsofanthropogenicsources of sound on fishes Journal of Fish Biology 75 455ndash489httpsdoiorg101111j1095-8649200902319x

PopperANHawkinsADFayRRMannDABartolSCarlsonT J hellip Halvorsen M B (2014) ASA S3SC14 TR-2014 SoundExposureGuidelinesforFishesandSeaTurtlesATechnicalReportprepared by ANSI-Accredited Standards Committee S3SC1 andregistered with ANSI SpringerBriefs in Oceanography httpsdoiorg101007978-3-319-06659-2_2 copy Acoustical Society ofAmerica

Popper A N Smith M E Cott P A Hanna B W MacGillivrayAOAustinMEampMannDA (2005) Effectsof exposure toseismic airgun use on hearing of three fish species Journal of the Acoustical Society of America 117 3958ndash3971 httpsdoiorg10112111904386

PorterMB(1995)The KRAKEN normal mode programNavalResearchLaboratory

PoumlrtnerHOBerdalBBlustBBrixOColisimoADeWachterB hellip Zakhartsev M (2001) Climate induced temperature ef-fectsongrowthperformancefecundityandrecruitment inmarinefishDevelopingahypothesis for causeandeffect relationships inAtlanticcod(Gadus morhua)andcommoneelpout(Zoarces viviparus)Continental Shelf Research211975ndash1997httpsdoiorg101016S0278-4343(01)00038-3

Przeslawski R Huang Z Anderson J Carroll A G EdmundsM Hurt L amp Williams S (2018) Multiple field-based methodsto assess the potential impacts of seismic surveys on scallopsMarine Pollution Bulletin 129 750ndash761 httpsdoiorg101016jmarpolbul201710066

Purser J amp Radford A N (2011) Acoustic noise induces attentionshifts and reduces foraging performance in three-spined stickle-backs (Gasterosteus aculeatus) PLoS ONE 6 e17478 httpsdoiorg101371journalpone0017478

RadfordANKerridgeEampSimpsonSD (2014)Acousticcommu-nication in a noisy world Can fish compete with anthropogenicnoiseBehavioural Ecology251022ndash1030httpsdoiorg101093behecoaru029

RadfordANLefegravebreLLecaillonGNedelecSLampSimpsonSD(2016)Repeatedexposurereducestheresponsetoimpulsivenoise

inEuropeanseabassGlobal Change Biology223349ndash3360httpsdoiorg101111gcb13352

Radford C A Montgomery J C Caiger P amp Higgs D M (2012)Pressure and particle motion detection thresholds in fish Are-examination of salient auditory cues in teleosts Journal of Experimental Biology 215 3429ndash3435 httpsdoiorg101242jeb073320

Rankin C H Abrams T Barry R J Bhatnagar S Clayton D FColomboJhellipMarslandS(2009)HabituationrevisitedAnupdatedandreviseddescriptionofthebehaviouralcharacteristicsofhabitu-ationNeurobiology of Learning amp Memory92135ndash138httpsdoiorg101016jnlm200809012

RindorfAampLewyP(2006)WarmwindywintersdrivecodnorthandhomingofspawnerskeepsthemthereJournal of Applied Ecology43445ndash453httpsdoiorg101111j1365-2664200601161x

Rogers P H Popper A N HastingsM C amp SaidelWM (1988)Processingof acoustic signals in theauditory systemofbony fishJournal of the Acoustical Society of America83338ndash349httpsdoiorg1011211396444

RogersPHampZeddiesDG(2009)Multipolemechanismsfordirec-tionalhearinginfishInJFWebbANPopperampRRFay(Eds)Fish bioacoustics Springer handbook of auditory research(pp233ndash252)NewYorkNYSpringerScience+BusinessMedia

Rosa P ampKoperN (2018) Integratingmultiple disciplines to under-stand effects of anthropogenic noise on animal communicationEcosphere9e02127httpsdoiorg101002ecs22127

RosenbergAAgnewDBabcockECooperAMorgensenCOBoyleRhellipSwaseyJ(2007)Setting annual catch limits for US fisheries An expert working group reportMRAGAmericasWashingtonDC36p

Rossington K Benson T Lepper P amp Jones D (2013) Eco-hydro-acousticmodelinganditsuseasanEIAtoolMarine Pollution Bulletin75235ndash243httpsdoiorg101016jmarpolbul201307024

RungeMCConverseSJampLyonsJE(2011)WhichuncertaintyUsing expert elicitation and expected value of information to de-signanadaptiveprogramBiological Conservation1441214ndash1223httpsdoiorg101016jbiocon201012020

SamsonJEMooneyTAGusseklooSWSampHanlonRT(2014)Gradedbehavioralresponsesandhabituationtosoundinthecom-moncuttlefishSepia officinalis Journal of Experimental Biology2174347ndash4355httpsdoiorg101242jeb113365

SandOampEngerPS(1973)EvidenceforanauditoryfunctionoftheswimbladderinthecodJournal of Experimental Biology59405ndash414

SandDM EngerP SKarlsenHEKnudsen FampKvernstuenT(2000)Avoidance responses to infrasound in downstreammigrat-ingEuropean silver eelsAnguilla anguillaEnvironmental Biology of Fishes57327ndash336

SandOampHawkinsAD(1973)Acousticprpertiesofthecodswim-bladder Journal of Experimental Biology58797ndash820

SandOampKarlsenHE(1986)DetectionofinfrasoundbytheAtlanticcod Journal of Experimental Biology125197ndash204

Sand O amp Karlsen H E (2000) Detection of infrasound and lin-ear acceleration in fish Philosophical Transactions of the Royal Society London B 355 1295ndash1298 httpsdoiorg101098rstb20000687

Santulli AModica AMessina C Ceffa L Curatolo A Rivas GhellipDAmelioV (1999)Biochemical responsesofEuropeanseabass(Dicentrarchus labrax L) to the stress inducedbyoff shore experi-mentalseismicprospectingMarine Pollution Bulletin381105ndash1114httpsdoiorg101016S0025-326X(99)00136-8

SapolskyRMRomeroLMampMunckAU(2000)Howdoglucocor-ticoidsinfluencestressresponsesIntegratingpermissivesuppres-sive stimulatory andpreparativeactionsEndocrinological Reviews2155ndash89

SavenkoffCCastonguayMChabotD FreacutechetAHammillMOampMorissette L (2006)Main prey and predators and estimates of

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 32: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

32emsp |emsp emspensp SLABBEKOORN Et AL

mortalityofAtlanticcod (Gadus morhua) in thenorthernGulfofStLawrenceduringthemid-1980smid-1990sandearly2000sCanadian Technical Report of Fisheries and Aquatic Sciences2666vi+32pp

SchellartNAMampMunckJC(1987)Amodelfordirectionalanddis-tancehearinginswimbladder-bearingfishbasedonthedisplacementorbitsofthehaircellsJournal of the Acoustical Society of America82822ndash829httpsdoiorg1011211395280

SchickRSKrausSDRollandRMKnowltonARHamiltonPKPettisHMhellipClarkJS (2013a)UsinghierarchicalBayestounderstandmovementhealthandsurvivalintheendangerednorthAtlanticrightwhalePLoS ONE8e64166httpsdoiorg101371journalpone0064166

SchickRSNewLFThomasLCostaDPHindellMAMcMahonCRampClarkJS(2013b)Estimatingresourceacquisitionandat-seabodyconditionofamarinepredatorJournal of Animal Ecology821300ndash1315httpsdoiorg1011111365-265612102

SchmidtH(1987)SAFARI (Seismo-acoustic fast field algorithm for range independent environments)Usersguide

SchreckCB(1990)Physiologicalbehaviouralandperformanceindi-catorsofstressAmerican Fisheries Society Symposium829ndash37

SchuijfA (1975)Directionalhearingofcod (Gadus morhua)underap-proximatefreefieldconditionsJournal of Comparative Physiology98307ndash332httpsdoiorg101007BF00709803

SchuijfAampBuwaldaRJA(1975)Onthemechanismofdirectionalhearing incod(Gadus morhuaL)Journal of Comparative Physiology98333ndash343httpsdoiorg101007BF00709804

SchuijfAampHawkinsAD(1983)AcousticdistancediscriminationbythecodNature302143ndash144httpsdoiorg101038302143a0

SchwalbeM A Bassett D K ampWebb J F (2012) Feeding in thedark Lateral-line-mediated prey detection in the peacock cichlidAulonocara stuartgranti Journal of Experimental Biology2152060ndash2071httpsdoiorg101242jeb065920

Sertlek H Ouml (2016)Aria of the Dutch North Sea PhD-thesis LeidenUniversitytheNetherlands

SertlekHOumlampAinslieMA (2015)AGORA Airgun source signature model its application for seismic survey maps in the North Sea UAC Conference ProceedingsGreece

Sertlek H Ouml Slabbekoorn H ten Cate C amp AinslieM A (2019)SourcespecificsoundmappingSpatialtemporalandspectraldistri-butionofsoundintheDutchNorthSeaEnvironmental Pollution2471143ndash1157httpsdoiorg101016jenvpol201901119

Shafiei Sabet S Neo Y Y amp Slabbekoorn H (2015) The effect oftemporalvariationinsoundexposureonswimmingandforagingbe-haviourofcaptivezebrafishAnimal Behaviour10749ndash60httpsdoiorg101016janbehav201505022

ShafieiSabetSvanDoorenDampSlabbekoornH(2016)Sonetlum-iere Sound and light effects on spatial distribution and swimmingbehaviorincaptivezebrafishEnvironmental Pollution212480ndash488httpsdoiorg101016jenvpol201602046

ShannonGMcKennaMFAngeloniLMCrooksKRFristrupKMBrownEhellipMcFarlandS (2016)Asynthesisof twodecadesofresearchdocumentingtheeffectsofnoiseonwildlifeBiological Reviews91982ndash1005httpsdoiorg101111brv12207

Sibert J R Hampton J Fournier D A amp Bills P J (1999) An ad-vectionndashdiffusionndashreactionmodel for theestimationof fishmove-ment parameters from tagging data with application to skipjacktuna(Katsuwonus pelamis)Canadian Journal of Fisheries and Aquatic Sciences56925ndash938

Sierra-Flores R Atack TMigaud H amp Davie A (2015) Stress re-sponse to anthropogenic noise in Atlantic cod Gadus morhua LAquacultural Engineering 67 67ndash76 httpsdoiorg101016jaquaeng201506003

SimpsonSDPurserJampRadfordAN(2015)AnthropogenicnoisecompromisesantipredatorbehaviourinEuropeaneelsGlobal Change Biology21586ndash593httpsdoiorg101111gcb12685

SimpsonSDRadfordANNedelecSLFerrariMOChiversDPMcCormickMIampMeekanMG(2016)AnthropogenicnoiseincreasesfishmortalitybypredationNature Communications71ndash7

Sivle L D Kvadsheim P H amp Ainslie M A (2014) Potential forpopulation-leveldisturbancebyactivesonarinherringICES Journal of Marine Science 72 558ndash567 httpsdoiorg101093icesjmsfsu154

SkalskiJRPearsonWHampMalmeCI(1992)Effectsofsoundfromageophysicalsurveydeviceoncatch-per-unit-effortinahook-and-linefisheryforrockfish(Sebastesspp)Canadian Journal of Fisheries and Aquatic Sciences 49 1357ndash1365 httpsdoiorg101139f92-151

Slabbekoorn H (2016) Aiming for progress in understanding under-water noise impact on fish Complementary need for indoor andoutdoorstudiesInANPopperampADHawkins(Eds)The effects of noise on aquatic life II (pp 1057ndash1066)NewYorkNY Springerhttpsdoiorg101007978-1-4939-2981-8

SlabbekoornHampBoutonN (2008)SoundscapeorientationAnewfield in need of sound investigationAnimal Behaviour 76 e5ndashe8httpsdoiorg101016janbehav200806010

SlabbekoornHBoutonNvanOpzeelandICoersAtenCateCampPopperAN(2010)AnoisyspringTheimpactofgloballyrisingunderwatersoundlevelsonfishTrends in Ecology and Evolution25419ndash427httpsdoiorg101016jtree201004005

SlabbekoornHampHalfwerkW(2009)BehaviouralecologyNoisean-noysatcommunitylevelCurrent Biology19R693ndashR695httpsdoiorg101016jcub200907002

SlotteAKansenADalenJampOnaE(2004)Acousticmappingofpelagicfishdistributionandabundanceinrelationtoaseismicshoot-ingareaofftheNorwegianwestcoastFisheries Research67143ndash150httpsdoiorg101016jfishres200309046

SmithEP(2002)BACIdesignInAHEl-ShaarawiampWWPiegorsch(Eds)Encyclopedia of environmetricsVolI(pp141ndash148)ChichesterUKJohnWileyampSonsLtd

SmithKB (2010)Modeling theacousticvector fieldusingparabolicequationandnormalmodemodelsJournal of the Acoustical Society of America1271819httpsdoiorg10112113384203

Smokorowski K E amp Randall R G (2017) Cautions on using theBefore-After-Control-Impactdesign inenvironmentaleffectsmon-itoring programs Facets 2 212ndash232 httpsdoiorg101139facets-2016-0058

SolanM Hauton C Godbold J AWood C L Leighton T G ampWhiteP (2016)Anthropogenic sourcesofunderwater soundcanmodify how sediment-dwelling invertebrates mediate ecosystemproperties Scientific Reports 6 20540 httpsdoiorg101038srep20540

SouthallBLBowlesAEEllisonWTFinneranJJGentryRLGreeneCRJrhellipTyackPL(2007)MarinemammalnoiseexposurecriteriaInitialscientificrecommendationsBioacoustics17273ndash275

StobutzkiIMillerMampBrewerD(2001)Sustainabilityoffisheryby-catchAprocessforassessinghighlydiverseandnumerousbycatchEnvironmental Conservation28167ndash181

StreeverBRabornSWKimKHHawkinsADampPopperAN(2016)ChangesinfishcatchratesinthepresenceofairgunsoundsinPrudhoeBayAlaskaArctic69346ndash358httpsdoiorg1014430arctic4596

SutherlandWJampBurgmanMA(2015)UseexpertswiselyNature526317ndash318httpsdoiorg101038526317a

TappertFDampNghiem-PhuL (1985)Anewsplit-stepFourieralgo-rithm for solving the parabolic wave equationwith rough surfacescattering Journal of the Acoustical Society of America 77 S101httpsdoiorg10112112022130

TashmukhambetovAM IoupG E Ioup JW SidorovskaiaNAamp Newcomb J J (2008) Three-dimensional seismic array char-acterization study Experiment and modeling The Journal of

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367

Page 33: Population‐level consequences of seismic surveys on fishes ... · 5.3 Airgun exposure studies with caged fish 16 5.4 Physiological stress responses to loud sounds 18 6 MODELLING

emspensp emsp | emsp33SLABBEKOORN Et AL

the Acoustical Society of America 123 4094ndash4108 httpsdoiorg10112112902185

TealLRvanHalRvanKootenTRuardijPampRijnsdorpA(2012)Bio-energetics underpins the spatial response ofNorth Sea plaiceand sole to climate changeGlobal Change Biology18 3291ndash3305httpsdoiorg101111j1365-2486201202795x

ThompsonPMHastieGDNedwellJBarhamRBrookesKLCordesLSampMcLeanN(2013)Frameworkforassessingimpactsofpile-drivingnoisefromoffshorewindfarmconstructiononahar-bour seal population Environmental Impact Assessment Review4373ndash85httpsdoiorg101016jeiar201306005

ThomsenFMueller-BlenkleCGillAMetcalfeJMcGregorPKBendall V hellipWood D (2012) Effects of pile driving on the be-haviourofcodandsoleInANPopperampADHawkins(Eds)The effects of noise on aquatic life(pp387ndash388)NewYorkNYSpringerhttpsdoiorg101007978-1-4419-7311-5

UnderwoodAJ(1991)BeyondBACIExperimentaldesignsfordetect-inghumanenvironmentalimpactsontemporalvariationsinnaturalpopulationsAustralian Journal of Marine and Freshwater Research42569ndash588httpsdoiorg101071MF9910569

Vaage S Haugland K amp Utheim T (1983) Signatures from sin-gle airguns Geophysical Prospecting 31 87ndash97 httpsdoiorg101111j1365-24781983tb01043x

VanderSluijsIGraySMAmorimMCPBarberICandolinUHendry A P hellipWong B B M (2011) Communication in trou-bled waters Responses of fish communication systems to chang-ing environments Evolutionary Ecology 25 623ndash640 httpsdoiorg101007s10682-010-9450-x

VanderVeerHWKooijmanSALMampvanderMeerJ(2001)Intra-andinterspeciescomparisonofenergyflowinNorthAtlanticflatfishspeciesbymeansofdynamicenergybudgetsJournal of Sea Research45303ndash320httpsdoiorg101016S1385-1101(01)00061-2

Van Leeuwen A De Roos A M amp Persson L (2008) How codshapes its world Journal of Sea Research 60 89ndash104 httpsdoiorg101016jseares200802008

Villegas-AmtmannSSchwarzLKSumichJLampCostaDP(2015)A bioenergetics model to evaluate demographic consequences ofdisturbanceinmarinemammalsappliedtograywhalesEcosphere6183httpsdoiorg101890ES15-001461

Von Benda-Beckmann A M Aarts G M Sertlek H Ouml Lucke Kvan Bemmelen R van Wees R M M hellip Ainslie M A (2015)Assessing the impact of underwater clearance of historical explo-sives on harbour porpoises (Phocoena phocoena) in the SouthernNorthSeaAquatic Mammals41503ndash523httpsdoiorg101578AM4142015503

Walker C (2014)Blended sources and node acquisition ndash the future of ocean bottom seismic(p47)LondonFindingPetroleumSeminar

WardleCSCarterTJUrquhartGGJohnstoneADFZiolkowskiAMHampsonGampMackieD(2001)Effectsofseismicairgunsonmarine fishContinental Shelf Research21 1005ndash1027 httpsdoiorg101016S0278-4343(00)00122-9

Weed D L (2005) Weight of evidence A review of con-cept and methods Risk Analysis 25 1545ndash1557 httpsdoiorg101111j1539-6924200500699x

Weilgart L S (2007) The impacts of anthropogenic ocean noise oncetaceans and implications for management Canadian Journal of Zoology851091ndash1116httpsdoiorg101139Z07-101

Weinburg H amp Burridge R (1974) Horizontal ray theory for oceanacoustics Journal of the Acoustical Society of America 55 63ndash79httpsdoiorg10112111919476

WeinholdRJampWeaverRR(1972)Seismic airguns effect on immature Coho salmon Contributions to the 42nd Annual Meeting of the Society of Exploration Geophysicists Anaheim California 15 p

Wendelaar-Bonga S E (1997) The stress response in fishPhysiological Reviews 77 591ndash625 httpsdoiorg101152physrev1997773591

Weston D E (1959) Guided propagation in a slowly varying me-dium Proceedings of the Physical Society 73(3) 365 httpsdoiorg1010880370-1328733304

WilliamsRWrightAJAsheEBlightLKBruintjesRCanessaRhellipThomasL(2015)ImpactsofanthropogenicnoiseonmarinelifePublicationpatternsnewdiscoveriesand futuredirections inresearchandmanagementOcean amp Coastal Management11517ndash24httpsdoiorg101016jocecoaman201505021

Willis J (2011) Modelling swimming aquatic animals in hydrody-namic models Ecological Modelling 222 3869ndash3887 httpsdoiorg101016jecolmodel201110004

Willsteed E Gill A B Birchenough S N R amp Jude S (2017)Assessing the cumulative environmental effects ofmarine renew-able energy developments Establishing common ground Science of the Total Environment 577 19ndash32 httpsdoiorg101016jscitotenv201610152

WysockiLEDittamiJPampLadichF(2006)ShipnoiseandcortisolsecretioninEuropeanfreshwaterfishesBiological Conservation128501ndash508httpsdoiorg101016jbiocon200510020

ZeddiesDGFayRRGrayMDAlderksPWAcobAampSisnerosJ A (2012) Local acoustic particle motion guides sound-sourcelocalization behaviour in the plainfin midshipman fish Porichthys notatus Journal of Experimental Biology 215 152ndash160 httpsdoi

org101242jeb064998

How to cite this articleSlabbekoornHDalenJdeHaanDetalPopulation-levelconsequencesofseismicsurveysonfishesAninterdisciplinarychallengeFish Fish 2019001ndash33 httpsdoiorg101111faf12367


Pre-Charged Pneumatic Airgun OWNER’S MANUAL...Crosman Corporation 7629 Rts. 5 & 20 Bloomfield, NY 14469 800-7-AIRGUN (724-7486) CH2009A515 Model CH2009 Pre-Charged Pneumatic Airgun

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Pre-Charged Pneumatic Airgun OWNER’S MANUAL · Pre-Charged Pneumatic Airgun OWNER’S MANUAL ... Push the safety to the forward position (away from the trigger). When the airgun

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Results from an acoustic modelling study of seismic airgun ... · PDF fileResults from an acoustic modelling study of seismic airgun survey noise in ... Airgun arrays ... Literature