Global meta‐analysis of soil‐disturbing vertebrates reveals strong … · 2019-01-23 · We...
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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)
4emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp5MALLEN‐COOPER Et AL
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)
33emsp|emspPublication bias
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
6emsp |emsp emspensp MALLEN‐COOPER Et AL
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)
emspensp emsp | emsp7MALLEN‐COOPER Et AL
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
Biocrustabundance 15 6 minus0822 0237 minus1287 minus0356
Clay 24 9 0293 0269 minus0234 0819
Invertebrateabundance 47 7 0443 0249 minus0044 0931
Invertebraterichness 14 6 0447 0289 minus0118 1013
Litter 65 15 0259 0185 minus0103 062
Microbialactivity 46 10 004 0196 minus0343 0424
Plantabundance 228 28 0327 0168 minus0003 0657
Plantdensity 46 9 0491 0189 0121 0862
Plantheight 23 6 minus0303 0268 minus0828 0222
Plantproductivity 96 24 0605 0188 0236 0973
Plantrecruitment 61 12 0266 0267 minus0258 079
Plantrichness 220 31 024 0172 minus0097 0578
Rootbiomass 29 10 minus1118 0313 minus1732 minus0505
Run‐off 21 6 minus0268 0277 minus081 0274
Soilcompaction 69 17 0183 0197 minus0203 0569
SoilC 125 23 0319 0184 minus0042 0679(Continues)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
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BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
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Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
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EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
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contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
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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
Included study Study code
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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
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)
4emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp5MALLEN‐COOPER Et AL
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)
33emsp|emspPublication bias
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
6emsp |emsp emspensp MALLEN‐COOPER Et AL
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)
emspensp emsp | emsp7MALLEN‐COOPER Et AL
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
Biocrustabundance 15 6 minus0822 0237 minus1287 minus0356
Clay 24 9 0293 0269 minus0234 0819
Invertebrateabundance 47 7 0443 0249 minus0044 0931
Invertebraterichness 14 6 0447 0289 minus0118 1013
Litter 65 15 0259 0185 minus0103 062
Microbialactivity 46 10 004 0196 minus0343 0424
Plantabundance 228 28 0327 0168 minus0003 0657
Plantdensity 46 9 0491 0189 0121 0862
Plantheight 23 6 minus0303 0268 minus0828 0222
Plantproductivity 96 24 0605 0188 0236 0973
Plantrecruitment 61 12 0266 0267 minus0258 079
Plantrichness 220 31 024 0172 minus0097 0578
Rootbiomass 29 10 minus1118 0313 minus1732 minus0505
Run‐off 21 6 minus0268 0277 minus081 0274
Soilcompaction 69 17 0183 0197 minus0203 0569
SoilC 125 23 0319 0184 minus0042 0679(Continues)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
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BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
Casas‐CrivilleacuteAampValeraF (2005)TheEuropeanbee‐eater (Merops apiaster) as an ecosystem engineer in arid environments Journal of Arid Environments 60 227ndash238 httpsdoiorg101016jjaridenv200403012
Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
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EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
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contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
NakagawaS(2015)MissingdataMechanismsmethodsandmessagesInGAFoxSNegrete‐YankelevichampVJSosa(Eds)Ecological sta‐tistics Contemporary theory and application(pp81ndash105)UKOxfordUniversityPress
NakagawaSampSantosES(2012)Methodologicalissuesandadvancesin biological meta‐analysis Evolutionary Ecology 26 1253ndash1274httpsdoiorg101007s10682‐012‐9555‐5
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
Included study Study code
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
Included study Study code
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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
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)
4emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp5MALLEN‐COOPER Et AL
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)
33emsp|emspPublication bias
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
6emsp |emsp emspensp MALLEN‐COOPER Et AL
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)
emspensp emsp | emsp7MALLEN‐COOPER Et AL
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
Biocrustabundance 15 6 minus0822 0237 minus1287 minus0356
Clay 24 9 0293 0269 minus0234 0819
Invertebrateabundance 47 7 0443 0249 minus0044 0931
Invertebraterichness 14 6 0447 0289 minus0118 1013
Litter 65 15 0259 0185 minus0103 062
Microbialactivity 46 10 004 0196 minus0343 0424
Plantabundance 228 28 0327 0168 minus0003 0657
Plantdensity 46 9 0491 0189 0121 0862
Plantheight 23 6 minus0303 0268 minus0828 0222
Plantproductivity 96 24 0605 0188 0236 0973
Plantrecruitment 61 12 0266 0267 minus0258 079
Plantrichness 220 31 024 0172 minus0097 0578
Rootbiomass 29 10 minus1118 0313 minus1732 minus0505
Run‐off 21 6 minus0268 0277 minus081 0274
Soilcompaction 69 17 0183 0197 minus0203 0569
SoilC 125 23 0319 0184 minus0042 0679(Continues)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
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BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
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Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
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EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
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contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
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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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
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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
Included study Study code
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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
4emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp5MALLEN‐COOPER Et AL
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)
33emsp|emspPublication bias
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
6emsp |emsp emspensp MALLEN‐COOPER Et AL
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)
emspensp emsp | emsp7MALLEN‐COOPER Et AL
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
Biocrustabundance 15 6 minus0822 0237 minus1287 minus0356
Clay 24 9 0293 0269 minus0234 0819
Invertebrateabundance 47 7 0443 0249 minus0044 0931
Invertebraterichness 14 6 0447 0289 minus0118 1013
Litter 65 15 0259 0185 minus0103 062
Microbialactivity 46 10 004 0196 minus0343 0424
Plantabundance 228 28 0327 0168 minus0003 0657
Plantdensity 46 9 0491 0189 0121 0862
Plantheight 23 6 minus0303 0268 minus0828 0222
Plantproductivity 96 24 0605 0188 0236 0973
Plantrecruitment 61 12 0266 0267 minus0258 079
Plantrichness 220 31 024 0172 minus0097 0578
Rootbiomass 29 10 minus1118 0313 minus1732 minus0505
Run‐off 21 6 minus0268 0277 minus081 0274
Soilcompaction 69 17 0183 0197 minus0203 0569
SoilC 125 23 0319 0184 minus0042 0679(Continues)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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ApletGAndersonSampStoneC(1991)AssociationbetweenferalpigdisturbanceandthecompositionofsomealienplantassemblagesinHawaiiVolcanoesNational ParkPlant Ecology95 55ndash62 httpsdoiorg101007BF00124953
AriasSMQuintanaRDampCagnoniM(2005)VizcacharsquosinfluenceonvegetationandsoilinawetlandofArgentinaRangeland Ecology and Management5851ndash57httpsdoiorg1021111551‐5028(2005)58lt51VIOVASgt20CO2
Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
relatedecosystemprocessesJournal of Arid Environments61261ndash275httpsdoiorg101016jjaridenv200409007
BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
Casas‐CrivilleacuteAampValeraF (2005)TheEuropeanbee‐eater (Merops apiaster) as an ecosystem engineer in arid environments Journal of Arid Environments 60 227ndash238 httpsdoiorg101016jjaridenv200403012
Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
Duval S amp Tweedie R (2000) Trim and fill A simple funnel‐plot‐based method of testing and adjusting for publicationbias in meta‐analysis Biometrics 56 455ndash463 httpsdoiorg101111j0006‐341X200000455x
EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
emspensp emsp | emsp11MALLEN‐COOPER Et AL
contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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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HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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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12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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AgnewWetal(1986)Floraandfaunaassociatedwithprairiedogcoloniesandadjacentungrazedmixed‐grassprairieinwesternSouthDakotaJournalofRangeManagement39135ndash139
Ag
AndersenDCandMacmahonJA(1985)PlantsuccessionfollowingtheMountStHelensvolcaniceruptionfacilitationbyaburrowingrodentThomomys talpoidesTheAmericanMidlandNaturalist11462ndash69
An
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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
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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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp5MALLEN‐COOPER Et AL
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)
33emsp|emspPublication bias
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
6emsp |emsp emspensp MALLEN‐COOPER Et AL
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)
emspensp emsp | emsp7MALLEN‐COOPER Et AL
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
Biocrustabundance 15 6 minus0822 0237 minus1287 minus0356
Clay 24 9 0293 0269 minus0234 0819
Invertebrateabundance 47 7 0443 0249 minus0044 0931
Invertebraterichness 14 6 0447 0289 minus0118 1013
Litter 65 15 0259 0185 minus0103 062
Microbialactivity 46 10 004 0196 minus0343 0424
Plantabundance 228 28 0327 0168 minus0003 0657
Plantdensity 46 9 0491 0189 0121 0862
Plantheight 23 6 minus0303 0268 minus0828 0222
Plantproductivity 96 24 0605 0188 0236 0973
Plantrecruitment 61 12 0266 0267 minus0258 079
Plantrichness 220 31 024 0172 minus0097 0578
Rootbiomass 29 10 minus1118 0313 minus1732 minus0505
Run‐off 21 6 minus0268 0277 minus081 0274
Soilcompaction 69 17 0183 0197 minus0203 0569
SoilC 125 23 0319 0184 minus0042 0679(Continues)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
relatedecosystemprocessesJournal of Arid Environments61261ndash275httpsdoiorg101016jjaridenv200409007
BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
Casas‐CrivilleacuteAampValeraF (2005)TheEuropeanbee‐eater (Merops apiaster) as an ecosystem engineer in arid environments Journal of Arid Environments 60 227ndash238 httpsdoiorg101016jjaridenv200403012
Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
Duval S amp Tweedie R (2000) Trim and fill A simple funnel‐plot‐based method of testing and adjusting for publicationbias in meta‐analysis Biometrics 56 455ndash463 httpsdoiorg101111j0006‐341X200000455x
EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
emspensp emsp | emsp11MALLEN‐COOPER Et AL
contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
NakagawaS(2015)MissingdataMechanismsmethodsandmessagesInGAFoxSNegrete‐YankelevichampVJSosa(Eds)Ecological sta‐tistics Contemporary theory and application(pp81ndash105)UKOxfordUniversityPress
NakagawaSampSantosES(2012)Methodologicalissuesandadvancesin biological meta‐analysis Evolutionary Ecology 26 1253ndash1274httpsdoiorg101007s10682‐012‐9555‐5
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
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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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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Bt
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Bn
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Cg
(Continues)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
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CoppockDetal(1983)Effectsofblack‐tailedprairiedogsonintraseasonalabovegroundplantbiomassandnutrientdynamicsandplantspeciesdiversityOecologia561ndash9
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Cu
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Cn
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Cs
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Da
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Dl
DesmetPandCowlingR(1999)PatchcreationbyfossorialrodentsakeyprocessintherevegetationofphytotoxicaridsoilsJournalofAridEnvironments4335ndash45
Dt
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Dh
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Dk
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Dw
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Du
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Ed
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El
EldridgeDJandRathD(2002)Hipholeskangaroo(Macropusspp)restingsitesmodifythephysicalandchemicalenvironmentofwoodlandsoilsAustralEcology27527ndash536
Er
EldridgeDJandSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)impactsonvegetationandsoilsandimplicationsformanagementofwoodedrangelandsBasicandAppliedEcology319ndash29
Es
EldridgeDJandWhitfordWG(2009)Badger(Taxidea taxus)disturbancesincreasesoilheteroge-neityinadegradedshrub‐steppeecosystemJournalofAridEnvironments7366ndash73
Ew
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Ee
EldridgeDJ(2011)Theresourcecouplingroleofanimalforagingpitsinsemi‐aridwoodlandsEcohydrology4623ndash630
Eg
EldridgeDJetal(2006)Short‐termvegetationandsoilresponsestomechanicaldestructionofrabbit(Oryctolagus cuniculusL)warrensinanAustralianboxwoodlandRestorationEcology1450ndash59
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Eb
EldridgeDJetal(2012)Animalforagingasamechanismforsedimentmovementandsoilnutrientdevelopmentevidencefromthesemi‐aridAustralianwoodlandsandtheChihuahuanDesertGeomorphology157131ndash141
Ef
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Ev
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Fi
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Fo
APPENDIX (CONTINUED)
(Continues)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
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Bc
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Gt
GuttermanY(1997b)TheinfluencesofdepressionsmadebyibexontheannualvegetationalongcliffsoftheZinValleyintheNegevDeserthighlandsIsraelIsraelJournalofPlantSciences45333ndash338
Gn
HagenahNandBennettNC(2013)MoleratsactasecosystemengineerswithinabiodiversityhotspottheCapeFynbosJournalofZoology28919ndash26
Hb
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Hk
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Hr
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He
HobbsRJandMooneyHA(1991)EffectsofrainfallvariabilityandgopherdisturbanceonserpentineannualgrasslanddynamicsEcology7259ndash68
Ho
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Ic
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Isselin‐NondedeuFetal(2006)ContributionsofvegetationcoverandcattlehoofprintstowardsseedrunoffcontrolonskipistesEcologicalEngineering27193ndash201
Is
JamesAIetal(2010)ForagingpitslitterandplantgerminationinanaridshrublandJournalofAridEnvironments74516ndash520
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Kk
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Kn
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Kr
KurekPetal(2014)Burrowingbybadgers(Meles meles)andfoxes(Vulpes vulpes)changessoilconditionsandvegetationinaEuropeantemperateforestEcologicalResearch291ndash11
Ku
KuznetsovaTAetal(2013)DesertgerbilsaffectbacterialcompositionofsoilMicrobialEcology66940ndash949
Kz
(Continues)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
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KyleGPetal(2008)InfluenceofpocketgophermoundsonnonnativeplantestablishmentinashrubsteppeecosystemWesternNorthAmericanNaturalist68374ndash381
Ky
LaraNetal(2007)Effectofherbivoryanddisturbancesbytuco‐tucos(Ctenomys mendocinus)onaplantcommunityinthesouthernPunaDesertArcticAntarcticandAlpineResearch39110ndash116
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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
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Ma
MartinsenGDetal(1990)ImpactofpocketgopherdisturbanceonplantspeciesdiversityinashortgrassprairiecommunityOecologia83132ndash138
Me
McMillanBRetal(2011)Vegetationresponsestoananimal‐generateddisturbance(bisonwallows)intallgrassprairieTheAmericanMidlandNaturalist16560ndash73
Mc
MiltonSetal(1997)Effectsofsmall‐scaleanimaldisturbancesonplantassemblagesofset‐asidelandinCentralGermanyJournalofVegetationScience845ndash54
Mn
MitchellJetal(2007)EcologicalimpactsofferalpigdiggingsinnorthQueenslandrainforestsWildlifeResearch34603ndash608
Mt
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Mh
MoodyAandJonesJA(2000)SoilresponsetocanopypositionandferalpigdisturbancebeneathQuercus agrifoliaonSantaCruzIslandCaliforniaAppliedSoilEcology14269ndash281
Mj
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Mo
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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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
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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
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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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
6emsp |emsp emspensp MALLEN‐COOPER Et AL
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)
emspensp emsp | emsp7MALLEN‐COOPER Et AL
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
Biocrustabundance 15 6 minus0822 0237 minus1287 minus0356
Clay 24 9 0293 0269 minus0234 0819
Invertebrateabundance 47 7 0443 0249 minus0044 0931
Invertebraterichness 14 6 0447 0289 minus0118 1013
Litter 65 15 0259 0185 minus0103 062
Microbialactivity 46 10 004 0196 minus0343 0424
Plantabundance 228 28 0327 0168 minus0003 0657
Plantdensity 46 9 0491 0189 0121 0862
Plantheight 23 6 minus0303 0268 minus0828 0222
Plantproductivity 96 24 0605 0188 0236 0973
Plantrecruitment 61 12 0266 0267 minus0258 079
Plantrichness 220 31 024 0172 minus0097 0578
Rootbiomass 29 10 minus1118 0313 minus1732 minus0505
Run‐off 21 6 minus0268 0277 minus081 0274
Soilcompaction 69 17 0183 0197 minus0203 0569
SoilC 125 23 0319 0184 minus0042 0679(Continues)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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
REFERENCES
AlkonPU (1999)Microhabitatto landscape impactsCrestedporcu-pinedigsintheNegevDeserthighlandsJournal of Arid Environments41183ndash202httpsdoiorg101006jare19980481
ApletGAndersonSampStoneC(1991)AssociationbetweenferalpigdisturbanceandthecompositionofsomealienplantassemblagesinHawaiiVolcanoesNational ParkPlant Ecology95 55ndash62 httpsdoiorg101007BF00124953
AriasSMQuintanaRDampCagnoniM(2005)VizcacharsquosinfluenceonvegetationandsoilinawetlandofArgentinaRangeland Ecology and Management5851ndash57httpsdoiorg1021111551‐5028(2005)58lt51VIOVASgt20CO2
Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
relatedecosystemprocessesJournal of Arid Environments61261ndash275httpsdoiorg101016jjaridenv200409007
BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
Casas‐CrivilleacuteAampValeraF (2005)TheEuropeanbee‐eater (Merops apiaster) as an ecosystem engineer in arid environments Journal of Arid Environments 60 227ndash238 httpsdoiorg101016jjaridenv200403012
Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
Duval S amp Tweedie R (2000) Trim and fill A simple funnel‐plot‐based method of testing and adjusting for publicationbias in meta‐analysis Biometrics 56 455ndash463 httpsdoiorg101111j0006‐341X200000455x
EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
emspensp emsp | emsp11MALLEN‐COOPER Et AL
contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
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12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
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PlattBFKolbDJKunhardtCGMiloSPampNewLG(2016)BurrowingthroughtheliteratureTheimpactofsoil‐disturbingver-tebratesonphysicalandchemicalpropertiesofsoilSoil Science181175ndash191httpsdoiorg101097SS0000000000000150
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RogersWEHartnettDCampElderB(2001)Effectsofplainspocketgo-pher(Geomys bursarius)disturbancesontallgrass‐prairieplantcommu-nitystructureThe American Midland Naturalist145344ndash357httpsdoiorg1016740003‐0031(2001)145[0344EOPPGG]20CO2
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SchielzethH (2010) Simplemeans to improve the interpretability ofregressioncoefficientsMethods in Ecology and Evolution1103ndash113httpsdoiorg101111j2041‐210X201000012x
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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
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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
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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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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An
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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
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Bz
BoekenBetal(1995)PatchinessanddisturbanceplantcommunityresponsestoporcupinediggingsinthecentralNegevEcography18410ndash421
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BoekenBetal(1998)Annualplantcommunityresponsestodensityofsmall‐scalesoildistur-bancesintheNegevDesertofIsraelOecologia114106ndash117
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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
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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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
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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
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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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
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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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp7MALLEN‐COOPER Et AL
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
Biocrustabundance 15 6 minus0822 0237 minus1287 minus0356
Clay 24 9 0293 0269 minus0234 0819
Invertebrateabundance 47 7 0443 0249 minus0044 0931
Invertebraterichness 14 6 0447 0289 minus0118 1013
Litter 65 15 0259 0185 minus0103 062
Microbialactivity 46 10 004 0196 minus0343 0424
Plantabundance 228 28 0327 0168 minus0003 0657
Plantdensity 46 9 0491 0189 0121 0862
Plantheight 23 6 minus0303 0268 minus0828 0222
Plantproductivity 96 24 0605 0188 0236 0973
Plantrecruitment 61 12 0266 0267 minus0258 079
Plantrichness 220 31 024 0172 minus0097 0578
Rootbiomass 29 10 minus1118 0313 minus1732 minus0505
Run‐off 21 6 minus0268 0277 minus081 0274
Soilcompaction 69 17 0183 0197 minus0203 0569
SoilC 125 23 0319 0184 minus0042 0679(Continues)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
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BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
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Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
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EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
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contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
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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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
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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
Included study Study code
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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
8emsp |emsp emspensp MALLEN‐COOPER Et AL
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
Moderator Levels n k Estimate SE Lower CI (5) Upper CI (95)
Soilinfiltration 39 8 0392 0273 minus0143 0926
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
Soilmoisture 67 15 0376 0195 minus0006 0758
Vertebrateabundance 29 3 minus659 2841 minus12157 minus1023
TABLE2emsp(Continued)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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AriasSMQuintanaRDampCagnoniM(2005)VizcacharsquosinfluenceonvegetationandsoilinawetlandofArgentinaRangeland Ecology and Management5851ndash57httpsdoiorg1021111551‐5028(2005)58lt51VIOVASgt20CO2
Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
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BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
Casas‐CrivilleacuteAampValeraF (2005)TheEuropeanbee‐eater (Merops apiaster) as an ecosystem engineer in arid environments Journal of Arid Environments 60 227ndash238 httpsdoiorg101016jjaridenv200403012
Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
Duval S amp Tweedie R (2000) Trim and fill A simple funnel‐plot‐based method of testing and adjusting for publicationbias in meta‐analysis Biometrics 56 455ndash463 httpsdoiorg101111j0006‐341X200000455x
EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
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contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
NakagawaS(2015)MissingdataMechanismsmethodsandmessagesInGAFoxSNegrete‐YankelevichampVJSosa(Eds)Ecological sta‐tistics Contemporary theory and application(pp81ndash105)UKOxfordUniversityPress
NakagawaSampSantosES(2012)Methodologicalissuesandadvancesin biological meta‐analysis Evolutionary Ecology 26 1253ndash1274httpsdoiorg101007s10682‐012‐9555‐5
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
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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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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Ba
BancroftWJetal(2005b)Burrowingseabirdsdrivedecreaseddiversityandstructuralcomplexityandincreasedproductivityininsular‐vegetationcommunitiesAustralianJournalofBotany53231ndash241
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Bt
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Bn
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Cg
(Continues)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
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CoppockDetal(1983)Effectsofblack‐tailedprairiedogsonintraseasonalabovegroundplantbiomassandnutrientdynamicsandplantspeciesdiversityOecologia561ndash9
Ck
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Cu
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Cn
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Cs
DavidsonADandLightfootDC(2006)KeystonerodentinteractionsprairiedogsandkangarooratsstructurethebioticcompositionofadesertifiedgrasslandEcography29755ndash765
Dv
DavidsonADandLightfootDC(2007)Interactiveeffectsofkeystonerodentsonthestructureofdesertgrasslandarthropodcommuni-tiesEcography30515ndash525
Da
DavidsonADandLightfootDC(2008)Burrowingrodentsincreaselandscapeheterogene-ityinadesertgrasslandJournalofAridEnvironments721133ndash1145
Dl
DesmetPandCowlingR(1999)PatchcreationbyfossorialrodentsakeyprocessintherevegetationofphytotoxicaridsoilsJournalofAridEnvironments4335ndash45
Dt
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Dh
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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
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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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
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Gaacutelvez‐BravoLetal(2011)Europeanrabbit(Oryctolagus cuniculus)engineeringeffectspromoteplantheterogeneityinMediterraneandehesapasturesJournalofAridEnvironments75779ndash786
Bc
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
Ga
GarkaklisMJetal(2003)Therelationshipbetweenanimalforagingandnutrientpatchinessinsouth‐westAustralianwoodlandsoilsSoilResearch41665ndash673
Gk
Goacutemez‐GarciaDetal(1995)VegetationdifferencescausedbypinevolemoundbuildinginsubalpineplantcommunitiesintheSpanishPyreneesVegetatio11761ndash67
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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
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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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
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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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
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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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp9MALLEN‐COOPER Et AL
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)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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ApletGAndersonSampStoneC(1991)AssociationbetweenferalpigdisturbanceandthecompositionofsomealienplantassemblagesinHawaiiVolcanoesNational ParkPlant Ecology95 55ndash62 httpsdoiorg101007BF00124953
AriasSMQuintanaRDampCagnoniM(2005)VizcacharsquosinfluenceonvegetationandsoilinawetlandofArgentinaRangeland Ecology and Management5851ndash57httpsdoiorg1021111551‐5028(2005)58lt51VIOVASgt20CO2
Barrios‐GarciaMampBallariS (2008) Impactofwildboar (Sus scrofa)initsintroducedandnativerangeAreviewBiological Invasions142283ndash2300httpsdoiorg101007s10530‐012‐0229‐6
BraggCDonaldsonJampRyanP(2005)DensityofCapeporcupinesin a semi‐arid environment and their impact on soil turnover and
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BrunoJFStachowiczJJampBertnessMD(2003)Inclusionoffa-cilitation intoecological theoryTrends in Ecology and Evolution18119ndash125httpsdoiorg101016S0169‐5347(02)00045‐9
Casas‐CrivilleacuteAampValeraF (2005)TheEuropeanbee‐eater (Merops apiaster) as an ecosystem engineer in arid environments Journal of Arid Environments 60 227ndash238 httpsdoiorg101016jjaridenv200403012
Cavin RM amp Butler D R (2015) Patterns and trends in the fieldsof bioturbation faunalturbation and zoogeomorphology Physical Geography36178ndash187httpsdoiorg1010800272364620151026763
ChewRM(1974)ConsumersasregulatorsofecosystemsAnalterna-tivetoenergeticsOhio Journal of Science74359ndash370
CogganNVHaywardMWampGibbH(2018)Aglobaldatabaseandldquostate of the fieldrdquo reviewof research into ecosystemengineeringbylandanimalsJournal of Animal Ecology87974ndash994httpsdoiorg1011111365‐265612819
Crooks J A (2002) Characterizing ecosystem‐level consequences ofbiologicalinvasionsTheroleofecosystemengineersOikos97153ndash166httpsdoiorg101034j1600‐07062002970201x
DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
Duval S amp Tweedie R (2000) Trim and fill A simple funnel‐plot‐based method of testing and adjusting for publicationbias in meta‐analysis Biometrics 56 455ndash463 httpsdoiorg101111j0006‐341X200000455x
EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
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contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
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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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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Ar
AshtonDandBassettO(1997)Theeffectsofforagingbythesuperblyrebird(Menura novae‐hol‐landiae)inEucalyptus regnansforestsatBeenakVictoriaAustralianJournalofEcology22383ndash394
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Ba
BancroftWJetal(2005b)Burrowingseabirdsdrivedecreaseddiversityandstructuralcomplexityandincreasedproductivityininsular‐vegetationcommunitiesAustralianJournalofBotany53231ndash241
Bh
BancroftWJetal(2008)VertebratefaunaassociatesoftheWedge‐tailedShearwaterPuffinus pacificuscoloniesofRottnestIslandinfluenceofanecosystemengineerPapersandProceedingsoftheRoyalSocietyofTasmania14221ndash30
Bt
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Bn
Barrios‐GarciaMNandSimberloffD(2013)LinkingthepatterntothemechanismHowanintroducedmammalfacilitatesplantinvasionsAustralEcology38884ndash890
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BarthCetal(2014)SoilchangeinducedbyprairiedogsacrossthreeecologicalsitesSoilScienceSocietyofAmericaJournal782054ndash2060
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Bd
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Bj
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Bi
BykovAetal(2008)Accumulationofmoistureandsoilerosionintheterritoryofsocialvole(Microtus socialis)settlementsinthenorthernCaspianLowlandEurasianSoilScience41902ndash906
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CanalsRMandSebastiagraveMT(2000)SoilnutrientfluxesandvegetationchangesonmolehillsJournalofVegetationScience1123ndash30
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Ch
ClarkKLetal(2016)Burrowingherbivoresaltersoilcarbonandnitrogendynamicsinasemi‐aridecosystemArgentinaSoilBiologyandBiochemistry103253ndash261
Cl
CogganNVetal(2016)TermiteactivityanddecompositionareinfluencedbydiggingmammalreintroductionsalonganariditygradientJournalofAridEnvironments13385ndash93
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ContrerasLCandGutieacuterrezJR(1991)EffectsofthesubterraneanherbivorousrodentSpalacopus cyanusonherbaceousvegetationinaridcoastalChileOecologia87106ndash109
Cg
(Continues)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
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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
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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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
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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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
10emsp |emsp emspensp MALLEN‐COOPER Et AL
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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DavidsonAampLightfootD (2008)Burrowingrodents increase land-scapeheterogeneityinadesertgrasslandJournal of Arid Environments721133ndash1145httpsdoiorg101016jjaridenv200712015
DavidsonALightfootDampMcIntyreJ (2008)EngineeringrodentscreatekeyhabitatforlizardsJournal of Arid Environments722142ndash2149httpsdoiorg101016jjaridenv200807006
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EldridgeD J (2004)Moundsof theAmericanbadger (Taxidea taxus)Significant features of North American shrub‐steppe ecosystemsJournal of Mammalogy 85 1060ndash1067 httpsdoiorg101644BEH‐1051
EldridgeDJampJamesAI(2009)Soil‐disturbancebynativeanimalsplays a critical role in maintaining healthy Australian landscapesEcological Management and Restoration 10 S27ndashS34 httpsdoiorg101111j1442‐8903200900452x
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
Eldridge D J amp Myers C A (2001) The impact of warrens ofthe European rabbit (Oryctolagus cuniculus L) on soil and eco-logical processes in a semi‐arid Australian woodland Journal of Arid Environments 47 325ndash337 httpsdoiorg101006jare20000685
EldridgeDJampSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)im-pactsonvegetationandsoilsand implications formanagementofwoodedrangelandsBasic and Applied Ecology319ndash29httpsdoiorg1010781439‐1791‐00078
FanN ZhouWWeiWWangQamp JiangY (1999) Ecologically‐basedrodentmanagementInGRSingletonLAHindsHLeirsampZZhang(Eds)Rodent pest management in the Qinghai‐Tibet alpine meadow ecosystem (pp 285ndash304) Canberra Australia AustralianCentreforInternationalAgriculturalResearch
FlemingPAAndersonHPrendergastASBretzMRValentineLEampHardyGES(2014)IsthelossofAustraliandiggingmammals
emspensp emsp | emsp11MALLEN‐COOPER Et AL
contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
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PlattBFKolbDJKunhardtCGMiloSPampNewLG(2016)BurrowingthroughtheliteratureTheimpactofsoil‐disturbingver-tebratesonphysicalandchemicalpropertiesofsoilSoil Science181175ndash191httpsdoiorg101097SS0000000000000150
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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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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Ar
AshtonDandBassettO(1997)Theeffectsofforagingbythesuperblyrebird(Menura novae‐hol‐landiae)inEucalyptus regnansforestsatBeenakVictoriaAustralianJournalofEcology22383ndash394
As
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Ay
BancroftWJetal(2005a)Burrowbuildinginseabirdcoloniesasoil‐formingprocessinislandecosystemsPedobiologia49149ndash165
Ba
BancroftWJetal(2005b)Burrowingseabirdsdrivedecreaseddiversityandstructuralcomplexityandincreasedproductivityininsular‐vegetationcommunitiesAustralianJournalofBotany53231ndash241
Bh
BancroftWJetal(2008)VertebratefaunaassociatesoftheWedge‐tailedShearwaterPuffinus pacificuscoloniesofRottnestIslandinfluenceofanecosystemengineerPapersandProceedingsoftheRoyalSocietyofTasmania14221ndash30
Bt
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Bn
Barrios‐GarciaMNandSimberloffD(2013)LinkingthepatterntothemechanismHowanintroducedmammalfacilitatesplantinvasionsAustralEcology38884ndash890
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Barrios‐GarciaMNetal(2014)Disparateresponsesofabove‐andbelowgroundpropertiestosoildisturbancebyaninvasivemammalEcosphere51ndash13
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BarthCetal(2014)SoilchangeinducedbyprairiedogsacrossthreeecologicalsitesSoilScienceSocietyofAmericaJournal782054ndash2060
Bx
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Bd
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Bj
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Bv
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BurbidgeAAetal(2007)RelictBettongia lesueur warrensinWesternAustraliandesertsAustralianZoologist3497ndash103
Bi
BykovAetal(2008)Accumulationofmoistureandsoilerosionintheterritoryofsocialvole(Microtus socialis)settlementsinthenorthernCaspianLowlandEurasianSoilScience41902ndash906
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CanalsRMandSebastiagraveMT(2000)SoilnutrientfluxesandvegetationchangesonmolehillsJournalofVegetationScience1123ndash30
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ChapmanTF(2013)Relicbilby(Macrotis lagotis)refugeburrowsassessmentofpotentialcontribu-tiontoarangelandrestorationprogramTheRangelandJournal35167ndash180
Ch
ClarkKLetal(2016)Burrowingherbivoresaltersoilcarbonandnitrogendynamicsinasemi‐aridecosystemArgentinaSoilBiologyandBiochemistry103253ndash261
Cl
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ContrerasLCandGutieacuterrezJR(1991)EffectsofthesubterraneanherbivorousrodentSpalacopus cyanusonherbaceousvegetationinaridcoastalChileOecologia87106ndash109
Cg
(Continues)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
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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
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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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
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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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp11MALLEN‐COOPER Et AL
contributing to a deterioration in ecosystem function Mammal Review4494ndash108httpsdoiorg101111mam12014
GarkaklisMJBradleyJampWoollerR(2004)Diggingandsoilturn-overbyamycophagousmarsupialJournal of Arid Environments56569ndash578httpsdoiorg101016S0140‐1963(03)00061‐2
Garner W amp Steinberger Y (1989) A proposed mechanism forthe formation of fertile islands in the desert ecosystem Journal of Arid Environments 16 257ndash262 httpsdoiorg101016S0140‐1963(18)30941‐8
Gelman A (2008) Scaling regression inputs by dividing by two stan-dard deviations Statistics in Medicine 27 2865ndash2873 httpsdoiorg101002sim3107
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
HobbsRJampMooneyHA(1985)Communityandpopulationdynam-icsofserpentinegrasslandannualsinrelationtogopherdisturbanceOecologia67342ndash351httpsdoiorg101007BF00384939
HuangJYuHGuanXWangGampGuoR(2016)Accelerateddry-landexpansionunderclimatechangeNature Climate Change6166
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
JonesCGLawtonJHampShachakM(1994)Organismsasecosys-temengineersInFBSamsonampFLKnopf(Eds)Ecosystem man‐agement(pp130ndash147)NewYorkNYSpringer
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
KerleyGIWhitfordWGampKayFR(2004)Effectsofpocketgo-phersondesertsoilsandvegetationJournal of Arid Environments58155ndash166httpsdoiorg101016jjaridenv200308001
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
NakagawaS(2015)MissingdataMechanismsmethodsandmessagesInGAFoxSNegrete‐YankelevichampVJSosa(Eds)Ecological sta‐tistics Contemporary theory and application(pp81ndash105)UKOxfordUniversityPress
NakagawaSampSantosES(2012)Methodologicalissuesandadvancesin biological meta‐analysis Evolutionary Ecology 26 1253ndash1274httpsdoiorg101007s10682‐012‐9555‐5
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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Bt
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Bn
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Cg
(Continues)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
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CoppockDetal(1983)Effectsofblack‐tailedprairiedogsonintraseasonalabovegroundplantbiomassandnutrientdynamicsandplantspeciesdiversityOecologia561ndash9
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Cu
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Da
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Dl
DesmetPandCowlingR(1999)PatchcreationbyfossorialrodentsakeyprocessintherevegetationofphytotoxicaridsoilsJournalofAridEnvironments4335ndash45
Dt
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Dh
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Dk
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Dw
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Du
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Ed
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El
EldridgeDJandRathD(2002)Hipholeskangaroo(Macropusspp)restingsitesmodifythephysicalandchemicalenvironmentofwoodlandsoilsAustralEcology27527ndash536
Er
EldridgeDJandSimpsonR(2002)Rabbit(Oryctolagus cuniculusL)impactsonvegetationandsoilsandimplicationsformanagementofwoodedrangelandsBasicandAppliedEcology319ndash29
Es
EldridgeDJandWhitfordWG(2009)Badger(Taxidea taxus)disturbancesincreasesoilheteroge-neityinadegradedshrub‐steppeecosystemJournalofAridEnvironments7366ndash73
Ew
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Ee
EldridgeDJ(2011)Theresourcecouplingroleofanimalforagingpitsinsemi‐aridwoodlandsEcohydrology4623ndash630
Eg
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Eb
EldridgeDJetal(2012)Animalforagingasamechanismforsedimentmovementandsoilnutrientdevelopmentevidencefromthesemi‐aridAustralianwoodlandsandtheChihuahuanDesertGeomorphology157131ndash141
Ef
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Fi
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Fo
APPENDIX (CONTINUED)
(Continues)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
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Bc
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Ic
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Ku
KuznetsovaTAetal(2013)DesertgerbilsaffectbacterialcompositionofsoilMicrobialEcology66940ndash949
Kz
(Continues)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
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KyleGPetal(2008)InfluenceofpocketgophermoundsonnonnativeplantestablishmentinashrubsteppeecosystemWesternNorthAmericanNaturalist68374ndash381
Ky
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Li
LitaorMIetal(1996)TheinfluenceofpocketgophersonthestatusofnutrientsinalpinesoilsGeoderma7037ndash48
Lt
LiuYetal(2013)Effectsofplateaupika(Ochotona curzoniae)onnetecosystemcarbonexchangeofgrasslandintheThreeRiversHeadwatersregionQinghai‐TibetChinaPlantandSoil366491ndash504
Lb
MahanCGandYahnerRH(2000)Effectsofforestfragmentationonbehaviourpatternsintheeasternchipmunk(Tamias striatus)CanadianJournalofZoology771991ndash1997
My
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Ml
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MartinsenGDetal(1990)ImpactofpocketgopherdisturbanceonplantspeciesdiversityinashortgrassprairiecommunityOecologia83132ndash138
Me
McMillanBRetal(2011)Vegetationresponsestoananimal‐generateddisturbance(bisonwallows)intallgrassprairieTheAmericanMidlandNaturalist16560ndash73
Mc
MiltonSetal(1997)Effectsofsmall‐scaleanimaldisturbancesonplantassemblagesofset‐asidelandinCentralGermanyJournalofVegetationScience845ndash54
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MitchellJetal(2007)EcologicalimpactsofferalpigdiggingsinnorthQueenslandrainforestsWildlifeResearch34603ndash608
Mt
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Mh
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Mj
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Nd
NugentDTetal(2014)Interactionsbetweenthesuperblyrebird(Menura novaehollandiae)andfireinsouth‐easternAustraliaWildlifeResearch41203ndash211
Nu
OrsquomeiliaMetal(1982)SomeconsequencesofcompetitionbetweenprairiedogsandbeefcattleJournalofRangeManagement35580ndash585
Om
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Pl
PrughLRandBrasharesJS(2012)PartitioningtheeffectsofanecosystemengineerkangarooratscontrolcommunitystructureviamultiplepathwaysJournalofAnimalEcology81667ndash678
Pb
QuestadEJandFosterBL(2007)VoledisturbancesandplantdiversityinagrasslandmetacommunityOecologia153341ndash351
Qf
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Rb
ReichmanOandJarvisJ(1989)Theinfluenceofthreesympatricspeciesoffossorialmole‐rats(Bathyergidae)onvegetationJournalofMammalogy70763ndash771
Re
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Rc
ReichmanO(1988)ComparisonoftheeffectsofcrowdingandpocketgopherdisturbanceonmortalitygrowthandseedproductionofBerteroa incanaTheAmericanMidlandNaturalist12058ndash69
Ra
ReichmanOetal(1993)Distinctanimal‐generatededgeeffectsinatallgrassprairiecommunityEcology741281ndash1285
Rn
RezsutekMandCameronGN(2000)VegetativeedgeeffectsandpocketgophertunnelsJournalofMammalogy811062ndash1070
Rz
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Ri
RogersWEetal(2001)Effectsofplainspocketgopher(Geomys bursarius)disturbancesontallgrass‐prairieplantcommunitystructureTheAmericanMidlandNaturalist145344ndash357
Ro
(Continues)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
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Sc
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Sy
SeastedtTetal(1986)MicroarthropodsandnematodesinkangarooratburrowsTheSouthwesternNaturalist31114ndash116
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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
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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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
12emsp |emsp emspensp MALLEN‐COOPER Et AL
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
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
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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
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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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp13MALLEN‐COOPER Et AL
APPENDIX DATA SOURCES
Included study Study code
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
Included study Study code
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)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
14emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp15MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
16emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp17MALLEN‐COOPER Et AL
Included study Study code
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
Included study Study code
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)
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
18emsp |emsp emspensp MALLEN‐COOPER Et AL
Included study Study code
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
CoombesMAandVilesHA(2015)Population‐levelzoogeomorphologythecaseoftheEurasianbadger(Meles melesL)PhysicalGeography36215ndash238
GarkaklisMJetal(1998)Theeffectsofwoylie(Bettongia penicillata)foragingonsoilwaterrepellencyandwaterinfiltrationinheavytexturedsoilsinsouthwesternAustraliaAustralianJournalofEcology23492ndash496
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)
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)
emspensp emsp | emsp19MALLEN‐COOPER Et AL
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
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
Studies (uncited elsewhere in the manuscript) from which body mass or disturbance area data were retrieved
Study code
VerdolinJLetal(2008)MorphologyofburrowsystemsAcomparisonofGunnisonrsquos(Cynomys gunnisoni)White‐Tailed(C leucurus)Black‐Tailed(C ludovicianus)andUtah(C parvidens)prairiedogsTheSouthwesternNaturalist53201ndash207
VleckD(1981)BurrowstructureandforagingcostsinthefossorialrodentThomomys bottae Oecologia 49391ndash396
WangJMetal(2006)Seasonalthermogenesisandbodymassregulationinplateaupikas(Ochotona curzoniae)Oecologia149373ndash382
WangZLetal(2012)cDNAcloningandexpressionoferythropoietinintheplateauzokor(Myospalax baileyi)fromtheQinghai‐TibetPlateauChineseScienceBulletin57997ndash1006
WelanderJ(2000)Spatialandtemporaldynamicsofwildboar(Sus scrofa)rootinginamosaiclandscapeJournalofZoology252263ndash271
WrightNI(2006)EcologicalimpactsofHighveldgerbils(Tatera brantsii)onarehabilitatedashdisposalsiteMastersthesisNorth‐WestUniversity
YoshiharaYetal(2009)EffectsofdisturbancebySiberianmarmots(Marmota sibirica)onspatialheterogeneityofvegetationatmultiplespatialscalesGrasslandScience5589ndash95
ZhangYM(2007)Thebiologyandecologyofplateauzokors(Eospalax fonatanierii)InBegallSBurdaHampSchleichCE(Eds)SubterraneanRodentsNewsfromUnderground(p237ndash249)SpringerHeidelberg
APPENDIX (CONTINUED)