When roads appear jaguars decline: Increased access to an Amazonian wilderness area reduces

18 Pages·2017·3.63 MB·English

RESEARCHARTICLE
When roads appear jaguars decline:
Increased access to an Amazonian wilderness
area reduces potential for jaguar
conservation
SantiagoEspinosa1,2*,GerardoCelis3,LynC.Branch4*
1 FacultaddeCiencias,UniversidadAuto´nomadeSanLuisPotos´ı,SanLuisPotos´ı,SanLuisPotos´ı,
Me´xico,2 EscueladeCienciasBiolo´gicas,PontificiaUniversidadCato´licadelEcuador,Quito,Pichincha,
a1111111111
Ecuador,3 CenterforEcosystemScienceandSociety,NorthernArizonaUniversity,Flagstaff,Arizona,
a1111111111
UnitedStatesofAmerica,4 DepartmentofWildlifeEcologyandConservation,UniversityofFlorida,
a1111111111
Gainesville,Florida,UnitedStatesofAmerica
a1111111111
a1111111111 *[email protected](SE);[email protected](LCB)
Abstract
OPENACCESS RoadsareamainthreattobiodiversityconservationintheAmazon,inpart,becauseroads
Citation:EspinosaS,CelisG,BranchLC(2018) increaseaccessforhunters.Weexaminehowincreasedlandscapeaccessbyhuntersmay
Whenroadsappearjaguarsdecline:Increased leadtocascadingeffectsthatinfluencethepreycommunityandabundanceofthejaguar
accesstoanAmazonianwildernessareareduces
(Pantheraonca),thetopAmazonianterrestrialpredator.Understandingsuchecological
potentialforjaguarconservation.PLoSONE13(1):
e0189740.https://doi.org/10.1371/journal. effectsoriginatingfromanthropogenicactionsisessentialforconservationandmanage-
pone.0189740 mentofwildlifepopulationsinareasundergoinginfrastructuredevelopment.Ourstudywas
Editor:MarcoApollonio,UniversitadegliStudidi conductedinYasun´ıBiosphereReserve,theprotectedareawithhighestpotentialforjaguar
Sassari,ITALY conservationinEcuador,andanareaboththreatenedbyroaddevelopmentandinhabited
Received:July7,2017 byindigenousgroupsdependentuponbushmeat.Wesurveyedpreyandjaguarabundance
withcameratrapsinfoursitesthatdifferedinaccessibilitytohuntersandusedsiteoccu-
Accepted:November30,2017
pancyandspatiallyexplicitcapture-recaptureanalysestoevaluatepreyoccurrenceand
Published:January3,2018
estimatejaguardensity,respectively.Higherlandscapeaccessibilitytohunterswaslinked
Copyright:©2018Espinosaetal.Thisisanopen withloweroccurrenceandbiomassofgame,particularlywhite-lippedpeccary(Tayassu
accessarticledistributedunderthetermsofthe
pecari)andcollaredpeccary(Pecaritajacu),theprimarygameforhuntersandpreyforjag-
CreativeCommonsAttributionLicense,which
permitsunrestricteduse,distribution,and uars.Jaguardensitywasupto18timeshigherinthemostremotesitecomparedtothe
reproductioninanymedium,providedtheoriginal mostaccessiblesite.Ourresultsprovideastrongcasefortheneedto:1)considerconser-
authorandsourcearecredited.
vationoflargecarnivoresandotherwildlifeinpoliciesaboutroadconstructioninprotected
DataAvailabilityStatement:Allrelevantdataare areas,2)coordinateconservationinitiativeswithlocalgovernmentssothatdevelopment
withinthepaperanditsSupportingInformation
activitiesdonotconflictwithconservationobjectives,and3)promotedevelopmentofcom-
files.
munity-basedstrategiesforwildlifemanagementthataccountfortheneedsoflarge
Funding:Thisworkwasconductedwiththe
carnivores.
financialsupportof:UniversityofFlorida’sWildlife
EcologyandConservationDepartment(www.wec.
ufl.edu)TCD),TropicalConservationand
DevelopmentProgram(www.tcd.ufl.edu),and
GordonandBettyMoore-AmazonConservation
LeadershipInitiative(http://uftcd.org/funding-
awards/);WorldWildlifeFund-RusselE.Train
PLOSONE|https://doi.org/10.1371/journal.pone.0189740 January3,2018 1/18
Landscapeaccesstohuntersandjaguarconservation
EducationforNatureProgram(www.worldwildlife. Introduction
org/initiatives/russell-e-train-fellowships);Wildlife
Manypopulationsoflargecarnivoresaredecliningandthreatenedwithextinctionworldwide
ConservationSociety-ResearchFellowship
Program(https://programs.wcs.org/rfp/);and [1].Becauselargepredatorshavebeenshowntoplaykeyrolesinthestructureandfunctionof
Panthera(www.panthera.org/).Thefundershadno manyecosystems,reductioninpopulationsofthesespecieshasaltereddynamicsofecosystems
roleinstudydesign,datacollectionandanalysis, rangingfromgrasslandstotropicalforest[1,2].Majorcausesoflargecarnivoredeclines
decisiontopublish,orpreparationofthe
includehabitatlossanddegradationwithhumandevelopment,mortalityfromhuman-carni-
manuscript.
voreconflictsorpoaching,preydepletion,andsynergismsamongthesefactors[1,3,4].Asa
Competinginterests:Theauthorshavedeclared resultoftheseprocesses,inthelastcentury,thejaguar(Panthera onca)hasdisappearedfrom
thatnocompetinginterestsexist.
overhalfofitsoriginalrange[5,6].
Currently,theAmazonBasinisthemainstrongholdforjaguarconservationasitsustains
89%ofthecat’sglobalpopulation[6].However,Amazoniafacesrapidchangesassociatedwith
large-scaledevelopmentthatcanthreatenthefutureofthejaguarintheregion.Forexample:
80,000km2offorestshavebeenconvertedtosoybeanplantationsintheBrazilianAmazon[7];
hydropowerdamsexist,areunderconstruction,orplannedinnumeroustributariesofthe
Amazon[8];andextractiveactivities,suchasthoseforhydrocarbonsandminerals,arewide-
spreadintheregionandinsomecasesoccurwithinprotectedareas[9,10].Thesedevelopmen-
talactivitiesareassociatedwithroaddevelopmentthatpromotesformationofnewsettlements,
increasescolonizationrates,andultimatelycatalyzeslandcoverchangeandbiodiversityloss
[11–13].
InfaceofcurrentandfuturechangeinAmazonianecosystems,jaguarconservation
dependsheavilyuponthelargesystemofprotectedareas,particularlymegareserves,inthis
region(i.e.,areas>10,000km2,[14,15].However,pressuretoconstructroadswithinwilder-
nessareasishigh[9,16].Traditionally,accessbyhuntershasbeenlimitedtoareasadjacentto
rivers.Asnewroadsaredevelopedintheregion,wecanexpectthatahigherproportionof
Amazoniawillbecomeaccessible,andthereforetheproportionofnaturalareasthatfunction
aswildliferefugesorsourceswilldecrease[17–19].Moreover,asroadnetworksincrease,mar-
ketsbecomemoreavailabletosubsistencehunterspromotingcommercializationofwildlife
andtargetedhuntingoflargegamespeciesthatprovidehighreturns[19–23].Theconse-
quencesofthisprocessforjaguarpopulationsmaybelargebecauseprogramsforsustainably
managinghuntinggenerallyarelacking,anddensityoflargecarnivorepopulationsoftenis
closelyrelatedtoabundanceoflarge-bodiedprey,suchasungulates,whichincreasinglyare
overexploited[24–26].
Basedontheseobservations,onecaninferthatthepotentialofprotectedareastoconserve
largecarnivoressuchasjaguarsmaybeseriouslycompromisediftheselandsbecomemore
accessiblebyroads.Thusfar,studiesthatcontributetounderstandingcascadingeffectsof
roadsonwildlifeintropicalforestshaveprimarilyinvestigatedimpactsofroadsonhunting
pressure[e.g.,18,20,22].Inthispaperweanalyzetheconsequencesofincreasingaccessibility
toawildernessareaforpopulationsofjaguarandtheirprey.Thisresearchwasconductedin
Yasun´ıBiosphereReservelocatedinEcuador’sAmazonregionwherepressuretoextractnatu-
ralresourcesishigh[27–29].
Materialsandmethods
Studyarea
Yasun´ıBiosphereReserve(hereafterYasun´ı)islocatedintheEcuadorianAmazonandformed
byYasun´ıNationalPark(ca.10,000km2)andtheadjacentWaoraniEthnicReserve(ca.8,000
km2)(Fig1).Yasun´ıismainlyinhabitedbytheWaorani,ahistoricallysemi-nomadicgroup
thatbeganadoptingasedentarylifestyleaftertheircontactwithwesterncultureinthemid-
PLOSONE|https://doi.org/10.1371/journal.pone.0189740 January3,2018 2/18
Landscapeaccesstohuntersandjaguarconservation
Fig1.CameratraparraysinfoursitesinYasun´ıBiosphereReserveorderedfromlowtohighhumanaccess.A)Lorocachi;B)Tiputini;C)Keweriono;
D)MaxusRoad.
https://doi.org/10.1371/journal.pone.0189740.g001
1950s[30];otherindigenousgroups,suchasKichwaandShuar,liveatthereservemargins.
Roadconstructionbeganintheearly1980swiththeAucaRoadtoaccessoilreservesinWaor-
aniterritory.Intheearly1990s,theMaxusRoadwasbuiltinthenorthernportionofYasun´ı
NationalPark(Fig1)andvariouspermanentWaoranisettlementswereformedalongthis
road.
VegetationinYasun´ıprimarilycomprisesevergreentropicalterrafirmeforestwithcanopy
heightbetween25–40m[31].FloodplainsandswampyareasdominatedbythepalmMauritia
flexuosaoccuralongmarginsofthemainrivers.Seasonsarenotmarked.Annualrainfallis
~3,000mmwith>100mmprecipitationinallmonths.Meanmonthlytemperaturesare22–
34˚C[31].
Studydesign
WehypothesizedthatinYasun´ı:1)abundanceoflargegameisstronglyinfluencedbyland-
scapeaccessibilitytohunters,and2)reductionsoflargegamecauselocaldeclinesinjaguar
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Landscapeaccesstohuntersandjaguarconservation
Table1. Hunter’saccessibilityatfourstudysitesinYasun´ı. Accessibilityismeasuredasdistance(meankm±SD)ofcameratrapstothreesourcesof
access:roads,riversandsettlements.
Studysites
Sourceofaccess Lorocachi Tiputini Keweriono MaxusRoad
Road 74.46±4.70 31.72±2.72 12.34±2.91 1.85±1.25
River 6.69±1.18 1.70±1.49 2.25±1.67 2.28±1.76
Settlement 11.61±5.09 15.06±2.93 2.96±1.53 3.56±1.62
https://doi.org/10.1371/journal.pone.0189740.t001
density.Indigenousinhabitantsintheseareasgenerallydonothuntjaguars[19,32–34].Based
onthis,wepredictedthatoccurrenceandbiomassofpreywouldbelowerinmoreaccessible
areasandthatwewouldobservelowerlocaldensitiesofjaguarsintheseareas.Toevaluateour
predictions,wesurveyedpreyandjaguarpopulationsinfoursitesinYasun´ıwithvarying
degreeofaccess.Orderedfromtheleasttothemostaccessible,thesesiteswereLorocachi[76˚
00’30”W,1˚42’23”S],Tiputini[76˚00’07”W,0˚42’35”S],Keweriono[77˚07’27”W,1˚00’49”S],
andMaxusRoad[76˚26’49”W,0˚40’11”S](Fig1;Table1).
Lorocachi(Fig1A)islocatedneartheCurarayRiveradjacenttothesouthernborderof
Yasun´ıinthebufferareaofthereserveandisaccessibleonlybyair.Thissiteisinhabitedbya
Kichwacommunityof120peopleanda300-personarmybase,bothestablishedin1953.Army
personnelarenotallowedtohuntandareprovisionedbyEcuador’sarmy.Proteindemandsof
theKichwaaremetwithpoultry,fishing,andhunting.KichwainLorocachihaveno-huntareas
andlimitedharvestofSalvin’scurassow(Mitusalvini),Amazoniantapir(Tapirusterrestris)and
white-lippedpeccaries(Tayassu pecari)withintheirhuntingarea[35].Oursurveyareawas
accessibleonlyonfootandextendedfrom3to21kmfromthecommunityofLorocachi.Based
onmaximumdistanceswalkedbyAmazonianhuntersfromsettlementsorsourcesofaccess
(i.e.,8–9km),weestimatethat70–80%ofthissurveyareaisoutofreachofhunters[18,19].
TheTiputinisite(Fig1B)islocatedonthenorthernmarginofYasun´ıaccessibleonlyby
theTiputiniRiver.Althoughthisareaisnotinhabited,weobservedammunition,remainsof
huntingcamps,andWaoraniandKichwahunterswhileconductingourstudy(oneandtwo
occasions,respectively).Ashuntershavetotravel3–5hoursfromtheirsettlementsbydugout
canoestoreachthissite,itislikelythathuntingoccurssporadically.
TheKewerionosite(Fig1C)iswithintheWaoraniEthnicReserveinthewesternportion
ofYasun´ı,andincludesthesettlementsofApaika(10inhabitants)andKeweriono(60inhabi-
tants)alongtheShiripunoRiver.ApaikaandKewerionoare15and25kmfromtheAuca
Road,respectively.Alloursurveyareaisaccessibletohuntersbyfoot,andhuntinghasbeen
continuousinthisareasinceestablishmentofKewerionoin1989.Huntingisprincipallyfor
subsistencepurposes,butsmokedbushmeatisoccasionallytradedalongtheAucaRoad
[30,33].HuntersfromApaikaandKewerionocangettotheroadonfoot(6–8hrs)orbytrav-
elingontheriver(3–6hrs).
TheMaxusRoadsite(Fig1D)encompasseshuntingareasoffourWaoranisettlements
(Guiyero,Tiwe,GanketaandTimpoka)withacombinedpopulationof70.Allthisareais
accessibletohuntersbyfootandhasbeenhuntedcontinuouslysincesettlementsformedin
theearly1990saftertheroadwasconstructed.Bushmeatextractionisgreateratthissitethan
ourotherstudysitesasWaoranialongthisroadusewildlifeasacommodity,tradingapproxi-
mately35%ofthetotalharvestatlocalmarkets[19].
Wildlifesurvey
Toevaluateoccurrenceofpreyandjaguardensityacrossareasthatdifferedinaccessibilityto
hunters,weconductedsemi-systematicsamplingwithcameratraps(LeafRiver™model
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Landscapeaccesstohuntersandjaguarconservation
C1-BUequippedwithpassiveheatandmotionsensors)for90consecutivedaysateachofour
foursites.Weplaced23–26cameratrapstations(hereafterstations)withinapolygonof104–
110km2ateachsite(S1Table).Stationswerelocated2–3kmapartalongtransectscutforthis
study(44–67kmoftransectspersite)withcamerasonoppositesidesofthetransectopening
tophotographbothflanksofananimaland,thus,maximizetheprobabilityofidentificationof
individualjaguarsfromfurrosettepatterns.Spacingofstationswasdesignedtoensurethatall
jaguarswithineachsurveyareahadsomeprobabilityofcapture[36].Camerasweremounted
ontrees30–40cmabovegroundandtestedtoensurecaptureofpreyspeciesassmallasblack
agouti(Dasyproctafuliginosa)andnine-bandedarmadillo(Dasypusnovemcinctus).Weplaced
stationsinoptimalmicrosites(e.g.,whereweobservedanimaltrailsandjaguarorpreytracks)
andonlyinterra-firmeforesttopreventequipmentfromflooding.Stationswerebaitedwith
sixdropsofamixofHawbacker’sWildcatluresNo.1and2(S.StanleyHawbaker&Sons,
FortLoudon,PA),whichweplacedonapieceofwoodydebrisbetweencameratrapsatinstal-
lationtimeandevery15dayswhenwecheckedcameras.
OurresearchprotocolwasreviewedbytheMinistryoftheEnvironmentofEcuadorand
thisMinistrygrantedusapermittoworkinYasun´ıNationalPark(PermitNo.012-IC-FA-P-
NYRSO).WealsoobtainedapermitfromtheWaoraniOrganization(NAWE)toworkin
theirterritory.Ourresearchprotocoldidnotincludeinvasivetechniquessuchasanimalhan-
dlingorsacrificeandwasapprovedbytheInstitutionalAnimalCareandUseCommittee
(IACUC-E812)ofUniversityofFlorida.
Analysesofpreyavailability
Preyavailabilityforjaguarsatthefoursiteswasestimatedusingtwomeasures:1)occurrence
ofpreyspeciesmeasuredasprobabilityofsiteoccupancyΨ[37],and2)biomasspercamera
trapstation.Ψmayreflectthechancejaguarshavetoencounterpreyataparticularsite,and
preybiomassisameasureofpotentialfoodavailability.Preyoccurrenceanddetectionproba-
bilitywereestimatedwithsingleseasonsiteoccupancymodelswithprogramPRESENCE
[37,38].Becausemedium-sizedandlargemammalsarehighlymobileandcouldenterand
leavethesurveyareaduringoursampling,theoccupancyestimatorisbestinterpretedasprob-
abilityofsiteuseratherthanprobabilityofoccupancy[37].Weusetraditionaloccupancyter-
minologyinthispaperforeaseofpresentation.Wedevelopedseparateoccupancymodelsfor
allspeciesfromourstudyareathathavebeenreportedtobeimportantpreyforjaguar:white-
lippedpeccary,collaredpeccary(Pecaritajacu),Amazoniantapir,redbrocket(Mazamaamer-
icana),Amazonianbrownbrocket(M.nemorivaga),paca(Cuniculuspaca),blackagouti,and
armadillos(DasypusnovemcinctusandD.kappleri;analyzedasasinglespeciesbecauseof
uncertaintyinspeciesidentificationfrompictures)[39].
Toestimateoccupancyforthese8preyspecies,wecombineddatafromourfourstudysites
(n=100stations)anddividedthe90-daysurveyperiodinto9trappingoccasionsof10days
each(S1Data).Wemodeledoccupancyasafunctionoflandscapeaccessibilitytohuntersrep-
resentedbytwocovariates:Euclideandistancesofstationstosettlementsandtonearestsource
ofaccess—roadornavigableriver.Becausehuntingbysubsistencehuntersisconcentrated
aroundsettlementsandnearmarginsofriversandroads,distancestotheselandscapefeatures
aregoodpredictorsofhuntingintensity[19,40].Weaddedhabitattypeasathirdpredictorof
occupancyrepresentedbyadummyvariablethatreflectsthemaintopographicalcategoriesin
terrafirmeinYasun´ı(ridgesandvalleys[31],S1Data).Weuseddistancebetweenpairedcam-
erasasapredictorofdetectionprobabilityanddeveloped15modelsforeachspeciesthat
includedallcombinationsofexplanatoryvariablesforoccupancyanddetectionprobability.
Best-fitmodelswereselectedwithAkaikeInformationCriterioncorrectedforsmallsamples
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Landscapeaccesstohuntersandjaguarconservation
(AIC ,[41].Weobtainedsite-specificΨestimatesbyaveragingtheΨestimatesofstations
c
withinsites.
Toassessthepreybaseforjaguars,weestimatedabiomassindexforeachstationdefined
P
R
as:BI ¼ i¼1niwi,whereRisthenumberofspeciesdetectedinastation,n isthenumberof
t i
individualsofspeciesi,w istheaverageweight(kg)ofspeciesi,andtisthetime(days)thesta-
i
tionwasactive.Averageweightofeachspecieswasobtainedfromanimalshuntedalongthe
MaxusRoadinaparallelstudy[19]orfromthedatabasePanTHERIA[42].Weestimated
threeBIsperstationthatincluded:1)allterrestrialspecieswithbodymass(cid:21)1kg,2)only
ungulates,and3)allterrestrialspeciesexcludingungulates.Weexcludedpuma(Pumaconco-
lor)fromtheseanalysesbecauseitisunlikelythatjaguarspreyonthislargecat.Pumashave
notbeenreportedaspreyinstudiesofjaguardiet[43–50].ToestimateBIsweconsideredpho-
tographsofthesamespeciestobeindependentwhenaminimumof1houroccurredbetween
detections.Ifmorethanonepictureofaspecieswastakenwithinaone-hourperiod,wechose
thepicturewiththelargestnumberofindividualsforBI.OurBIisameasureofbiomassper
unitoftime(kg/day)foreachstationandthereforedoesnotstrictlyreflectbiomass(i.e.,mass
oflivingmaterialperunitofarea),however,weusethetermbiomassthroughoutourmanu-
scriptforconvenience.Wetestedfordifferencesinbiomassamongourfourstudysiteswitha
Kruskal-Wallistest.
Finally,toevaluatetherelationshipsbetweenungulatepreybiomassandmeasuresofland-
scapeaccessibility(distancetoroad,river,andsettlement)weconductedaPearsoncorrelation.
Weestimatedcoefficient95%highestdensityintervalsusingBayesianbootstrapmethodwith
1,000posteriorresamplesdrawswithRpackage‘bayesboot’[51]
Estimationofjaguardensity
Weusedtwoapproachestoestimatejaguardensityateachsitebasedonadultindividualscap-
turedwithinthe90-daysampleperiod.First,weestimatedjaguardensitywithaspatially
explicitcapture-recapturemodel(SECR).SECRmodelsdonotrelyonestimatinganeffective
trappingareaand,therefore,areparticularlyusefulintheabsenceofgeographicclosure.We
usedaBayesianapproachforSECR,implementedbyRpackageSPACECAP[52,53],which
reliesonMarkovchainMonteCarlo(MCMC)simulationforparameterestimationandisless
sensitivetosmallsamplesizesthanmethodsusingasymptoticinference[52,54].Densityesti-
mationwithSECRinvolvestwogroupsofmodels.Astateprocessmodelsimulatespotential
individualhomerangecentersthatareuniformlydistributedwithinanarea,thestate-spaceS,
whichincludesthetrappingarray.ThesizeofSmustbelargeenoughthatnoanimalscaptured
onthetrappingarrayhaveaprobabilityofbeingcapturedoutsideofS.Asecondgroupof
observationmodelssimulatesdetectionprobabilityofindividualswithinS.Observationmod-
elsincludeadetectionfunctionandacaptureencountermodelandprovidetwobasicparame-
ters:1)λ ,thedetectionprobabilitywhenthedistancebetweenananimal’shomerangecenter
0
andcameratrapequalszero;and2)σ,whichrepresentsthespatialscaleatwhichdetection
probabilitydecreases.
Bayesian-SECRmodelsusedataaugmentationthatconsistsofaddinganextranumberof
individualsMwith“all-zero”capturehistories.Misassumedtocontainthetruepopulation
number,N,withinS.InthecontextofBayesianinference,Mcanbeinterpretedasanupper
boundofanuninformativeuniformprior(0,M)forN[52,53].SPACECAPprovidesestimates
ofpopulationsizeinthelargerstate-space(N ),Density(D ),andψ,whichisthefrac-
super SECR
tionofMthatactuallyrepresentsthetruepopulation[53].
Foreachsite,werannullmodelsthatdescribedthedetectionfunctionwithahalf-normal
distributionandcaptureencounterswithaBernoulliprocess.TodefineSweuseda15-km
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Landscapeaccesstohuntersandjaguarconservation
bufferaroundeachtraparrayenvelope,withpotentialindividualhomerangecentersdistrib-
uteduniformlyatadensityofoneperkm2.Potentialhomerangecenterswereassociatedwith
adummyvariableofhabitatsuitability(i.e.,1forsuitable,0otherwise).Alldatausedforjaguar
densityestimationwithSPACECAPareavailableinS2Data.Fordataaugmentationweused
20–40timesthenumberofindividualsobservedineachsite(S2Table).WeranMCMCsimu-
lationswithaburn-inperiodof50%,athinningrateof10andincreasedthenumberofitera-
tionsprogressively,from50,000to600,000,untilconvergenceofparameterswasachieved(S2
Table).Weevaluatedmodelconvergencewiththez-statisticderivedfromtheGeweke’sdiag-
nosticontheMarkovchainMonteCarloanalysis;valuesofthez-statisticbetween-1.6and1.6
indicatemodelconvergence[53].
Foroursecondapproachweestimateddensityas:D¼ N^ ,whereN^ isanestimateofpopu-
ETA
lationsizederivedfromacapture-recapturemodelofclosedpopulations,andETAisanesti-
mateofeffectivetrappingarea.WeestimatedN^ withprogramCAPTURE[55]andusedthe
M modelwithajackknifeestimatortoallowfordifferentcaptureprobabilitiesamongindi-
h
viduals,whichhasmorebiologicalmeaningthanassumingcapturehomogeneity[56].Estima-
tionofN^ hastwocriticalassumptions:1)demographicclosure(i.e.,nomigration,birthsor
deaths)duringthestudyperiod;and2)allindividualshaveaprobabilitygreaterthanzeroof
beingcaptured[57].Wedevelopedonematrixpersitewhererowscorrespondedtoiindividu-
alsidentifiedateachsiteandcolumnstojtrappingoccasions.Atrappingoccasionwasdefined
asthreeconsecutivetrappingdays(i.e.,totalof30trappingoccasionspersite).Theentryin
theX matrixwas1ifanindividualwasrecordedduringatrappingoccasionand0otherwise
ij
(S2Data).
TheN^=ETAmethodhasbeenwidelyusedtoestimatejaguardensityinotherareas,despite
itslimitations,andthusfacilitatescomparisonsacrossstudies[58].Estimatesofdensityfrom
N^=ETAaredependentontrapspacingandthenumberofrecapturesofindividuals[59],
whichcanbeproblematicwhenstudyinglargefelidsthathavelargehomerangesandnaturally
lowabundance.Also,althoughestimationofN^ isstraightforward,estimationofETAisdiffi-
cultwhensamplingareashavenophysicalboundaries.Toaddressthisproblem,aboundary
stripoftenisplacedaroundthesamplingareathatequalshalforthefullmeanmaximumdis-
tancemoved(MMDM)byindividualsderivedfromcapturesofindividualsatdifferenttraps
[56,60,61].WeusedthefullMMDMasabufferaroundeachstationbecausethisbufferpro-
videsmoreconservativedensityestimatesandissupportedbytelemetryandsimulationstud-
iesofjaguardensity[60,62].ToestimateMMDMweusedthepooledmaximumdistancesof
allstudysitesandexcludedrecapturesofindividualsatthesamestations.ThisMMDMwas
6.08±SE0.73kmestimatedfrom15jaguars.Wecalculatedthestandarderrorofdensitywith
theformulaprovidedinKaranthandNichols[56].
Results
Weobtainedatotalof4,565independentphotographsofterrestrialmammalsandbirdswith
bodysize(cid:21)1kg,correspondingto24speciesofmammals(3,454photographs)and5speciesof
birds(1,111photographs;S3Table).
Preyavailability
Accessibilityoftheforesttohumanswasanimportantpredictorofoccurrencefor7ofthe8
preyspeciesanalyzed(Table2;S1Appendix).Forallspeciesexceptblackagouti,best-fitmod-
elsofoccupancyincludeddistancetosettlementsasacovariatewithapositivecoefficient,
indicatingthatthefurtherthedistancefromsettlementsthehighertheoccurrenceofprey.
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Landscapeaccesstohuntersandjaguarconservation
Table2. OccupancymodelsforjaguarpreyinYasun´ı. Untransformedestimatesofcoefficientsforcovariatesβ(SE)topredictpreyprobabilityofsite
occupancyΨasafunctionof:distancetonearestroadorriver(RR),distancetonearestsettlement(ST)andhabitat(H).Detectionprobabilitypismodeledas
afunctionofdistancebetweenpairedcameras(DC)orasconstant(.).
Species, InterceptΨ β β β Interceptp β
RR ST H DC
best-fitmodel
White-lippedpeccary,Ψ(ST)p(DC) -5.73 - 0.77 - -2.78 0.19
Collaredpeccary, -2.26 1.63 0.43 - -1.49 0.10
Ψ(RR+ST)p(DC)
Amazoniantapir, -0.88 - 0.20 - -3.13 0.21
Ψ(ST)p(DC)
Red-brocket, 0.59 - 0.13 - -3.49 0.30
Ψ(ST)p(DC)
Amazonianbrown-brocket, -1.38 - 0.13 -1.03 -1.62 -
Ψ(ST+H)p(.)
Paca, 0.14 - 0.14 -1.37 -1.52 -
Ψ(ST+H)p(.)
Blackagouti, 1.91 - - -0.82 -0.52 -
Ψ(H)p(.)
Armadillos, 0.01 - 0.07 - -0.60 -0.09
Ψ(ST)p(DC)
https://doi.org/10.1371/journal.pone.0189740.t002
Distancetoroadsandriversalsowasanimportantpredictorofoccurrenceofcollaredpecca-
ries,andtypeofterrafirme(ridgevs.valley)wasincludedinbest-fitmodelsforthetwolarge
rodentsandbrownbrocketdeer(Table2;S1Appendix).Attheleastaccessiblesites,Lorocachi
andTiputini,occurrencesofthefivespeciesofungulateswerenotablyhigherthaninthemost
accessiblesites,KewerionoandMaxusRoad(Fig2).Themostextremecasewaswhite-lipped
peccarieswhichwereneverdetectedinKewerionoandscarcelydetectedintheMaxusRoad,
butexhibitedanoccupancyprobability(cid:21)0.75atothersites.Also,theoccurrenceofarmadillos
andpacaswas15–50%higherinthetwoleastaccessiblesites.Incontrast,occurrenceofagou-
tisdidnotdifferwithaccessibilityofsitestohumans(Fig2).
Preybiomassalsodeclinedashumanaccessincreased.Overallmeanpreybiomasswas
greaterbyafactorof2.0–4.5atthetwositeswithlowesthumanaccessascomparedtothehigh
accesssites(Kruskal-WallisX2=52.43,df=3,P<0.001,Table3).Thesedifferenceswere
drivenby2.5–7.8foldchangesinthetotalbiomassofungulatesbetweenlowaccessandhigh
accesssites(Kruskal-WallisX2=55.69,df=3,P<0.001,Table3).Forexample,biomassof
white-lippedpeccarieswas15and46timeshigherinLorocachiandTiputini,respectively,
thaninMaxusRoad.Biomassofcollaredpeccarieswas2–3timeshigherinthetwomostiso-
latedsitesthaninthemostaccessiblesites(S3Table).Biomassofnon-ungulatepreyspecies
wassimilaramongall4sites(Kruskal-WallisX2=0.84,df=3,P=0.839;Table3).
Weobservedapositiverelationshipofungulatepreybiomasswithdistancetosettlements
(r=0.71;P<0.001;HDI =0.61to0.79;Fig3A)anddistancetoroads(r=0.34;P<0.001;
95
HDI =0.21to0.48;Fig3B),andamarginallysignificantrelationshipwithaccesstorivers
95
(r=0.19;P=0.06,HDI =0.02to0.33;Fig3C).
95
JaguarabundanceinYasun´ı
Densityestimateswerebasedonatotalof59capturesthatcorrespondedto30adultjaguars
(18males,7femalesand5un-sexedanimals,S4Table).Atotalof13jaguarswerecapturedin
Lorocachi(ourmostisolatedstudysite),6inTiputini,8inKewerionoand3inMaxusRoad
(ourmostaccessiblestudysite).Both,thespatially-explicitandtheN^=ETAmethodsprovided
similarresults.ForSECRanalyses,weachievedconvergenceforN andψatallsitesbutnot
super
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Landscapeaccesstohuntersandjaguarconservation
Fig2.ProbabilityofsiteoccupancyofeightimportantjaguarpreyspeciesatfoursitesinYasun´ıBiosphereReserve.Sitesarearrangedfromleast
tomostaccessible(darktolight).Asapointofclarification,white-lippedpeccarieswereneverrecordedincameratrapsatKeweriono,however,occupancy
modelspredictasmallprobabilityofoccurrenceofthisspeciesatthissitebasedoncovariates.
https://doi.org/10.1371/journal.pone.0189740.g002
forσandλ (S5Table).Densitydecreasedfrom5.44±SD2.04individuals/100km2inour
0
leastaccessiblesiteto0.29±SD0.26individuals/100km2inourmostaccessiblesite(Fig4;S6
Table).FortheN^=ETAmethodweobtainedeffectivetrappingareasthatvariedfrom458–486
km2(S6Table)andjaguardensitiesfollowedasimilarpatterntoSECRanalyses,withamaxi-
mumdensityof3.91±SE1.11andaminimumof0.65±SE0.26individuals/100km2inour
Table3. BiomassofjaguarpreyatfoursitesinYasun´ıBiosphereReserve. Dataaretheaverageofbiomassindexes(kg/day)forcameratrapstations
ateachsite.LorocachiandTiputiniarethemostisolatedsitesandKewerionoandMaxusRoadarethemostaccessiblesites.
Studysites
Biomass Lorocachi(n=26) Tiputini(n=25) Keweriono(n=23) MaxusRoad(n=26)
Allpreyspecies 10.23±7.06 16.57±7.13 3.65±2.00 4.97±3.51
Ungulates 8.4±6.9 14.73±6.98 1.90±1.85 3.28±3.06
Non-ungulates 1.84±1.14 1.83±0.94 1.75±0.88 1.69±1.13
https://doi.org/10.1371/journal.pone.0189740.t003
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Landscapeaccesstohuntersandjaguarconservation
Fig3. Relationshipbetweenungulatepreybiomassandlandscapeaccessibilitymeasuredasdistancefromcameratrapstations(km)to
settlements(A),roads(B)andrivers(C).Datapointsareanindexofungulatebiomass(kg/day)ateachstation.
https://doi.org/10.1371/journal.pone.0189740.g003
leastandmostaccessiblesites,respectively(Fig4;S6Table).Theassumptionofdemographic
closurefornon-spatialmodelsheldforallfoursites(S6Table).
Discussion
Weshowthatfacilitationofhunteraccesstoanaturallandscapecanleadtodevelopment-
inducedimpactsonpredatorsandpreythatendwithreducingabundanceofjaguar,thetop
predatorofourstudysystem.Ourfindingsclearlysupportourfirsthypothesisthathigher
landscapeaccessibility(i.e.,proximitytosettlements,roadsandrivers)tohuntersleadsto
reductionofprey.Theseresultsareconsistentwithstudiesthatshowhuntingeffortishigher
nearsettlementsorsourcesofaccess[18,19,63].Occurrenceandbiomassofthetwospeciesof
peccaries,thespeciesmostharvestedbyWaorani[19,32–34],alongwithtapirandtwospecies
ofbrocketdeer,werereducedinareashighlyaccessibletohunters.Thispatternwasevident
eventhoughourstudysiteswerewithinalargerelativelyintactforestwheresource-sink
dynamicscouldhavedilutedourcapacitytodetectsuchpatterns[17].
Oursecondhypothesis,thatreductionoflargegamefromhuntingwouldcauselocal
declinesinjaguardensity,wasframedbasedonthecloserelationshipobservedbetweenabun-
danceoflarge-bodiedpreyandotherlargecats[24,26].Althoughjaguarsareopportunistic
predators,theyareknowntopreferentiallyuselargepreywhenavailablesuchascapybara
(Hydrochoerushydrochaeris),caiman(Caimancrocodilus),andespeciallywhite-lippedand
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