Stable isotopes reveal limited Eltonian niche conservatism across … · 2019-02-05 · The conservation of Grinnellian niche characteristics ... martens predominating in mainland

Functional Ecology 201933335ndash345 wileyonlinelibrarycomjournalfec emsp|emsp335copy 2018 The Authors Functional Ecology copy 2018 British Ecological Society

Received6July2018emsp |emsp Accepted3December2018DOI1011111365-243513266

R E S E A R C H A R T I C L E

Stable isotopes reveal limited Eltonian niche conservatism across carnivore populations

Philip J Manlick1 emsp|emspShelby M Petersen1emsp|emspKatie M Moriarty2emsp|emspJonathan N Pauli1

1DepartmentofForestandWildlifeEcologyUniversityofWisconsin-MadisonMadisonWisconsin2PacificNorthwestResearchStationUSDAForestServiceOlympiaWashington

CorrespondencePhilipJManlickEmailpmanlickwiscedu

Funding informationDivisionofGraduateEducationGrantAwardNumberDGE-1144752

HandlingEditorClareMcArthur

Abstract1 NicheconservatismmdashtheretentionofecologicaltraitsacrossspaceandtimemdashisanemergingtopicofinterestbecauseitcanpredictresponsestoglobalchangeTheconservationofGrinnelliannichecharacteristicslikespecies-habitatassocia-tionshasreceivedwidespreadattentionbuttheconservationofEltoniantraitssuchasconsumerndashresourceinteractionsremainspoorlyunderstood

2 TheinabilitytoquantifyEltoniannichesthroughspaceandtimehashistoricallylimitedtheassessmentofEltoniannicheconservatismandthedynamicsofforag-ingacrosspopulationsConsequentlytherelativeinfluenceofendogenousfac-tors like phylogeny versus exogenous features like environmental context hasrarelybeenaddressed

3 WetestedEltoniannicheconservatismusingapaireddesigntocompareforagingamongfourpopulationsofAmericanmartensMartes americana and Pacific mar-tensMartes caurinamorphologicallyandecologicallysimilarsistertaxathatareallopatrically distributed throughout western North AmericaWe developed athree-stage isotopic framework and then quantified dietary niche overlap be-tween thesister speciesandpaired island-mainlandsites toassess the relativeinfluenceofendogenous (iespecies)versusexogenous (ieenvironment)fac-torsonEltoniannichesFirstwecalculatedpairwisedietaryoverlapinscaledδ-spaceusingstandardellipsesWethenestimatedproportionaldiets (ldquop-spacerdquo)forindividualsusingisotopicmixingmodelsanddevelopedanovelutilizationdis-tribution overlap approach to quantify proportional dietary overlap Lastlyweestimatedpopulation-levelproportionaldietsandquantifiedthedifferentialuseoffunctionalpreygroupsacrosssites

4 Wedetectednopairwiseoverlapofdietarynichesinδ-spaceanddistributionsofindividualdietsinp-spacerevealedlittleoverlapincoredietsacrosspopulationsAllpairwisecomparisonsofindividualsrevealedsignificantdifferencesindietandpopulation-levelcomparisonsdetectedcontrastinguseoffunctionalpreygroups

5 Wedevelopedamulti-facetedisotopicframeworktoquantifyEltoniannichesandfoundlimitedevidenceofEltoniannicheconservatismacrosscarnivorepopula-tionsOurfindingsareconsistentwiththegrowingrecognitionofdietaryplastic-ityinconsumersandsuggestthatconsumerndashresourcedynamicsarelargelydrivenbyexogenousenvironmentalfactorslikelandcoverandcommunitycomposition

336emsp |emsp emspenspFunctional Ecology MANLICK et AL

1emsp |emspINTRODUC TION

Ecologistshavelongbeenfascinatedbytraitdifferencesacrosspop-ulationsandspecies(MacArthur1972)Asoneofthemostinfluentialconceptsinecologynichetheoryhasbeencentraltoidentifyingcausesofecologicaldivergenceamongtaxa(ChaseampLeibold2003)Morere-centlytheretentionofecologicaltraitsacrossspaceandtimemdashnicheconservatismmdashhasemergedasaprimaryinterestofecologists(WiensampGraham2005)Nicheconservatismhelpsexplainthestructureofbiodiversitygradients(AllenampGillooly2006Buckleyetal2010)andimprovespredictionsofspeciesrsquoresponsestoglobalchange(CooperFreckletonampJetz2011PearmanGuisanBroennimannampRandin2008)andspeciesinvasions(WiensampGraham2005)Moreovernicheconservatismisafundamentalassumptionofmanyspeciesdistribu-tionmodelsusedtomapGrinnelliannichesthenon-interactiveenvi-ronmentalaspectsofaspeciesrsquorange(Grinnell1917)ConsequentlyGrinnellian niches have been the primary focus of ecological nicheconservatismanda renewed interest in species-habitat associations(Petersonetal2011)Similarlyphylogeneticnicheconservatismortheretentionofancestralecologicaltraitsamongrelatedtaxahasalsoreceivedwidespreadattentionshedding lightoncommunityassem-blyandtheadaptabilityofspeciesacrosssystems(Cooperetal2011Losos2008)Meanwhilebioticinteractionshaveremainedacorner-stoneofecology(ChaseampLeibold2003)yettheconservationofcon-sumerndashresourcedynamicsdefinedbytheEltonianniche(Elton1927)hasremainedrelativelyunderstudied(Olalla-TaacuterragaGonzaacutelez-SuaacuterezBernardo-MadridRevillaampVillalobos2016RosadoFigueiredodeMattosampGrelle2016)Giventheimportanceofsuchtrophicdynam-icsforecologicalprocesses(Estesetal2011)understandingtheroleofEltoniannicheconservatismandthecapacityforadaptabilitywillbekeytobothpreservingandrestoringecosystemfunctionsinthefaceofcontinuingglobalchange

Re-establishing trophic interactions has become a global eco-logical priority (Dobson etal 2006 Estes etal 2011) and therestorationofpredatorshasbeenproposedtobothpreserveeco-systemfunctionality(Ritchieetal2012)andpromotebiodiversity(Terborgh2015) Inparticularthere-establishmentofmammaliancarnivoresisincreasinglypromotedtorestoreecosystemfunction-alitylargelythroughthetransferenceofconsumerndashresourcedynam-ics and top-down forcing (Ripple etal 2014Ritchie etal 2012)Restoring these functional relationships among consumers how-everremainschallenging(Fraseretal2015)mostlyduetothedy-namicnatureofforagingecologyandtheinabilitytoquantifytrophicinteractions throughspaceandtime Indeedsuchpredator-driven

ecologicalrestorationhingesonEltoniannicheconservatismandthepreservationofconsumerndashresourcedynamicsbuttheseprocessesremainpoorlyunderstood

Eltonian niche conservatism is governed by foraging ecologywhichisgenerallyafunctionofclimatelandcoverandbioticinter-actions(StephensBrownampYdenberg2007)Atthesitelevelcli-mateoftendeterminesprimaryproductivitylandcovercompositionandspeciesrichness(ChapinMatsonampVitousek2011MacArthur1972)which in turn regulates resourceavailabilityAt the individ-uallevelclimateandlandcoverinfluenceactivitylevelsbyalteringforagingratesandmetaboliccosts(KearneyShineampPorter2009)Similarlybioticinteractionslikepredationandcompetitioninteractwithclimateandlandcovertomodifyresourceaccessibilityandalterforagingdynamics(DarimontPaquetampReimchen2009)Giventhenumber of exogenous factors influencing foraging ecology acrossscalestheconservationofEltoniannicheshasbeenunsurprisinglyboth supported (Boumlhning-GaeseampOberrath1999) andcontested(Olalla-Taacuterragaetal2016)

While Grinnellian and phylogenetic niche conservatism havebeen widely observed in mammals (Cooper etal 2011 Olalla-Taacuterragaetal2011PetersonSoberoacutenampSaacutenchez-Cordero1999)idiosyncraticpatternsofdivergenceandconservatismhavebeenob-servedacrosscarnivorecladesincludingfelidscanidsandmustelids(Buckleyetal2010Diniz-FilhoTerribileDaCruzampVieira2010)Nevertheless Grinnellian niche axes are correlatedwith resourceavailability suggesting that Eltonian niches are also conserved inboth space and time (Soberoacuten 2007) IndeedOlalla-Taacuterraga etal(2016)observedEltoniannicheconservatisminmammalsatbroadphylogeneticscaleshowevercarnivoresexhibitedtheweakestre-sponseofallmammalianordersandlimiteddietaryinformationledtocontrastingconclusionsRecentfine-scaleanalyseshavesimilarlyrevealed remarkable foraging plasticity among carnivore species(Darimont etal 2009NewsomeGarbeWilsonampGehrt 2015)suggestingexogenousdrivers like landcoverandcompetitionmayregulateEltoniannichesratherthanphylogenyConsequentlyfunc-tionalrolescoupledtoforagingmaybesimilarlydynamicwithim-portantconsequencesforecologicalprocessesacrossecosystems

To assess Eltonian niche conservatismwe examined the dietsof two generalist and closely related carnivores in northwesternNorth America American martens Martes americana and Pacific martensMartes caurinaThesemustelidsarerecentlydivergedsistertaxathatpossesscomparablemorphologicalandecologicalcharac-teristicsandoccupysimilarlandcovertypesacrosswesternNorthAmerica (Dawsonetal2017)Though isolatedformillenniaboth

These results illustrate the context-dependent nature of foraging and indicateconsumerfunctionalitycanbedynamic

K E Y W O R D S

AlaskaBritishColumbiaforagingfunctionalrolesMartesnicheconservatismpredatorrestoration

emspensp emsp | emsp337Functional EcologyMANLICK et AL

species occur throughout the Pacific Northwest with Americanmartens predominating in mainland populations to the north andPacific martens occupying coastal regions to the south (Dawsonetal2017)Inadditioncomplexcolonizationhistorieshaveledtosporadicdistributionsofboth species throughout thearchipelagicsystemsofAlaskaandBritishColumbia(Paulietal2015)LikemanyNorthAmericancarnivoresbothmartenspeciesareforesthabitatspecialists but dietary generalists (Martin 1994) Moreover bothspeciesaresensitivetoland-usechangeandregularlycompetewithothercarnivoresbothofwhicharehypothesizedtoaffectforagingdynamics(ManlickWoodfordZuckerbergampPauli2017ZielinskiTuckerampRennie2017)

To quantify Eltonian niche conservatism in American andPacific martens we developed a novel stable isotope frame-work Measuring Eltonian niches has long troubled ecologistsand the inability toaccuratelyassessbiotic interactions like for-aging across space and time has resulted in the Eltonian short-fall (Rosado etal 2016) and limited estimates of Eltonian nicheconservatism(Olalla-Taacuterragaetal2016)HoweverstableisotopeanalyseshaveemergedasanidealtooltoquantifyEltoniannichesbecausetheymeasuretheassimilationofresources inconsumertissuesandcapturebioticinteractionsthataremediatedbyforag-ing(ComteCucheroussetampOlden2016LarsonOldenampUsio2010 Newsome Martinez del Rio Bearhop amp Phillips 2007)Herein we use stable isotope analyses to assess differences inforagingacrossspeciesandenvironmentalcontextbyestimatingthedietsofAmericanandPacificmartensonmainlandandislandsites inthePacificNorthwestofNorthAmericathatdiffer inbi-oticinteractions(iecarnivorerichness)dominantlandcoverandlevelofhumandisturbance(Figure1)Specificallywedevelopeda three-stage isotopic framework thatcomparedEltoniannichesacross populationsby calculating (a) pairwisedietaryoverlap inisotopicδ-space(b)individualdietsusingisotopicmixingmodelsandpairwisenicheoverlapusinganovelimplementationofutiliza-tiondistributionoverlapindicesinproportionaldietaryspaceand(c)pairwisedifferencesintheproportionaluseoffunctionalpreygroupsusingpopulation-leveldietsfromisotopicmixingmodels

2emsp |emspMATERIAL S AND METHODS

21emsp|emspStudy areas

We compared diets of American and Pacific marten populationsin a 2times2 paired design of mainland and island sites (Figure1)Mainland populations includedMisty Fjords National MonumentAlaska(hereafterMainlandamericana)andOregonDunesNationalRecreationArea(hereafterMainlandcaurina)Islandpopulationsin-cludedPrinceofWales IslandAlaska (hereafter Islandamericana)andHaidaGwaiiIslands(formerlyQueenCharlotteIslandshereaf-terIslandcaurina)Allpopulationswerecoastalandpotentialexog-enousdriversofforagingsuchaspreycompetitorsandlandcovercompositionweresimilaracrosssites(TablesS1andS2SupportingInformation)Preygroupswere largelyconservedacrosssitesand

eachpopulationhadaccesstofiveprimarypreyknowntosupportmartens small mammals birds deer berries and marine-derivedresources(Martin1994)Converselycarnivorerichnesswhichhasthepotentialtomediateforagingthroughcompetitiveinteractionsdiddifferby locationandwashigheratmainlandthan islandsites(Figure1 Table S1 Supporting Information) enabling inferenceson biotically mediated foraging differences across populationsEstimatesofpreyavailabilityandpredatorabundancedatawerenotavailable for this studyMainlandamericana Islandamericana and Islandcaurinasitesarecomposedoftemperatecoastalrainforestscharacterizedbydenseold-growthforestThesouthernmostsiteMainland caurina features sand dunes andwetlands bounded byericaceous shrubs with a broader landscape dominated by xericconiferforestsHoweverthedominantlandcoverattheMainlandcaurinasitewasimpervioussurfaces(Figure1) indicatingsubstan-tialhumanimpacts

F I G U R E 1 emspComparisonofmainlandandislandsitesincludingdominantlandcoverprecipitationlevelandcarnivorerichnessvaluesCross-hatchedregionsillustrateMartes americanapresencewhileblackregionsillustrateMartes caurinapresenceThreeraindropsindicatehighlevelsofprecipitation(gt170mmmonth)andoneraindropindicateslowlevelsofprecipitation(lt140mmmonth)Carnivorerichnessindicatesthenumberofcarnivorespresentateachsite

130 00W

130 00W140 00W

120 00W

550

0N

500

0N

500

0N

450

0N

450

0N0 150 300

Kilometres plusmn


22emsp|emspSampling

Wecollectedallhairsamplesfrommartenswithin2kmofthecoastto ensure every individual had access to the same primary preygroupsSampleswerecollectedinfallandwinterusingactivecap-ture techniques (MoriartyBaileySmytheampVerschuyl2016)andtrapperharvestedsamples(Paulietal2015)(TableS2SupportingInformation)Hairisaninerttissuethatrepresentsdietoverthepe-riod itwassynthesizedandpeakmartenhairgrowthoccursfromJuly throughOctober (PauliBen-DavidBuskirkDePueampSmith2009) Therefore our samples represent the assimilated diets ofmartens inautumnPreysampleswerecollectedopportunisticallyfromeachsiteorderivedfromtheliterature(TableS2SupportingInformation) In total we sampled all primary prey groups (smallmammalsbirdsdeerberriesandmarine-derivedresources)ateachsiteAllsamplingadheredtotheethicalguidelinesestablishedbytheAmericanSocietyofMammalogists(Sikes2016)wasapprovedbytheUniversityofWyomingandUSDAForestServicesInstituteforAnimalCareandUseCommittee(USFS2015-002)andwaspermit-tedbytheOregonDepartmentofFishandWildlife(ODFW119-15)AlaskaDepartment of Fish andGame (ADFG06-016) andBritishColumbiaMinistryoftheEnvironment

23emsp|emspStable isotope analyses

Marten and prey hair samples were rinsed 3times with a 21chloroformmethanolsolutiontoremovesurfacecontaminantsho-mogenizedwithsurgicalscissorsanddriedat56degCforaminimumof 72hr Similarly all vegetationmarine and tissue sampleswererinsed3timeswitha21chloroformmethanolsolutionanddriedat56degCfor72hrbutsamplesweresubsequentlyhomogenizedwitheitheraballmillmixeroramortarandpestleSampleswereweighedintotincapsulesforδ13Candδ15NanalysisonaCostech4010elementalanalyser(ValenciaCA)coupledtoaThermoScientificDeltaVmassspectrometer at the University of NewMexico Center for StableIsotopesResultswere calculated asparts permil (permil) ratios rela-tivetotheinternationalstandardsViennaPeedeebelemnite(C)andatmosphericnitrogen(N)

Toassess isotopicnicheoverlap inδ-spaceand to identify thecomparabilityof isoscapesweemployedamulti-responsepermu-tationprocedure (MRPP) using10000 iterations in the r packagevegan(Oksanenetal2013)totestfordifferencesinmeansandvari-ancesamongfunctionalpreygroupsBecauserawδvaluesofpreygroupsdifferedsignificantlyacrossallsitesandcomparisonsacrossvariableisoscapescanbemisleading(NewsomeYeakelWheatleyampTinker2012)wetrophicallycorrectedallmartenisotopicsignatures(δ13C=minus26δ15N=minus34Vulpes vulpesRothampHobson2000)andscaled them to their respectivemixing spaces resulting in a unit-lessmultidimensional isoscapethatenabledinter-populationcom-parisons (seeCucheroussetampVilleacuteger2015 fordetails)Toassessdietarynicheoverlapbetweensiteswecalculated isotopicnichesforeachpopulationusingstandardellipsescorrectedforsamplesize(SEAC)andquantifiedSEACoverlapinδ-spaceusingtherpackage

siar(ParnellIngerBearhopampJackson2010)WethenemployedaMRPPinusing10000iterationstotestforpairwisedifferencesinthemeansofscaledisotopicvaluesbetweenmartenpopulations

Toestimatetheproportionaldietarycontributionsforeachpop-ulationwefirstidentifiedpreygroupsusingaKnearest-neighbourrandomizationtest (RosingBen-DavidampBarry1998)todifferen-tiatepreyitemswithineachsiteandwethencomparedacrosslo-cations to identify the finest resolutionof prey groups consistentacrosssitesThisresultedinthreeisotopicallydistinct(allpairwisep lt 005) functional prey groups thatwere available tomartens ineach population berriesmarine-derived resources and terrestrialvertebrates Isotopicsignaturesofsongbirdsdeerandsmallmam-mals were indistinguishable from one another and aggregated tocomprise the terrestrial vertebrate group Likewise salmon crabsand intertidalmolluscsdominatedmarine-derivedpreywhileber-riessegregatedasasinglegroupWeestimateddietaryproportionsusingBayesian-basedisotopicmixingmodelsinSIAR(Parnelletal2010)andweestimatedindividualdietsusingtheldquosiarsolomcmcv4rdquomodel and population-level diets using the ldquosiarmcmcdirichletv4rdquomodelAllmodelsincorporatedconcentrationdependenceusingthemeanelementalconcentrationsforeachpreygroupwerecorrectedfortrophicenrichmentofmartensamples(asaboveRothampHobson2000)andincorporatedonlyuniformpriordistributionsEachmodelran 200000 iterations with an additional 25 burn-in and wassampled10000times

To quantify dietary overlap in p-spacewe usedmean dietaryproportions estimated for each individual and employed an iso-metriclog-ratiotransformationtoconvertcompositionaldietsintoCartesian coordinates suitable for multivariate analyses (EgozcuePawlowsky-Glahn Mateu-Figueras amp Barceloacute-Vidal 2003) Usingthetransformeddietaryestimateswegenerated50and95ker-neldensityestimatesofdietarydistributionsforeachpopulationandthencalculatedproportionaloverlapofdietsandthepairwiseutili-zationdistributionoverlapindex(UDOIsensuFiebergampKochanny2005)indietaryp-spaceusingtherpackageadehabitathr(Calenge2006)With this framework50UDOIs represent theoverlapofldquocorerdquodietswhile95UDOIs representoverlapof ldquoavailablerdquodi-etary resources for each population (Fieberg amp Kochanny 2005)Estimatesofoverlaprangefromzero(nooverlap)toone(completeoverlap)andareakintotheHurlbertIndexofnicheoverlap(Fiebergamp Kochanny 2005)We then tested for significant differences inproportionaldietsbetweenpopulationsusingthetransformeddietestimatesandpairwiseMRPPswith10000iterations

Lastly we assessed pairwise differences in functional preygroupsusingtheposteriordistributionsofpopulation-leveldietses-timatedinSIARFollowingHopkinsKochFergusonandKalinowski(2014)we extracted themarginal posterior distributions for eachdiet item per site and calculated the probability that populationsconsumeddifferentproportionsoffunctionalpreygroupsForeachcomparison we created two new distributionsY=X1ij ndash X2ik and Z=X2ik ndash X1ijwhereX1ij is themarginal posterior distribution fordietitemiinpopulationj and X2ikisthemarginalposteriordistribu-tionfordietitemiinpopulationkToidentifysignificantdifferences


inpreyusebetweensiteswethencalculatedthetwo-sidedprob-abilitythatthedifferencebetweenmarginalposteriordistributionsY and ZwaslessthanzerogivenbyP(Ylt0)+P(Zgt0)(seeHopkinsetal2014fordetails)Thistestisanalogoustoattestandsignifi-cancewasassessedatα=005001and0001

3emsp |emspRESULTS

We sampled 158 American martens 65 Pacific martens and 296preyitemsacrossallfoursites(Table1)UsingscaledisotopicvalueswedetectednooverlapinSEACbetweenanypairwisecomparisonsin δ-space (Figure2) Similarly permutation tests detected signifi-cantdifferences(p lt 005)inscaledisotopicsignaturesforallcom-parisons(Figure2)

Utilizationdistributionoverlapindicesrevealedlittletonoover-lap incorediets (00ndash01050UDOITable2Figure3)buthighoverlap in available diets (95UDOI) forM americana and islandpopulations (Table2)Moreoverpercentoverlapofdietarydistri-butionsinp-spacewashigh(gt50)forthemajorityofcomparisons(Table2)NeverthelesspairwiseMRPPsdetectedsignificantdiffer-encesinthedistributionofindividualdietsforallpairwisecompar-isons(Figure3)

Proportional diets of individuals and populations indicatedthat in generalmainlandmarten populations exhibited specializeddiets dominatedby terrestrial vertebrateswhile islandpopulations

exhibited generalist tendencieswith evenlydistributeduseof preygroups (Table1Figures3and4)Pairwisecomparisonsofpreyuseacrosspopulationswerewidelyidiosyncraticbutwedetectedmoresignificantdifferencesinpreyusebetweenspeciesthanbetweenis-landandmainland sites (Figure4)Wedetected littledivergence inuse of terrestrial vertebrates (all populations ge30 use) and bothmainland populations exhibited gt50 reliance on this resource(Table2Figure3)Allpopulationsdisplayedge30useofmarine-de-rived resources except forMainlandcaurinawhere the limiteduseofmarine prey (12) drove all significant differences among com-parisons including the only significant difference betweenM cau-rinapopulations(Figure3)Likewisetheconsumptionofberrieswashighlyvariable(98ndash362)andexhibitedsignificantdifferencesin3of4pairwisecomparisonsincludingtheonlysignificantdifferenceinM americanapopulations

4emsp |emspDISCUSSION

We employed a series of stable isotope analyses to quan-tify Eltonian niches across marten populations in the PacificNorthwestandouranalysesrevealed littledietarynicheoverlapacross populationsWe detected no overlap in isotopic δ-spacelimitedoverlapofcoredietsinp-spaceandhighlyvariableuseoffunctional prey groups acrosspopulationsAll analysesdetectedsignificant differencesbetweenpopulations These findings sug-gest thatmartens in thePacificNorthwestexhibit littleEltoniannicheconservatismacrosseitherspeciesorsitesOurstudyisoneof few to explicitly assess Eltonian niche conservatism and thefirst to assess fine-scaleEltonianniches as a functionof endog-enousversusexogenousdrivers(Comteetal2016Larsonetal2010 Olalla-Taacuterraga etal 2016) Nevertheless our results areconsistentwith recent studies illustrating the plasticity ofmam-maliandietaryniches(TerryGuerreampTaylor2017)andthelackofnicheconservatismamongcarnivoresinparticular(Buckleyetal2010Diniz-Filhoetal2010)

Eltoniannichesarenotoriouslydifficulttoquantify(Rosadoetal2016)andqualitativemeasuresofdietarybreadthhavepreviouslyledtocontrastingevidenceofEltoniannicheconservatisminmam-mals (Olalla-Taacuterragaetal2016)Wedevelopedanisotopicframe-workusingcomplimentaryanalysesofisotopicδ-spaceanddietaryp-space to clearly illustrate the variable nature of foraging acrosscarnivorepopulationsNumerousstudiesassessisotopicnicheover-lapinδ-spaceorcalculateproportionaldietsbutfewcombinetheseapproachestoquantitativelyassessdietvariabilityMoreoverquan-tifiablemetricsofdietaryoverlapinp-spacearenascent(Newsomeetal 2007 Parnell etal 2010)Our approach quantifies overlapinbothisotopicnichesanddietaryproportionsanditcanbeusedto quantify dietary differences between populations or speciesthroughspaceandtimeIndeedwhileweimplementedthisframe-worktoassessdietaryoverlapandmeasureEltoniannicheconser-vatismacrossfourpopulationswithsimilarenvironmentalcontextsanalogous approaches could be used to quantify niche overlap in

TA B L E 1 emspEstimatedmeanproportionalcontributionofeachfunctionalpreygrouptosampledmartenpopulations(with95confidenceintervals)

Site Prey groupDietary proportion ()

Islandamericana (n = 98)

Berries(n = 45) 252(205ndash299)

Marine-derived(n = 25)

325(289ndash361)

Terrestrialverte-brates(n = 37)

424(365ndash483)

Mainlandamericana (n = 55)



383(288ndash471)


519(401ndash647)

Islandcaurina(n = 52) Berries(n = 20) 348(283ndash412)


349(314ndash385)


303(225ndash387)

Mainlandcaurina (n = 13)



121(00ndash264)


517(225ndash815)


competitorsshifts indietsthroughtimeorforagingdynamicsfol-lowinganthropogenicdisturbance

While our approach employed three complimentary analyseseach has important limitations For examplewhen comparing iso-topicsignaturesofconsumersinδ-spaceacrossecosystemsdietaryrelationshipscanbeskewedbyisoscapevariability(Newsomeetal2012)Weaccountedforsuchdifferencesinisoscapesbystandard-izingeachpopulationtoitsownisotopicmixingspace(CucheroussetampVilleacuteger2015)butthisassumesallpreyspeciesareaccountedforandthatthetotal isotopicvariabilityofthesitehasbeencapturedDespiteourextensivepreysamplingitisunlikelythatwecapturedthe entire isotopic landscape However transforming isotopic sig-naturestop-spaceviamixingmodelsremovesthepotentialscalingdiscrepanciespresentinδ-space(Newsomeetal2007)Moreovermixingmodelsallowedustoestimateproportionaldietsformartensand thendeterminep-spaceoverlapusinganovelUDOIapproachtraditionally used to quantify spatial overlap Analogous to homerangeanalysesdietaryoverlapfromUDOImaybesensitivetosam-plesizesandtheparametersdefiningkerneldensityestimates(ErranampPowell1996FiebergampKochanny2005)butthisapproachallowsfor quantitative estimates of p-space overlap viamethods familiartomostecologistsSimilarlyquantifyingthedifferentialuseofprey

viaposteriordistributionoverlapprovidesaclearandtractableana-lyticalapproachanalogoustoattestNeverthelesstheseanalysesrelyonmixingmodelswithimportantconstraintsForinstanceourfunctionalpreygroupsexhibitedconsiderable linearityateachsiteresultinginnegativecorrelationsbetweenposteriorprobabilitiesofdietaryproportionsforbothindividualandpopulation-leveldietesti-mates(FiguresS1andS2SupportingInformation)Thismeansthereweremultiplesolutionstoeachmixingmodelthoughtherewaslittlevariation in posterior probabilities formostmodels (Figure4) sug-gestingdietaryestimateswereconsistentdespitecollinearityinpreyisotope signatures It is worth noting however thatmodel uncer-taintyandvariationinposteriorprobabilitiescouldreducepowertodetectdifferencesindietsbetweenpopulationsAdditionallytrophicdiscrimination factors can influence estimates frommixingmodels(Phillipsetal2014)andspecies-specificdiscriminationfactorswereunavailable for this studyHowever our applied enrichment factorhasbeenwidelyusedtoestimatecarnivorediets(Carlsonetal2014Darimontetal 2009Yeakel etal 2009) and fallswithin thepre-dictedrangeformartens(Healyetal2018)Despitethesenuancesweimplementedthreeindependentapproachestoquantifydietaryoverlapandobservedequivalentresultstherebyreinforcingourcon-clusionsandthepowerofthesecomplimentaryanalysesUltimately

F I G U R E 2 emspNicheoverlapincorrectedδ-spaceforMartes americana(a)Martes caurina(b)islandmartens(c)andmainlandmartens(d)fromfourstudysitesinnorthwesternNorthAmericaPairwiseisotopicnicheoverlap(O)amongstandardellipsescorrectedforsmallsamplesize(SEACblack)waszeroforallcomparisonsandp-valuesindicatesignificanceofamulti-responsepermutationprocedure(MRPP)comparingthedistributionofindividualsincorrectedδ-space

00

02

04

06

08

10

00 02 04 06 08 10

δ15N

sca

led

(a)

O = 00p lt 005

Mainland americanaIsland americana

00

02

04

06

08

10

00 02 04 06 08 10

(b)

O = 00p lt 005

Mainland caurinaIsland caurina

00

02

04

06

08

10

00 02 04 06 08 10

δ13C scaled

δ15N

sca

led

(c)

O = 00p lt 005

Island americanaIsland caurina

00

02

04

06

08

10

00 02 04 06 08 10

δ13C scaled

(d)

O = 00p lt 005

Mainland americanaMainland caurina


thisframeworkprovidesablueprintforfutureecologiststoquantita-tivelytestdietarydifferencesinspaceandtime

WefoundlimitedevidenceforEltoniannicheconservatismandpairwisedietcomparisonsrevealedtrade-offsintheuseofresourcesacrosspopulationsForinstanceallindividualsweresampledwithin2kmof thePacific coast yetMainlandcaurinamartensdisplayeda significantly lower use of marine resources compared to othersites but compensated with the highest consumption of berriesUnlike theother locationsvegetation in theMainlandcaurina sitetypicallydoesnotextend to theshorelineandallochthonousma-rineresources(egsalmon)havebeenseverelydepleted(NehlsenWilliamsampLichatowich1991)ThusMainlandcaurina individualswereconfinedtovegetatedareas(LinnellMoriartyGreenampLevi2018)andaccesstomarineresourceswaslikelylimitedtoinletsandseasonal flooding Moreover the 13Mainland caurina individuals

sampledconstituteuptoaquarterofallindividualsinthisisolatedpopulation(Linnelletal2018)buttheareaharboursoveradozencompetingcarnivoresthatcouldhavealsopreventedaccesstoma-rineresourcesIndeedwhilemainlandpopulationsgenerallyreliedonterrestrialvertebratesislandpopulationsexhibitedmoregener-alistdietslikelyduetolowercarnivorerichnessandreducedinter-specificcompetitionforalternativeresources(sensuDarimontetal2009)Islandcaurinathesitewiththelowestcarnivorerichnessdis-playednearlyuniformdietaryproportionswhilebothmainlandsitesexhibitedhighcarnivorerichnessandskeweddietaryproportionsinmartens (Table2 Figure3) These results indicate that exogenousenvironmental factors like prey availability (eg allochthonous re-sources)andcompetitionmayhaveastrongerinfluenceonforagingecologythanphylogenywithlandscapecompositionlikelymediat-ing foraging through competition resource availability and access

TA B L E 2 emspEstimatedEltoniannicheoverlapofmartenpopulationsinproportionaldietaryspaceviautilizationdistributionoverlapindicesforcoredietaryspace(50UDOI)andavailabledietaryspace(95UDOI)Inadditiontotaloverlapof95kerneldensitydietestimates(percentoverlap)wasestimatedforIslandamericana(IA)Mainlandamericana(MA)Islandcaurina(IC)andMainlandcaurina(MC)populationsIAMAarrangementindicatesthepercentofIslandamericanadietsoverlappingMainlandamericanadietsfollowedbythepercentofMainlandamericanadietsoverlappingIslandamericanadietswithcodificationmaintainedforallcomparisons

Comparison 50 UDOI 95 UDOI Per cent overlap

Americana(IAMA) 007 073 874617

Caurina(ICMC) 000 003 128523

Island(IAIC) 010 096 663895

Mainland(MAMC) 000 008 128100

F I G U R E 3 emspTernaryplotsofproportionaldietaryspaceforMartes americana and Martes caurinapopulationsusingindividualdietaryestimatesfromisotopicmixingmodelsAxesdenoteproportion()ofeachfunctionalpreygroupestimatedforeachpopulationpointsdenoteestimatedindividualdietsdarkgreypolygonsdenote50confidenceintervalsforthepopulationandlightgreypolygonsdenote95confidenceintervalsforthepopulationInsetarrowsshowpairwiseutilizationdistributionoverlapindicesofcorediets(50UDOI)rangingfromnooverlap(00)tocompleteoverlap(10)andasterisksindicatesignificance(α=005)ofamulti-responsepermutationprocedure(MRPP)comparingthedistributionofestimatedproportionaldietsforindividuals

20

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1002040

6080

100

20 40 60 80 100

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1002040

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1002040

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20 40 60 80 100

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1002040

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20 40 60 80 100

Berries

Marine

Verte

brat

es Berries

Marine

Verte

brat

es

Berries

Marine

Verte

brat

es Berries

Marine

Verte

brat

es

Isla

nd p

opul

atio

ns

Martes americana Martes caurina

Mai

nlan

d po

pula

tions


toresourcesOurworkaimedtoquantifydietaryoverlapandnicheconservatism and therefore did not explicitly quantify underlyingenvironmentalfactorssuchascompetitionpreyavailabilityorfine-scale habitat use that influence carnivore foraging Neverthelesspairwise overlap of individual diet distributions and 95 UDOIsindicatedthatthedietaryspaceldquoavailablerdquotoeachpopulationwassimilarwithgt50overlapinbothmetricsobservedforthemajorityof comparisons (Table2) Future studies should further assess therelationshipbetween landscapespreyavailabilityandcompetitioninorder to test the relativestrengthsof thesedriverson foraginganddietarynicheplasticity

Whilewedetectedsignificantdifferencesindietsacrosspopula-tionswealsofoundthatmartendietsdifferedmorebetweenspecies(M americana vsM caurina) than between environmental contexts(islandsvsmainland)TheseresultssuggestthattheEltoniannichesof martens could in part be conserved phylogenetically For exam-ple islandpopulationsdiffered in theiruseofberriesandterrestrialvertebrateswhilemainlandpopulationsdifferedintheuseofberriesandmarinepreyConverselyM americanadietsdifferedonly intheuseofberriesandM caurinadietsdifferedonlyintheuseofmarineprey thoughuncertainty inthemainlandcaurinadietestimatesmayhavelimitedourpowertodetectsuchdifferencesNeverthelessweobservedsignificantdifferencesintheuseoffunctionalpreygroupsacrossallcomparisonsandthisvariationcouldhaveconsiderableim-plications for the functional roles of carnivores across ecosystemsIndeedgiventheabilityofmartenstodisperseseeds(Willson1993)andmarine-derivednutrients(Ben-DavidHanleyampSchell1998)aswellas regulatediseaseand invasivespecies throughsmallmammalpredation (Hofmeester etal 2017 Sheehy Sutherland OReilly ampLambin2018)suchdifferencesinpopulation-leveldietscouldtrans-latetoimportantdifferencesinfunctionalrolesacrosssitesMoreover

limitedisotopicvariabilityandknowledgeonpreyavailabilityrequiredtheuseofhighlygeneralizedpreygroupsforouranalysesbutmar-tensacrosstheirdistributionshavebeenshowntospecializeonawiderangeofspeciesincludingcricetids(egmicevoles)snowshoeharesLepus americanus and even deer (Carlson etal 2014 Raine 1987ZielinskiampDuncan2004)Whilewedetectedextensiveuseofterres-trialvertebrates it ispossiblethatmartensacrossoursampledpop-ulationsfurtherdifferedintheiruseofspecificpreyitemsLikewiseseasonalandinter-annualvariationinresourcesalongwithincreasesinanthropogenicsubsidiescanhavesimilareffectsonforaging(Ben-DavidFlynnampSchell1997Newsomeetal2015)indicatingthatthefunctionalrolesofcarnivoresarelikelyregulatedbyexogenousenvi-ronmentalfactorsratherthanendogenousphylogeneticconstraints

Ecologistshavehistoricallyviewedcarnivoresincludingmartensashabitatandresourcespecialists(Rosenzweig1966)buttheglobalrecovery of carnivores across diverse landscapes has questionedthisparadigm (PauliDonadioampLambertucci2018)Weobservedhighly variable diets across marten populations and our findingsare consistent with recent studies illustrating widespread dietaryplasticity among carnivores across ecosystems (Davis etal 2015Newsomeetal2015SmithWangampWilmers2016)Forexamplecougars Puma concolor in the Intermountain West have exhibitedisotopicniche shifts fromhistorical specialization to contemporarysemi-generalizationfollowingchanges in landuse(MossAlldredgeLoganampPauli 2016)while evenhighly specialized carnivores likeblack-footed ferretsMustela nigripes have demonstrated surprisinglevelsofdietaryplasticity(BricknerGrenierCrosierampPauli2014)Moreoverourresultsreinforcethegrowingbodyofliteratureshow-ingthatexogenousfactorslikeresourceavailabilityandcompetitionregulateforagingecologyandnicheplasticityinbothapexandmeso-predators(Darimontetal2009Newsomeetal2015Smithetal

F I G U R E 4 emspPosteriordistributionsofberriesmarine-derivedresourcesandterrestrialvertebratesestimatedforsampledAmerican(Martes americana)andPacific(Martes caurina)populationsusingBayesian-basedisotopicmixingmodelsInsetp-valuesdenoteresultsoft testsquantifyingdifferencesinposteriordistributionsbetweenmainlandandislandM americana(pAmericana)mainlandandislandM caurina (pCaurina)islandM americanaandislandM caurina(pIsland)andmainlandMartes americana and M caurina(pMainland)Significancewasassessedatα=005()001()and0001()

Berries Marine Terrestrial vertebrates

000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

5

10

15

20

Proportion of diet

Den

sity

Island Americana Island Caurina Mainland Americana Mainland Caurina

p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099


2016) Nevertheless ecologists often assume that the functionalroles of carnivores are conserved across ecosystems and cladesConsequentlytherestorationofcarnivoreshasbeenpromotedasameanstore-establishtrophicrelationshipsandlostfunctionalroles(Rippleetal2014)andmanyeffortstargetcarnivorerecoverywiththe explicit goal of resurrecting lost trophic relationships (Donlan2005) or interactions observed in different landscapes (RippleWirsing Beschta amp Buskirk 2011) However such strategies arecontingentuponEltoniannicheconservatismandtrophicstationar-ityandourresultssuggestthatEltoniannichesandfunctionalrolesarenotconservedevenamongcloselyrelatedspecies incompara-bleecosystemsConsequentlythesefindingssuggestthatforagingdynamicsandtherealizedfunctionalrolesofcarnivoresmaynotbetransferableacrossecosystemspresentingadditionalcomplexitytocallsforcarnivore-drivenrestorationefforts

ACKNOWLEDG EMENTS

SurveyeffortsfortheInlandcaurinaportionwerefundedbytheUSDAForest Service PacificNorthwest Research Station SiuslawNationalForesttheUSFishandWildlifeServicesPortlandOfficeandthroughsupportfromtheAmericanSocietyofMammalogistsSupportoffieldlogisticsvehicleshousingandequipmentwasprovidedbytheCentralCoastRangerDistrictSiuslawNationalForestTongassNationalForestandBritishColumbiaMinistryoftheEnvironmentSupportforPJMwasprovided by the National Science Foundations Integrated GraduateEducationResearchandTraining(IGERT)programme(DGE-1144752)ThankstoMarkLinnellJoshThomasandAdamKotaichforassistancewithfieldworkandtoBillBridgelandandShawnStephensenoftheUSFishandWildlifeServiceforadditionalsamples

AUTHORSrsquo CONTRIBUTIONS

AllauthorsdevelopedtheideasanddesignedthestudyKMMandJNPcollectedbiological samplesSMPprocessed isotopicdataandPJM performed statistical analyses PJM andSMPwrotethemanuscript andall authors contributedcritically to thedraftsandgavefinalapprovalforpublication

DATA ACCE SSIBILIT Y

AllisotopicsignaturesareavailableathttpsfigsharecomarticlesManlick_et_al_2018_FigSahre_xlsx7252994

ORCID

Philip J Manlick httpsorcidorg0000-0001-9143-9446

R E FE R E N C E S

AllenAPampGilloolyJF(2006)Assessinglatitudinalgradientsinspe-ciationratesandbiodiversityattheglobalscaleEcology Letters 9(8)947ndash954httpsdoiorg101111j1461-0248200600946x

Ben-DavidM Flynn RW amp Schell DM (1997) Annual and sea-sonal changes in diets of martens Evidence from stable isotopeanalysis Oecologia 111(2) 280ndash291 httpsdoiorg101007s004420050236

Ben-DavidMHanleyTAampSchellDM(1998)Fertilizationofterres-trialvegetationbyspawningPacificSalmonTheroleoffloodingandpredatoractivityOikos 83(1)47httpsdoiorg1023073546545

Boumlhning-GaeseKampOberrathR(1999)Phylogeneticeffectsonmor-phological life-history behavioural and ecological traits of birdsEvolutionary Ecology Research 1(3)347ndash364httpwwwevolution-ary-ecologycomabstractsv01n03iiar1017pdf

Brickner K M Grenier M B Crosier A E amp Pauli J N (2014)Foragingplasticityinahighlyspecializedcarnivoretheendangeredblack-footed ferret Biological Conservation 169 1ndash5 httpsdoiorg101016jbiocon201310010

BuckleyLBDaviesTJAckerlyDDKraftNJBHarrisonSPAnackerBLampWiensJJ(2010)PhylogenynicheconservatismandthelatitudinaldiversitygradientinmammalsProceedings of the Royal Society B Biological Sciences 277(1691) 2131ndash2138 httpsdoiorg101098rspb20100179

CalengeC(2006)ThepackageadehabitatfortheRsoftwareAtoolfortheanalysisofspaceandhabitatusebyanimalsEcological Modelling 197 516ndash519

CarlsonJEGilbertJHPokallusJWManlickPJMossWEampPauliJN(2014)PotentialroleofpreyintherecoveryofAmericanmartenstoWisconsinThe Journal of Wildlife Management 78 1499ndash1504httpsdoiorg101002jwmg785

ChapinFSIIIMatsonPAampVitousekP(2011)Principles of terres-trial ecosystem ecologyNewYorkNY Springer-Verlag httpsdoiorg101007978-1-4419-9504-9

ChaseJampLeiboldM(2003)Ecological niches Linking classical and con-temporary approachesChicagoILUniversityofChicagoPress

ComteLCucheroussetJampOldenJD(2016)GlobaltestofEltonianniche conservatism of nonnative freshwater fish species betweentheirnativeandintroducedrangesEcography 40(3)384ndash392

CooperNFreckletonRPampJetzW(2011)Phylogeneticconserva-tismof environmental niches inmammalsProceedings of the Royal Society B Biological Sciences 278(1716) 2384ndash2391 httpsdoiorg101098rspb20102207

Cucherousset J amp Villeacuteger S (2015) Quantifying the multiple fac-ets of isotopic diversity New metrics for stable isotope ecol-ogy Ecological Indicators 56 152ndash160 httpsdoiorg101016jecolind201503032

Darimont C T Paquet P C amp Reimchen T E (2009) Landscapeheterogeneity and marine subsidy generate extensive in-trapopulation niche diversity in a large terrestrial verte-brate Journal of Animal Ecology 78(1) 126ndash133 httpsdoiorg101111j1365-2656200801473x

DavisNEForsythDMTriggsBPascoeCBenshemeshJRobleyAampLumsdenLF(2015)InterspecificandgeographicvariationinthedietsofsympatriccarnivoresDingoeswilddogsandredfoxesin South-Eastern Australia PLoS ONE 10 e0120975 httpsdoiorg101371journalpone0120975

DawsonNGColella JP SmallMP StoneKDTalbot S LampCookJA (2017)Historicalbiogeographysetsthefoundationforcontemporaryconservationofmartens(genusMartes)innorthwest-ernNorthAmericaJournal of Mammalogy 98(3)715ndash730httpsdoiorg101093jmammalgyx047

Diniz-FilhoJAFTerribileLCDaCruzMJRampVieiraLCG(2010) Hidden patterns of phylogenetic non-stationarity over-whelm comparative analyses of niche conservatism and diver-gence Global Ecology and Biogeography 19(6)916ndash926httpsdoiorg101111j1466-8238201000562x

DobsonALodgeDAlderJCummingGSKeymerJMcGladeJhellipXenopoulosMA(2006)Habitatlosstrophiccollapseandthe


declineofecosystemservicesEcology 87(8)1915ndash1924httpsdoiorg1018900012-9658(2006)87[1915HLTCAT]20CO2

Donlan J (2005)Re-wildingNorthAmericaNature 436(7053) 913ndash914httpsdoiorg101038436913a

EgozcueJJPawlowsky-GlahnVMateu-FiguerasGampBarceloacute-VidalC (2003) Isometric logratio transformations for compositionaldata analysis Mathematical Geology 35(3) 279ndash300 httpsdoiorg101023A1023818214614

EltonCS(1927)Animal ecologyLondonUKSidgwichampJacksonErranDSampPowellRA(1996)Anevaluationoftheaccuracyofker-

neldensityestimatorsforhomerangeanalysisEcology 77(7)2075ndash2085httpsdoiorg1023072265701

EstesJTerborghJBrasharesJSPowerMEBergerJBondWJampWardleDA(2011)TrophicdowngradingofplanetearthScience 333301ndash306httpsdoiorg101126science1205106

FiebergJampKochannyC(2005)Quantifyinghome-rangeoverlapTheimportanceofutilizationdistributionJournal of Wildlife Management 69(4) 1346ndash1359 httpsdoiorg1021930022-541X(2005)69[1346QHOTIO]20CO2

FraserLHHarrowerWLGarrisHWDavidsonSHebertPDNHowieRampWilsonD(2015)AcallforapplyingtrophicstructureinecologicalrestorationRestoration Ecology 23(5)503ndash507httpsdoiorg101111rec12225

GrinnellJ(1917)TheNiche-relationshipsoftheCaliforniathrasherThe Auk 34(4)427ndash433httpsdoiorg1023074072271

HealyKGuillermeTKellySBAIngerRBearhopSampJacksonAL(2018)SIDERAnRpackageforpredictingtrophicdiscrimina-tionfactorsofconsumersbasedontheirecologyandphylogeneticrelatednessEcography 41(8) 1393ndash1400 httpsdoiorg101111ecog03371

Hofmeester T R Jansen P AWijnenH J Coipan E C FonvilleM Prins HH T hellip VanWieren S E (2017) Cascading effectsof predator activity on tick-borne disease risk Proceedings of the Royal Society B Biological Sciences 284(1859) 0ndash7 httpsdoiorg101098rspb20170453

Hopkins J B Koch P L Ferguson JMampKalinowski S T (2014)ThechanginganthropogenicdietsofAmericanblackbearsoverthepastcenturyinYosemiteNationalParkFrontiers in Ecology and the Environment 12(2)107ndash114httpsdoiorg101890130276

KearneyMShineRampPorterWP(2009)Thepotentialforbehavioralthermoregulation to buffer lsquocold-bloodedrsquo animals against climatewarming Proceedings of the National Academy of Sciences 106(10)3835ndash3840httpsdoiorg101073pnas0808913106

LarsonEROldenJDampUsioN(2010)DecoupledconservatismofGrinnellianandEltoniannichesinaninvasivearthropodEcosphere 1(6)art16httpsdoiorg101890es10-000531

LinnellMAMoriartyKMGreenDSampLeviT (2018)DensityandpopulationviabilityofcoastalmartenArareandgeographicallyisolated small carnivore PeerJ 6 e4530 httpsdoiorg107717peerj4530

LososJB(2008)Phylogeneticnicheconservatismphylogeneticsignalandtherelationshipbetweenphylogeneticrelatednessandecolog-icalsimilarityamongspeciesEcology Letters 11995ndash1003httpsdoiorg101111j1461-0248200801229x

MacArthurR(1972)Geographical ecology Patterns in the distribution of speciesPrincetonNJPrincetonUniversityPress

Manlick P J Woodford J E Zuckerberg B amp Pauli J N (2017)Niche compression intensifies competition between reintroducedAmericanmartens(Martes americana)andfishers(Pekania pennanti)Journal of Mammalogy 98(3) 690ndash702 httpsdoiorg101093jmammalgyx030

MartinS(1994)FeedingecologyofAmericanmartensandfishersInSBuskirkAHarestadMRaphaelampRPowell(Eds)Martens sables and fishers Biology and conservation(pp297ndash315)IthacaNewYorkCornellUniversityPress

Moriarty K M Bailey J D Smythe S E amp Verschuyl J (2016)Distribution of Pacific Marten in Coastal Oregon Northwestern Naturalist 97(2)71ndash81httpsdoiorg101898NWN16-011

MossWEAlldredgeMWLoganKAampPauliJN(2016)Humanexpansion precipitates niche expansion for an opportunistic apexpredator (Puma concolor) Scientific Reports 6 39639 httpsdoiorg101038srep39639

NehlsenWWilliamsJEampLichatowichJA (1991)PacificsalmonatthecrossroadsStocksatriskfromCaliforniaOregonIdahoandWashingtonFisheries 16(2)4ndash21httpsdoiorg1015771548-8446(1991)016amplt0004PSATCSampgt20CO2

Newsome S D Garbe H M Wilson E C amp Gehrt S D (2015)Individual variation in anthropogenic resource use in an urbancarnivore Oecologia 178(1) 115ndash128 httpsdoiorg101007s00442-014-3205-2

NewsomeSDMartinezdelRioCBearhopSampPhillipsDL(2007)AnicheforisotopicecologyFrontiers in Ecology and the Environment 5(8)429ndash436httpsdoiorg10189006015001

Newsome SD Yeakel JDWheatley PVamp TinkerM T (2012)Tools for quantifying isotopic niche space and dietary variation atthe individual and population level Journal of Mammalogy 93(2)329ndash341httpsdoiorg10164411-MAMM-S-1871

OksanenJBlanchetFGKindtRLegendrePMinchinPROharaRBhellipOksanenMJ(2013)Package lsquoveganrsquoCommunityecologypackageversion29

Olalla-Taacuterraga M Aacute Gonzaacutelez-Suaacuterez M Bernardo-Madrid RRevillaEampVillalobosF(2016)Contrastingevidenceofphyloge-netictrophicnicheconservatisminmammalsworldwideJournal of Biogeography 4499ndash110httpsdoiorg101111jbi12823

Olalla-Taacuterraga M Aacute Mcinnes L Bini L M Diniz-Filho J A FFritz S A Hawkins B A amp Purvis A (2011) Climatic nicheconservatism and the evolutionary dynamics in species rangeboundaries Global congruence across mammals and amphib-ians Journal of Biogeography 38(12) 2237ndash2247 httpsdoiorg101111j1365-2699201102570x

ParnellACIngerRBearhopSampJacksonAL(2010)Sourcepar-titioningusingstableisotopesCopingwithtoomuchvariationPLoS ONE 5(3)e9672httpsdoiorg101371journalpone0009672

Pauli J N Ben-David M Buskirk S DePue J amp Smith W(2009) An isotopic technique to mark mid-sized vertebratesnon-invasively Journal of Zoology 278 141ndash148 httpsdoiorg101111j1469-7998200900562x

Pauli J N Donadio E amp Lambertucci S A (2018) The corruptedcarnivore How humans are rearranging the return of the carni-vore-scavengerrelationshipEcology 99(9)2122ndash2124httpsdoiorg101002ecy2385

PauliJNMossWEManlickPJFountainEDKirbyRSultaireSM ampHeaton TH (2015) Examining the uncertain origin andmanagement role of martens on Prince of Wales Island AlaskaConservation Biology 29(5) 1257ndash1267 httpsdoiorg101111cobi12491

PearmanPBGuisanABroennimannOampRandinCF(2008)Nichedynamics in space and timeTrends in Ecology and Evolution 23(3)149ndash158httpsdoiorg101016jtree200711005

PetersonATSoberoacuten JPearsonRGAndersonRPMartiacutenez-MeyerENakamuraMampBastosAraujoM(2011)Ecological niches and geographic distributions Princeton NJ Princeton UniversityPresshttpsdoiorg105860CHOICE49-6266

PetersonATSoberoacutenJampSaacutenchez-CorderoV(1999)ConservatismofecologicalnichesinevolutionarytimeScience 285(5431)1265ndash1267httpsdoiorg101126science28554311265

PhillipsDLIngerRBearhopSJacksonALMooreJWParnellACampWardEJ (2014)Bestpracticesforuseofstable isotopemixing models in food web studies Canadian Journal of Zoology 835(August)823ndash835httpsdoiorg101139cjz-2014-0127


RaineRM(1987)Winterfoodhabitsandforagingbehaviouroffish-ers(Martes pennanti)andmartens(Martes americana)insoutheasternManitobaCanadian Journal of Zoology 65(3) 745ndash747 httpsdoiorg101139z87-112

RippleW JEstes JABeschtaRLWilmersCCRitchieEGHebblewhiteMhellipWirsingA J (2014)Statusandecologicalef-fectsoftheworldslargestcarnivoresScience 343(6167)1241484httpsdoiorg101126science1241484

RippleWJWirsingAJBeschtaRLampBuskirkSW(2011)CanrestoringwolvesaidinlynxrecoveryWildlife Society Bulletin 35(4)514ndash518httpsdoiorg101002wsb59

Ritchie E G Elmhagen B Glen A S Letnic M Ludwig G ampMcDonald R A (2012) Ecosystem restoration with teeth Whatrole forpredatorsTrends in Ecology and Evolution 27(5) 265ndash271httpsdoiorg101016jtree201201001

RosadoBHPFigueiredoMS L deMattosEAampGrelleCEV(2016)EltonianshortfallduetotheGrinnellianviewFunctionalecologybetweenthemismatchofnicheconceptsEcography 39(11)1034ndash1041httpsdoiorg101111ecog01678

Rosenzweig M (1966) Community structure in sympatric car-nivora Journal of Mammalogy 47(4) 602ndash612 httpsdoiorg1023071377891

RosingMN Ben-DavidM ampBarry R P (1998) Analysis of sta-ble isotope data A K nearest-neighbors randomization testJournal of Wildife Management 62(1) 380ndash388 httpsdoiorg1023073802302

RothJDampHobsonKA(2000)StablecarbonandnitrogenisotopicfractionationbetweendietandtissueofcaptiveredfoxImplicationsfordietaryreconstructionCanadian Journal of Zoology 78(5)848ndash852httpsdoiorg101139cjz-78-5-848

SheehyESutherlandCOReillyCampLambinX(2018)TheenemyofmyenemyismyfriendNativepinemartenrecoveryreversesthedeclineoftheredsquirrelbysuppressinggreysquirrelpopulationsProceedings of the Royal Society B Biological Sciences 285(1874)20172603httpsdoiorg101098rspb20172603

Sikes R S (2016) 2016 Guidelines of the American Society ofMammalogistsfortheuseofwildmammalsinresearchandeduca-tionJournal of Mammalogy 97(3)663ndash688httpsdoiorg101093jmammalgyw078

Smith J AWang YampWilmers CC (2016) Spatial characteristicsofresidentialdevelopmentshiftlargecarnivorepreyhabitsJournal of Wildlife Management 80(6)1040ndash1048httpsdoiorg101002jwmg21098

SoberoacutenJ (2007)GrinnellianandEltoniannichesandgeographicdis-tributionsofspeciesEcology Letters 10(12)1115ndash1123httpsdoiorg101111j1461-0248200701107x

StephensDBrownJampYdenbergR(Eds)(2007)Foraging Behavior and ecologyChicagoILUniversityofChicagoPress

Terborgh J W (2015) Toward a trophic theory of species diversityProceedings of the National Academy of Sciences 112(37) 11415ndash11422httpsdoiorg101073pnas1501070112

TerryRCGuerreMEampTaylorDS(2017)HowspecializedisadietspecialistNicheflexibilityandlocalpersistencethroughtimeoftheChisel-toothedkangarooratFunctional Ecology 31(10)1921ndash1932httpsdoiorg1011111365-243512892

WiensJJampGrahamCH(2005)NicheconservatismIntegratingevo-lutionecologyandconservationbiologyAnnual Review of Ecology Evolution and Systematics 36519ndash539httpsdoiorg101146an-nurevecolsys36102803095431

WillsonM F (1993)Mammals as seed-dispersalmutualists inNorthAmericaOikos 67(1)159httpsdoiorg1023073545106

YeakelJDPattersonBDFox-DobbsKOkumuraMMCerlingTEMooreJWampDominyNJ(2009)Cooperationandindivid-ualityamongman-eating lionsProceedings of the National Academy of Sciences 106(45) 19040ndash19043 httpsdoiorg101073pnas0905309106

ZielinskiWJampDuncanNP(2004)DietsofsympatricpopulationsofAmericanmartens(Martes americana)andfishers(Martes pennanti)inCaliforniaJournal of Mammalogy 85(3)470ndash477httpsdoiorg1016441545-1542(2004)085amplt0470DOSPOAampgt20CO2

ZielinskiWJTucker JMampRennieKM (2017)Nicheoverlapofcompeting carnivores across climatic gradients and the conserva-tion implications of climate change at geographic range marginsBiological Conservation 209 533ndash545 httpsdoiorg101016jbiocon201703016

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleManlickPJPetersenSMMoriartyKMPauliJNStableisotopesreveallimitedEltoniannicheconservatismacrosscarnivorepopulationsFunct Ecol 201933335ndash345 httpsdoiorg1011111365-243513266


1emsp |emspINTRODUC TION

Ecologistshavelongbeenfascinatedbytraitdifferencesacrosspop-ulationsandspecies(MacArthur1972)Asoneofthemostinfluentialconceptsinecologynichetheoryhasbeencentraltoidentifyingcausesofecologicaldivergenceamongtaxa(ChaseampLeibold2003)Morere-centlytheretentionofecologicaltraitsacrossspaceandtimemdashnicheconservatismmdashhasemergedasaprimaryinterestofecologists(WiensampGraham2005)Nicheconservatismhelpsexplainthestructureofbiodiversitygradients(AllenampGillooly2006Buckleyetal2010)andimprovespredictionsofspeciesrsquoresponsestoglobalchange(CooperFreckletonampJetz2011PearmanGuisanBroennimannampRandin2008)andspeciesinvasions(WiensampGraham2005)Moreovernicheconservatismisafundamentalassumptionofmanyspeciesdistribu-tionmodelsusedtomapGrinnelliannichesthenon-interactiveenvi-ronmentalaspectsofaspeciesrsquorange(Grinnell1917)ConsequentlyGrinnellian niches have been the primary focus of ecological nicheconservatismanda renewed interest in species-habitat associations(Petersonetal2011)Similarlyphylogeneticnicheconservatismortheretentionofancestralecologicaltraitsamongrelatedtaxahasalsoreceivedwidespreadattentionshedding lightoncommunityassem-blyandtheadaptabilityofspeciesacrosssystems(Cooperetal2011Losos2008)Meanwhilebioticinteractionshaveremainedacorner-stoneofecology(ChaseampLeibold2003)yettheconservationofcon-sumerndashresourcedynamicsdefinedbytheEltonianniche(Elton1927)hasremainedrelativelyunderstudied(Olalla-TaacuterragaGonzaacutelez-SuaacuterezBernardo-MadridRevillaampVillalobos2016RosadoFigueiredodeMattosampGrelle2016)Giventheimportanceofsuchtrophicdynam-icsforecologicalprocesses(Estesetal2011)understandingtheroleofEltoniannicheconservatismandthecapacityforadaptabilitywillbekeytobothpreservingandrestoringecosystemfunctionsinthefaceofcontinuingglobalchange

Re-establishing trophic interactions has become a global eco-logical priority (Dobson etal 2006 Estes etal 2011) and therestorationofpredatorshasbeenproposedtobothpreserveeco-systemfunctionality(Ritchieetal2012)andpromotebiodiversity(Terborgh2015) Inparticularthere-establishmentofmammaliancarnivoresisincreasinglypromotedtorestoreecosystemfunction-alitylargelythroughthetransferenceofconsumerndashresourcedynam-ics and top-down forcing (Ripple etal 2014Ritchie etal 2012)Restoring these functional relationships among consumers how-everremainschallenging(Fraseretal2015)mostlyduetothedy-namicnatureofforagingecologyandtheinabilitytoquantifytrophicinteractions throughspaceandtime Indeedsuchpredator-driven

ecologicalrestorationhingesonEltoniannicheconservatismandthepreservationofconsumerndashresourcedynamicsbuttheseprocessesremainpoorlyunderstood

Eltonian niche conservatism is governed by foraging ecologywhichisgenerallyafunctionofclimatelandcoverandbioticinter-actions(StephensBrownampYdenberg2007)Atthesitelevelcli-mateoftendeterminesprimaryproductivitylandcovercompositionandspeciesrichness(ChapinMatsonampVitousek2011MacArthur1972)which in turn regulates resourceavailabilityAt the individ-uallevelclimateandlandcoverinfluenceactivitylevelsbyalteringforagingratesandmetaboliccosts(KearneyShineampPorter2009)Similarlybioticinteractionslikepredationandcompetitioninteractwithclimateandlandcovertomodifyresourceaccessibilityandalterforagingdynamics(DarimontPaquetampReimchen2009)Giventhenumber of exogenous factors influencing foraging ecology acrossscalestheconservationofEltoniannicheshasbeenunsurprisinglyboth supported (Boumlhning-GaeseampOberrath1999) andcontested(Olalla-Taacuterragaetal2016)

While Grinnellian and phylogenetic niche conservatism havebeen widely observed in mammals (Cooper etal 2011 Olalla-Taacuterragaetal2011PetersonSoberoacutenampSaacutenchez-Cordero1999)idiosyncraticpatternsofdivergenceandconservatismhavebeenob-servedacrosscarnivorecladesincludingfelidscanidsandmustelids(Buckleyetal2010Diniz-FilhoTerribileDaCruzampVieira2010)Nevertheless Grinnellian niche axes are correlatedwith resourceavailability suggesting that Eltonian niches are also conserved inboth space and time (Soberoacuten 2007) IndeedOlalla-Taacuterraga etal(2016)observedEltoniannicheconservatisminmammalsatbroadphylogeneticscaleshowevercarnivoresexhibitedtheweakestre-sponseofallmammalianordersandlimiteddietaryinformationledtocontrastingconclusionsRecentfine-scaleanalyseshavesimilarlyrevealed remarkable foraging plasticity among carnivore species(Darimont etal 2009NewsomeGarbeWilsonampGehrt 2015)suggestingexogenousdrivers like landcoverandcompetitionmayregulateEltoniannichesratherthanphylogenyConsequentlyfunc-tionalrolescoupledtoforagingmaybesimilarlydynamicwithim-portantconsequencesforecologicalprocessesacrossecosystems

To assess Eltonian niche conservatismwe examined the dietsof two generalist and closely related carnivores in northwesternNorth America American martens Martes americana and Pacific martensMartes caurinaThesemustelidsarerecentlydivergedsistertaxathatpossesscomparablemorphologicalandecologicalcharac-teristicsandoccupysimilarlandcovertypesacrosswesternNorthAmerica (Dawsonetal2017)Though isolatedformillenniaboth

These results illustrate the context-dependent nature of foraging and indicateconsumerfunctionalitycanbedynamic

K E Y W O R D S

AlaskaBritishColumbiaforagingfunctionalrolesMartesnicheconservatismpredatorrestoration









130 00W

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Kilometres plusmn


22emsp|emspSampling











3emsp |emspRESULTS













325(289ndash361)


424(365ndash483)




383(288ndash471)


519(401ndash647)



349(314ndash385)


303(225ndash387)




121(00ndash264)


517(225ndash815)






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sca

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O = 00p lt 005


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O = 00p lt 005


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δ15N

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(c)

O = 00p lt 005


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δ13C scaled

(d)

O = 00p lt 005









Caurina(ICMC) 000 003 128523

Island(IAIC) 010 096 663895



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000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

5

10

15

20

Proportion of diet

Den

sity


p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099



ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S
























































































130 00W

130 00W140 00W

120 00W

550

0N

500

0N

500

0N

450

0N

450

0N0 150 300

Kilometres plusmn


22emsp|emspSampling











3emsp |emspRESULTS













325(289ndash361)


424(365ndash483)




383(288ndash471)


519(401ndash647)



349(314ndash385)


303(225ndash387)




121(00ndash264)


517(225ndash815)






00

02

04

06

08

10

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δ15N

sca

led

(a)

O = 00p lt 005


00

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06

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(b)

O = 00p lt 005


00

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δ13C scaled

δ15N

sca

led

(c)

O = 00p lt 005


00

02

04

06

08

10

00 02 04 06 08 10

δ13C scaled

(d)

O = 00p lt 005









Caurina(ICMC) 000 003 128523

Island(IAIC) 010 096 663895



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000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

5

10

15

20

Proportion of diet

Den

sity


p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099



ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S

















































































22emsp|emspSampling











3emsp |emspRESULTS













325(289ndash361)


424(365ndash483)




383(288ndash471)


519(401ndash647)



349(314ndash385)


303(225ndash387)




121(00ndash264)


517(225ndash815)






00

02

04

06

08

10

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δ15N

sca

led

(a)

O = 00p lt 005


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O = 00p lt 005


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δ15N

sca

led

(c)

O = 00p lt 005


00

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δ13C scaled

(d)

O = 00p lt 005









Caurina(ICMC) 000 003 128523

Island(IAIC) 010 096 663895



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000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

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Proportion of diet

Den

sity


p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099



ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S


















































































3emsp |emspRESULTS













325(289ndash361)


424(365ndash483)




383(288ndash471)


519(401ndash647)



349(314ndash385)


303(225ndash387)




121(00ndash264)


517(225ndash815)






00

02

04

06

08

10

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δ15N

sca

led

(a)

O = 00p lt 005


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(b)

O = 00p lt 005


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δ15N

sca

led

(c)

O = 00p lt 005


00

02

04

06

08

10

00 02 04 06 08 10

δ13C scaled

(d)

O = 00p lt 005









Caurina(ICMC) 000 003 128523

Island(IAIC) 010 096 663895



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000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

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Proportion of diet

Den

sity


p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099



ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S





















































































00

02

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06

08

10

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δ15N

sca

led

(a)

O = 00p lt 005


00

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(b)

O = 00p lt 005


00

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δ13C scaled

δ15N

sca

led

(c)

O = 00p lt 005


00

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08

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δ13C scaled

(d)

O = 00p lt 005









Caurina(ICMC) 000 003 128523

Island(IAIC) 010 096 663895



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Berries

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Berries

Marine

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Marine

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nd p

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pula

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000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

5

10

15

20

Proportion of diet

Den

sity


p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099



ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S























































































Caurina(ICMC) 000 003 128523

Island(IAIC) 010 096 663895



20

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Berries

Marine

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Berries

Marine

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Marine

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nd p

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pula

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000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

5

10

15

20

Proportion of diet

Den

sity


p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099



ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S























































































000 025 050 075 100000 025 050 075 100000 025 050 075 100

0

5

10

15

20

Proportion of diet

Den

sity


p Americana lt 0001

p Caurina = 089

p Island lt 005

p Mainland lt 005

p Americana = 026

p Caurina lt 001

p Island = 083

p Mainland lt 001

p Americana = 016

p Caurina = 017

p Island lt 005

p Mainland = 099



ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S


















































































ACKNOWLEDG EMENTS






ORCID


R E FE R E N C E S





































































































































































Documents

Stable isotopes reveal limited Eltonian niche conservatism across … · 2019-02-05 · The conservation of Grinnellian niche characteristics ... martens predominating in mainland