Differential resilience of Amazonian otters along the Rio Negro in the aftermath of the 20th century

19 Pages·2017·13.24 MB·English

RESEARCHARTICLE
Differential resilience of Amazonian otters
along the Rio Negro in the aftermath of the
th
20 century international fur trade
NataliaC.Pimenta1,2*,Andre´P.Antunes3,AdrianA.Barnett1,ValêncioW.Macedo4,
GlennH.Shepard,Jr.5
1 AmazonMammalResearchGroup,NationalInstituteforAmazonianResearch,Manaus,Amazonas,
Brazil,2 InstitutionalCapacityBuildingProgram/MCTIC,DepartmentofAnthropology,Em´ılioGoeldi
Museum,Bele´m,Para´,Brazil,3 DepartmentofEcology,NationalInstituteforAmazonianResearch,Manaus,
a1111111111
Amazonas,Brazil,4 ComunidadeUrumutumLago,rioAyari,EscolaInd´ıgenaBaniwaeCoripacoPama´ali,
a1111111111
SãoGabrieldaCachoeira,Amazonas,Brazil,5 DepartmentofAnthropology,EmilioGoeldiMuseum,Bele´m,
a1111111111 Para´,Brazil
a1111111111
a1111111111 *[email protected]
Abstract
OPENACCESS Commercialhuntingfortheinternationaltradeinanimalhidesinthe20thcenturydecimated
Citation:PimentaNC,AntunesAP,BarnettAA, manypopulationsofaquaticwildlifeinAmazonia.However,impactsvariedsignificantly
MacedoVW,ShepardGH,Jr.(2018)Differential betweendifferentspeciesandregions,dependinguponhuntingintensity,accessibilityof
resilienceofAmazonianottersalongtheRioNegro
habitat,andtheinherentresilienceofvariousspeciesandtheirhabitats.Weinvestigated
intheaftermathofthe20thcenturyinternationalfur
thedifferentialresponsesoftwoAmazonianMustelidspecies,theneotropicalotterand
trade.PLoSONE13(3):e0193984.https://doi.org/
10.1371/journal.pone.0193984 giantotter,tocommercialhuntingpressurealongtheupperRioNegroinBrazil,andexam-
inedhistoricalfactorsthatinfluencedspatialandtemporalvariationincommercialexploita-
Editor:RobSlotow,UniversityofKwazulu-Natal,
SOUTHAFRICA tion.Weanalyzedpreviouslyunanalyzeddatafromhistoricalrecordsofhideshipmentsto
trackchangesinhidesalesandpricesforthetwospeciesinthelate20thcentury.Wealso
Received:November21,2017
gatheredoralhistoriesfromolderBaniwapeoplewhohadwitnessedorparticipatedincom-
Accepted:February21,2018
mercialotterhunting.Thesecomplimentarydatasourcesrevealhowintrinsicbiologicaland
Published:March30,2018
socialcharacteristicsofthetwootterspeciesinteractedwithmarketforcesandregionalhis-
Copyright:©2018Pimentaetal.Thisisanopen tory.Whereasgiantotterpopulationsweredriventolocalorregionalextinctionduringthe
accessarticledistributedunderthetermsofthe late20thcenturybycommercialhunting,neotropicalotterspersisted.Inrecentdecades,
CreativeCommonsAttributionLicense,which
giantotterpopulationshavereturnedtosomepartsoftheupperRioNegro,adevelopment
permitsunrestricteduse,distribution,and
reproductioninanymedium,providedtheoriginal whichlocalpeoplewelcomeaspartofageneralizedrecoveryoftheecosystemsintheirter-
authorandsourcearecredited. ritoryasaresultofthebanningofanimalpeltexportsandindigenouslanddemarcation.
DataAvailabilityStatement:Allrelevantdataare Thispaperexpandsthescopeofthefieldhistoricalecologyandreflectsontheroleoflocal
withinthepaperanditsSupportingInformation knowledgeinbiodiversityconservation.
files.
Funding:NCPreceivedMasterscholarshipfrom
Coordenac¸ãodeAperfeic¸oamentodePessoalde
N´ıvelSuperior(http://www.capes.gov.br);
scholarshipfromConselhoNacionalde Introduction
DesenvolvimentoCient´ıficoeTecnolo´gicothrough
ResourceusepatternsthroughoutAmazoniahavebeenshapedbytheenduringlegacyofthe
theInstitutionalCapacityBuildingProgramofthe
RubberBoomattheturnofthe20thcentury(1895–1912).Tosupplyinternationaldemand
EmilioGoeldiMuseum(http://www.museu-goeldi.
br/),grantnumber:301089/2017-5;financial forwildrubber,merchantsfromAmazoniancitiessentcommercialfleetsintohinterlandsto
PLOSONE|https://doi.org/10.1371/journal.pone.0193984 March30,2018 1/19
DifferentialresilienceofAmazonianotterstocommercialhunting
supporttofieldlogisticsfromTheRufford exploitrubbertappersinasystemofdebtpeonageknowninBrazilasaviamento[1].When
Foundation(http://www.rufford.org),grant wildrubberpricescollapsedin1912duetothesuccessofrubberplantationsinMalaysia,some
number:16845-1;andequipmentdonationforfield
rubbermerchantssurvivedbyusingtheirexistingfleetsandroutestoexploitalternativeforest
activitiesfromIdeaWild(http://www.ideawild.org).
products,especiallywildanimalhides[2].TheinternationaltradeinAmazonianhidesreached
APAreceivedDoctoralscholarshipfromConselho
itsfirstpeakduringWWII,whenthecaptureofMalaysianrubberplantationsbytheJapanese
NacionaldeDesenvolvimentoCient´ıficoe
Tecnolo´gico(http://cnpq.br),grantnumber: ledtoabriefsecondRubberBoomin1942–1945[3].FueledbydemandfromUSandEuro-
140222/2011-1,anexchangescholarshipfrom peanmarkets,atleast23millionanimalswerehuntedinthewesternAmazonfortheirhides
Coordenac¸ãodeAperfeic¸oamentodePessoalde between1904and1969[2,4].Aseriesoflaws[5,6]attemptedtoregulatethistrade,untilthe
N´ıvelSuperior,grantnumber14646/13-7and
completeprohibitionofcommercialhuntinginBrazilin1967[7].However,anextensionof
financialsupportfromFundac¸ãodeAmparoà
thedeadlineforliquidating“stockpiled”hidesandskinsresultedinthemaintenanceofillegal
PesquisadoEstadodoAmazonas(http://www.
fapeam.am.gov.br),grantnumber:062.00427/ commercialhuntinguntil1974[8].OnlyafterBrazil’sadherencetothe1975Conventionon
2013.Thefundershadnoroleinstudydesign,data theInternationalTradeinEndangeredSpecies(CITES),whichbannedtheotterskintrade
collectionandanalysis,decisiontopublish,or completely,wasthereasignificantreductioninthecommercialdemandand,consequently,in
preparationofthemanuscript.
thelegalhuntingofwildanimals[9].
Competinginterests:Theauthorshavedeclared Commercialhuntinghadespeciallysevereimpactsonlargeaquaticspecies,leadingtothe
thatnocompetinginterestsexist. widespreadcollapseofpopulationsofgiantotter(Pteronurabrasiliensis),blackcaiman(Mela-
nosuchusniger)andmanatee(Trichechus inunguis)acrosstheAmazonBasin[10].Therelative
easeofaccesstoriverinehabitatsandtheconcentrationofhumanpopulationalongthemajor
waterwayscontributedtothis"EmptyRiver"scenario[4,10].Theneotropicalotterandthe
giantotter,bothsemi-aquaticMustelidecarnivores,werehuntedcommerciallyfortheirpelts.
Inthelate1960s,asingleneotropicalotterskinwouldsellontheinternationalmarketforUS$
175.00andagiantotterskinforUS$440.00(calculatedat2015values).From1904to1969,at
least390,000giantotters,and370,000neotropicalotters,werekilledfortheirpeltsinthecen-
tral-westernBrazilianAmazon[4].Otterpopulationsdeclinedseverelyinareaswhereverthey
werehuntedcommercially[11,12].Asadirectresultofthiscommercialhunting,thegiant
otter,originallydistributedwidelyfromVenezuelatoArgentina,isnowconsideredextinctin
muchofitshistoricrange[12,13].
EachAmazoniaregionhasitsownuniquehistoricaltrajectorywithregardtosubsistence
andcommercialhunting[4],reflectinglocalfactorssuchaschangesinhuntingintensity
throughspaceandtime,marketaccess,socioeconomicandculturalvariationandenviron-
mentalcarryingcapacity[4,14,15].Analyzingtheresponseofanimalpopulationstohunting
pressurehelpsrefineconceptsrelatingtospeciesresilience,extinctionandotherlarge-scale
ecologicalprocesses[4,15].Todate,moststudiesinvestigatingtheimpactofhuntingonNeo-
tropicalwildlifehavebeenrestrictedtoterrestrialfauna[16–18].Also,theyaregenerallybased
onacentral-placeforagingmodel[19–23],whichcanbeinappropriatewhenconsideringthe
differentialaccessibilityofterrestrialenvironmentsvs.wetlandsinAmazoniaanddistinctive
patternsofmobilityinsuchhabitats.
Thestudyofpastecologicaleventsrequirestheintegrationofmultiplesourcesofinforma-
tion,includinghistoricaldocuments,oralhistoriesandethnographicdata;sourcesnottypi-
callyusedinecologicalstudies[24,25].Historicaldata,whenavailableandproperlyanalyzed,
canyieldasurprisingwealthofinformationaboutspeciesandecosystemsinthepast,informa-
tionthatwouldbeimpossibletoobtainusingstandardecologicalresearchmethods[4,26–29].
Oralhistoriesprovidedbyinhabitantsofregionswherecommercialhuntingtookplacecan
providefundamentalinsightstoourunderstandingsoftheimpactsonandresilienceoftar-
getedspeciespopulations.Suchhistoricalmethodscanbeappliedtostudiesofcontemporary
managementandconservation,contributingtotheemergingfieldof“historicalecology”[30].
Inthisstudy,wedrawonhistoricaldocumentsfromregionalportregistriesandshipping
manifestsaswellasoralhistoriesoflocalindigenoushunterstoassesstheimpactsoftheinter-
nationalfurtradeonotterpopulationsofthemidandupperRioNegro,AmazonianBrazil.
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DifferentialresilienceofAmazonianotterstocommercialhunting
Wereconstructtheoverallharvestofthetwootterspeciesinthemid-upperRioNegro
throughoutthetwentiethcenturyfrombothprimarydocumentsandoralhistories.Finally,we
assessthebiologicalunderpinningsofthedifferentialresilienceofthetwospecieswithinthe
RioNegrobasin.
Studyareaandculturalcontext
Themid-upperRioNegroislocatedinthenorthwestAmazonwithintheBrazilianmunicipali-
tiesofBarcelos,SantaIzabeldoRioNegroandSãoGabrieldaCachoeira(Fig1),alongthebor-
derwithColombiaandVenezuela.Theregionishometoatremendousdiversityofindigenous
peoples,includingsometwentyethnicgroups,speakinglanguagesbelongingtofivedistinctive
cultural-linguisticfamilies:Tukanoan,Arawakan,Maku,YanomamiandTupi-Guarani[31].
TheirtraditionalterritoryinBraziliscurrentlyprotectedbyfiveindigenousreservestotaling
10.6millionhectares,knowncollectivelyastheUpperRioNegroIndigenousLands[32].The
Baniwa,andtheircloselyrelatedneighborsinColombia,theCoripaco,belongtotheArawakan
languagefamilyandhaveinhabitedtheIc¸anariverbasinforcenturies[33].Duringthesecond
halfofthetwentiethcentury,BaniwahuntersoftheRioIc¸anasoldotterskinstotheManaus-
basedrivertradingempireofJ.G.AraujoLtda,andlatertoseveralothercompanies.Older
Baniwamenwhohuntedduringthistimerepresentavaluable,butdisappearing,sourceof
informationaboutthistradeanditsimpactonotterpopulations.
InBrazil,theIc¸anabasinisablackwaterriversystemdominatedbylow-productivitywhite-
sandsavannas.Localvariationsinwaterlevel,soiltypeandhumanhabitationhistorycreatea
diversemosaicoflandscapesandvegetationtypes[34,35].ThemiddleIc¸ana,intheconfluence
withtheRioAyari,isdominatedbyseasonally-floodedigapóforestsonsandysoils.Though
extremelypoorinnutrientsandmostlyinappropriateforagricultureduetoannualflooding,
thisregioncontainsnumerousblackwaterlakesthatarevaluedbylocalpeoplefortheirrela-
tivelyabundantfishpopulations[35].Suchlakesalsoprovidesgoodhabitatforotters[13,36].
ThisregioncomprisesthetraditionalterritoryoftheDzawinaior“jaguarpeople,”oneofseveral
patrilinealBaniwaclans.
TheDzawinai,oncefearedandrespectedfortheirbraveryandshamanicprowess,weredeci-
matedbyviolenceandexploitationbyrubbermerchantsandBrazilianandColombianmilitary
forcesduringandaftertheRubberBoom[33].Today,this“lakesregion”astheBaniwacallit,
coveringsome65kmofriverextension,ishometotenBaniwacommunitiesfromseveraldif-
ferentclans.Wevisitednineofthesecommunitiesforthisstudy:JanduCachoeira,Tucumã,
BelaVista,UrumutumLago,SãoJose´doAyari,Arapasso,Tucunare´Lago,TarumãandSanta
Marta.
Methods
Baniwaoralhistories
ToreconstructthehistoryofcommercialhuntingontheRioIc¸ana,wecarriedoutsemi-struc-
turedinterviews[37]withall11residents,aged59to88,fromtheninestudycommunities
whowereoldenoughtohaveparticipatedinotterpelthuntingalongtheIc¸ana.Researchwas
carriedoutbetweenSeptemberandNovemberof2015.Allinterviewswereconductedinthe
companyofourBaniwaco-authorandresearchcollaborator(ValêncioW.Macedo),who
translatedandotherwisefacilitatedcommunicationandcommunityrelations(seeS1Appen-
dixfordetails).Respondentswerefreetorefuseparticipationintheresearch.Allthosewho
participatedsignedaformalTermofFreeandInformedConsent.Thestudywasapprovedby
theEthicsCommitteeonHumanResearchoftheNationalInstituteofAmazoniaResearch
(permitnumber1.166.446)andbytheNationalResearchEthicsCommittee(permitnumber
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DifferentialresilienceofAmazonianotterstocommercialhunting
Fig1.Studyarea.LocationofBaniwacommunitiesonthemiddleRioIc¸anavisitedduringthisstudy(top),andtwentiethcenturymunicipalcentersalongtheRioNegro,
Amazonas,Brazil(bottom).
https://doi.org/10.1371/journal.pone.0193984.g001
1.337.043).Ethnographicdataconcerningdirectinformantmemorieswassupplementedwith
areviewofanthropologicalandhistoricalsourcesontheBaniwaandotherindigenousgroups
oftheupperRioNegro,concerningtheirrelationshipswithtwentiethcenturytraders.
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DifferentialresilienceofAmazonianotterstocommercialhunting
Commercialshippingrecords
Toassesstheimpactofcommercialhuntingonneotropicalandgiantotterpopulationsofthe
RioNegro,weanalyzedbillsofsaleandcargomanifests(Fig2)forboatsandshipsattheport
ofManausbetween1936and1968.Wehadtwosourcesofhistoricaldocumentscoveringtwo
distinctperiods:
(A)1936–1953:-shippingrecords,cargomanifestsandfinancialdocumentsofcommercial
boatsownedbyJ.G.AraujoLtda.,nowdepositedintheAmazonianMuseumoftheFederal
UniversityofAmazonasState;
(B)1958–1968:shippingrecordsgleanedfromcargomanifestsofboatsandshipsfromseveral
tradingcompaniesbasedatthePortofManaus,aspublishedinthedailycommercialship-
pingnewspaperBoletimInformativo Corel.See[4]forfurtherdetailsaboutthesehistorical
documents.
Sincethestructureofthetwodatasetsisconsiderablydifferent,wemodeledthenumberof
peltstradedperspeciesseparatelyforeachtimeseries.Tocapturetemporaltrendsinthetrade
Fig2.Billofsaleofhidestransportedbytheboat“Tupana”fromSãoGabrieldaCachoeira(portofSantaIzabeldoRioNegro)toManausbythe
companyJ.G.AraujoLtda.in1939.Thebillspecifiesonebundlecontainingnineteenhidesof“ariranha”giantotter(Pteronurabrasiliensis)andtwo
hidesof“lontra”neotropicalotter(Lontralongicaudis);asecondbundlecontainingtwohidesof“maracaja´”genericcommercialnameforbothocelot
(Leoparduspardalis)andmargay(L.wiedii),onehideof“veado”redbrocketdeer(Mazamaamericana),sixhidesof“caititu”collaredpeccaries(Pecari
tajacu)andfivehidesof“queixada”white-lippedpeccaries(Tayassupecari).
https://doi.org/10.1371/journal.pone.0193984.g002
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DifferentialresilienceofAmazonianotterstocommercialhunting
ofotterpeltswemodeledbothtimeseriesusingallLinearModels,GeneralizedLinearModels
(GLM)andGeneralizedAdditiveModels(GAM).Wethenselectedthebestmodelsbyminimiz-
ingAIC(seeS1Tablefordetails).Touseourmodeledharvesttrendcurvestodrawinferences
aboutpopulationresilienceduringthehidetrade,wecomparedthenumberofpeltstradedatthe
beginningandendofbothtimeseries,duringwhichperiodshuntingincentiveswerestrongdue
tohighmarketpeltprices(Fig3).Forspeciesi,theestimatedpercentagechangewasgivenby:
P P P P
100f ^gðlast3yearsÞ(cid:0) g^ ðfirst3yearsÞ= ^gðfirst3yearsÞg,where ^gdenotesthesum
i i i i
ofestimatedharvests^gðtÞoverfirstorlastthreeconsecutiveyears.Allanalyseswereperformed
i
inR(RDevelopmentCoreTeam)withthemgcvpackageforGAM[38].Graphicswerecon-
structedusingthevisregpackage[39].
BecauseoftheunregulatedandopportunisticnatureofhuntingpracticesinAmazonia,
thereisnodirectinformationabouthuntingeffortovertime.However,thereisstrongsecond-
aryevidencetoassumethathuntingeffortwasincreasing:bothmarketpricesandtherural
humanpopulationinthecentral-westernBrazilianAmazonsurgedduringthe1960s(seehis-
toricaldemographicserieson[40]),soitisreasonabletoassumethathuntingeffortwasalso
increasingduringthestudyfrom1940to1970period.Huntingeffortisunlikelytohave
decreasedinresponsetodeclinesinexploitedpopulationsbecausethewiderangeofcommer-
cially-attractivespeciesensuredthathunterscouldtradewhatevertheycouldcatch.Also,since
animalskinsconstitutedjustoneofmanyextractiveproductsshippedbythefluvialtransport
network,theopportunitytosellhidespersistedevenwhenthevolumeoftradediminished.It
isthereforereasonabletoassumethatharvesttrendsreflectedanimalpopulationstatusto
somedegree,especiallyinthecasewherelowharvestswereregistereddespitestrongmarket
incentivesandahighhumanpopulation.Completerawdatafromshippingrecordsispresent
inS2andS3Tables.
Fig3.Huntingeffortduringthestudyperiod.Leftside:priceofotterpeltsbyspecies(notethequicklyrisingpriceforgiantotterpeltsduringthe1960);rightside:rural
populationinAmazonasState.
https://doi.org/10.1371/journal.pone.0193984.g003
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DifferentialresilienceofAmazonianotterstocommercialhunting
Results
HistoryofcommercialhuntingontheupperRioNegro
DuringtheinitialRubberBoomattheturnofthe20thcentury,commerceontheRioNegro
wascontrolledbyJ.G.Araujo[41].AccordingtothetraveloguesofethnologistGordonMac-
Creagh,whovisitedtheregionin1926,“J.G.”(asSr.Araujowasknown)warnedhimnotto
visittheRioIc¸ana,notingboththedifficultyofitsaccessandthehostilityoftheBaniwainhab-
itantstowardnon-indigenouspeople[41].TheBaniwa’sfiercereputationatthetimestemmed
fromtheirviolentrebellionagainstrubberbossesandregatões(merchantshipowners)during
thelate19thcentury[33].Despitethesewarnings,MacCreaghvisitedtheBaniwaanddescribed
themasfriendly,butnotedinterethnicviolenceresultingfromcompetitionbetweenthe“King
oftheIc¸ana”,aSpanishmerchantwhocontrolledcommercealongthisriver,andthe“Kingof
theVaupes,”aPortuguesecolonistwhocontrolledtheneighboringriver’scommerceandwas
notoriousas"themanwhomakesthewaterbloody"(seep.251–274inref.[41]).
AccordingtoBaniwaoralhistories,somelocalcommercialactivitiesontheIc¸anabeganwith
theestablishmentofaSalesianmissiononthelowerIc¸anainthe1920s.Commercialhunting
wasfurtherincentivizedduringthe1940swiththearrivalofSophiaMuller,anAmericanProtes-
tantmissionaryoftheNewTribesMissionwhoevangelizedsomeBaniwaclansandtheneigh-
boringCoripaco[33].ThecombinedpresenceofCatholicmissionariesonthelowerIc¸anaand
ProtestantmissionariesonthemiddleandupperIc¸anabroughtanendtothereignofthewar-
ring“Kings”describedbyMacCreagh,andopenedtheIc¸anatooutsidetraders.
PriortoWorldWarII,commercialtradeontheupperRioNegroinvolveddiverseforest
productssuchasbreuresin(Protiumspp.,Burseraceae),sorva(Coumaspp.,Apocynaceae),Bra-
zilnuts(Bertholethiaexcelsa,Lecythidaceae)andbushmeat,aswellasnativecraftslikemanioc
gratersandtraditionalbasketry.Around1945,accordingtoourinformants,agroupofBaniwa
menmigratedtothetownsofSantaIzabelandBarcelosonthemiddleRioNegrotoharvestBra-
zilnutsandextractrubber.Asaresult,traderstherebecameawareofthecommercialpotential
thatexistedfartherupriver.Twoofourinterviewparticipantsmentionedisolatedcasesofpelt
huntingontheIc¸anainthe1920sand1940s(Table1),butitwasonlyaround1950thatcom-
mercialpelthuntingbecametrulycommonontheIc¸ana.Bytheearly1960s,pelthuntingwas
themaincommercialactivityintheregion.
“Duringthistimetherewerelotsofgiantotters,everywhere.Youdidn’thavetogofarto
huntthem,noindeed”.
PedroBrazão(71yearsold,Tucumãcommunity)
Bytheearly1960s,tradingboatsfromSãoGabrielandManaushadbecomeacommon
sightalongtheIc¸ana.TheywouldstopatBaniwasettlementstopurchaseorplace“orders”for
luxurypeltsofbothotterspecies,aswellasfelidslikejaguar(Panthera onca),ocelot(Leopardus
pardalis),andmargay(Leoparduswiedii).Giantotterandjaguarpeltswerethemostprofitable.
Atopqualitygiantotterpeltcouldpurchaseuptothreenewrifleswhileaneotropicalotter
peltwasworthonlyonerifle.Althoughajaguarskinhadaboutthesamevalueasthatofa
giantotter,jaguarhuntingwasmoredifficultanddangerouswhencomparedwithotters,
whichcouldbeencounteredopportunisticallyonfishingexpeditions.
Atthattime,otterswerefoundallalongtheIc¸anaRiver,inlargelakesandontributary
streams.Inthelakesregion,hunterstypicallyconductedhuntingexpeditionslasting15–20
days,andwouldtargetentiregiantottersocialgroups.Theneotropicalotterwasnotinitially
targetedbecauseofitslowervalue,butindividualsweresometimeskilledopportunistically
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DifferentialresilienceofAmazonianotterstocommercialhunting
Table1. BaniwaoralhistoriesofcommercialhuntingactivityonthemiddleIc¸anaduringthe20thcenturyinternationalfurtrade.
Age Baniwa’sreports Start Decline Endreasons
84 “ThegiantotterhuntingbeganwhenIwasstilllivingonPama´alicreek,justbeforeIgotmarried.Imusthave ±1951 1975 Giantotterextinction
beenabout20atthetime.”
88 “Iwasveryyoungthenthewhitesbeganthehuntinghere.Iwas14whenIwentaftergiantotterforthefirst ±1940 1948 Giantotterextinction
time.”
71 “Iwasverysmallwhenthehuntingstartedhere,butIremembermydadandgranddadgoinghunting.They ±1950 >1960 1967’slawandgiantotter
wouldtellmehowtheyhunted,andsaidthatthewhitesbegantoappeararoundabout1950.” extinction
62 “Myself,Ididn’tactuallyhunt.Myfathersaidthatinthetimebeforehegotmarriedmanypeopleweretakento ±1950 >1960 Giantotterextinction
workinBarcelos.Thatstoppedaround1950,whichwaswhenthehuntingandthetradingstartedhere.”
59 “Idon’trememberthedates,butIwasalreadygrownupwhentherivertradersarrivedhereinAyarilookingfor ±1966 1969 Giantotterextinction
skins.Iwasalreadyfishingatthetime.Iwasabout12whentheyfirstappeared.”
66 “ItwaswhenSophieMullerarrivedthatthewhitetradersarrivedandstartedtradingontheRioIc¸ana.However, ±1954 <1960 Giantotterextinction
huntingofgiantottersonlyhappenedafterwards.Thosetraderscameabout10yearslater”
62 “I’mnotreallysurewhenthehuntingstartedhere.ButbythetimeIwas14,therewerealreadywhitetraders <1967 ±1972 Giantotterextinction
comingtothecommunitieslookingtobuyskins.Weswappedtheskinsforsalt,sugar,soap...”
62 “Myfathersaidthatwhenheandhisbrothersfoundedthiscommunity,therewerealreadytradersintheregion 1925 >1960 Giantotterextinction
lookingforskinsofgiantotter,riverotter,jaguar...”
59 “Mygrandfathersaidthatwhenhearrivedinthecommunity(1925)therewerealreadyrivertradersinthe ±1956 >1970 Giantotterextinction
region,buttherewerefew.ItwasinJuscelino’stimethatthetradeinskinsreallybegan.”
52 “WhenIwasborn,therewerenolongeranygiantottersintheregion.Butmydadtoldmethathewouldgoand <1955 1963 Giantotterextinction
huntuponPama´aliCreekbeforemovinghere.”
63 “Imusthavebeenlessthan10,butIremembertheIc¸anafullofwhitetraders’boats,insearchofskinsofjaguar, >1955 >1960 Giantotterextinction
margay,riverotterandgiantotter.Thetradelastednearly10years,untiltheanimalsdisappearedfromaround
here.No-onesawgiantottersagain.”
https://doi.org/10.1371/journal.pone.0193984.t001
whenencountered.Atfirst,theBaniwahuntedwithbow-and-arroworusedacone-shaped
trapcalleddzaarokanainBaniwa(matapiinPortuguese)madefromMauritiaflexuosapalm
fibers,traditionallyusedtocatchfishinriverrapids[42].Theywouldfollowgiantotters
groupsalldayinordertolocatetheden.Whenusingbowsandarrows,orlaterrifles,hunters
wouldcampoutandwaituntilsunrise,killingasmanyofthegroupaspossiblewhenthey
emerged.Whenusingthematapi,theyplacedthetrapatthedenentranceatnightfall,trapping
theentiregroupwhenitemergedthenextmorning(Fig4).Trapswereveryefficientand
ensuredhigherqualitypelts(andhigherprices)withoutarrowholes.However,cartridgesand
gunpowderbecamethemainformofpaymentforpelts,replacingtraditionalhuntingtech-
niqueswithfirearmsandprobablyincreasinghuntingsuccess[20].
“Westoppedhuntingbecausetherewerenomoregiantotterstohunt.Theyfledtothe
streamheadwaterswherenohunterscouldgetthemWecontinuedhuntingneotropical
otters,therewerestillplentyofthose.”
Lu´cioPereiraPaiva(59years-old,Arapassocommunity).
ThehuntingboomfortheBaniwawasshort-lived.Accordingtooralhistories,inthemid-
dle1960sgiantotterpopulationsalongtheIc¸anabegantodeclineprecipitously.Bytheearly
1970stherewerenomoregiantotterstobefoundonthemiddleIc¸ana.Apparently,surviving
giantottergroupsmovedtoremotestreamheadwaters,whichbecamerefugeareasforthespe-
cies[36].Neotropicalotterspersistedatlowerdensitiesthanbeforethehuntingboom.How-
ever,lowerprices,andtheultimatecollapseofthefurtrade,madethespecieslessattractivefor
commercialharvest.Forasummarytimelineofthesehistoricalevents,seeFig5.
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DifferentialresilienceofAmazonianotterstocommercialhunting
Fig4.Huntingwithmatapifishingtrap.Duringtheheydayofthe20thcenturyfurtrade,Baniwahunterscapturedgiantottersbyplacingthematapitrapattheentrance
totheden(IllustrationbyRamiroMelinski).
https://doi.org/10.1371/journal.pone.0193984.g004
“WeBaniwadidn’thunttheotters.Wedon’teattheseanimals.Itwasthewhitepeoplewho
toldustohuntthemtotaketheirskins.Oncethewhitepeopleleftnoonehereeverhunted
themagain,andthat’swhythey’recomingbacknow.”
Alberto(84years-old,JanduCachoeiracommunity)
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DifferentialresilienceofAmazonianotterstocommercialhunting
Fig5.Timelineofhistoricalevents.National,internationalandregionalhistoricaleventsreconstructedbasedonethnographicinformationandBaniwaoralhistories
concerningthecommercialhuntingfortheinternationalfurtradeinthelate20thcentury.
https://doi.org/10.1371/journal.pone.0193984.g005
HarvesttrendsintheotterfurtradeontheRioNegro
OuranalysisofhistoricalrecordsofotterpeltslandedattheportofManausbetween1936and
1968fromtheRioNegro(Fig6)confirmsthedirecttestimoniesofBaniwahuntersconcerning
thedifferentialimpactsofcommercialhuntingontwospeciesofAmazonianotters.From1936
to1953therewasadeclineof64%inthenumberofgiantotterpeltsand76%inneotropical
otterpeltstradedbyJ.G.Araujo’scommercialfleet(Table2),despitecontinuingdemandand
highprices.Datagleanedfromtheportnewspaperfrom1958to1968showaseveredeclineof
90%inthenumberofgiantotterpeltslanded.However,despiteanoveralldeclineof39%in
neotropicalotterpeltsinthesecondtimeseries(Table2),therewasasignificantincreaseinthe
numberofpeltsofthisspeciesinthemid-1960s,coincidingwithasecondpeakininternational
demandfromthefashionindustry[2].Wepresumethatthelessvaluableandmoreelusiveneo-
tropicalotterbecamethetargetspeciesasgiantotterpopulationsweredrivenextinctinaccessi-
blelocalities,aswaspreviouslyreportedina1985investigationofthecontinuingillegalinpelts
inBrazildespitethelegalprohibition[43].
AlthoughotterlandingsfromthelowerandmiddleNegrodecreaseoverallfrom1936–1968,
theportofSta.Izabel,themaincenterofcommercefortheupperRioNegroatthetime,shows
aslightincreaseingiantotterpeltlandingsduringthe1950s(Fig7),thoughstillattainingless
PLOSONE|https://doi.org/10.1371/journal.pone.0193984 March30,2018 10/19