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PhytoplanktonClimateRegulationinPositiveandNegativeFeedback

Systems:TheCLAWandanti-CLAWhypotheses

AdamStoer,UndergraduateStudent,DalhousieUniversityAbstract

Theglobalclimatecrisisisbiggernowthanithaseverbeenbefore,pushingformuch-needed research on the consequences of climate change. In 1987, Charlson, Lovelock,Andreae,andWarrenproposedtheCLAWhypothesiswhichstatedthatphytoplanktoncontributetotheproductionofasignificantamountofcloudcondensationnuclei(CCN)whichinturncreatesanegativefeedbackloopafterthereisaninitialtemperaturerise.Manyyearslater,in2006,Lovelockproposedtheanti-CLAWhypothesis,whicharguesthata similarprocessoccursexcept that itworksasapositive feedbacksystem.Bothhypotheses have created much controversy about the effects phytoplankton has onclimate and climate regulation. Research has shown that different types ofphytoplankton tend to have higher growth rates within a temperature range.CoccolithophoresareknownfortheircontributionofDMSP,acompoundthatformstomake CCN aswell as their carbon sequestration abilities. This type of phytoplanktontypically function at a thermal niche where nutrient stratification is not stronglylimiting,makingthemactlikeabufferagainstfurthertemperaturerisesintermsoftheCLAWhypothesis.Basedonthephysiologicalcapabilitiesofphytoplanktonwithintheirenvironment, both the CLAW and anti-CLAW mechanisms correlate strongly withcoccolithophoridalgae.

1.IntroductionAfterCharlson,Lovelock,Andreae,andWarrenintroducedtheCLAWhypothesisin1987(whereCLAWisanacronymforthefourauthor’snames),muchdiscussionhasbeengeneratedaroundthetopic.Essentially,theCLAWhypothesisdescribesphytoplanktongrowthasamechanismthatcancounteractincreasingglobaltemperatures.TheCLAWhypothesisassumesthatphytoplanktongrowthwillsignificantlyincreasewhenthesurfaceseawatertemperaturerises.Afteralargephytoplanktonbloom,thephytoplanktondie,releasingthecompounddimethylsulfoniopropionate(DMSP),whichisthenbrokendownbymarinebacteriaintodimethylsulphide(DMS).DMSthengetstransferredtotheatmospherefromtheocean,whichgoesontooxidizeintomethanesulphonate(MSA)andnon-sea-saltsulphates(NSS-sulphate).TheproductsofDMSbecomeaerosolswhichactascloudcondensationnuclei(CCN)thatcontributetotheformationofclouds.Sincecloudshaveahighalbedo,theyreflectsunlight,andconsequentlyreducesurfacetemperature.Charlsonetal.(1987)arguethatphytoplanktongrowthandthefollowingriseinCCNcreatesanegativefeedbackmechanismthatoffsetstemperatureriseandhelpsregulatetheclimate.Morerecently,Lovelock(2006)proposedasimilarsystemthatactsasapositivefeedbackmechanism,appropriatelynamedtheanti-CLAWhypothesis.Underfutureglobalwarming,

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theanti-CLAWhypothesisproposesthatphytoplanktongrowthwillfallwhenseawatersurfacetemperaturerises.ThelossofphytoplanktonbiomasswillresultinlessCCNandthusclouds,allowingforevenmorewarmingtooccur(Lovelock,2006).BothhypothesesarevisuallypresentedinFigure1.

Figure1.DiagramoftheCLAWhypothesisleft(Charlsonetal.,1987)andtheanti-CLAWhypothesis,right(Lovelock,2006).However,thereisstillsomeuncertaintyonhowphytoplanktongroupsactinaccordancetotheCLAWhypothesisandanti-CLAWhypothesissincetherearemultiplefactorsthatcancontributetophytoplanktonhealthandreproduction(Cox1997).ThegoalofthisreviewistoshowthatboththeCLAWandtheanti-CLAWprocessesimpactphytoplanktongrowthdependingontemperatureconditions.Unlikeotherreviewpapersthatsupportonlyonehypothesis,thisreviewwillattempttoshowthatbothcanhypotheticallycoexist.ItisimportanttostudythepracticalityoftheCLAWandanti-CLAWhypothesessothereisabetterunderstandingonhowtheEarthcouldorcouldnotberesilienttoclimatechange;alackofresearchwouldleavepeoplewithabenightedviewontheEarth’sabilitytorecover.Therefore,thispaperwilllookattheeffectsoftemperatureonphytoplanktongrowthamongdifferenttaxonomicgroups,andthecorrelationsbetweenalgalbloomsandcloudformationandproposesapossiblerelationshipbetweenthetwohypothesesandphytoplanktongrowth.

2.PhytoplanktonandtheCLAWandanti-CLAWHypothesesThehugecontributionthattheCLAWhypothesismadein1987toclimatesciencehasledtomuchresearchintotherelationshipsbetweenbiologyandclimate.Subsequently,anextensiveinvestigationintophytoplanktongrowthandclimateregulationgaverisetotheanti-CLAWhypothesis,theopposingpositivefeedbacksystem.Althoughtheprocessesworkdifferently,bothstillconsistofthesamecomponents,whichare:phytoplanktongrowth,DMSproduction,andcloudproduction.Fortherestofthispaper,itisimportanttokeepthesemainfactorsinmindasthepaperwilldrawoneachofthesepointsinthecontextofphytoplanktongrowth.

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3.EffectsofTemperatureonPhytoplanktonGrowthandCommunitiesTemperatureplaysamoreimportantrolethansunlightinregulatingphytoplanktonreproduction(MiaoandYang2009;Steemann-Nielson1975).Generally,phytoplanktonreproductionratesandmetabolicactivitywillincreasewithrisesinseawatertemperature(Eppley1972).Bycompilingdatafromotherexperimentsusingculturedphytoplankton,Bingzhang(2015)showsthatgrowthispositivelycorrelatedwithtemperatureuntiltheyreachamaximumtemperature.Atthistemperature,or‘thermallimit’,growthbeginstoplateauandthendecreases,resultinginphytoplanktonmortality(MiaoandYang2009).Theoptimalgrowthtemperatureistypicallyhigherthanthemeanenvironmentaltemperature,meaningthatwhenenvironmentaltemperaturerises,phytoplanktonarefunctioningandreproducingatahigherrate(Figure2;Bingzhang2015;Lovelock1995).Withmorephytoplanktonbiomass,theCLAWhypothesispresumesthatthesemarineprimaryproducerswillstartcounteractingtheinitialriseintemperaturewithincreasedproductionofDMSP.ThephysiologicalcapabilitiesinthesemarinephytoplanktonsupportstheideaofaCLAWmechanism:increasedtemperaturesleadtoincreasedphytoplanktongrowth.

Figure2.Scatterplotofoptimalgrowthtemperatureandenvironmentalannualmeantemperature.Theblackdotsrepresentmarinephytoplankton;thetrianglesrepresentfreshwatercyanobacteria;theblacklinerepresentstheregressionlineformarinephytoplanktonwhilethedashedlinerepresentstheregressionlineforfreshwatercyanobacteria.Thethindottedlinesrepresentthe95%confidenceintervals(Bingzhang2015)WhenconsideringtheactualrangeoftemperaturethataCLAWmechanismcanfunctionat,itisimportanttokeepnutrientsinmind.Phosphorus,silicon,andnitrogenallplaysignificantrolesinphytoplanktondevelopmentandgrowth.Intermsoftemperature,elevatedseawatersurfacetemperaturestratifiesnutrients,whichcreatesabarrierbetweenaccessiblenutrientsandphytoplankton,ultimatelyslowingthegrowthofalgal

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communities.Bothnitrogenandphosphorusdeficiencycanreducethecapacitytophotosynthesize(MiaoandYang2009;YangandZhu1990).Temperaturealonecanlimittheamountofnutrientsmadeavailabletophytoplanktoncommunities,sonutrientstratificationmustbeminimalinordertosupporttheCLAWhypothesis.Intropicalregions,wherethesurfacewatersarestratifiedandlackingsufficientnutrients,phytoplanktonaremorelikelytofollowanti-CLAWhypothesis;thus,theCLAWmechanismcouldonlyfunctioninrelativelycolderwaters.4.TheSignificanceofPhytoplanktonGroupsinBiogeochemicalProcessesAlthoughdifficulttomeasure,theproductionofcloudproducingagentsafterphytoplanktonbloomsarekeypieceofevidencesupportingtheCLAWandanti-CLAWhypotheses.Overan8-dayperiodusingsatellitedata,MeskhidzeandNenes(2007)measuredchlorophyll-aconcentrationandcloudeffectiveradiusoverasectionoftheSouthernOcean.Theyfoundthatcloudsconsistentlyformdirectlyafterphytoplanktonblooms,asshowninFigure3.SoonafterDMSforms,itispresumedthatCCNbecomesmoreabundantintheatmosphere.Itisunclearifthissamemechanismwilloccurincoolerclimates,andphytoplanktoninmidtohighlatitudeswillproducealgalbloomsthatwillgeneratesufficientamountsofDMStocontributetocloudproduction.

Figure3.The8dayaverageofSeaWiFS-observedchlorophyll-a(A)andMODISretrievedcloudeffectiveradius(B)bothobservedbetween49°to54°Sand35°to41°W.Whitespotsindicatemissingdata;chl-adataisgriddedataresolutionof9by9kmandeffectiveradiusisgriddedby1by1°(MeskhidzeandNenes2007)Inordertounderstandtheeffectoflatitudeonphytoplankton,itisnecessarytounderstandhowdifferentthermalrangesaffecttheabilitytogrowfordifferentgroupsofphytoplanktonspecies.Coccolithophores,atypeofphytoplankton,areknownfortheirdistinctivelightgreenalgalbloomsinthecolderregionsoftheocean.Emilianiahuxleyi,arguablythemostabundanttypeofcalcifyingcoccolithophore,tendstofavourtemperaturesaround16-21°C,withoptimalreproductionratesinthatrange.Whentemperaturesareabove22°C,thesecoccolithophoreswillnotgrow(Huertas,Rouco,Lopez-RodasandCostas2010).Calcifyingcoccolithophoresgenerallyshareasimilaroptimaltemperaturerange.However,dinoflagellates,anothertypeofphytoplankton,can

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toleratehighertemperaturesupto30-33°C.(Boydetal.2013).Theoptimumgrowthtemperatureissimilarfordiatoms(Ruth1971;Admiraal1976).Withrisingtemperature,thetaxonomicgroupsinphytoplanktoncommunitieschangedrastically,resultinginmicrothermalspeciesbeingreplacedbymesothermalandmegathermalspecies,whichcanhandlehighertemperatures(Fott1971;MiaoandYang2009).Generally,eachgroupofphytoplanktonhasa‘thermalniche’,oraspecifictemperaturerangewhereoptimalgrowthoccurs.Itisimportanttokeepinmindthateachspecieswithinthesegroupsmayhaveadifferentoptimumgrowthtemperature,butingeneralcoccolithophoridalgaeperformbetteratalowerthermallevelthandinoflagellatesanddiatoms.Usingshipboardincubationofalgalcommunities,Leeetal.(2009)subjectedphytoplanktontoincreasedcarbondioxideconditions(690ppm)andtemperature(16°C)thatwouldrepresentfutureclimateconditionsunderglobalwarming.Attheendoftheexperiment,coccolithophoreabundancesincreased,whilediatomanddinoflagellateabundancesdecreasedasseeninFigure4.Simultaneously,therelativeDMSPlevelswerenearly50-60%greaterthanunderambientcontrols(12°C,390ppmCO2).TherelativeincreasesinbothDMSPandcoccolithophoresshowthatthereisacorrelationbetweenthetwo,whichcouldsignifyaCLAWmechanisminactionwiththesepredominantlymidandhighlatitudephytoplanktoncommunities.Assuch,largerphytoplanktonbloomsthatarepredominantlymadeupofcoccolithophorescouldhelpmitigategrowingcarbondioxideconcentrations.CalcifyingcoccolithophoresshouldmitigaterisesincarbondioxideandtemperaturesincetheirphysiologyinthepolarenvironmentisconsistentwiththemainaspectsoftheCLAWhypothesis.Theanti-CLAWhypothesisisonlyattainableinareaswithheavilystratifiedwaters,suchastropicalregionsthathaveverylowphytoplanktonconcentrations,orextremelywarmwaters.Itisimportanttorememberthefindingsfromthesestudiesshownhereareusedinageneralmanner,andmaynotreflecttheabilitiesallofdiatoms,coccolithophores,anddinoflagellates.Sincemostofthesestudieswereeitherperformedinsituorinincubationtanksoverashortperiodoftime,usuallyonlyspanningoverafewweeks,therelationshipsdescribedheremaynotreflectlongtermtrendsoftemperaturedrivenphytoplanktongrowth.5.ThePrevalenceoftheCLAWFeedbackMechanismintheCurrentClimateInhigherlatitudeswherephytoplanktonaremoreconcentrated,itispresumedthatlargeramountsofdimethylsulfidearereleasedforminghigherconcentrationsofCCN,comparedtolatitudesaroundtheequator.OnestudymeasuredastrongrelationshipbetweentheseasonalcyclesofbiologicallyproducedDMSandtheseasonalvariationoftheproductsofDMS:methanesulphonateandnon-sea-saltsulphate(Ayersetal.1991).ThestudyshowedthatasDMSlevelsincreasedconcentrationsofMSAandNSS-sulphateincreasedbyafactorof12-25and5-10respectively.AyersandGras(1991)alsofoundastrongcorrelationbetweenCCNnumbersandatmosphericsulphurproducts.

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However,thisinformationdoesnotmeanthatplanetaryalbedoisincreasing;contradictorysatellitedatahasshownthatthereisanincreasingamountofradiationhittingtheEarth’ssurface(Pinkeretal.2005).Low-lyingcloudstendtobemoreeffectiveatreflectingsolarradiationthanhigh-levelclouds(Figure4)andtherehasbeenanotabledeclineintheselow-lyingcloudsoverthepast30years(Figure5),helpingtoexplaintheincreasedradiationhittingtheEarth'ssurface(ISCCP2011).ItmayseemthattheCLAW-likemechanismisnotapparentbecauseofthis,howeveritisalsopossiblethatthismechanismdoesoccur.Insteadtheprocessisweakenedwhileinaninterglacialstate,orwarmperiod,andisdiminishedevenfurtherbyheavyanthropogenicactivities

Figure4.Therelationshipbetweenlowlevelcloudcover(%)andglobalsurfacetemperature(°C).(ISCCP2011).

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Figure5.Atmosphericwater(black)istheaverageamountofwaterpresentinthe

atmosphere;cloudcoverpercentageoflow-levelclouds(blue),middle-levelclouds(green),andhigh-levelclouds(red)inthepast30years.(ISCCP2011)

TheCLAWhypothesisismeanttobeaglobalconceptsupportingLovelock’sGaiaTheory(1995),whichistheunifyingtheorydepictingtheimportanceofmarineandterrestrialbiomassincontributingtoclimateregulation.Puttingthelong-termgeologicaltimelineintoperspective,Lovelock(2006)describesinterglacialperiodsasEarth’sfeverorsickstate,andglacialperiodsasEarth’shealthystate.WhentheEarthisinaglacialperiod,thereismoreicereflectingmoresunlight,resultinginalowerglobaltemperature.Onceoceansrecede,morelandandforestsarecreatedaswellasstrongeroceancurrents,ultimatelyallowingformorebiomasstocontributetoclimateregulation.Ina'feverstate'orinterglacialperiod,theEarthhaslessiceloweringplanetaryalbedoandconsequentlyweakeningtheEarth’sbioticclimateregulation.Theanti-CLAWhypothesisbetterrepresentsawarmerperiodbecauseseawatertendstobelesssalty,lessnutrientabundant,andwarmer.Phytoplanktonandothermarinephotosynthesizerswillhypotheticallyhaveaweakereffectinclimateregulation.Inadditiontothis,humanshaveessentiallyremovedasignificantamountofthenaturalecosystemandreplaceditwithfarmsandurbanlandscape.ItispossiblethathundredsofyearsofchangingthelandandoceancouldhaveunprecedentedeffectsontheabilityforanaturalnegativefeedbackmechanismliketheonedescribedbytheCLAWhypothesis,tocombatcarbondioxidefluxesandotherseverechangesintheenvironment.

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ThecombinedeffectsofstronganthropogenicactivityandinterglacialperioddynamicsprobablyhaveweakenedtheCLAWmechanismtoapointwhereitmaynothaveasignificanteffectonclimateregulation.Inotherwords,ifaCLAWmechanismwasoccurringbeforehumansstartedchangingthecompositionoftheatmosphere,itmaynothaveanoticeableeffecttodayandwouldnotbeobservableincloudcoveragedata(e.g.Figure5)6.HypotheticalRelationshipBetweenGrowthandtheCLAWandanti-CLAWHypothesesCombined,thereviewedinformationrevealstherelationshipbetweenbothhypotheseswithphytoplanktongrowthasafunctionoftemperature.Essentially,theresearchimpliesthattheCLAWmechanismactsupuntilanoptimaltemperature,atwhichthatpointtheanti-CLAWhypothesisisactivated,assumingthatheavynutrientstratificationisnotalreadylimitinggrowthattheoptimaltemperature.AsshowninFigure6,whiletheCLAWmechanismisinaction,thereisadownwardpressureornegativefeedbackactinginattempttoreturntoregularenvironmentaltemperatures.WhileundertheCLAWhypothesis,phytoplanktonwouldincreasereproductionwithincreasedtemperaturesintheirenvironment,excludingtheeffectofnutrientstratification.Inthecasethattemperaturedoescontinuetoincreasepasttheoptimaltemperature,theanti-CLAWmechanismgoesintoeffectcausingapositivefeedback,pushingphytoplanktongrowthtozero.Thisrelationshipwouldbemosteffectivewithcoccolithophoridalgaebecausegrowthpeaksarealowertemperaturewherestratificationisnotasheavilylimitingaswoulditbewithothertaxonomicgroups.

Figure6.HypotheticalrelationshipforphytoplanktongrowthasafunctionoftemperaturerelativetotheCLAW(blue)andanti-CLAWmechanisms(red)inaction.Note:the

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temperaturerangewhereeithermechanismisfunctionalissubjecttoshiftdependingonthespeciesandenvironment.7.ConclusionTounderstandtherelationshipbetweentheCLAWandanti-CLAWhypotheseswithdifferentmarinephytoplanktongroups,onemustreviewthephysiologicalcapabilitiesandlimitsofthesetaxonomicgroupsrelatedtorisingtemperatures.ThepurposeofthispaperwastoshowthatthephysiologyofphytoplanktoncloselycorrelateswithboththeCLAWandanti-CLAWhypothesesasafunctionoftemperatureandgrowth(asdescribedinFigure6).Coccolithophorescansufficientlyreproduceincolderwaterand,byproducinghighlevelsofDMSP,cancontributetocloudformation.Whentemperaturesreachrangesofabout16-21°C,phytoplanktongrowthisatitsoptimumlevelafterthisoptimumlevelispassed,phytoplanktongrowthbeginstodeclineduetotheinaccessibilityofnutrientsinstratifiedwater;inotherwords,theCLAWmechanismgiveswaytotheanti-CLAWmechanism.Toconclude,coccolithophoridalgaephysiologyshowsthatbothhypothesescanexistasbiogeochemicaloceanprocesses,ratherthanonlyone.Futureresearchshouldbeperformedoveralong-termperiod,spanningseveralyears,lookingatthecorrelationbetweenchlorophyll-aconcentration,cloudcoverage,NSS-aerosols,andDMSlevels.Inadditiontothestudyneedinglongtermfunding,itwouldalsoneedtohaveaccesstoamultitudeofsatellitedataandoceanobservationbuoysthatareabletorecordinformationsuchasDMSlevelsandNSS-aerosolsintheatmosphere.Sincephytoplankton-bornCCNhaveonlybeenstudiedonarelativelysmallscale,along-termstudysuchasthiscouldgreatlyimprovetheunderstandingabouttherolethatphytoplanktonplayinregulatingtheclimate;furthermore,helpingcreatebettermodelsthatpredicthowlifeonEarthwillreacttothecurrentclimatewarmingcrisis.ReferencesAdmiraalW.1977.InfluenceofLightandTemperatureontheGrowthRateofEstuarine

BenthicDiatomsinCulture.MarBiol.39:1-9.AyersGP,CaineyJM.2007.TheCLAWhypothesis:areviewofmajordevelopments.Environ

Chem.4:366-374.AyersGP,GrasJL.1991.SeasonalRelationshipbetweencloudcondensationnucleiand

aerosolmethanesulphonateinmarineair.Nature.353:834-835.AyersGP,IveyJP,GilletRW.1991.Coherencebetweenseasonalcyclesofdimethyl

sulphide,methanesulphonate,andsulphateinmarineair.Nature.349:404-406.BingzhangC.2015.Patternsofthermallimitsofphytoplankton.J.PlanktonRes.37(2):285-

292.BoydPW,RynearsonTA,ArmstrongEA,FuF,HayashiK,ZhangxiH,HutchinsDA,Kudela

RM,LitchmanE,MulhollandMR,etal.2013.Marinephytoplanktontemperature

A.Stoer\OceansFirst,Issue4,2017,pgs.43-52. 52

versusgrowthresponsesfrompolartotropicalwaters-outcomeofascientificcommunity-widestudy.PLoSONE.8(5):e63091.[about17p.].

CharlsonRJ,LovelockJE,AndreaeMO,StephenG.1987.Oceanicphytoplankton

atmosphericsulphur,cloudalbedoandclimate.Nature.326(6114):655-661.CoxRA.1997.Atmosphericsulphurandclimate-whathavewelearned?PhilTransRSoc

Lond.352:251-254.DongfangY,PeigangW.2004.Influenceofseawatertemperatureonphytoplanktongrowth

inJiaozhouBay,China.ChinJOceanolLimn.22(2):166-175.LovelockJ.1995.AgesofGaia:AbiographyofourlivingEarth.NewYork:OxfordUniversity

Press.LovelockJ.2006.TherevengeofGaia:Earth’sclimatecrisis&thefateofhumanity.New

York:BasicBooksPublishing.MiaoZ,YangD.2009.Solarlight,seawatertemperature,andnutrients,whichoneismore

importantinaffectingphytoplanktongrowth?ChinJOceanolLimn.27(4):825-831.MeskhidzeN,NenesA.2006.PhytoplanktonandcloudinessintheSouthernOcean.

Science.314(5804):1419-1423.LeePA,RudisillJR,NeeleyAR,MaucherJM,HutchinsDA,FengY,HareCE,LeblancK,Rose

JM,WilhelmSW.2009.EffectsofincreasedCO2andtemperatureontheNorthAtlanticyangSpringBloom.III.Dimethylsulfoniopropionate.MarEcoProgSer.388:41-49.

PinkerRT,ZhangB,DuttonEG.Dosatellitesdetecttrendsinsurfacesolarradiation?

Science.308(5723):850-854.RuthP.1971.Theeffectsofincreasinglightandtemperatureonthestructureofdiatom

communities.ASLO.16(2):405-421.TheInternationalSatelliteCloudClimatologyProject(ISCCP).2011.

www.climate4you.com.[nodatemodified;accessed2016Dec1].http://www.climate4you.com/ClimateAndClouds.htm#Cloudalbedo

XieY,TilstoneGH,WiddicombeC,WoodwardE,HarrisC,BarnesBK.2015.Effectsof

increasesintemperatureandnutrientsonphytoplanktoncommunitystructureandphotosynthesisinthewesternEnglishChannel.MarEcolProgSer.519:61-73.

YangXandZhuM.1990.Thedevelopmentofphytoplanktonmetabolismstudy.JOceano

HuanghaiandBohaiSeas.3:65-72.