global meta‐analysis of soil‐disturbing vertebrates reveals strong … · 2019-01-23 · we...

Global Ecol Biogeogr 20191ndash19 wileyonlinelibrarycomjournalgeb emsp|emsp1copy 2019 John Wiley amp Sons Ltd

Received28March2018emsp |emsp Revised3November2018emsp |emsp Accepted5November2018DOI 101111geb12877

M E T A ‐ A N A L Y S I S

Global meta‐analysis of soil‐disturbing vertebrates reveals strong effects on ecosystem patterns and processes

Max Mallen‐Cooper12 emsp|emspShinichi Nakagawa2emsp|emspDavid J Eldridge12

1CentreforEcosystemScienceSchoolofBiologicalEarthandEnvironmentalSciencesUniversityofNewSouthWalesSydneyNewSouthWalesAustralia2EcologyandEvolutionResearchCentreSchoolofBiologicalEarthandEnvironmentalSciencesUniversityofNewSouthWalesSydneyNewSouthWalesAustralia

CorrespondenceMaxMallen‐CooperCentreforEcosystemScienceSchoolofBiologicalEarthandEnvironmentalSciencesUniversityofNewSouthWalesSydneyNewSouthWales2052AustraliaEmailmmallen‐cooperunsweduau

Funding informationAustralianResearchCouncilGrantAwardNumberFT130100268

EditorSallyKeith

AbstractAim Organismsthatdisturbthesoilwhile foragingorcreatingshelter (ecosystemengineers)canhaveprofoundeffectsonecosystemsSoilejectafromthesedistur-bancescanenhancesurfacenutrientsandtheresultingdepressionsaccrueorganicmatteranddevelopintobiologicalhotspotsHerewedescribeaglobalmeta‐analysisofstudiesthatassessedtheimpactsofvertebratesoildisturbanceonbothbioticandabioticcomponentsofecosystemsLocation GloballandsurfaceTime period 1941ndash2016Major taxa studied VertebratesMethods Afterconductingasystematicliteraturesearchwequantitativelysynthe-sizedthefindingsof149publishedstudiesthatcompareddisturbedandundisturbedsurfacesOurmeta‐analysisincluded64engineerspeciesprimarilycomprisedofro-dentsandasubsetofothermammalsResults Wefoundthatvertebratesoildisturbancesignificantlyenhancedsoilnitro-gen (by 77) and phosphorus (35) and the productivity (32) and recruitment(32)ofvascularplantsDisturbanceshadagreatercoverofbaresoil(126)thanundisturbed controls and higher abundances of secondary vertebrates (1233)thatusepre‐constructedburrowsasshelterandforaginggroundsSoildisturbancesignificantlyreducedwaterrun‐off(63)andtheabundanceofbiocrusts(82)Soildisturbanceeffectsgenerallyintensifiedwithincreasingaridityandthemagnitudeof soil disturbance effects was not moderated by the area of the disturbanceDisturbancesolderthan12monthsweremoredistinctfromthesurroundingmatrixthanfreshdisturbancesThephylogenyofengineerswasunrelatedtotheirecosys-temeffectsindicatingthatthesamefunctionalitycouldreadilyevolveindifferenttaxaMain conclusions In general disturbances become localized patches of elevatedfunctioningprovidingstrongevidencethatvertebrateengineersespeciallythoseindrylandsareanimportantsourceofenvironmentalheterogeneity

K E Y WO RD S

biopedturbationbioturbationecosystemengineeringfaunalpedturbationfertileislandsheterogeneitymeta‐analysissoildisturbancezoogeomorphology

2emsp |emsp emspensp MALLEN‐COOPER Et AL

1emsp |emspINTRODUCTION

Positive (facilitatory) interactions among organisms are equallyas important as negative (competitive) interactions in structur-ing ecosystems (see eg Bruno Stachowicz amp Bertness 2003Machicote Branch amp Villarreal 2004) Terrestrial vertebratesforexamplecanmodifyplantspeciescompositionbydispersingseeds or alter the dominant plant growth form through grazing(Chew1974KerleyampWhitford2000)Positiveinteractionscanalso result fromnon‐trophicmechanisms suchasecosystemen-gineeringwherebyanorganisminducesachangeinthephysicalenvironment thatalters theavailabilityof resources tootheror-ganismsor to themselves (JonesLawtonampShachak1994)ForexampleIndiancrestedporcupines(Hystrix indica)createsurfacepitsinordertoconsumebulbsofthedeserttulip(Tulipa systola)intheNegevDesertAlthoughtheporcupinesconsume60ndash90ofthebulbstheconditionsfortheremainingbulbsareenhancedbytheadditionalwater andnutrient‐rich sediment capturedby thepits (Gutterman 1987) Soil disturbances such as these are themostwell‐documentedformofecosystemengineering in terres-trialvertebrates(CogganHaywardampGibb2018)andwillbethefocusofthepresentstudy

Itisusefultoconceptualizesoildisturbanceastwodistinctphys-ical processes resulting in (a) theexcavationof apit scrape rest-ingformorburrowand(b)thedepositionofamoundofsoil(ejectamound)adjacenttothedisturbance(Figure1)Thedepressioncre-atedby soil removal acts as an accreting surfacewhichgraduallyinfillswitherodingsediment litterwaterseedsandotherorganicmaterialsVacatedburrowsoftenbecomehabitatforsecondaryan-imalssuchasburrowingowls(Athene cunicularia hypugaea)Floridamice (Podomys floridanus) and various lizard and beetle specieswhich use the burrows as shelter and foraging grounds (Casas‐Crivilleacute amp Valera 2005 Davidson Lightfoot amp McIntyre 2008Lantz Conway amp Anderson 2007) The ejectamound acts as anerodingsurfaceandtheconstituentmaterialisredistributedacrossthelandscapebyfluvialandaeolianerosionuntiltheoriginalsurfaceeventuallyre‐emergesInsomecasesejectamoundsmaybestabi-lizedbyvegetationandbiocrustandbecomepersistenttopograph-icalfeatures(Eldridge2004)

Intheactofremovingsoilvertebrateengineersremoveground-storeyplantsandexpose thesubsoiloften reducing soil aggrega-tionandalteringsurfacemicroclimate (PlattKolbKunhardtMiloamp New 2016) Soil removal reduces run‐off and has often beenreported to increase soil moisture and infiltration by creating amacropore removinghydrophobic soil crustsorcompacted layersandclearingplantswhichextractaportionofsoilwater(ValentineBretzRuthrofFisherampHardy2017)SoilejectahowevercoversanexistingsoilsurfacesmotheringgroundstoreyplantsSoilejectaoftenhasamarkedlydifferentchemicalsignaturetotheoriginaltop-soilintermsofpHcationsandcarbonandnitrogenpools(EldridgeampKoen2008KerleyWhitfordampKay2004)Assoilnutrientpoolsrecoverinthedepressionandtheejectaisredistributedplantsandsoilorganismsbegintorecolonizethedisturbedsurfaces

We analysedpublisheddata on the effects of vertebrate engi-neers on plants soils and associated biota to derive a global syn-thesis There have been several important qualitative reviews ofvertebrateengineerswithfocionbioticinteractions(Cogganetal2018)soilfunction(Plattetal2016)andspecificsystemssuchasdrylands (WhitfordampKay 1999)However quantitative synthesesthusfarhavebeenrestrictedtopropertiesrelatingtodiversityandbiomass(RomeroGonccedilalves‐SouzaVieiraampKoricheva2015Root‐BernsteinampEbensperger2013)TherehasyettobeaquantitativesynthesisattheglobalscalethatexaminesboththebioticandabioticeffectsofvertebrateengineersSuchasynthesisistimelyifwearetoadvanceourunderstandingoftheecologicaldimensionsofverte-brateengineershowtheyinfluenceawiderangeofpatternsandpro-cessesacrossarangeofecosystemshowtheseimpactsvaryunderdifferentclimateconditionsandthusthelikelyimpactsoftheirlossfromecosystemsortheirreintroductionintodegradedecosystems

Ecosystem theory suggests that the impactof vertebrateengi-neersshouldincreasewithdecliningecosystemproductivity(WrightandJones2004)Thiswouldoccurbecausethecaptureofevensmallamountsofresourcessuchaswaterandorganicmatterwithinsurfacedisturbancesinresource‐poorenvironmentswouldresultinthecre-ationofpatchesthataredistinctlyresource‐richcomparedwiththe

F I G U R E 1 emspConceptualdiagramofsoildisturbanceshowingthetwotypesofstructuresproduced(anejectamoundandadepression)andhowtheychangeovertimeThedepressioninfillswitherodingsedimentwaterandorganicmatterTheejectamoundisredistributedacrossthelandscapebyerosionBothtypesofstructurescanleadtocompositionalshiftsinbiota

Resource redistribuon

Resourcecapture

Bioc shi13s

MOUND DEPRESSION

Enhanced funcon

emspensp emsp | emsp3MALLEN‐COOPER Et AL

surroundingmatrixWemight also expect that larger disturbanceswouldhavemorepronouncedimpactsonecosystempropertiesbe-cause they could influenceprocesses that occur at broader spatialscales(Wiens1989)Vegetationisalsoknowntorecovermoreslowlyonlargersoildisturbances(RogersampHartnett2001)Consequentlyoursynthesisaimedtoaddressthreeimportantquestionsrelatingtohow vertebrate engineers affect ecosystems by disturbing soil (a)whataretheglobalecosystemeffectsofsoildisturbancebyverte-brates(b)areanyimpactsofdisturbancegreaterinmorearideco-systemsand(c)doestheimpactofdisturbancevarywiththesizeorageofthedisturbanceWealsoexaminedwhetherphylogenywasimportantinexplainingvariationintheseeffectsamongspecies

2emsp |emspMETHODS

21emsp|emspLiterature search

RecordswerecollectedbysystematicallysearchingonlinedatabasesandthenscreenedinaccordancewithPreferredReportingItemsforSystematic Reviews and Meta‐Analyses (PRISMA) guidelines (seeSupportingInformationAppendixS1)AlistofdatasourcescanbefoundintheAppendixSoildisturbanceisknownbymanytermsde-pendingonthefieldofsciencethedisturbingagentsandthebiomeinwhichthedisturbanceisbeinginvestigated(CavinampButler2015)Ecosystemengineeringandseveralvariantsofbiopedturbation(egfaunalpedturbation) areusedbyecologistswhile zoogeomorphol-ogyand ichnologyaremorecommonlyusedbygeoscientistsWecapturedresearchfrombothfieldsbysearchingGoogleScholarandthe Institute forScientific Information (ISI)WebofKnowledge forthe following keyword strings biopedturbation biopedoturbationfaunalpedoturbation faunalturbation lsquoforaging pitsrsquo and zoogeo-morphologyRecordswerealsoretrievedfromthecompleterefer-ence listsofsevenkeyreviewpapers (seeSupporting InformationAppendixS1)Therelevantliteratureonwildboar(Sus scrofa)wassoextensivethatastudybyBarrios‐GarciaandBallari(2008)despiteitssingularfocusonwildboarwaschosenasakeypapertoensurethatallpertinentstudieswerecapturedbyoursearchStudiespub-lishedatanydateuptoandincludingNovember2016wereincluded

Retrieved records were screened to identify primary peer‐re-viewedpublicationsthatcomparedanecosystemeffectofsoildis-turbancebyavertebrateagainstapairedundisturbedcontrolOnlyone included study was manipulative (Prugh amp Brashares 2012)andthemajorityofcomparisonswereconductedatthepatchscale(disturbanceversusundisturbedadjacentcontrol)Werestrictedourstudy to terrestrial ecosystems and excluded human‐created dis-turbancesWechosenottoincludesoiltemperatureandcationsaspropertiesbecausetheirrolesinecosystemprocessesarenotwellcharacterizedOnlyclaycontentwasincludedasameasureofsoiltexture due to strong correlationswith silt and sand contentWeexcluded aquatic disturbing agents unless they directly impacteda terrestrial property The full criteria are shown in SupportingInformation Appendix S1 From the studies that satisfied our cri-teriaweextracted the rawmeansandvariancesof themeasured

ecosystem properties Data presented in figures were extractedusing the Figure Calibration plugin in ImageJ (Schneider RasbandEliceiriSchindelinampArganda‐Carreras2012)

22emsp|emspModerating variables

We collected data on three moderators aridity disturbance areaand disturbance age We extracted values of the aridity index(precipitationpotential evapotranspiration) for each location fromthe Consultative Group for International Agricultural ResearchConsortium for Spatial Information (CGIAR‐CSI) Global‐AridityDatabase (httpwwwcgiar‐csiorg Zomer Trabucco Bossio ampVerchot2008)Wetooktheadditiveinverseofthearidityindex(iearidity=minus1timesaridityindex)sothathighervaluescorrespondedtogreaterdrynessThedisturbanceareaandbodymassofeachverte-bratespecieswereextractedfromvarioussources(seeSupportingInformationAppendixS2)Disturbanceareawascalculatedas thetotal horizontal areaofdisturbed soil includingunderground tun-nels and ejectamounds Aridity and disturbance areawere log(x)transformedtoimprovenormalityandz‐transformed(standardized)inordertoimprovetheinterpretationofregressioncoefficientsbyputtingthemallonacommonscale(Schielzeth2010)

Exactdisturbanceagewasrarelyreportedasthiscanusuallyonlybedeterminedinartificialdisturbancesbutwewereabletoextracta binary variable frommost studies comprising fresh disturbances(lt1yearold)andolddisturbances(ge1yearold)lsquoActiversquoorlsquooccupiedrsquosoildisturbancesweretreatedasfreshdisturbancesalthoughweac-knowledgethatthisapproachiscoarseanddoesnotcapturethecom-plexitiesofdisturbancehistoryFreshdisturbanceswereassignedavalueofminus1andolddisturbancesavalueof1suchthatthemeanwasapproximately0andstandarddeviationapproximately1andthere-forethevariablecouldbereliablycomparedwithotherstandardizedmoderators(seeGelman2008)NotethatthiscodingdoesnotallowforthecalculationofseparateslopesforfreshandolddisturbancesRatherthesingleslopeestimateindicatestherelativeeffects(slopeispositivewhentheeffectisgreaterinolddisturbances)

23emsp|emspData analysis

Toexaminethemeaneffectsofsoildisturbancewecalculatedthelog response ratio lnRR for eachdatapair (HedgesGurevitchampCurtis1999)Thelogresponseratiowascalculatedasln(xD)ndashln(xU)where xD isthemeanvalueforthedisturbedsiteandxUthevaluefor the undisturbed site Thus negative values of lnRR representsituationswheresoildisturbancereducesaparticularpropertyandviceversaWeusedasingleimputationtomanagezerosinthedataset which comprised 07 of all effect sizes (Lajeunesse 2013Nakagawa2015)That iswhenxD=0weset lnRRtothe lowestvalueoflnRRinthedatasetandthensolvedforxDThesamepro-cesswasusedtoreplacezerosinundisturbedmeansbutinthiscasewesetlnRRtothehighestvalueForzerosinstandarddeviation(SD)weperformedalinearregressionof ln(x)~ln(SD)andusedthere-gressioncoefficientstoback‐calculateSDvalues(Nakagawa2015)


Ourfinaldatasetincluded24ecosystempropertiesPropertieswithfewerthan10effectsizesandthatcouldnotbegroupedintoother properties were removed (eg biocrust richness) The finaldatasetcomprised1609effectsizes from149studiespublishedfrom1941to2016(seeAppendix)

The interceptmodel (iemeta‐analysis) andmeta‐regressionwereperformedinR(RCoreTeam2017)usingthemetafor pack-age version 19ndash8 (Viechtbauer 2010) The intercept model isthemodel thatderives the centre and spreadof all effect sizeswhilethemeta‐regressionincorporatesmoderators(fixedeffects)toaccountforvariation intheeffectsizesTheestimatederivedfromtheinterceptmodelislargelyuninformativebecauseweex-pectmany of the ecosystem effects of soil disturbance to havedifferentsignsandeffectivelycanceloutHowevertheinterceptmodel is useful in partitioning variance among random factorswhichinthiscasearephylogenyspeciesstudyandresidualvari-ancePhylogenywasimplementedasacorrelationmatrixderivedfromanultrametricphylogenetic treewhichwasbasedondataprovided by theOpen Tree Taxonomy (Hinchliff Smith AllmanBurleighampChaudhary2015)Thetransformationbetweenphylo-genetictreeandcorrelationmatrixusingthelsquovcvrsquofunctionintheRpackageape (ParadisClaudeampStrimmer2004)assumedtheBrownianmodelofevolutionTheinterceptmodelenabledustopartitionthevarianceamongrandomfactorsI2(heterogeneity)isthevariationamongeffectsizesthat isnotaccountedforbythesamplingerrorvariance(HigginsampThompson2002)Themeta‐re-gressionincludedfourmoderatorsndashdisturbanceagedisturbancearea property and the interaction of property and aridity ndash inadditiontothefourrandomeffectsAsameasureofvarianceineachmodelwecreatedacovariancematrixtoaccountforeffectsizeswith sharedcontrols (NobleLagiszampOdeaampNakagawa2017) True intercepts and standard errors were calculated foreach levelofecosystempropertysothatresultsreflectedgroupmeansratherthancontraststoareferencegroupWeconsideredaresultsignificantwhenthe95confidenceinterval(CI)didnotcrosszeroWecalculatedthevarianceaccountedbymoderatorsasmarginalR2(sensuNakagawaampSchielzeth2013)

Onlytwovertebratespeciesweremeasuredintheirnon‐nativerangetheEuropeanrabbit(Oryctolagus cuniculus)andthewildboarThesespecieswerealsomeasuredintheirnativerangesallowingustoexploredifferencesinsoildisturbanceeffectsamongnativeandnon‐native ranges Ecosystem engineers in non‐native ranges areknowninsomecasestopromotefurtherinvasionsofexoticspeciessoonedifferencemightbeagreatereffectonbioticcompositioninthenon‐nativerange(Crooks2002)Wethereforeconductedasep-aratemeta‐regressionwithrangestatusasafixedeffectandstudyasarandomeffectusingonlydatafromthesetwospecies(N=235)Thesedatawere insufficient to include interactionswithdifferentecosystempropertiesinthemodel

24emsp|emspPublication bias

Funnel plots were produced by plotting the precision (or inversestandard error) of log response ratios against the meta‐analytic

residuals (sensuNakagawaampSantos2012)whichwereextractedusing Markov chain Monte Carlo techniques in the R packageMCMCglmm version 224 (Hadfield 2010 Hadfield amp Nakagawa2010) We also performed a trim‐and‐fill test (Duval amp Tweedie2000)usingtheR0estimatorandamodifiedversionofEggerregres-sion(sensuSterneampEgger2005)toassesspublicationbias

3emsp |emspRESULTS

31emsp|emspVariety and extent of soil disturbances by vertebrates

Our final data set included 64 vertebrate animal species 60 ofwhichweremammalsand40ofwhichwererodents(seeSupportingInformationAppendixS2)Birdsandreptilesweremarkedlyunder-representedVertebrateengineerscausedfivetypesofsoildistur-banceburrows(734ofanimals)foragingdigs(172)restingdigs(31)areasoftrampledsoil(16)andwallows(16)Twoanimalsinthedatasetthegreaterbilby(Macrotis lagotis)andtheburrowingbettong(Bettongia lesueur)haddocumentedeffectsofbothforagingdigsandmuchlargerburrowsThedistributionofanimalmasswashighlyskewedtowardssmalleranimalswith75ofspeciesweigh-inglessthan5kgalthoughthestudydidincludeseveral largeun-gulates(seeSupportingInformationAppendixS2)Wildboarwhichdisturbsoilwhileexcavatingplanttubersandfossorialanimalscon-stituted20oftheextractedestimates(15ofstudies)themostofanyincludedspeciesLargeranimalstendedtoproducesmallforag-ingdigsandrestingformsratherthanburrowswhichweregenerallymorespatiallyexpansive

Thevastmajorityofstudies(953)wereconductedinthemid‐latitudeswiththeremainingstudies(47)beingconductedinthetropics(Figure2)TheUSAwasanareaofparticularlyhighresearchoutput (46 of studies) Apart from tundra (Ntundra = 4) allmajorcommunity typeswerewell represented (Nforest =261Nwoodland =212Nshrubland=458Ngrassland=674)

32emsp|emspEffects of soil disturbance on ecosystem properties

Ourmeta‐analysisshowedthatsoildisturbancedidnotconsistentlyenhanceor reduce thestudiedecosystemproperties [lnRR0039(95CI minus0053ndash0130) Table1]Rather theeffectsof soil dis-turbancevariedamongproperties (Figure3Table2)Disturbancesignificantlyenhancedplantrecruitmentandproductivitybothby32andsoilnitrogenandphosphorusby77and35respectivelyDisturbedareasalsohadmorebaresoil (126)andmoresecond-ary vertebrates (eg various birds and lizards) using the space ashabitat (1233)Theabundancesofvascularplantsandbiocrustswerereducedby23and82respectivelyandrun‐offwasreducedby 63Although not significant disturbance generally increasedsoilrespirationclaycontentinvertebrateactivityandsoilmoisturewhilereducingsoilcompactionandstability

ThemarginalR2fromthemeta‐regressionmodelwas2752Theeffectsofsoildisturbancedidnotvarysignificantlywithdisturbance


area[lnRRminus0056(95CIminus0151ndash0039)]Howeverdisturbancesge1yearoldweremoredistinctfromundisturbedcontrols(typicallythesurroundingmatrix) thanfreshdisturbancesModellingthe in-teractionofecosystempropertyandaridityrevealedthatformostpropertiesdisturbancesbecameincreasinglydistinctfromthesur-roundingmatrixasaridityincreased(Figure3)Mostnotablydistur-banceeffectsonsoilnitrogenandphosphorussoilrespirationandplantproductivityanddensityweregreaterinmorearidsystemsBycontrasttheeffectsofsoildisturbanceonbiocrustabundancerootbiomassandtheabundanceofsecondaryvertebratesweregreaterinmorehumidsystems

We found very high heterogeneity in the intercept model (I2 = 997) which indicates a high degree of unexplained variation(Table1)Soil‐disturbingactivitieswerelargelyunrelatedtothephy-logeneticrelatednessofanimalspecies(I2[phylogeny]lt001)butweresimilar within a species (I2[species] = 024) Themodel also showedmoderatebetween‐studyvariance(I2[study]=255)andhighvarianceattheeffectsizelevel(I2[residual]=718)

For European rabbits andwild boar therewere negligible dif-ferences in soil disturbance effects among native and non‐nativeranges(SupportingInformationAppendixS3)


Visualinspectionrevealednoobviousasymmetryinthefunnelplot(Figure4)Trim‐and‐filltestssupportedthisassertionestimatingnomissing studies Egger regression further indicated no significantpublicationbiasinthedata(z=1751p=080)

4emsp |emspDISCUSSION

Muchhasbeenwrittenonthenon‐trophicengineeringeffectsofsoil‐disturbinganimalsonpropertiesasbroadassoilchemistryhab-itatameliorationandplantcommunitydynamics (HastingsByersCrooks Cuddington amp Jones 2007 Lavelle Decaeumlns AubertBarotampBlouin2006WrightJonesampFlecker2002)DespitethislargebodyofworktherehasbeennoquantitativeglobalsynthesisofanimaleffectsonecosystemsacrossthefullrangeofecosystempropertiesHereweusedanextensiveglobaldatasetofpeer‐re-viewedliteraturetoassessthenon‐trophiceffectsofsoil‐disturb-ing vertebrates Compared with undisturbed soil we found thatsoildisturbancereducedplantabundancebiocrustabundanceand

F I G U R E 2 emspWorldmapshowingthelocationsofallincludedstudiesofsoil‐disturbingvertebrates

TA B L E 1 emspSummaryofglobalmeta‐analysisofsoil‐disturbingvertebrates(n=numberofeffectsizesk=numberofsoil‐disturbingspeciesCI=confidenceinterval)

n k Estimate SE I2[total] I2

[phylogeny] I2[species] I2

[study] I2[residual] Lower CI (5) Upper CI (95)

1609 64 0039 0047 997 000 024 255 718 minus0053 0130


run‐offandenhancedsoilnitrogensoilphosphorusplantproduc-tivityplant recruitment theabundanceofsecondaryvertebratesand thecoverofbare soilMostof theseeffects intensifiedwithincreasing aridityDisturbances that had recovered for at least 1year were more distinct from the surrounding matrix than fresh

disturbancesTherewasnoevidence that thephylogenyofengi-neersisanimportantdeterminantoftheirecosystemeffectsOurstudyprovidesstrongempiricalevidencethatsurfacedisturbancebyvertebrateengineershassubstantialeffectsonarangeofeco-systemproperties

F I G U R E 3 emspTheeffectsofdisturbanceageandarea(lsquomaineffectsrsquo)onvertebratesoildisturbanceandtheeffectsofvertebratesoildisturbanceonecosystempropertiesandtheinteractionofpropertiesandariditySignificantresultsareshowninred(negative)andblue(positive)anderrorbarsrepresent95confidenceintervalsOnepropertytheabundanceofsecondaryvertebrateswasexcludedfromthefigureforgraphicalreasons(butseeTable2)


TA B L E 2 emspSummaryofmeta‐regressionmodel(R2=2752n=numberofeffectsizesk=numberofsoil‐disturbingspecies)

Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)

Disturbanceage

1609 64 0091 003 0032 0149

Disturbancearea

1609 64 minus0056 0049 minus0151 0039

Property Baresoil 33 15 0817 0133 0557 1077

Biocrustabundance 15 6 minus1695 0228 minus2141 minus1249

Clay 24 9 0198 015 minus0096 0492

Invertebrateabundance 47 7 0169 0166 minus0157 0494

Invertebraterichness 14 6 0153 021 minus0259 0565

Litter 65 15 minus0241 0111 minus0457 minus0024

Microbialactivity 46 10 0062 0123 minus018 0303

Plantabundance 228 28 minus0256 0076 minus0405 minus0107

Plantdensity 46 9 0228 0154 minus0075 053

Plantheight 23 6 minus0593 0176 minus0938 minus0247

Plantproductivity 96 24 0275 0096 0086 0463

Plantrecruitment 61 12 0278 0139 0006 055

Plantrichness 220 31 minus0027 0071 minus0165 0111

Rootbiomass 29 10 minus0477 0149 minus0769 minus0185

Run‐off 21 6 minus0983 02 minus1375 minus059

Soilcompaction 69 17 minus0177 0095 minus0364 001

SoilC 125 23 minus0026 0082 minus0186 0134

Soilinfiltration 39 8 0131 0178 minus0217 0479

SoilN 158 28 0569 0079 0413 0724

SoilP 58 16 0298 0116 007 0526

SoilpH 67 18 002 0094 minus0165 0205

Soilrespiration 12 6 031 0226 minus0133 0752

Soilstability 17 5 minus0222 0189 minus0593 0148

Soilmoisture 67 15 0156 01 minus004 0351

Vertebrateabundance 29 3 2591 0752 1117 4065

Propertyaridity

Baresoil 33 15 minus0113 0118 minus0344 0118


Clay 24 9 0293 0269 minus0234 0819



Litter 65 15 0259 0185 minus0103 062


Plantabundance 228 28 0327 0168 minus0003 0657

Plantdensity 46 9 0491 0189 0121 0862

Plantheight 23 6 minus0303 0268 minus0828 0222


Plantrecruitment 61 12 0266 0267 minus0258 079

Plantrichness 220 31 024 0172 minus0097 0578


Run‐off 21 6 minus0268 0277 minus081 0274

Soilcompaction 69 17 0183 0197 minus0203 0569

SoilC 125 23 0319 0184 minus0042 0679(Continues)


In general the findings from our meta‐analysis are consistentwithourpredictions It isclearthatburrowsare importanthabitatforsecondaryvertebrateswith12timesgreaterabundancesthanundisturbedsurfacesInsomecasessecondaryburrowinhabitantscanfurthermodifythedisturbanceinitiatingaldquoburrowingcascaderdquo(KinlawampGrasmueck 2012) Unsurprisingly run‐offwas reducedbydisturbancewhichisknowntoenhancesoilporosityandbreakup hydrophobic soil crusts (Platt et al 2016) Elevated levels ofsoil nitrogen and phosphorus in disturbances are probably due totrappedorganicmatter(JamesEldridgeampHill2009)andinsomecasesnutrient‐richsoilsbeingtranslocatedfromdeepersoillayersduringexcavation(Plattetal2016)Non‐engineeringeffectssuchasexcretionsand food residue leftby theanimal couldhavealsoplayedaroleinthisnutrienteffect(Plattetal2016)Ouranalysisrevealedthatsoildisturbancespromoteplantrecruitmentandpro-ductivity reinforcing the notion that disturbances are favourablesitesforplantgerminationandgrowthlargelyduetotheelevatednutrient levels (Alkon 1999 James et al 2009) The finding that

disturbances reducedplantheight isprobablyconfoundedbybur-rowinganimalsactivelyconsumingorclearingvegetationaroundtheburrow(AriasQuintanaampCagnoni2005EldridgeampMyers2001WhickerampDetling1988)

Given that disturbance generally promotes plant recruitmentthe finding that soil disturbance reduces plant abundance mightseemcounter‐intuitiveHowevermost(73)oftheplantabundancemeasurementswererecordedwithin1yearofthedisturbancebeingcreatedThesedataarethuslikelytorepresentatemporaryphasebetweenplantsbeingclearedorsmotheredduringexcavationandnewplantsrecolonizingRatesofplantrecolonizationonsoildistur-bancesarenotwellknownbutinahumidgrasslandsystemRogersHartnett andElder (2001) found that plant richness and biomassrecoveredtopre‐disturbancelevelsafter2yearsIncreasesinbaresoilcoverarealso in largepartrepresentativeoftheinitialphaseofpost‐disturbancerecoverywith76ofmeasurementsrecordedwithin1yearofdisturbanceAlthoughbiocrusteffectsaresimilarlybiased disturbancesmight also reduce biocrust abundance in the

F I G U R E 4 emspFunnelplotshowingprecision(inversestandarderror)againstmeta‐analyticresidualsfromthemeta‐regressionmodeloftheeffectsofvertebratesoildisturbanceThedashedlinerepresentsthemeta‐analyticmeanlnRR=logresponseratio



SoilN 158 28 0354 018 0001 0707

SoilP 58 16 0476 0207 0071 088

SoilpH 67 18 0268 019 minus0105 064

Soilrespiration 12 6 0608 0217 0182 1034

Soilstability 17 5 021 0304 minus0385 0806


Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023

TABLE2emsp(Continued)


longtermbypromotingvascularplantrecruitmentandproductivityVascularplantstendtosuppressbiocruststhroughshadingandlitterfall(ZhangAradottirSerpeampBoeken2016)

Soil disturbance initiates substantial shifts in biotic communitycomposition so that accreting and eroding surfaces often supporta community that is distinct from the surrounding matrix (ApletAndersonampStone1991Goacutemez‐GarciaBorghiampGiannoni1995JonesHalpernampNiederer 2008) Shiftsmay occur stochasticallyorbecausedisturbances favourorganismswithparticular resourcerequirementsortraitsrelatingtocolonizationanddisturbancetoler-ance(EldridgeampJames2009)Paststudieshavegenerallyobservedashifttowardsmoreannualplantdominatedcommunities(Eldridgeamp Simpson 2002 Kyle Kulmatiski amp Beard 2008Moroka BeckampPieper 1982)While disturbances often support distinct speciesassemblagesoverallrichnessmaynotchangeOurfindingthatsoildisturbance did not have a significant effect on plant or inverte-braterichnesseitherindicatesthatrichnesstendstobemaintainedthroughcompositionalshiftsorthatrichnesseffectsarehighlyvari-ableamongdifferentsystemsThelatterexplanationissupportedbyRoot‐BernsteinandEbensperger(2013)whoreportthatsoildistur-bancetendstohavestrongnegativeorpositiveeffectsonrichnessdependingonfactorssuchasstudyscaleandfertilityAlthoughunde-tectablebyourpatch‐scaleanalysisreportedshiftsinbioticcompo-sitionindicatethatsoildisturbanceplaysacriticalroleinmaintainingamosaicofpatchesatthelandscapescale(EldridgeampJames2009Korn amp Korn 1989 Yoshihara Ohkuro Bayarbaatar amp Takeuchi2009)ForexampleMcMillanPfeiffer andKaufman (2011) foundthat16oftheirrecordedplantspeciesonlyoccurredinbisonwal-lowsimplyingthatsoildisturbancescanbearefugeforspeciesthatcannotpersistelsewhereParallelscanbedrawntoother formsofdisturbancesuchasfireortreefallswhichalsopromotespeciesrich-nessbyenhancingenvironmentalheterogeneity(JonssonampEsseen1990SaffordampHarrison2004SteinGerstnerampKreft2014)

Arecurringissueinthebiopedturbationliteratureisthelackoftemporalreplication(Cogganetal2018)Whilesomeeffectsofsoildisturbanceare instantaneous (egenhancedsurfacerough-ness)othersoccurafterseveralmonthsoryearsTheseeffectsarealsovariableintimeForexampleGuttermanGolanandGarsani(1990)reportthatplantrichnessandbiomassfollowedaunimodalrelationship with time such that they were maximized when aporcupine (Hystrix indica) digging was 50ndash60 infilled Using acoarse binary indexwewere able to detect a general effect ofdisturbanceageindicatingthatmanyeffectsofdisturbancemayintensifywithageAlthoughwewereunabletomodeltheinterac-tionofageandecosystempropertyduetostatistical limitationsweexpect thiseffect isdrivenbysoilnutrientswhichgraduallyaccrueovertimeandpropertiesassociatedwithplantswhichre-colonizeovermonthsoryearsdependingoncertaintraits(RogersampHartnett2001)Furtherstudiesareneededtoimproveourun-derstandingof theprogressionofecosystemeffects throughoutthelifeofasoildisturbance

Itisthoughtthatdisturbancesareparticularlyimportantindry-lands creating fertile lsquoislandsrsquo of locally elevated nutrients which

canbetheonlynichesabletosupportbioticactivityintheotherwiseresource‐poormatrix(GarnerampSteinberger1989JamesampEldridge2007 Ochoa‐Hueso Eldridge Delgado‐Baquerizo Soliveres ampBowker2018)Thisassertionwasborneout inour resultswhichshowedthattheeffectsofsoildisturbanceonmostproperties in-tensifiedwith increasing aridity The role of soil‐disturbing verte-bratesasasourceofheterogeneity is thusmore important in lowproductivitysystemsWefoundsignificantpositiveinteractionsbe-tweenaridityandplantproductivityanddensityandsoilPandNOurworkalsosuggeststhereforethattheeffectsofsoil‐disturbinganimalson thesepropertieswill increaseasglobaldrylandsexpe-rienceshiftsto lowerrainfallandhighertemperatures (HuangYuGuanWangampGuo 2016) For example disturbancesmight par-tiallymediatereductionsinplantproductivitywithincreasesinarid-itySimilarlysoilPwhichislargelyunderabioticcontrolandderivedmainlyfromparentmaterial(LambersBrundrettRavenampHopper2011) is likely to increasewith the increasedsoildisturbanceanderosionthattypicallyaccompaniesincreasedaridity

Ourstudyfailedtofindanimportanteffectofphylogenyindi-catingthateffectsarenotphylogeneticallycontrolledandthereforethat the same functionality could readily evolve in different taxaHowevergiventhat94oftheecosystemengineers inourstudyweremammals (67ofwhichwererodents)additionalstudiesontheeffectsofsoildisturbancebyamphibiansreptilesandbirdsarenecessarytoconfirmtherearenophylogeneticeffectsWedidfindthatengineersfromthesamespeciestendedtohavesimilardistur-banceeffectswhichcouldbedrivenbysimilarities indisturbancemorphologies and rates of production (Eldridge Koen KillgoreHuangampWhitford2012)Withrespecttoboarandrabbitdistur-bances the finding thateffectswereconsistentacrossnativeandnon‐nativerangesindicatesthatecosystemsrespondsimilarlytothesametypeofdisturbance

There is considerable misunderstanding of the ecological im-portanceofecosystemengineersgloballySomeengineeringfaunasuchasplateaupikas(Ochotona spp)andzokors(Eospalax spp)areactivelyexterminatedduetotheperceptionthattheycompetewithlivestockforforageandthattheydegradeecosystemsthroughtheirsoildisturbance(Fanetal1999ZhangZhangampLiu2003)Thisperceptionisthoughttohaveoriginatedfromaspuriouscorrelationbetweenthedensitiesoftheserodentsandgrasslanddegradation(SmithZahlerampHinds2006)Itisnowwellestablishedthatover-grazingwas themaincauseof thedegradation and thedegradedstate provided favourable conditions for pikas and zokors (Zhanget al 2003)There ismountingevidence thatplateaupikas facili-tatenutrientcyclingandgrassproductivitythroughburrowingal-thoughtheseeffectsaredependentonpopulationdensity(PangampGuo2017YuPangWangJinampShu2017)Giventheirimportantrole in ecosystemswewould expect the loss of ecosystem engi-neerssuchaspikastohavesubstantialconsequencesforecosystemfunctioning (Fleming Anderson Prendergast Bretz amp Valentine2014)Reintroducinglocallyextinctengineersorintroducingnovelengineersmay prove to be a viable strategy tomanage degradedlandscapes(ManningEldridgeampJones2015)


41emsp|emspConcluding remarks

Therestillremainsmuchtobelearnedabouttheeffectsofsoildis-turbanceonecosystemssuchastherolesofbirdsandreptilesandwhether the reintroductionof locallyextinctengineerscouldhelpto restore ecosystem functions to states that were typical priortoanthropogenic changeWhilenot all theeffectswouldbecon-sidered facilitatory (eg biocrust abundance is reduced by distur-bance)ourstudyhighlightsthefactthatvertebrateengineersplayanimportantroleinecosystemscreatingamosaicofnutrient‐richhighlyproductivepatchesGiventhatengineersdisturb034ndash30ofthesoilsurfaceannuallyinareaswheretheyareprevalent(BraggDonaldsonampRyan2005HobbsampMooney1985)andasingleen-gineering organism can displace up to 48 tonnes of soil per year(GarkaklisBradleyampWooller2004)vertebratedisturbancesareamajorsourceofheterogeneityatfinespatialscalesLikeotherdis-turbancessuchasfiretheenvironmentalheterogeneitycreatedbysoil disturbance is a substantial driver of biodiversity at the land-scapescale(DavidsonampLightfoot2008)

ACKNOWLEDGMENTS

WeacknowledgetheUniversityofNewSouthWales(UNSW)FacultyofScienceforprovidingfinancialsupportintheformofaSummerVacationResearchScholarshipSNwassupportedbyanAustralianResearch Council (ARC) Future Fellowship (FT130100268) WethankSamanthaTraversforvaluablecommentsonthemanuscript

DATA ACCESSIBILITY

AlldataandcodesupportingtheresultshavebeendepositedintheOpenScienceFramework1017605OSFIOCA7QK

ORCID

Max Mallen‐Cooper httpsorcidorg0000‐0002‐8799‐8728

David J Eldridge httpsorcidorg0000‐0002‐2191‐486X

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Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763

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Eldridge D J amp Koen T B (2008) Formation of nutrient‐poorsoil patches in a semi‐arid woodland by the European rabbit(Oryctolagus cuniculus L) Austral Ecology 33 88ndash98 httpsdoiorg101111j1442‐9993200701793x

EldridgeD J Koen T B Killgore AHuangN ampWhitfordWG(2012)Animalforagingasamechanismforsedimentmovementandsoil nutrient development Evidence from the semi‐arid Australianwoodlands and theChihuahuanDesertGeomorphology157 131ndash141httpsdoiorg101016jgeomorph201104041

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EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078

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contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014

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Goacutemez‐GarciaDBorghiCampGiannoni S (1995)Vegetationdiffer-encescausedbypinevolemoundbuildinginsubalpineplantcommu-nitiesintheSpanishPyreneesPlant Ecology11761ndash67httpsdoiorg101007BF00033259

Gutterman Y (1987)Dynamics of porcupine (Hystrix indica Kerr) dig-gingsTheirroleinthesurvivalandrenewalofgeophytesandhemic-ryptophytesintheNegevDeserthighlandsIsrael Journal of Botany36133ndash143

Gutterman Y Golan T amp GarsaniM (1990) Porcupine diggings asauniqueecological system inadesertenvironmentOecologia85122ndash127httpsdoiorg101007BF00317352

Hadfield JD (2010)MCMCmethods formulti‐responsegeneralizedlinearmixedmodelsTheMCMCglmmRpackageJournal of Statistical Software331ndash22

Hadfield J amp Nakagawa S (2010) General quantitative geneticmethods for comparative biology Phylogenies taxonomiesand multi‐trait models for continuous and categorical charac-ters Journal of Evolutionary Biology 23 494ndash508 httpsdoiorg101111j1420‐9101200901915x

Hastings A Byers J E Crooks J A Cuddington K Jones C GLambrinos J G hellip Wilson W G (2007) Ecosystem engineer-ing in space and time Ecology Letters 10 153ndash164 httpsdoiorg101111j1461‐0248200600997x

HedgesLVGurevitchJampCurtisPS(1999)Themeta‐analysisofre-sponseratiosinexperimentalecologyEcology801150ndash1156httpsdoiorg1018900012‐9658(1999)080[1150TMAORR]20CO2

Higgins J amp Thompson SG (2002)Quantifying heterogeneity in ameta‐analysis Statistics in Medicine 21 1539ndash1558 httpsdoiorg101002sim1186

HinchliffCESmithSAAllmanJFBurleighJGChaudharyRhellipCranstonKA(2015)Synthesisofphylogenyandtaxonomyintoacom-prehensivetreeoflifeProceedings of the National Academy of Sciences USA11212764ndash12769httpsdoiorg101073pnas1423041112

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James A I amp Eldridge D J (2007) Reintroduction of fossorial na-tivemammalsandpotential impactsonecosystemprocesses inanAustralian desert landscapeBiological Conservation138 351ndash359httpsdoiorg101016jbiocon200704029

JamesA I EldridgeD JampHillBM (2009)Foraginganimals cre-atefertilepatchesinanAustraliandesertshrublandEcography32723ndash732httpsdoiorg101111j1600‐0587200905450x

Jones C C Halpern C B amp Niederer J (2008) Plant suc-cession on gopher mounds in western Cascade mead-ows Consequences for species diversity and heterogeneityThe American Midland Naturalist 159 275ndash286 httpsdoiorg1016740003‐0031(2008)159[275PSOGMI]20CO2

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JonssonBGampEsseenP (1990)TreefalldisturbancemaintainshighbryophytediversityinaborealspruceforestThe Journal of Ecology78924ndash936httpsdoiorg1023072260943

Kerley G I ampWhitfordW G (2000) Impact of grazing and de-sertification in the Chihuahuan Desert Plant communitiesgranivores andgranivoryThe American Midland Naturalist14478ndash91 httpsdoiorg1016740003‐0031(2000)144[0078IOGADI]20CO2

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KinlawAampGrasmueckM (2012)EvidenceforandgeomorphologicconsequencesofareptilianecosystemengineerTheburrowingcas-cadeinitiatedbythegophertortoiseGeomorphology157108ndash121httpsdoiorg101016jgeomorph201106030

Korn H amp Korn U (1989) The effect of gerbils (Tatera brantsii) onprimary production and plant species composition in a southernAfrican savanna Oecologia 79 271ndash278 httpsdoiorg101007BF00388488

Kyle G P Kulmatiski A amp Beard K H (2008) Influence ofpocket gopher mounds on nonnative plant establishment in ashrubsteppe ecosystemWestern North American Naturalist 68374ndash381 httpsdoiorg1033981527‐0904(2008)68[374IOPGMO]20CO2

LajeunesseMJ (2013)Recoveringmissingorpartialdatafromstud-ies A survey of conversions and imputations for meta‐analysisIn J Koricheva J Gurevitch amp KMengersen (Eds)Handbook of meta‐analysis in ecology and evolution (pp 195ndash206)NJ PrincetonUniversityPress

Lambers H Brundrett M C Raven J A amp Hopper S D (2011)Plant mineral nutrition in ancient landscapes High plant speciesdiversity on infertile soils is linked to functional diversity for nu-tritional strategies Plant and Soil 348 7 httpsdoiorg101007s11104‐011‐0977‐6

Lantz S J Conway C J amp Anderson S H (2007)Multiscale hab-itat selection by burrowing owls in black‐tailed prairie dog colo-nies Journal of Wildlife Management 71 2664ndash2672 httpsdoiorg1021932006‐221

Lavelle P Decaeumlns T Aubert M Barot S Blouin M Bureau Fhellip Rossi J P (2006) Soil invertebrates and ecosystem servicesEuropean Journal of Soil Biology42S3ndashS15

Machicote M Branch L C amp Villarreal D (2004) Burrowingowls and burrowing mammals Are ecosystem engineers in-terchangeable as facilitators Oikos 106 527ndash535 httpsdoiorg101111j0030‐1299200413139x

Manning A Eldridge D amp Jones C (2015) Policy implications ofecosystem engineering for multiple ecosystem benefits In D PArmstrongMWHaywardDMoroampPJSeddon(Eds)Advances in reintroduction biology of Australian and New Zealand fauna(pp167ndash184)ClaytonSouthAustraliaCSIROPublishing

McMillanBRPfeifferKAampKaufmanDW(2011)Vegetationre-sponsestoananimal‐generateddisturbance(bisonwallows)intall-grass prairieThe American Midland Naturalist165 60ndash73 httpsdoiorg1016740003‐0031‐165160

MorokaNBeckRFampPieperRD(1982)Impactofburrowingac-tivityofthebannertailkangarooratonsouthernNewMexicodesertrangelandsJournal of Range Management35707ndash710httpsdoiorg1023073898244

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NakagawaSampSantosES(2012)Methodologicalissuesandadvancesin biological meta‐analysis Evolutionary Ecology 26 1253ndash1274httpsdoiorg101007s10682‐012‐9555‐5


NakagawaSampSchielzethH(2013)AgeneralandsimplemethodforobtainingR2fromgeneralizedlinearmixed‐effectsmodelsMethods in Ecology and Evolution4133ndash142

Noble D W Lagisz M Orsquodea R E amp Nakagawa S (2017)Nonindependenceandsensitivityanalyses inecologicalandevolu-tionarymeta‐analysesMolecular Ecology262410ndash2425httpsdoiorg101111mec14031

Ochoa‐HuesoR EldridgeD JDelgado‐BaquerizoM Soliveres SBowkerMAGrossNhellipMaestreFT(2018)Soilfungalabun-dance and plant functional traits drive fertile island formationin global drylands Journal of Ecology 106 242ndash253 httpsdoiorg1011111365‐274512871

Pang X P ampGuo ZG (2017) Plateau pika disturbances alter plantproductivity and soil nutrients in alpinemeadows of theQinghai‐TibetanPlateauChinaThe Rangeland Journal39133ndash144httpsdoiorg101071RJ16093

Paradis EClaude JampStrimmerK (2004)APEAnalysesof phylo-genetics and evolution inR languageBioinformatics20 289ndash290httpsdoiorg101093bioinformaticsbtg412

PlattBFKolbDJKunhardtCGMiloSPampNewLG(2016)BurrowingthroughtheliteratureTheimpactofsoil‐disturbingver-tebratesonphysicalandchemicalpropertiesofsoilSoil Science181175ndash191httpsdoiorg101097SS0000000000000150

PrughLRampBrasharesJS(2012)Partitioningtheeffectsofaneco-system engineer Kangaroo rats control community structure viamultiplepathways Journal of Animal Ecology81667ndash678httpsdoiorg101111j1365‐2656201101930x

RCoreTeam(2017)RAlanguageandenvironmentforstatisticalcom-puting R Foundation for Statistical Computing Vienna AustriahttpswwwR‐projectorg

RogersWEampHartnettDC(2001)Temporalvegetationdynamicsandrecolonizationmechanismsondifferent‐sizedsoildisturbancesin tallgrass prairie American Journal of Botany 88 1634ndash1642httpsdoiorg1023073558408

RogersWEHartnettDCampElderB(2001)Effectsofplainspocketgo-pher(Geomys bursarius)disturbancesontallgrass‐prairieplantcommu-nitystructureThe American Midland Naturalist145344ndash357httpsdoiorg1016740003‐0031(2001)145[0344EOPPGG]20CO2

RomeroGQGonccedilalves‐Souza TVieiraCampKoricheva J (2015)Ecosystemengineeringeffectson speciesdiversity across ecosys-temsAmeta‐analysisBiological Reviews90877ndash890httpsdoiorg101111brv12138

Root‐BernsteinM amp Ebensperger L A (2013)Meta‐analysis of theeffects of small mammal disturbances on species diversity rich-ness and plant biomass Austral Ecology 38 289ndash299 httpsdoiorg101111j1442‐9993201202403x

SaffordHDampHarrisonS(2004)Fireeffectsonplantdiversityinser-pentinevs sandstonechaparralEcology85 539ndash548httpsdoiorg10189003‐0039

SchielzethH (2010) Simplemeans to improve the interpretability ofregressioncoefficientsMethods in Ecology and Evolution1103ndash113httpsdoiorg101111j2041‐210X201000012x

SchneiderCARasbandWSampEliceiriKW(2012)NIHimagetoim-ageJ25yearsofimageanalysisNature Methods9671ndash675httpsdoiorg101038nmeth2089

SmithATZahlerPampHindsLA(2006)ConservationBiologyinAsiaIn JAMcNeelyTMMcCarthyASmithampLOlsvig‐Whittaker(Eds) Society for Conservation Biology Asia Section and Resources Himalaya Foundation(pp285ndash293)KathmanduNepal

Stein A Gerstner K amp KreftH (2014) Environmental heterogene-ityasauniversaldriverofspeciesrichnessacrosstaxabiomesandspatialscalesEcology Letters17866ndash880httpsdoiorg101111ele12277

Sterne J A amp Egger M (2005) Publication bias in meta‐analysisPreventionassessmentandadjustmentsInHRothsteinASutton

ampMBorenstein(Eds)Regression methods to detect publication and other bias in meta‐analysis(pp99ndash110)ChichesterUKWiley

Valentine L EBretzMRuthrofKX FisherRHardyG E S JampFlemingPA (2017)ScratchingbeneaththesurfaceBandicootbioturbationcontributestoecosystemprocessesAustral Ecology42265ndash276httpsdoiorg101111aec12428

ViechtbauerW(2010)Conductingmeta‐analysesinRwiththemetaforpackageJournal of Statistical Software361ndash48

Whicker A D amp Detling J K (1988) Ecological consequencesof prairie dog disturbances BioScience 38 778 httpsdoiorg1023071310787

WhitfordWGampKayFR(1999)Biopedturbationbymammalsindes-ertsAreviewJournal of Arid Environments41203ndash230httpsdoiorg101006jare19980482

WiensJA(1989)SpatialscalinginecologyFunctional Ecology3385ndash397httpsdoiorg1023072389612

Wright J P Jones C G amp Flecker A S (2002) An ecosystem engi-neer the beaver increases species richness at the landscape scaleOecologia13296ndash101httpsdoiorg101007s00442‐002‐0929‐1

YoshiharaYOhkuroTBayarbaatarBampTakeuchiK(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialhet-erogeneityofvegetationatmultiplespatialscalesGrassland Science5589ndash95

YuCPangXPWangQJinSHShuCCampGuoZG(2017)Soilnutrientchanges inducedby thepresenceand intensityofplateaupika(Ochotona curzoniae)disturbancesintheQinghai‐TibetPlateauChina Ecological Engineering 106 1ndash9 httpsdoiorg101016jecoleng201705029

ZhangYAradottirALSerpeMampBoekenB(2016)InteractionsofbiologicalsoilcrustswithvascularplantsInBWeberBBuumldelampJBelnap(Eds)Biological soil crusts An organizing principle in drylands (pp385ndash406)NewYorkNYSpringer

Zhang Y Zhang Z amp Liu J (2003) Burrowing rodents as eco-system engineers The ecology and management of plateauzokors Myospalax fontanierii in alpine meadow ecosystems onthe Tibetan Plateau Mammal Review 33 284ndash294 httpsdoiorg101046j1365‐2907200300020x

ZomerRJTrabuccoABossioDAampVerchotLV(2008)Climatechange mitigation A spatial analysis of global land suitability forclean development mechanism afforestation and reforestationAgriculture Ecosystems and Environment 126 67ndash80 httpsdoiorg101016jagee200801014

How to cite this articleMallen‐CooperMNakagawaSEldridgeDJGlobalmeta‐analysisofsoil‐disturbingvertebratesrevealsstrongeffectsonecosystempatternsandprocessesGlobal Ecol Biogeogr 2019001ndash19 httpsdoiorg101111geb12877

BIOSKETCHES

Max Mallen‐Cooper isa functionalecologistwhoexploreshowvarious phenomena including soil disturbance and climatechange affect functioning in a range of diverse ecosystemsRecentlyMaxhasbeguntousebiologicalsoilcrustsasamodelsystem to examine the functional consequences of climatechangeandlandusechange

ShiniChi nakagawa and DaviD elDriDge areleadingexpertsinthefieldsofmeta‐analysisandsoildisturbancerespectively


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AgnewWetal(1986)Floraandfaunaassociatedwithprairiedogcoloniesandadjacentungrazedmixed‐grassprairieinwesternSouthDakotaJournalofRangeManagement39135ndash139

Ag

AndersenDCandMacmahonJA(1985)PlantsuccessionfollowingtheMountStHelensvolcaniceruptionfacilitationbyaburrowingrodentThomomys talpoidesTheAmericanMidlandNaturalist11462ndash69

An

AriasSMetal(2005)VizcacharsquosinfluenceonvegetationandsoilinawetlandofArgentinaRangelandEcologyandManagement5851ndash57

Ar

AshtonDandBassettO(1997)Theeffectsofforagingbythesuperblyrebird(Menura novae‐hol‐landiae)inEucalyptus regnansforestsatBeenakVictoriaAustralianJournalofEcology22383ndash394

As

AyarbeJPandKieftTL(2000)MammalmoundsstimulatemicrobialactivityinasemiaridshrublandEcology811150ndash1154

Ay

BancroftWJetal(2005a)Burrowbuildinginseabirdcoloniesasoil‐formingprocessinislandecosystemsPedobiologia49149ndash165

Ba

BancroftWJetal(2005b)Burrowingseabirdsdrivedecreaseddiversityandstructuralcomplexityandincreasedproductivityininsular‐vegetationcommunitiesAustralianJournalofBotany53231ndash241

Bh

BancroftWJetal(2008)VertebratefaunaassociatesoftheWedge‐tailedShearwaterPuffinus pacificuscoloniesofRottnestIslandinfluenceofanecosystemengineerPapersandProceedingsoftheRoyalSocietyofTasmania14221ndash30

Bt

BaronJ(1982)Effectsofferalhogs(Sus scrofa)onthevegetationofHornIslandMississippiTheAmericanMidlandNaturalist107202ndash205

Bn

Barrios‐GarciaMNandSimberloffD(2013)LinkingthepatterntothemechanismHowanintroducedmammalfacilitatesplantinvasionsAustralEcology38884ndash890

Bg

Barrios‐GarciaMNetal(2014)Disparateresponsesofabove‐andbelowgroundpropertiestosoildisturbancebyaninvasivemammalEcosphere51ndash13

Bs

BarthCetal(2014)SoilchangeinducedbyprairiedogsacrossthreeecologicalsitesSoilScienceSocietyofAmericaJournal782054ndash2060

Bx

BartzSetal(2007)Responseofplantandrodentcommunitiestoremovalofprairiedogs(Cynomys gunnisoni)inArizonaJournalofAridEnvironments68422ndash437

Bz

BoekenBetal(1995)PatchinessanddisturbanceplantcommunityresponsestoporcupinediggingsinthecentralNegevEcography18410ndash421

Bo

BoekenBetal(1998)Annualplantcommunityresponsestodensityofsmall‐scalesoildistur-bancesintheNegevDesertofIsraelOecologia114106ndash117

Be


BorchardPandEldridgeDJ(2011)Thegeomor-phicsignatureofbare‐nosedwombats(Vombatus ursinus)andcattle(Bos taurus)inanagriculturalriparianecosystemGeomorphology130365ndash373

Bf

BorchardPetal(2009)Dobare‐nosedwombat(Vombatus ursinus)moundsinfluenceterrestrialmacroinvertebrateassemblagesinagriculturalriparianzonesAustralianJournalofZoology57329ndash336

Bd

BraggCJetal(2005)DensityofCapeporcupinesinasemi‐aridenvironmentandtheirimpactonsoilturnoverandrelatedecosystemprocessesJournalofAridEnvironments61261ndash275

Bj

BrattonSP(1974)TheeffectoftheEuropeanwildboar(Sus scrofa)onthehigh‐elevationvernalflorainGreatSmokyMountainsNationalParkBulletinoftheTorreyBotanicalClub101198ndash206

Br

BravoLGetal(2009)EuropeanrabbitsasecosystemengineerswarrensincreaselizarddensityanddiversityBiodiversityandConservation18869ndash885

Bv

BrockREandKeltDA(2004)KeystoneeffectsoftheendangeredStephensrsquokangaroorat(Dipodomys stephensi)BiologicalConservation116131ndash139

Bk

BryceRetal(2013)Metapopulationdynamicsofaburrowingherbivoredrivespatio‐temporaldynamicsofriparianplantcommunitiesEcosystems161165ndash1177

By

BuenoCGetal(2013)OccurrenceandintensityofwildboardisturbanceseffectsonthephysicalandchemicalsoilpropertiesofalpinegrasslandsPlantandSoil373243ndash256

Bu

BurbidgeAAetal(2007)RelictBettongia lesueur warrensinWesternAustraliandesertsAustralianZoologist3497ndash103

Bi

BykovAetal(2008)Accumulationofmoistureandsoilerosionintheterritoryofsocialvole(Microtus socialis)settlementsinthenorthernCaspianLowlandEurasianSoilScience41902ndash906

Bl

CanalsRMandSebastiagraveMT(2000)SoilnutrientfluxesandvegetationchangesonmolehillsJournalofVegetationScience1123ndash30

Ca

ChapmanTF(2013)Relicbilby(Macrotis lagotis)refugeburrowsassessmentofpotentialcontribu-tiontoarangelandrestorationprogramTheRangelandJournal35167ndash180

Ch

ClarkKLetal(2016)Burrowingherbivoresaltersoilcarbonandnitrogendynamicsinasemi‐aridecosystemArgentinaSoilBiologyandBiochemistry103253ndash261

Cl

CogganNVetal(2016)TermiteactivityanddecompositionareinfluencedbydiggingmammalreintroductionsalonganariditygradientJournalofAridEnvironments13385ndash93

Co

ContrerasLCandGutieacuterrezJR(1991)EffectsofthesubterraneanherbivorousrodentSpalacopus cyanusonherbaceousvegetationinaridcoastalChileOecologia87106ndash109

Cg

(Continues)



CoppockDetal(1983)Effectsofblack‐tailedprairiedogsonintraseasonalabovegroundplantbiomassandnutrientdynamicsandplantspeciesdiversityOecologia561ndash9

Ck

CuevasMFetal(2012)EffectsofwildboardisturbanceonvegetationandsoilpropertiesintheMonteDesertArgentinaMammalianBiology‐ZeitschriftfuumlrSaumlugetierkunde77299ndash306

Cu

CurtinCetal(2000)Ontheroleofsmallmammalsinmediatingclimaticallydrivenvegeta-tionchangeEcologyLetters3309ndash317

Cn

CushmanJetal(2004)VariableeffectsofferalpigdisturbancesonnativeandexoticplantsinaCaliforniagrasslandEcologicalApplications141746ndash1756

Cs

DavidsonADandLightfootDC(2006)KeystonerodentinteractionsprairiedogsandkangarooratsstructurethebioticcompositionofadesertifiedgrasslandEcography29755ndash765

Dv

DavidsonADandLightfootDC(2007)Interactiveeffectsofkeystonerodentsonthestructureofdesertgrasslandarthropodcommuni-tiesEcography30515ndash525

Da

DavidsonADandLightfootDC(2008)Burrowingrodentsincreaselandscapeheterogene-ityinadesertgrasslandJournalofAridEnvironments721133ndash1145

Dl

DesmetPandCowlingR(1999)PatchcreationbyfossorialrodentsakeyprocessintherevegetationofphytotoxicaridsoilsJournalofAridEnvironments4335ndash45

Dt

DunhamAE(2011)Soildisturbancebyverte-bratesaltersseedpredationmovementandgerminationinanAfricanrainforestJournalofTropicalEcology27581ndash589

Dh

DunkellDOetal(2011)Runoffsedimenttransportandeffectsofferalpig(Sus scrofa)exclusioninaforestedHawaiianwatershedPacificScience65175ndash194

Dk

DuvalBandWhitfordWG(2009)Camelspider(Solifugae)useofprairiedogcoloniesWesternNorthAmericanNaturalist69272ndash276

Dw

DuvalBDandWhitfordWG(2012)ReintroducedprairiedogcolonieschangearthropodcommunitiesandenhanceburrowingowlforagingresourcesImmediateScienceEcology112ndash23

Du

El‐BanaMI(2009)Effectsoftheabandonmentoftheburrowingmoundsoffatsandrat(Psammomys obesus Cretzschamar1828)onvegetationandsoilsurfaceattributesalongthecoastaldunesofNorthSinaiEgyptJournalofAridEnvironments73821ndash827

Ed

EldridgeDJandKoenTB(2008)Formationofnutrient‐poorsoilpatchesinasemi‐aridwoodlandbytheEuropeanrabbit(Oryctolagus cuniculusL)AustralEcology3388ndash98

Ek


EldridgeDJandMensingaA(2007)Foragingpitsoftheshort‐beakedechidna(Tachyglossus aculeatus)assmall‐scalepatchesinasemi‐aridAustralianboxwoodlandSoilBiologyandBiochemistry391055ndash1065

Em

EldridgeDJandMyersCA(2001)TheimpactofwarrensoftheEuropeanrabbit(Oryctolagus cuniculusL)onsoilandecologicalprocessesinasemi‐aridAustralianwoodlandJournalofAridEnvironments47325ndash337

El

EldridgeDJandRathD(2002)Hipholeskangaroo(Macropusspp)restingsitesmodifythephysicalandchemicalenvironmentofwoodlandsoilsAustralEcology27527ndash536

Er

EldridgeDJandSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)impactsonvegetationandsoilsandimplicationsformanagementofwoodedrangelandsBasicandAppliedEcology319ndash29

Es

EldridgeDJandWhitfordWG(2009)Badger(Taxidea taxus)disturbancesincreasesoilheteroge-neityinadegradedshrub‐steppeecosystemJournalofAridEnvironments7366ndash73

Ew

EldridgeDJ(2009)Badger(Taxidea taxus)moundsaffectsoilhydrologicalpropertiesinadegradedshrub‐steppeTheAmericanMidlandNaturalist161350ndash358

Ee

EldridgeDJ(2011)Theresourcecouplingroleofanimalforagingpitsinsemi‐aridwoodlandsEcohydrology4623ndash630

Eg

EldridgeDJetal(2006)Short‐termvegetationandsoilresponsestomechanicaldestructionofrabbit(Oryctolagus cuniculusL)warrensinanAustralianboxwoodlandRestorationEcology1450ndash59

Ec

EldridgeDJetal(2010)Interactiveeffectsofthreeecosystemengineersoninfiltrationinasemi‐aridMediterraneangrasslandEcosystems13499ndash510

Eb

EldridgeDJetal(2012)Animalforagingasamechanismforsedimentmovementandsoilnutrientdevelopmentevidencefromthesemi‐aridAustralianwoodlandsandtheChihuahuanDesertGeomorphology157131ndash141

Ef

EvinerVTandChapinFS(2005)SelectivegopherdisturbanceinfluencesplantspecieseffectsonnitrogencyclingOikos109154ndash166

Ev

FieldsMJetal(1999)Burrowingactivitiesofkangarooratsandpatternsinplantspeciesdominanceatashortgrasssteppe‐desertgrasslandecotoneJournalofVegetationScience10123ndash130

Fi

FoxJF(1985)PlantdiversityinrelationtoplantproductionanddisturbancebyvolesinAlaskantundracommunitiesArcticandAlpineResearch17199ndash204

Fo

APPENDIX (CONTINUED)

(Continues)



Gaacutelvez‐BravoLetal(2011)Europeanrabbit(Oryctolagus cuniculus)engineeringeffectspromoteplantheterogeneityinMediterraneandehesapasturesJournalofAridEnvironments75779ndash786

Bc

GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496

Ga

GarkaklisMJetal(2003)Therelationshipbetweenanimalforagingandnutrientpatchinessinsouth‐westAustralianwoodlandsoilsSoilResearch41665ndash673

Gk

Goacutemez‐GarciaDetal(1995)VegetationdifferencescausedbypinevolemoundbuildinginsubalpineplantcommunitiesintheSpanishPyreneesVegetatio11761ndash67

Go

GrantWetal(1980)EffectsofpocketgophermoundsonplantproductioninshortgrassprairieecosystemsTheSouthwesternNaturalist25215ndash224

Gr

GrootBruinderinkGandHazebroekE(1996)Wildboar(Sus scrofaL)rootingandforestregenerationonpodzolicsoilsintheNetherlandsForestEcologyandManagement8871ndash80

Gb

GuoQ(1996)Effectsofbannertailkangarooratmoundsonsmall‐scaleplantcommunitystructureOecologia106247ndash256

Gu

GurneyCMetal(2015)Restorationofnativeplantsisreducedbyrodent‐causedsoildisturbanceandseedremovalRangelandEcologyandManagement68(4)359ndash366

Gy

GuttermanY(1997a)IbexdiggingsintheNegevDeserthighlandsofIsraelasmicrohabitatsforannualplantsSoilsalinitylocationanddiggingdepthaffectingvarietyanddensityofplantspeciesJournalofAridEnvironments37665ndash681

Gt

GuttermanY(1997b)TheinfluencesofdepressionsmadebyibexontheannualvegetationalongcliffsoftheZinValleyintheNegevDeserthighlandsIsraelIsraelJournalofPlantSciences45333ndash338

Gn

HagenahNandBennettNC(2013)MoleratsactasecosystemengineerswithinabiodiversityhotspottheCapeFynbosJournalofZoology28919ndash26

Hb

HakonsonT(1999)TheeffectsofpocketgopherburrowingonwaterbalanceanderosionfromlandfillcoversJournalofEnvironmentalQuality28659ndash665

Hk

HancockGetal(2015)DoesintroducedfaunainfluencesoilerosionAfieldandmodellingassessmentScienceoftheTotalEnvironment518189ndash200

Ha


HartleyLMetal(2009)IntroducedplaguelessenstheeffectsofanherbivorousrodentongrasslandvegetationJournalofAppliedEcology46861ndash869

Hr

HeskeEJetal(1993)EffectsofkangarooratexclusiononvegetationstructureandplantspeciesdiversityintheChihuahuanDesertOecologia95520ndash524

He

HobbsRJandMooneyHA(1991)EffectsofrainfallvariabilityandgopherdisturbanceonserpentineannualgrasslanddynamicsEcology7259ndash68

Ho

IckesKetal(2001)Effectsofnativepigs(Sus scrofa)onwoodyunderstoreyvegetationinaMalaysianlowlandrainforestJournalofTropicalEcology17191ndash206

Ic

InouyeRetal(1987)Pocketgophers(Geomys bursarius)vegetationandsoilnitrogenalongasuccessionalsereineastcentralMinnesotaOecologia 72178ndash184

In

Isselin‐NondedeuFetal(2006)ContributionsofvegetationcoverandcattlehoofprintstowardsseedrunoffcontrolonskipistesEcologicalEngineering27193ndash201

Is

JamesAIetal(2010)ForagingpitslitterandplantgerminationinanaridshrublandJournalofAridEnvironments74516ndash520

Ja

JonesCCetal(2008)PlantsuccessionongophermoundsinwesternCascademeadowsconse-quencesforspeciesdiversityandheterogeneityTheAmericanMidlandNaturalist159275ndash286

Jo

KaczorSAandHartnettDC(1990)Gophertortoise(Gopherus polyphemus)effectsonsoilsandvegetationinaFloridasandhillcommunityTheAmericanMidlandNaturalist123100ndash111

Ka

KornHandKornU(1989)Theeffectofgerbils(Tatera brantsii)onprimaryproductionandplantspeciescompositioninasouthernAfricansavannaOecologia 79271ndash278

Kk

KotanenPM(1995)ResponsesofvegetationtoachangingregimeofdisturbanceeffectsofferalpigsinaCaliforniancoastalprairieEcography18190ndash199

Kn

KretzerJEandCullyJF(2001a)PrairiedogeffectsonharvesterantspeciesdiversityanddensityJournalofRangeManagement5411ndash14

Kr

KurekPetal(2014)Burrowingbybadgers(Meles meles)andfoxes(Vulpes vulpes)changessoilconditionsandvegetationinaEuropeantemperateforestEcologicalResearch291ndash11

Ku

KuznetsovaTAetal(2013)DesertgerbilsaffectbacterialcompositionofsoilMicrobialEcology66940ndash949

Kz

(Continues)




KyleGPetal(2008)InfluenceofpocketgophermoundsonnonnativeplantestablishmentinashrubsteppeecosystemWesternNorthAmericanNaturalist68374ndash381

Ky

LaraNetal(2007)Effectofherbivoryanddisturbancesbytuco‐tucos(Ctenomys mendocinus)onaplantcommunityinthesouthernPunaDesertArcticAntarcticandAlpineResearch39110ndash116

La

LaundreacuteJW(1998)EffectofgroundsquirrelburrowsonplantproductivityinacooldesertenvironmentJournalofRangeManagement638ndash643

Lu

LiXGetal(2009)Dynamicsofsoilpropertiesandorganiccarbonpoolintopsoilofzokor‐mademoundsatanalpinesiteoftheQinghaindashTibetanPlateauBiologyandFertilityofSoils45865ndash872

Li

LitaorMIetal(1996)TheinfluenceofpocketgophersonthestatusofnutrientsinalpinesoilsGeoderma7037ndash48

Lt

LiuYetal(2013)Effectsofplateaupika(Ochotona curzoniae)onnetecosystemcarbonexchangeofgrasslandintheThreeRiversHeadwatersregionQinghai‐TibetChinaPlantandSoil366491ndash504

Lb

MahanCGandYahnerRH(2000)Effectsofforestfragmentationonbehaviourpatternsintheeasternchipmunk(Tamias striatus)CanadianJournalofZoology771991ndash1997

My

MaliziaAIetal(2000)Influenceofthesubterra-neanherbivorousrodentCtenomys talarum on vegetationandsoilZeitschriftfuumlrSaumlugetierkunde65172ndash182

Ml

Martiacutenez‐EsteacutevezLetal(2013)PrairiedogdeclinereducesthesupplyofecosystemservicesandleadstodesertificationofsemiaridgrasslandsPLoSONE8e75229

Ma

MartinsenGDetal(1990)ImpactofpocketgopherdisturbanceonplantspeciesdiversityinashortgrassprairiecommunityOecologia83132ndash138

Me

McMillanBRetal(2011)Vegetationresponsestoananimal‐generateddisturbance(bisonwallows)intallgrassprairieTheAmericanMidlandNaturalist16560ndash73

Mc

MiltonSetal(1997)Effectsofsmall‐scaleanimaldisturbancesonplantassemblagesofset‐asidelandinCentralGermanyJournalofVegetationScience845ndash54

Mn

MitchellJetal(2007)EcologicalimpactsofferalpigdiggingsinnorthQueenslandrainforestsWildlifeResearch34603ndash608

Mt

MohrDetal(2005)WildboarandreddeeraffectsoilnutrientsandsoilbiotainsteepoakstandsoftheEifelSoilBiologyandBiochemistry(4)693ndash700

Mh

MoodyAandJonesJA(2000)SoilresponsetocanopypositionandferalpigdisturbancebeneathQuercus agrifoliaonSantaCruzIslandCaliforniaAppliedSoilEcology14269ndash281

Mj


MorokaNetal(1982)ImpactofburrowingactivityofthebannertailkangarooratonsouthernNewMexicodesertrangelandsJournalofRangeManagement35707ndash710

Mo

NaderiGetal(2011)EffectofvegetationandsoilconditionsonburrowstructureandsiteselectionofraredesertrodentndashIranianJerboa(Allactaga firouzi)PolishJournalofEcology59403ndash411

Nd

NugentDTetal(2014)Interactionsbetweenthesuperblyrebird(Menura novaehollandiae)andfireinsouth‐easternAustraliaWildlifeResearch41203ndash211

Nu

OrsquomeiliaMetal(1982)SomeconsequencesofcompetitionbetweenprairiedogsandbeefcattleJournalofRangeManagement35580ndash585

Om

PlattWJ(1975)Thecolonizationandformationofequilibriumplantspeciesassociationsonbadgerdisturbancesinatall‐grassprairieEcologicalMonographs45285ndash305

Pl

PrughLRandBrasharesJS(2012)PartitioningtheeffectsofanecosystemengineerkangarooratscontrolcommunitystructureviamultiplepathwaysJournalofAnimalEcology81667ndash678

Pb

QuestadEJandFosterBL(2007)VoledisturbancesandplantdiversityinagrasslandmetacommunityOecologia153341ndash351

Qf

RebolloSetal(2002)VolemoundeffectsanddisturbancerateinaMediterraneanplantcommunityunderdifferentgrazingandirrigationregimesPlantEcology169227ndash243

Rb

ReichmanOandJarvisJ(1989)Theinfluenceofthreesympatricspeciesoffossorialmole‐rats(Bathyergidae)onvegetationJournalofMammalogy70763ndash771

Re

ReichmanOandSCSmith(1985)ImpactofpocketgopherburrowsonoverlyingvegetationJournalofMammalogy66720ndash725

Rc

ReichmanO(1988)ComparisonoftheeffectsofcrowdingandpocketgopherdisturbanceonmortalitygrowthandseedproductionofBerteroa incanaTheAmericanMidlandNaturalist12058ndash69

Ra

ReichmanOetal(1993)Distinctanimal‐generatededgeeffectsinatallgrassprairiecommunityEcology741281ndash1285

Rn

RezsutekMandCameronGN(2000)VegetativeedgeeffectsandpocketgophertunnelsJournalofMammalogy811062ndash1070

Rz

RischACetal(2010)Grubbingbywildboars(Sus scrofaL)anditsimpactonhardwoodforestsoilcarbondioxideemissionsinSwitzerlandOecologia164773ndash784

Ri

RogersWEetal(2001)Effectsofplainspocketgopher(Geomys bursarius)disturbancesontallgrass‐prairieplantcommunitystructureTheAmericanMidlandNaturalist145344ndash357

Ro

(Continues)




SanguinettiJandKitzbergerT(2010)Factorscontrollingseedpredationbyrodentsandnon‐nativeSus scrofainAraucariaaraucanaforestspotentialeffectsonseedlingestablishmentBiologicalInvasions12689ndash706

Sa

SchiffmanPM(1994)Promotionofexoticweedestablishmentbyendangeredgiantkangaroorats(Dipodomys ingens)inaCaliforniagrasslandBiodiversityandConservation3524ndash537

Sc

SchooleyRetal(2000)Influenceofsmall‐scaledisturbancesbykangarooratsonChihuahuanDesertantsOecologia125142ndash149

Sy

SeastedtTetal(1986)MicroarthropodsandnematodesinkangarooratburrowsTheSouthwesternNaturalist31114ndash116

Se

SeifanMetal(2010)ContributionofmolehilldisturbancestograsslandcommunitycompositionalongaproductivitygradientActaOecologica36569ndash577

Sf

SherrodSKandSeastedtTR(2001)Effectsofthenorthernpocketgopher(Thomomys talpoides)onalpinesoilcharacteristicsNiwotRidgeCOBiogeochemistry55195ndash218

Sh

SiemannEetal(2009)ExperimentaltestoftheimpactsofferalhogsonforestdynamicsandprocessesinthesoutheasternUSForestEcologyandManagement258546ndash553

Si

SimkinSMetal(2001)PlantresponsefollowingsoildisturbanceinalongleafpineecosystemJournaloftheTorreyBotanicalSociety128208ndash218

Sb

SingerFJetal(1984)EffectsofwildpigrootinginadeciduousforestTheJournalofWildlifeManagement48464ndash473

Sr

SpencerSRetal(1985)InfluenceofpocketgophermoundsonaTexascoastalprairieOecologia66111ndash115

Sn

StappP(2007)Rodentcommunitiesinactiveandinactivecoloniesofblack‐tailedprairiedogsinshortgrasssteppeJournalofMammalogy88241ndash249

Sp

SummerhayesVS(1941)Theeffectofvoles(Microtus agrestis)onvegetationJournalofEcology2914ndash48

Su

SwihartRKandPiconePM(1991)EffectsofwoodchuckactivityonwoodyplantsnearburrowsJournalofMammalogy72607ndash611

St

SwihartRK(1991)InfluenceofMarmota monax on vegetationinhayfieldsJournalofMammalogy72791ndash795

Sw

TardiffSEandStanfordJA(1998)GrizzlybeardiggingeffectsonsubalpinemeadowplantsinrelationtomineralnitrogenavailabilityEcology792219ndash2228

Ta

TaylorDetal(2011)Theimpactofferalpigs(Sus scrofa)onanAustralianlowlandtropicalrainforestWildlifeResearch38437ndash445

Ty


TheimerTCandGehringCA(1999)Effectsofalitter‐disturbingbirdspeciesontreeseedlinggerminationandsurvivalinanAustraliantropicalrainforestJournalofTropicalEcology15737ndash749

Th

TraversSKetal(2012)AnimalforagingpitsoilenhancestheperformanceofanativegrassunderstressfulconditionsPlantandSoil352341ndash351

Tr

UmbanhowarJrCE(1992)AbundancevegetationandenvironmentoffourpatchtypesinanorthernmixedprairieCanadianJournalofBotany70277ndash284

Um

ValentineLEetal(2016)ScratchingbeneaththesurfaceBandicootbioturbationcontributestoecosystemprocessesAustralEcology

Va

VillarrealDetal(2008)Alterationofecosystemstructurebyaburrowingherbivoretheplainsvizcacha(Lagostomus maximus)JournalofMammalogy 89700ndash711

Vi

WangT‐Cetal(2008)Four‐yeardynamicofvegetationonmoundscreatedbyzokors(Myospalax baileyi)inasubalpinemeadowoftheQinghai‐TibetPlateauJournalofAridEnvironments7284ndash96

Wa

WeiXetal(2007)SoilerosionandvegetationsuccessioninalpineKobresiasteppemeadowcausedbyplateaupikamdashacasestudyofNagquCountyTibetChineseGeographicalScience1775ndash81

Wb

WescheKetal(2007)Habitatengineeringunderdryconditionstheimpactofpikas(Ochotona pallasi)onvegetationandsiteconditionsinsouthernMongoliansteppesJournalofVegetationScience18665ndash674

We

WhitesidesCJandButlerDR(2016)BioturbationbygophersandmarmotsanditseffectsonconifergerminationEarthSurfaceProcessesandLandforms412269ndash2281

Wd

WhitfordWGandSteinbergerY(2010)Packrats(Neotomaspp)KeystoneecologicalengineersJournalofAridEnvironments741450ndash1455

Wh

WilliamsLRandCameronGN(1986)EffectsofremovalofpocketgophersonaTexascoastalprairieTheAmericanMidlandNaturalist115216ndash224

Wc

WilskeBetal(2015)EffectsofshorttermbioturbationbycommonvolesonbiogeochemicalsoilvariablesPLoSONE10e0126011

Wk

WilsonMCandSmithAT(2015)ThepikaandthewatershedTheimpactofsmallmammalpoisoningontheecohydrologyoftheQinghai‐TibetanPlateauAmbio4416ndash22

Ws

WirthnerSetal(2012)Dochangesinsoilpropertiesafterrootingbywildboars(Sus scrofa)affectunderstoryvegetationinSwisshardwoodforestsCanadianJournalofForestResearch42585ndash592

Wi

(Continues)




YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95

Ys

YoshiharaYetal(2010a)ResponsesofvegetationtosoildisturbancebySiberianmarmotswithinalandscapeandbetweenlandscapepositionsinHustaiNationalParkMongoliaGrasslandScience5642ndash50

Yh

YoshiharaYetal(2010b)Pollinatorsareattractedtomoundscreatedbyburrowinganimals(marmots)inaMongoliangrasslandJournalofAridEnvironments74159ndash163

Yo

YurkewyczRPetal(2014)GophermoundsdecreasenutrientcyclingratesandincreaseadjacentvegetationinvolcanicprimarysuccessionOecologia1761135ndash1150

Yu

ZhangYandLiuJ(2003)Effectsofplateauzokors(Myospalax fontanierii)onplantcommunityandsoilinanalpinemeadowJournalofMammalogy84644ndash651

Zh

Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved

AntinuchiCDandBuschC(1992)BurrowstructureinthesubterraneanrodentCtenomys talarumZeitschriftfuumlrSaumlugetierkunde57163ndash168

BancroftWJetal(2004)AnewmethodforcalculatingvolumeofexcavatedburrowsthegeomorphicimpactofWedge‐TailedShearwaterburrowsonRottnestIslandFunctionalEcology18752ndash759

BegallSandGallardoMH(2000)Spalacopus cyanusanextremistintunnelconstructingandfoodstoringamongsubterraneanmammalsJournalofZoology25153ndash60

BennettNCetal(2009)Bathyergus suillus (RodentiaBathyergidae)MammalianSpecies8281ndash7

BodekSandEilamD(2015)RevisitingthevisibleburrowsystemTheimpactofthegroupsocialrankandgenderonvolesunderowlattackPhysiologyampBehaviour14679ndash85

BraunSE(1985)HomerangeandactivitypatternsofthegiantkangarooratDipodomys ingensJournalofMammalogy661ndash12

BuharevaOAandBykovAV(2014)Spatialandthermalcharacteristicsofsocialvole(Microtus socialis)burrowsinclaysemidesertofTrans‐VolgaregionZoologicheskyZhurnal931461ndash1469

CameronGNetal(1988)ActivityandburrowstructureofAttwaterrsquospocketgopher(Geomys attwateri)JournalofMammalogy69667ndash677

CincottaRP(1989)Noteonmoundarchitectureoftheblack‐tailedprairiedogTheGreatBasinNaturalist49621ndash623


Study code

CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238


GrodzinskiW(1967)DailymetabolismrateandbodysizeofcommonvolesMicrotus arvalis Pall SmallMammalNewsletter15ndash6

Hatough‐BouranA(1990)TheburrowinghabitsofdeserticrodentsJaculus jaculus and Gerbillus dasyurusintheShaumariReserveinJordanMammalia54341ndash359

HawkinsLK(1996)BurrowsofkangarooratsarehotspotsfordesertsoilfungiJournalofAridEnvironments32239ndash249

KolbHH(1985)TheburrowstructureoftheEuropeanrabbit(Oryctolagus cuniculusL)JournalofZoology206253ndash262

KroacutelEetal(2005)EffectofphotoperiodonbodymassfoodintakeandbodycompositioninthefieldvoleMicrotus agrestisJournalofExperimentalBiology208571ndash584

LottDF(1974)SexualandaggressivebehaviorofadultmaleAmericanbison(Bison bison)IUCNPublications24382ndash394

MankinPCandGetzLL(1994)BurrowmorphologyasrelatedtosocialorganizationofMicrotus ochrogasterJournalofMammalogy75492ndash499

MoonDetal(2007)DistributionandmorphologyofcatecholaminergicandserotonergicneuronsinthebrainofthehighveldgerbilTatera brantsii JournalofChemicalNeuroanatomy34134ndash144

OrlowskaLetal(2012)Carcassweightconditionandreproductionofwildboarharvestedinnorth‐westernPolandPestManagementScience69367ndash370

ParadisEetal(1998)BodymassdynamicsintheMediterraneanpinevoleMicrotus duodecimcostatus JournalofZoology245299ndash305

PeckDRandCongdonBC(2006)Sex‐specificchickprovisioninganddivingbehaviourinthewedge‐tailedshearwaterPuffinus pacificusJournalofAvianBiology37245ndash251

RoperTJetal(2002)BurrowuseandtheinfluenceofectoparasitesinBrantsrsquoWhistlingRatParotomys brantsiiEthology108557ndash564

(Continues)




Study code

RosiMIetal(2000)ArchitectureofCtenomys mendocinus(Rodentia)burrowsfromtwohabitatsdifferinginabundanceandcomplexityofvegeta-tionActaTheriologica45491ndash505

SchoonmakerWJ(1966)TheworldofthewoodchuckLippincottPhiladelphia

SetonET(1909)Life‐historiesofnorthernmammalsanaccountofthemammalsofManitobaCharlesScribnerrsquosSonsNewYork

ShenbrotGetal(2002)Habitat‐dependentdifferencesinarchitectureandmicroclimateoftheburrowsofSundevallrsquosjird(Meriones crassus)(RodentiaGerbillinae)intheNegevDesertIsraelJournalofAridEnvironments51265ndash279

SimkinSMandMichenerWK(2005)FaunalsoildisturbanceregimeofalongleafpineecosystemSoutheasternNaturalist4133ndash152

SmithFAetal(1998)TheinfluenceofclimatechangeonthebodymassofwoodratsNeotoma in anaridregionofNewMexicoUSAEcography21140ndash148

SsemakulJ(1983)AcomparativestudyofhoofpressuresofwildanddomesticungulatesAfricanJournalofEcology21325ndash328

StuartCandStuartT(2001)FieldguidetomammalsofsouthernAfricaStruikPublishersCapeTown

TassellS(2014)Theeffectofnon‐nativesuperblyrebird(Menura novaehollandiae)onTasmanianforestecosystemsPhDthesisUniversityofTasmania

TriggsB(2009)WombatsCSIROPublishingMelbourne

ValentineLEetal(2013)Foragingactivitybythesouthernbrownbandicoot(Isoodon obesulus)asamechanismforsoilturnoverAustralianJournalofZoology60419ndash423


Study code

VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207

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WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271

WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity


ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg



1emsp |emspINTRODUCTION

Positive (facilitatory) interactions among organisms are equallyas important as negative (competitive) interactions in structur-ing ecosystems (see eg Bruno Stachowicz amp Bertness 2003Machicote Branch amp Villarreal 2004) Terrestrial vertebratesforexamplecanmodifyplantspeciescompositionbydispersingseeds or alter the dominant plant growth form through grazing(Chew1974KerleyampWhitford2000)Positiveinteractionscanalso result fromnon‐trophicmechanisms suchasecosystemen-gineeringwherebyanorganisminducesachangeinthephysicalenvironment thatalters theavailabilityof resources tootheror-ganismsor to themselves (JonesLawtonampShachak1994)ForexampleIndiancrestedporcupines(Hystrix indica)createsurfacepitsinordertoconsumebulbsofthedeserttulip(Tulipa systola)intheNegevDesertAlthoughtheporcupinesconsume60ndash90ofthebulbstheconditionsfortheremainingbulbsareenhancedbytheadditionalwater andnutrient‐rich sediment capturedby thepits (Gutterman 1987) Soil disturbances such as these are themostwell‐documentedformofecosystemengineering in terres-trialvertebrates(CogganHaywardampGibb2018)andwillbethefocusofthepresentstudy

Itisusefultoconceptualizesoildisturbanceastwodistinctphys-ical processes resulting in (a) theexcavationof apit scrape rest-ingformorburrowand(b)thedepositionofamoundofsoil(ejectamound)adjacenttothedisturbance(Figure1)Thedepressioncre-atedby soil removal acts as an accreting surfacewhichgraduallyinfillswitherodingsediment litterwaterseedsandotherorganicmaterialsVacatedburrowsoftenbecomehabitatforsecondaryan-imalssuchasburrowingowls(Athene cunicularia hypugaea)Floridamice (Podomys floridanus) and various lizard and beetle specieswhich use the burrows as shelter and foraging grounds (Casas‐Crivilleacute amp Valera 2005 Davidson Lightfoot amp McIntyre 2008Lantz Conway amp Anderson 2007) The ejectamound acts as anerodingsurfaceandtheconstituentmaterialisredistributedacrossthelandscapebyfluvialandaeolianerosionuntiltheoriginalsurfaceeventuallyre‐emergesInsomecasesejectamoundsmaybestabi-lizedbyvegetationandbiocrustandbecomepersistenttopograph-icalfeatures(Eldridge2004)

Intheactofremovingsoilvertebrateengineersremoveground-storeyplantsandexpose thesubsoiloften reducing soil aggrega-tionandalteringsurfacemicroclimate (PlattKolbKunhardtMiloamp New 2016) Soil removal reduces run‐off and has often beenreported to increase soil moisture and infiltration by creating amacropore removinghydrophobic soil crustsorcompacted layersandclearingplantswhichextractaportionofsoilwater(ValentineBretzRuthrofFisherampHardy2017)SoilejectahowevercoversanexistingsoilsurfacesmotheringgroundstoreyplantsSoilejectaoftenhasamarkedlydifferentchemicalsignaturetotheoriginaltop-soilintermsofpHcationsandcarbonandnitrogenpools(EldridgeampKoen2008KerleyWhitfordampKay2004)Assoilnutrientpoolsrecoverinthedepressionandtheejectaisredistributedplantsandsoilorganismsbegintorecolonizethedisturbedsurfaces

We analysedpublisheddata on the effects of vertebrate engi-neers on plants soils and associated biota to derive a global syn-thesis There have been several important qualitative reviews ofvertebrateengineerswithfocionbioticinteractions(Cogganetal2018)soilfunction(Plattetal2016)andspecificsystemssuchasdrylands (WhitfordampKay 1999)However quantitative synthesesthusfarhavebeenrestrictedtopropertiesrelatingtodiversityandbiomass(RomeroGonccedilalves‐SouzaVieiraampKoricheva2015Root‐BernsteinampEbensperger2013)TherehasyettobeaquantitativesynthesisattheglobalscalethatexaminesboththebioticandabioticeffectsofvertebrateengineersSuchasynthesisistimelyifwearetoadvanceourunderstandingoftheecologicaldimensionsofverte-brateengineershowtheyinfluenceawiderangeofpatternsandpro-cessesacrossarangeofecosystemshowtheseimpactsvaryunderdifferentclimateconditionsandthusthelikelyimpactsoftheirlossfromecosystemsortheirreintroductionintodegradedecosystems

Ecosystem theory suggests that the impactof vertebrateengi-neersshouldincreasewithdecliningecosystemproductivity(WrightandJones2004)Thiswouldoccurbecausethecaptureofevensmallamountsofresourcessuchaswaterandorganicmatterwithinsurfacedisturbancesinresource‐poorenvironmentswouldresultinthecre-ationofpatchesthataredistinctlyresource‐richcomparedwiththe

F I G U R E 1 emspConceptualdiagramofsoildisturbanceshowingthetwotypesofstructuresproduced(anejectamoundandadepression)andhowtheychangeovertimeThedepressioninfillswitherodingsedimentwaterandorganicmatterTheejectamoundisredistributedacrossthelandscapebyerosionBothtypesofstructurescanleadtocompositionalshiftsinbiota

Resource redistribuon

Resourcecapture

Bioc shi13s

MOUND DEPRESSION

Enhanced funcon



2emsp |emspMETHODS

















3emsp |emspRESULTS




















1609 64 0039 0047 997 000 024 255 718 minus0053 0130








Disturbanceage

1609 64 0091 003 0032 0149

Disturbancearea

1609 64 minus0056 0049 minus0151 0039



Clay 24 9 0198 015 minus0096 0492
















SoilN 158 28 0569 0079 0413 0724

SoilP 58 16 0298 0116 007 0526

SoilpH 67 18 002 0094 minus0165 0205





Propertyaridity



Clay 24 9 0293 0269 minus0234 0819



Litter 65 15 0259 0185 minus0103 062



Plantdensity 46 9 0491 0189 0121 0862
















SoilN 158 28 0354 018 0001 0707

SoilP 58 16 0476 0207 0071 088

SoilpH 67 18 0268 019 minus0105 064

















ACKNOWLEDGMENTS


DATA ACCESSIBILITY


ORCID



REFERENCES




























































































BIOSKETCHES







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(Continues)




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Study code












2emsp |emspMETHODS

















3emsp |emspRESULTS




















1609 64 0039 0047 997 000 024 255 718 minus0053 0130








Disturbanceage

1609 64 0091 003 0032 0149

Disturbancearea

1609 64 minus0056 0049 minus0151 0039



Clay 24 9 0198 015 minus0096 0492
















SoilN 158 28 0569 0079 0413 0724

SoilP 58 16 0298 0116 007 0526

SoilpH 67 18 002 0094 minus0165 0205





Propertyaridity



Clay 24 9 0293 0269 minus0234 0819



Litter 65 15 0259 0185 minus0103 062



Plantdensity 46 9 0491 0189 0121 0862
















SoilN 158 28 0354 018 0001 0707

SoilP 58 16 0476 0207 0071 088

SoilpH 67 18 0268 019 minus0105 064

















ACKNOWLEDGMENTS


DATA ACCESSIBILITY


ORCID



REFERENCES




























































































BIOSKETCHES







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(Continues)




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Study code

















3emsp |emspRESULTS




















1609 64 0039 0047 997 000 024 255 718 minus0053 0130








Disturbanceage

1609 64 0091 003 0032 0149

Disturbancearea

1609 64 minus0056 0049 minus0151 0039



Clay 24 9 0198 015 minus0096 0492
















SoilN 158 28 0569 0079 0413 0724

SoilP 58 16 0298 0116 007 0526

SoilpH 67 18 002 0094 minus0165 0205





Propertyaridity



Clay 24 9 0293 0269 minus0234 0819



Litter 65 15 0259 0185 minus0103 062



Plantdensity 46 9 0491 0189 0121 0862
















SoilN 158 28 0354 018 0001 0707

SoilP 58 16 0476 0207 0071 088

SoilpH 67 18 0268 019 minus0105 064

















ACKNOWLEDGMENTS


DATA ACCESSIBILITY


ORCID



REFERENCES




























































































BIOSKETCHES







Ag


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Study code















(Continues)




Study code













Study code























1609 64 0039 0047 997 000 024 255 718 minus0053 0130








Disturbanceage

1609 64 0091 003 0032 0149

Disturbancearea

1609 64 minus0056 0049 minus0151 0039



Clay 24 9 0198 015 minus0096 0492
















SoilN 158 28 0569 0079 0413 0724

SoilP 58 16 0298 0116 007 0526

SoilpH 67 18 002 0094 minus0165 0205





Propertyaridity



Clay 24 9 0293 0269 minus0234 0819



Litter 65 15 0259 0185 minus0103 062



Plantdensity 46 9 0491 0189 0121 0862
















SoilN 158 28 0354 018 0001 0707

SoilP 58 16 0476 0207 0071 088

SoilpH 67 18 0268 019 minus0105 064

















ACKNOWLEDGMENTS


DATA ACCESSIBILITY


ORCID



REFERENCES




























































































BIOSKETCHES







Ag


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(Continues)




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Study code

















Disturbanceage

1609 64 0091 003 0032 0149

Disturbancearea

1609 64 minus0056 0049 minus0151 0039



Clay 24 9 0198 015 minus0096 0492
















SoilN 158 28 0569 0079 0413 0724

SoilP 58 16 0298 0116 007 0526

SoilpH 67 18 002 0094 minus0165 0205





Propertyaridity



Clay 24 9 0293 0269 minus0234 0819



Litter 65 15 0259 0185 minus0103 062



Plantdensity 46 9 0491 0189 0121 0862
















SoilN 158 28 0354 018 0001 0707

SoilP 58 16 0476 0207 0071 088

SoilpH 67 18 0268 019 minus0105 064

















ACKNOWLEDGMENTS


DATA ACCESSIBILITY


ORCID



REFERENCES




























































































BIOSKETCHES







Ag


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Study code

















SoilN 158 28 0354 018 0001 0707

SoilP 58 16 0476 0207 0071 088

SoilpH 67 18 0268 019 minus0105 064

















ACKNOWLEDGMENTS


DATA ACCESSIBILITY


ORCID



REFERENCES




























































































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ACKNOWLEDGMENTS


DATA ACCESSIBILITY


ORCID



REFERENCES




























































































BIOSKETCHES







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Bl


Ca


Ch


Cl


Co


Cg

(Continues)




Ck


Cu


Cn


Cs


Dv


Da


Dl


Dt


Dh


Dk


Dw


Du


Ed


Ek



Em


El


Er


Es


Ew


Ee


Eg


Ec


Eb


Ef


Ev


Fi


Fo


(Continues)




Bc


Ga


Gk


Go


Gr


Gb


Gu


Gy


Gt


Gn


Hb


Hk


Ha



Hr


He


Ho


Ic


In


Is


Ja


Jo


Ka


Kk


Kn


Kr


Ku


Kz

(Continues)





Ky


La


Lu


Li


Lt


Lb


My


Ml


Ma


Me


Mc


Mn


Mt


Mh


Mj



Mo


Nd


Nu


Om


Pl


Pb


Qf


Rb


Re


Rc


Ra


Rn


Rz


Ri


Ro

(Continues)





Sa


Sc


Sy


Se


Sf


Sh


Si


Sb


Sr


Sn


Sp


Su


St


Sw


Ta


Ty



Th


Tr


Um


Va


Vi


Wa


Wb


We


Wd


Wh


Wc


Wk


Ws


Wi

(Continues)





Ys


Yh


Yo


Yu


Zh












Study code















(Continues)




Study code













Study code













Ck


Cu


Cn


Cs


Dv


Da


Dl


Dt


Dh


Dk


Dw


Du


Ed


Ek



Em


El


Er


Es


Ew


Ee


Eg


Ec


Eb


Ef


Ev


Fi


Fo


(Continues)




Bc


Ga


Gk


Go


Gr


Gb


Gu


Gy


Gt


Gn


Hb


Hk


Ha



Hr


He


Ho


Ic


In


Is


Ja


Jo


Ka


Kk


Kn


Kr


Ku


Kz

(Continues)





Ky


La


Lu


Li


Lt


Lb


My


Ml


Ma


Me


Mc


Mn


Mt


Mh


Mj



Mo


Nd


Nu


Om


Pl


Pb


Qf


Rb


Re


Rc


Ra


Rn


Rz


Ri


Ro

(Continues)





Sa


Sc


Sy


Se


Sf


Sh


Si


Sb


Sr


Sn


Sp


Su


St


Sw


Ta


Ty



Th


Tr


Um


Va


Vi


Wa


Wb


We


Wd


Wh


Wc


Wk


Ws


Wi

(Continues)





Ys


Yh


Yo


Yu


Zh












Study code















(Continues)




Study code













Study code













Bc


Ga


Gk


Go


Gr


Gb


Gu


Gy


Gt


Gn


Hb


Hk


Ha



Hr


He


Ho


Ic


In


Is


Ja


Jo


Ka


Kk


Kn


Kr


Ku


Kz

(Continues)





Ky


La


Lu


Li


Lt


Lb


My


Ml


Ma


Me


Mc


Mn


Mt


Mh


Mj



Mo


Nd


Nu


Om


Pl


Pb


Qf


Rb


Re


Rc


Ra


Rn


Rz


Ri


Ro

(Continues)





Sa


Sc


Sy


Se


Sf


Sh


Si


Sb


Sr


Sn


Sp


Su


St


Sw


Ta


Ty



Th


Tr


Um


Va


Vi


Wa


Wb


We


Wd


Wh


Wc


Wk


Ws


Wi

(Continues)





Ys


Yh


Yo


Yu


Zh












Study code















(Continues)




Study code













Study code













Ky


La


Lu


Li


Lt


Lb


My


Ml


Ma


Me


Mc


Mn


Mt


Mh


Mj



Mo


Nd


Nu


Om


Pl


Pb


Qf


Rb


Re


Rc


Ra


Rn


Rz


Ri


Ro

(Continues)





Sa


Sc


Sy


Se


Sf


Sh


Si


Sb


Sr


Sn


Sp


Su


St


Sw


Ta


Ty



Th


Tr


Um


Va


Vi


Wa


Wb


We


Wd


Wh


Wc


Wk


Ws


Wi

(Continues)





Ys


Yh


Yo


Yu


Zh












Study code















(Continues)




Study code













Study code













Sa


Sc


Sy


Se


Sf


Sh


Si


Sb


Sr


Sn


Sp


Su


St


Sw


Ta


Ty



Th


Tr


Um


Va


Vi


Wa


Wb


We


Wd


Wh


Wc


Wk


Ws


Wi

(Continues)





Ys


Yh


Yo


Yu


Zh












Study code















(Continues)




Study code













Study code













Ys


Yh


Yo


Yu


Zh












Study code















(Continues)




Study code













Study code












Study code













Study code










global meta‐analysis of soil‐disturbing vertebrates reveals strong … · 2019-01-23 · we...

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