Oil palm monoculture induces drastic erosion of an Amazonian forest mammal fauna

19 Pages·2017·10.27 MB·English

RESEARCHARTICLE
Oil palm monoculture induces drastic erosion
of an Amazonian forest mammal fauna
AnaCristinaMendes-Oliveira1,2☯*,CarlosA.Peres2☯,PaulaCristinaR.deA.Maue´s1,
GeovanaLinharesOliveira1‡,IvoG.B.Mineiro1‡,SusanneL.SilvadeMaria1‡,RenataC.
S.Lima1‡
1 LaboratoryofEcologyandZoologyofVertebrate,InstituteofBiologicalScience,FederalUniversityofPara´,
Bele´m,Para´,Brazil,2 CentreforEcology,EvolutionandConservation,SchoolofEnvironmentalSciences,
UniversityofEastAnglia,Norwich,Norfolk,UnitedKingdom
a1111111111 ☯Theseauthorscontributedequallytothiswork.
a1111111111 ‡Theseauthorsalsocontributedequallytothiswork.
*[email protected]
a1111111111
a1111111111
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Abstract
Oilpalmmonoculturecomprisesoneofthemostfinanciallyattractiveland-useoptionsin
tropicalforests,butcroplandsuitabilityoverlapsthedistributionofmanyhighlythreatened
OPENACCESS vertebratespecies.Weinvestigatedhowforestmammalsrespondtoalandscapemosaic,
Citation:Mendes-OliveiraAC,PeresCA,Maue´s includingmatureoilpalmplantationsandprimaryforestpatchesinEasternAmazonia.
PCRdA,OliveiraGL,MineiroIGB,deMariaSLS,et Usingbothline-transectcensuses(LTC)andcamera-trapping(CT),wequantifiedthegen-
al.(2017)Oilpalmmonocultureinducesdrastic
eralpatternsofmammalcommunitystructureandattemptedtoidentifybothspecieslife-his-
erosionofanAmazonianforestmammalfauna.
PLoSONE12(11):e0187650.https://doi.org/ torytraitsandtheenvironmentalandspatialcovariatesthatgovernspeciesintolerancetooil
10.1371/journal.pone.0187650 palmmonoculture.Consideringmammalspeciesrichness,abundance,andspeciescom-
Editor:DaniloRusso,UniversitàdegliStudidi position,oilpalmplantationswereconsistentlydepauperatecomparedtotheadjacentpri-
NapoliFedericoII,ITALY maryforest,butresponsesdifferedbetweenfunctionalgroups.Thedegreeofforesthabitat
Received:August11,2017 dependencywasaleadingtrait,determiningcompositionaldissimilaritiesacrosshabitats.
ConsideringboththeLTCandCTdata,distancefromtheforest-plantationinterfacehada
Accepted:October21,2017
significanteffectonmammalassemblageswithineachhabitattype.Approximately87%of
Published:November8,2017
allspeciesdetectedwithinoilpalmwereneverfartherthan1300mfromtheforestedge.
Copyright:©2017Mendes-Oliveiraetal.Thisisan Ourstudyclearlyreinforcesthenotionthatconventionaloilpalmplantationsareextremely
openaccessarticledistributedunderthetermsof
hostiletonativetropicalforestbiodiversity,whichdoesnotbodewellgivenprospectsforoil
theCreativeCommonsAttributionLicense,which
permitsunrestricteduse,distribution,and palmexpansioninbothagingandnewAmazoniandeforestationfrontiers.
reproductioninanymedium,providedtheoriginal
authorandsourcearecredited.
DataAvailabilityStatement:Allrelevantdataare
withinthepaperanditsSupportingInformation
files.
Introduction
Funding:ConservationInternational-Brazil
Some20%ofthe~5millionkm2BrazilianAmazonhasalreadybeendeforestedsince1970[1].
providedfinancialsupportduringthefirststageof
Anthropogenicland-use,suchaslivestockranching,timberextraction,miningandmore
theproject.A.C.M.O.wassupportedbyaCNPq
Post-Doctoralgrantduringastudyleaveat recently,large-scaleintensiveagriculture,hashistoricallydriveneconomicdevelopmentacross
UniversityofEastAnglia. theregion,whichisreflectedinaregional-scalegrowthinGrossDomesticProduct(GPD)
~1.4%higherthanthatoftherestofBrazil[2].However,thesedevelopmentfrontiershave
Competinginterests:Theauthorshavedeclared
thatnocompetinginterestsexist. broughtunprecedentedenvironmentalimpactstotheregion,includingelevateddeforestation,
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OilpalmmonocultureandmammalfaunainAmazonforest
greenhousegasemissions,forestdegradation,defaunation,soilerosion,andwholesaleindis-
criminatespreadofagriculturalpesticides,allofwhichareunaccountedforincountry-scale
measuresofwealth[2][3].
OilpalmplantationshavebecomeoneofthemostfinanciallyattractivecropsinAmazonia,
notleastbecauseoftheintroductionofgovernment-subsidizedbiodieseltotheBrazilian
energygridsince2010[4]andrestrictionsimposedonbiofuelcroplandexpansioninSoutheast
Asia[5].PalmoilextractedfromElaeisguineensis(Jacq.),yieldshigherproductivitythanother
sourcesofbiofuel[6][7]butalsosatiatestheburgeoningdemandforthisversatileproduct
fromfood,chemical,andcosmeticsindustries.BrazilianAmazoniacurrentlyhasoneofthe
world’slargestpotentialareasforoilpalmexpansion(~2.3millionkm2),relatedtoclimatic,
edaphicandtopographiccropsuitability[8][9].TheBraziliangovernmenthasactivelyencour-
agedoilpalmexpansion,whichisextolledasanewopportunitytobringaboutsocioeconomic
developmentandrecoveryofdegradedareasinAmazonia.Newstate-levellegislationhasbeen
sanctionedtoregulateoilpalmplantationsonforestareas(includingsecondaryandlogged
primaryforest),oronfallowland(e.g.,InstruçãoNormativaSEMAS/PA/2011).Inparticular,
theStateofPara´haslegallyproposedthatsilvicultureofexoticspecies,suchasoilpalm,should
counttowardstherestorationofupto30%ofnaturalforestset-asideswithinallprivateland-
holdings,whichismandatoryunderBrazilianenvironmentallegislation(FederalLawNo.
12.651/2012).Also,lowlandprices,cheaplabor,cheapenergysourcesfromhydropowerinfra-
structureandgovernment-subsidizedroad-building[8][10],havefurtherfueledtheAmazon’s
potentialtobecometheworld’slargestoilpalmproducerwithinafewdecades[6].
Givenitseconomyofscale,oilpalmcultivationrequireslargetractsofland,whichhas
resultedintheconversionofover14MhaofforestinSoutheastAsia[9][11].Incontrastwith
theoriginalold-growthforeststheyreplace,theseplantationspresentanuniformhabitatand
treeagestructure[12],changesinsoilfertility[13]andintheinteractionwithsoilmicrobes
[14],anarrowspectrumoffoodresources,low-densityunderstory,exposedsoils,reducedleaf
litter[15][16],highlyvolatilemicroclimate[17],andamuchlowerdiscontinuouscanopy[18].
Faunaldiversityresponsestothesestructuralchangesdependingonboththelandscapecon-
textofplantationsandspeciesecologicalplasticityintermsoftolerancetoaseverelymodified
habitat[19][20][21].Ecologicalstudiesaddressingmultipletaxa,includingbirds[20][21][22]
[23][24],reptiles[20],non-flyingsmallmammals[25],bats,primates[26],butterflies[27],ants
[28]andaquaticinvertebrates[29],haveallshownthatoilpalmplantationsaresignificantly
moredepauperatethanadjacentprimaryforests,evenifthesehadbeenselectively-logged[12].
Thetotalamountanddistributionofremainingnaturalforestcoverarecriticaldetermi-
nantsofthefractionofnativebiodiversity,retainedwithinagriculturallandscapes[30][31].
However,physicaldistancefromadjacentprimaryhabitatsandthepermeabilityofacropland
matrix,havesignificanteffectsonlocalpatternsofdiversity[30][32].Pairwisecomparisons
betweenoilpalmandforesthabitatscouldmaskorunderestimatedifferencesinspeciesrich-
nessifsamplingeffortisconcentratedatfixeddistances,especiallynearforestedges[33].On
theotherhand,responsestothespatialconfigurationofagriculturalmosaicscanbehighlyvar-
iableamongspeciesfunctionalgroups[34].Speciesattributessuchasbodymass,trophiclevel,
homerangesize,dispersalcapacityanddegreeofhabitatspecialization,definetheecological
plasticitybywhichseveralspeciesmayormaynotbeabletotolerateseverelymodifiedhabi-
tats[35][36].
Bothterrestrialandarborealforestmammalscanbeseverelyaffectedbyabroadspectrum
ofanthropogenichabitatdisturbanceinAmazonianforests[37][38].However,thehighdiver-
sityofphenotypesandecologicaltraitsofdifferentfunctionalgroups,reflecttheirdiverse
responsestoenvironmentalchange[39].InPeninsularMalaysia,terrestrialmammalspecies
richnessinoilpalmmonoculturewassignificantlyreduced,comparedtonaturalforest
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OilpalmmonocultureandmammalfaunainAmazonforest
patches[40].Vertebratescharacterizedbystrictforesthabitataffiliation,suchasneotropical
primates,areapparentlymostaffectedbyforestconversiontocropland[41].Wide-ranging
specieswithvastspatialrequirements,suchaslargecarnivores,canoccasionallyuseoilpalm
habitatsnearremainingforestpatches[40].Smallcarnivores,includingsmallcatsandcivets,
frequentlyuseoilpalmplantationsinSumatra,buttheiroccupancyisaffectedbyproximityto
theforestedge[42].SpeciesreportedtouseoilpalmlandscapemosaicsinPeninsularMalaysia,
typicallyhavegeneralistdiets[40].AllavailableevidencefromstudiesinSoutheastAsia,there-
fore,indicatesthatbothspeciestraitsandthegrainandspatialconfigurationofoilpalm
monocultureaffecttheiroverallpatternofforestwildlifeoccupancy.
InAmazonia,areasmostlikelytobeconvertedtooilpalmplantationsoverlapthehighest
speciesrichnessofthreatenedbirdsandmammals[43].Therehasbeennoattempttoexamine
theeffectsofprimaryandsecondaryforestconversionintooilpalmmonocultureonthe
Amazonianmammalfauna.Here,weinvestigatehowmidsizedtolarge-bodiedterrestrialand
arborealmammalsrespondtoanEasternAmazonianlandscapemosaic,includingoilpalm
plantationsandlargeremnantsofprimaryforest.Thesemammaltaxaaccountforadispropor-
tionateamountoftheoverallvertebratebiomassinAmazonianforests[44].Soanyadverse
effectstothesespeciescouldamounttoprofoundrepercussionstoecosystemfunctioning
acrossentirelandscapemosaics.Wecompareddifferentcompartmentsofoilpalmplantations
withadjacentprimaryforestset-asides,usingastandardizededge-distancegradientwithin
eachhabitat.Wedescribehabitatdifferencesinspeciesrichness,overallabundanceandspecies
composition,andattempttopinpointkeyspecieslife-historytraitsthatgovernspeciesintoler-
ance(orlackthereof)tooilpalmmonoculture.Finallywediscusstheimplicationsofthese
effectsonbiodiversity,consideringtheprospectsforoilpalmexpansioninbothagingandnew
Amazoniandeforestationfrontiers.
Materialandmethods
Studysite
Thisstudywasconductedwithinthe103,000-hectareAgropalmaprivatelandholding
(1˚55’57”S,48˚45’49”W).ThestudyareaislocatedinanEasternAmazonianlandscapewithin
theStateofPara´,Brazil,whichcontains39,000haofoilpalmplantationsand64,000haof
unflooded(terrafirme)primaryforest(Fig1).Followingahistoryofdeforestationsincethe
1970s[45],remainingforestpatchesinterspersedwithoilpalmplantationsrangedfrom1,500
to15,000ha(Fig1).Thisregionhadbeenexploitedmainlybyconventionaltimberextraction
andforestconversionintocattlepastures,butmorerecentlyagovernment-subsidizedprocess
offorestconversionintooilpalmplantations.Mostextensiveoilpalmplantationswereconsol-
idatedsincethe1980s,particularlyinthemunicipalcountiesofMojuandTailaˆndia[46].The
broaderlandscapewithinthestudyregioniscurrentlyamosaicofanthropogenicopen-habitat
areasandnaturalforestremnantsundervaryingdegreesofdegradation[47](Fig1).
Terra Firmeforestsinthestudylandscape,whicharerepresentativeofthenativeforestsin
thiseasternAmazonianregion,wereset-asideasLegalReserveswithintheAgropalmaland-
holding,asrequiredbyBrazilianlaw.Primaryforestsitessampledherehadnotsuccumbedto
understoryfiresbuthadbeenexposedtoahistoryofsmall-scaleselectivelogging,although
thiswasdiscontinuedatleast20yearspriortothestudy.Forestcanopyheightsaretypicallyin
therangeof25–35manddominanttreefamiliesincludedtheLecythidaceae,Sapotaceae,Bur-
seraceae,Moraceae,Violaceae,andLeguminosae.Meanannualtemperatureis~26.6˚C,mean
annualprecipitationis~2,500mm,andsoilsthroughoutthestudylandscapearemainlyhighly
weatheredacidicoxisols.
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OilpalmmonocultureandmammalfaunainAmazonforest
Fig1.Locationofthestudyarea.LocationofthestudyareainEasternBrazilianAmazonia(solidsquareininsetmapofSouthAmerica).
Themainmaprepresentstheboundariesofthestudyareaandthespatialdistributionof16transects(whitelines)inbothhabitattypes,
alongwhichline-transectcensusesandcamera-trappingsurveyswereconducted.Darkgreenandorangepolygonsindicateprimaryforest
andoilpalmplantations,respectively,withinthelandscapemosaic.Thediagram(lowerright)providesdetailsofthespatialconfigurationof
camera-trappingstationsalongoneofthetransects.Insetfiguresshowthetypicalstructureandverticalprofileofeachhabitattype:oilpalm
plantations(above)andprimaryforest(below).Thebackgroundshowsremainingforestcover,representedbydifferentshadesofgreen,
andanthropogeniclandcover(e.g.,pastureandagriculture,showninlightbrown)acrosstheentireneighboringregion.Themapand
satellitefreesource:MapBiomasProject[2017]Brazil’sAnnualCoverageandLandUseMapSeries,acessedin[2017]link:[http://
mapbiomas.org].
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Mammalpopulationsurveys
Weselectedeightoilpalm(OP)plantationsitesofcomparableagesinrelationtooverallhabitat
structure(7–15years-old),whichwerepairedwitheightneighboringprimaryforest(PF)sites
(Fig1).PairedOP-PFsiteswereatleast4kmapartfromoneanother,therebymaximizingthe
degreeofspatialindependence.Transectsof5kminlengthwerecutandmarkedevery50min
bothallOPandPFsitessurveyed.WithinOPsites,weavoidedplacinganyportionoftransects
within500mofthenearestremnantsofriparianforestalongperennialstreams,whichwere
alsolegallyrequiredforestset-asides,tocontrolforanyadditionalforestedgeeffects.Our
pairwisedesignrequiredthattransectswereplacedinneighboringOPandPFsites,thereby
creatingadistancegradientintoeachofthesetwomainhabitattypes,butgiventhespatial
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OilpalmmonocultureandmammalfaunainAmazonforest
constraintsofthestudylandscape,itwasrarelypossibletosetupacontinuous10-kmtransect
eithersideoftheOP-PFhabitatinterface(Fig1).ThreeoftheeightPFtransectswereplaced
fartherawayfromforestedges,therebyallowingustosamplesitesatfartherdistances(5–12
km)fromthenearestoilpalmplantations.ThesamewasthecasefortwooftheeightOPtran-
sects,whichwerefarapart(0.5–5.5km)fromthenearestareasofprimaryforest.
Weconductedmammalsurveysinbothhabitattypes(OPandPF)usingtwomethods:line
transectcensuses(LTC)byobserversonfootandcameratrapping(CT).Atotalof627kmof
transectcensuswalkswerecarriedoutinApril-MayandOctober-November2013,which
includedboththedryandwetseasons.Slowcensuswalks(~1250mh–1)wereconductedbyat
leasttwoindependentobserversfromearlyinthemorning(05:30hto09:30h)andintheafter-
noon(15:30hto19:30h)alongalternatetransectstomatchthetypicallybimodalactivity
rhythmofmostforestvertebrates[48].Tomaximizetemporalindependence,weneversur-
veyedthesametransectwithinlessthana4-dayintervalbetweenconsecutivecensuswalks.In
addition,atotalsamplingeffortof6,720cameratrap-nightswasdeployedfromDecember
2014toDecember2015,whichalsoincludedboththedryandwetseasons.Wedeployedseven
CTstationspertransect,eachofwhichwasspacedapartbyapproximately(butneverless
than)700m(Fig1,S1Fig),withagroupoffourpairedtransects(twoinOPandtwoinPF)
sampledsimultaneously.Thisallowedustocamera-trapall16transectswithin12months.
EachCTdeploymentwasexposedforperiodsof60consecutivedays,usinghigh-capacity
memorycards.Althoughwealwaysattemptedtodeployallcamerasfor68days,occasional
malfunctionandtheftresultedininconsistentdeploymentdurations.Whencameraswere
removed,anotewasmadeofanyproblemsormalfunctionssuchaswateringress,insect
attack,dislodgementorbatteryfailure.Meanfunctioningcamera-trapnight(FCTNs)perCT
deploymentwas54.61±20.23.CTphotographsweredefinedasanindependenteventifcon-
secutivephotosrecorded(i)oneormoreindividualsofdifferentspecies;or(ii)oneormore
individualsofthesamespeciesoveraminimumtimeintervalgreaterthan60min[49].Using
thesecriteria,allphotosdefinedasnon-independentwereexcludedfromsubsequentanalyses.
Habitatstructure
Wequantifiedtheforesthabitatstructureatallmammalsurveysitestounderstandhowthis
mayaffectmammalspeciesrichness,compositionandabundance.Alongeachtransect,we
placed14plotsof10x50minbothhabitats,sevenofwhichoneithersideofeachtransect(S1
Fig),whichamountedtoatotalof224plots.Withineachplot,wemeasuredalltreeslarger
than5cmDBH(DiameteratBreastHeight)andcalculatedtheforestbasalarea(BA,inm2/
ha)usingtheequationBA=π.DBH2/4.OilpalmtreeswithinOPsiteswereexcludedfromthis
measure,asweaimedtorestrictoursamplingtonativevegetationfeatures.
Inaddition,usingtheQGis(v.2.14)software,wemeasuredthenearestdistancefromeach
samplingpointtoanyperennialstreamandtothenearestedgeborderingtheadjacentmatrix
(OPinthecaseofPF,orvice-versa).Wealsocalculatedthehabitatpatcharea(ha)ofallsam-
plingsites,selectingshapepolygonsusingtheFieldCalculatorfunctioninQGis.Inadditionto
habitattype,wethereforealsoconsideredasenvironmentalpredictorsofmammalcommunity
structurethe(i)distancefromeachsamplingpointtothenearestOP-PFhabitatinterface
(EDGE);(ii)basalareaofnativetrees(BA);(iii)nearestdistancetoanypermanentwatercourse
(STREAM);and(iv)forestpatcharea(AREA).
Dataanalysis
Weanalysedtheline-transectcensus(LTC)andcamera-trapping(CT)dataseparately,as
thesetwotechniquestargetdifferentcomponentsofthemammalfauna,someofwhichare
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OilpalmmonocultureandmammalfaunainAmazonforest
mutuallyexclusive,withdiurnal/arborealandnocturnal/terrestrialvertebratessampledpri-
marilybyLTCandCT,respectively.AllLTCdataanalysesconsideredindividualspeciesrec-
ordsper10-kmofcensuswalks,whereasCTdataweretreatedasindependentphotographic
recordsper100FCTNs.WefirstusedStudent´spairedt-teststoexaminedifferencesintotal
speciesrichness,totalnumericalabundance,totalbiomass,andevennessvaluesofthemam-
malfaunabetweenhabitattypesonpairedtransectsineitherOPorPF,consideringeach
surveytechniqueseparately.Tostandardizethedifferencesinsamplesizes(i.e.numberof
detectioneventsineitherLTCorCT),weestimatedthespeciesrichnesspertransectbasedon
abundance-basedrarefactioncurvesusingChao1estimator,consideringthelowestnumberof
detections[50].EvennessvalueswerecalculatedasthePielouindex(J’),whichwasderived
fromtheShannonindex,usingtheDiversitypackagewithinR.Weselectedthisevennessmea-
surebecauseitisthemostwidelyusedinecology,andisanexcellentspeciesabundancepre-
dictorofspeciesrichnessintropicalforests[51].J’valuesrangefrom0.0to1.0,withhigher
valuesrepresentingmoreevenspeciesdistributions.
WeexaminedthemultivariatepatternsofspeciescompositionineitherOPorPFsites
usingPrincipalCoordinatesAnalysis(PCoA)basedonspeciesabundances,Bray-Curtis
dissimilaritydistances,and1000randomizationsusingtheveganRpackage.Ananalysisof
speciesassemblagesimilaritybetweensampleswasthenconductedusingPermutationalMulti-
variateAnalysisofVariance(PERMANOVA),inwhicheachtransectwassegmentedatevery
700-m.Thisallowedustoexaminedifferencesinmammalassemblagestructurealongtran-
sectsasafunctionoflocallandscapecontext.WeusedSimilarityPercentagesAnalysis(SIM-
PER)tobreakdownthecontributionofeachspeciestotheoverallobservedsimilaritybetween
samples.Wealsocalculatedthemean(±SE)detectionratepertransecttoconsiderindividual
speciesresponsestoeachhabitattype.Toassesstheimportanceofhabitatedgeeffectstodif-
ferencesinassemblagestructurewithineachhabitattype,weusedAnalysisofCovariance
(ANCOVA).Wecomparedthespeciescompositionandabundanceacrossneighbouringhabi-
tats,usingdistancesfromthenearestedge(withineitherOPorPF)asacovariate.
Tounderstandtheeffectofmammallife-historytraitsonpatternsofspeciesoccupancyin
eitherhabitattype,weusedMultipleRegressionMatrices(MRM).Thisapproachcombinesa
responsematrix,whichinthiscaserepresentedthespecies-by-sitematrixweighedintermsof
localabundance,withotherdissimilaritymatricescalculatedfromexplanatoryspeciesdata,
includingbodymass,locomotionhabit,degreeofdietaryspecialization,phylogeneticdistance,
anddegreeofprimaryforesthabitatdependenceorspecialization.Thesemorpho-ecological
traits,whichincludedcategories,ranksandcontinuousvalues,aredescribedinS1Table.To
assesstherelativeimportanceofdifferentenvironmentalpredictorsonmammalspeciesrich-
nessandabundance,consideringtheLTCandCTdataseparately,weappliedGeneralizedLin-
earMixedModels(GLMM)usingtheglmmPQLfunctionwithinthemassRpackage.GLMMs
werestructuredusingaspatiallyhierarchicaldesign,wherebycensuswalksontransectseg-
mentsorCTdeploymentswerenestedwithintransects,whichareheredefinedarandomvari-
able.Environmentalpredictors(EDGE;BA;STREAMandAREA),definedabove,wereincludedin
theGLMMsmodels.
Results
Basedonbothline-transectcensuses(LTC)andcamera-trapping(CT),werecorded1,059
observationsof36mediumandlarge-bodiedterrestrialmammalspecies,including310sight-
ingsduringLTCsurveysand749independentphotosfromCT.Atotalof32and23species
wererecordedonthebasisofeitherLTCorCT,respectively,inbothprimaryforestandoil
palmplantations(S2–S6FigsandS1Table).Consideringdatafrombothsurveytechniques,
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OilpalmmonocultureandmammalfaunainAmazonforest
Fig2.Comparisonbetweenoilpalmplantationsandforestconsideringoverallpatternsofmammal
assemblage.Boxandviolinplotscomparingthegeneralpatternsofmammalcommunitystructurebetween
primaryforest(ingreen)andoilpalmplantations(inyellow),basedoneitherlinetransectcensuses(left
panels)orcameratrappingsurveys(rightpanels).Fourmammalassemblagepropertieswerequantified:(A)
Rarefiedspeciesrichness;(B)Aggregateabundance;(C)Aggregatebiomass;and(D)Communityevenness.
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overallspeciesrichnessandabundanceweresignificanthigherinprimaryforestcomparedto
oilpalmmonoculture(Fig2Aand2B;S2Table).Aggregatebiomasswasalsosignificantly
greaterinPF,comparedtoOP(Fig2CandS2Table).However,therewerenodifferencesin
evennessestimatesbetweenthetwohabitattypes(Fig2DandS2Table),suggestingsimilarrel-
ativeabundancedistributionsofrareandcommonspecies.
Nocturnalterrestrialmammals(S1Table)weremostefficientlyrepresentedinCTsamples
(Fig3Aand3B),whereasarborealandscansorialspecieswerefarmorefrequentlyrecorded
duringLTCs(Fig3Cand3D).Atotalof18ofall36mammalspeciesrecordedinthisstudy
weredetectedbybothLTCandCT,andthesesurveytechniquesrevealedsimilarpatternsof
relativeabundancebetweenPFandOPsitesfor83%ofthosespecies(Fig3).
Virtuallyallarborealspecies,includingsloths(CholoepusdidactylusandBradypusvariega-
tus),squirrels(Guerlinguetusaestuans),kinkajous(Potosflavus),andparticularlyprimates,
failedtobedetectedinoilpalmplantations(Fig3Aand3C).Consideringprimates,black-
handedtamarins(Saguinusursulus)andbrowncapuchinmonkeys(Sapajusapella)werethe
onlyspeciesobservedusingoilpalmpatches,butinallcases,theyweredetectedwithin300m
ofprimaryforest(Fig4).Consideringxenarthrans,thetwosloths,giantanteater(Myrmeco-
phagatridactyla)andgiantarmadillo(Priodontesmaximus)wereonlyrecordedinprimary
forest(Fig3),whereasthreespeciesofgeneralistarmadillos(Dasypusnovemcinctus,Dasypus
septemcinctusandCabassousunicinctus)wererecordedinbothhabitats(Fig3).Conversely,
crab-eatingfoxes(Cerdocyonthous),whichrarelyuseforestsandaretypicalofmoreopenhab-
itats,werefrequentlyandexclusivelyrecordedinoilpalmplantations.Thiswasalsothecaseof
greatergrison(Galictisvittata),butthiscarnivorespecieswasrarelydetected(Fig3).Thecrab-
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OilpalmmonocultureandmammalfaunainAmazonforest
Fig3.Relativeabundanceratesofterrestrialandarborealmammalspeciesobservedinoilpalm
plantationsandprimaryforest.Relativeabundanceratesinoilpalmplantations(leftpanels:A,C)and
primaryforest(rightpanels:B,D)onthebasisofcameratrapping(upperpanels:A,B)andlinetransect
censuses(lowerpanels:C,D).Mammalspeciesarerepresentedbythefirstfourlettersofeachgenusand
firstfourlettersofeachspecies,andorderedtoptobottomindecreasinglevelsofabundanceinprimary
forest.
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eatingraccoon(Procyoncancrivorus)wasalsomorefrequentlydetectedatoilpalmpatches
thanatforestsites.Thesespecies,aswellasjaguar(Panthera onca)andsmallercats(jaguarun-
dis,Pumayagouaroundi andocelots,Leoparduspardalis)clearlyindicatethatallterrestrialcar-
nivoreswereeithertolerantoforpreferredoilpalmmonoculture.Mostotherspeciesdetected
inbothhabitatsweremoreabundantinprimaryforest,particularlyungulates(e.g.lowland
tapir,Tapirus terrestris,greybrocketdeer,Mazamanemorivagaandcollaredpeccary,Pecari
tajacu)andlarge-bodiedrodents,suchaspacas(Cuniculuspaca)andagoutis(Dasyprocta
prymnolopha)(Fig3andS1Table).
PCoAordinationshowedcleardifferencesbetweensampleclusterswithineitherprimary
forestoroilpalmplantations,consideringthespeciescompositiononthebasisofbothLTC
(Fig5A)andCT(Fig5B),whichwasfurtherconfirmedbypermutationtests(PERMANOVA;
LTC:F =19.84,p=0.001;CT:F =24.91,p=0.001).However,PCoAclustersderived
(80) (79)
fromtheCTdatashowmoreoverlapbetweensamplesindifferenthabitats,suggestingthat
severalterrestrialmammalspeciesdetectedinPFalsousedOPpatches(Fig5B).SIMPERanal-
ysisfurthershowedthatonthebasisofCT,twoterrestrialspecies(agoutiandcrab-eatingfox)
hadasignificantcontributiontotheoverallsimilaritybetweenforest(23.0%)andoilpalm
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OilpalmmonocultureandmammalfaunainAmazonforest
Fig4.Relativeabundanceofterrestrialandarborealmammalspeciesalongadistancegradient
intersectingbothoilpalmplantationsandprimaryforest.Distancegradientofoilpalmplantations
(yellowcircles)andprimaryforest(greencircles).Surveydistancescoveredagradientofupto3500minoil
palmandover12,000minprimaryforest.Verticalreddashedlinerepresentsa0-mdistancealongtheedge
interfacebetweenthesetwohabitattypes.Speciesareorderedaccordingtotheirhighermammaliantaxa
(orders).Panelsontheleft(A)andright(B)representdatabasedoncameratrappingandlinetransect
censuses,respectively.Circlesizesarescaledaccordingtolog-transformed(lnx+1)measuresoflocal
abundancebasedoneithersamplingtechnique.Verysmalldotsrepresentnon-detectionsatanygiven
samplingpoint.
https://doi.org/10.1371/journal.pone.0187650.g004
samples(17.3%),respectively.ConsideringtheLTCdata,SIMPERanalysisshowedthatcrab-
eatingfoxalsohadasignificantcontributiontothesimilaritybetweenPFandOPsamples
(14.4%).However,threeprimatespecies—black-handedtamarin,browncapuchinmonkey
andred-handedhowlermonkey(Alouattabelzebul)—contributedwith11.8%,9.1%and8.4%,
respectively,andjointlywithagoutis(11.7%),werethemaincontributorstotheoverallsimi-
laritybetweenPFsamples(Fig5A).
DistancestothenearestOP-PFedgeinterfacehadasignificanteffectonmammalassem-
blagestructurewithineitherhabitattypeconsideringboththeLTC(ANCOVA;F(2,81)=41.77,
p<0.001)andCTdata(F =19.97,p<0.001;Fig5).Atotalof20ofall23(87%)species
(2.77)
recordedinoilpalmplantationswereneverdetectedfartherthan1300mfromprimaryforest,
andexcludingtheonlytrulynon-forestspecies(crab-eatingfox),mediandistancesfromthe
nearestforestedgeforanymammaldetectedinoilpalmwas960mforCTdetections(N=55
photos)and927mforLTCdetections(N=47sightings).Exceptforafewrecordsofterrestrial
carnivoresfarfortheforestedge(>2000m),suchascrab-eatingraccoonandjaguar,only
Fig5.PrincipalCoordinatesAnalysis(PCoA)ordinationofthemammalassemblagestructurein
primaryforestandoilpalmplantationsacrossthestudylandscape.Mammalassemblagestructurein
primaryforest(PF,greencircles)andoilpalmplantations(OP,yellowcircles).PCoAplotsarebasedonthe
dissimilaritymatrixderivedfromtherelativeabundancedataforeachspeciesbasedoneither(A)linetransect
censusesor(B)cameratrapping.
https://doi.org/10.1371/journal.pone.0187650.g005
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OilpalmmonocultureandmammalfaunainAmazonforest
crab-eatingfoxesweredetectedathighabundanceinoilpalm(N=34sightingsfromLTCand
N=104photosfromCT;Fig4).
OnthebasisofthefirstPCoAaxisdescribingthemammalspeciescomposition,pairedsites
alongthesameorneighboringtransectscuttingacrossneighboringoilpalmandprimaryfor-
estsiteswerenotnecessarilylessdissimilarthansitessampledalongtransectsfartherapart
(ANOVA;LTCdata:F =282.6,P<0.001;CTdata:F =266.2,P<0.001).Transectiden-
1,80 1,78
tityhadnoeffect(LTCdata:P=0.975;CTdata:P=0.601),indicatingthathabitattypewasfar
moreimportantthanthespatialeffectsoftransectidentityindifferentiatingthecommunity
structure.
MultipleRegressionMatricesanalysisshowedthatspecieslife-historytraitshadasignifi-
canteffectontheoverallpatternofspeciescompositioninbothhabitattypes(R2=0.17,
p=0.001),andthatthiseffectcanbeprimarilyattributedtospeciesdifferencesinthedegree
offoresthabitatspecificity(R2=0.04,p=0.001)(S1Table).Thissuggeststhatgeneralistor
opencountrysidespeciesthatrangewidelyintoopenhabitatareasaretolerantofoilpalm
plantations,whereasbotharborealandterrestrialforestspecialistsarenot.Thisreinforcesthe
detrimentaleffectofoilpalmhabitatstructureparticularlyonstrictlyarborealspeciessuchas
primatesandsloths,forexample.Conversely,habitatgeneraliststhatarewidelyknowntouse
openareas,suchascrab-eatingfox,wereclearlyfavoredbyoilpalmplantations.
GLMMsrevealedthatforestbasalareaanddistancetothenearesthabitatinterfaceweresig-
nificantpredictorsofmammalspeciesrichness,consideringtheLTCandCTdata,respectively
(Fig6Aand6B).Ontheotherhand,consideringtheCTdataalone,forestbasalareawasasig-
nificantnegativepredictorofoverallabundance,whereasdistancetotheinterfacebetweenOP
andPFhadtheoppositeeffect(Fig6D).Distancetoneighboringstreamsandforestpatchsize
failedtoexplaineithermammalspeciesrichnessorabundance(Fig6).
Discussion
Wehaveshownthatwell-establishedoilpalmplantationsinEasternAmazoniahavecleardet-
rimentaleffectsontheassemblageofmidsizetolarge-bodiedmammals,andthatsomelife-his-
torytraitswerekeydeterminantsofspeciesresponses.Oilpalmplantationswereconsistently
impoverishedcomparedtoneighboringnativeforests,intermsofthegeneralpatternsof
assemblageorganization,includingspeciesrichness,overallabundanceandameasureof
aggregatebiomassacrossallspecies.Ofall23terrestrial,11arborealandtwoscansorialmam-
malspeciesconsideredinthisstudy,onlythreecouldbedescribedasthrivinginoilpalm
monoculture;allotherspeciesmayuseoilpalmpatchesintheirimmediateforestneighbor-
hood,butwouldlikelybeextirpatedinthecompleteabsenceofprimaryforestwithinthe
widerlandscapemosaic.
Thisgeneralpatternisconsistentwithcomparableresultsonthelocalavifaunasurveyed
withinthesameforestlandscape,whichshowedthatoilpalmplantationsweremoreimpover-
ishedinspeciescompositionthancattlepastures,secondaryforestsandprimaryforestswithin
thesameregion[23].InanotherstudyinnaturalsavannasoftheColombianLlanos,species
richnessandabundancewereseverelyreducedinareasconvertedintooilpalm,andthere
weremarkeddifferenceinspeciescompositionbetweenhabitats[24].Incontrast,astudyin
theColombianAmazonshowedthatants,dungbeetles,andbirdsweremorediverseinoil
palmplantationsthaninpastureareas,andthatoilpalmcouldsupportawiderangeofforest
species[20].However,studiesusingspace-for-timesubstitution(i.e.thoselacking“beforeand
after”data),shouldpaycloseattentiontothenatureofbaselineforestsitesinferredascontrols
orpseudo-controls.Inthisstudy,theAgropalmastudyareahasbeenhistoricallyembedded
withinanoldAmazoniandeforestationfrontier,wherevirtuallyallremainingprimaryforest
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