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Estimating the global conservation status of over 15000 Amazonian tree species PDF

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RESEARCH ARTICLE ECOLOGY 2015©TheAuthors,somerightsreserved; exclusivelicenseeAmericanAssociationfor Estimating the global conservation status of theAdvancementofScience.Distributed underaCreativeCommonsAttribution more than 15,000 Amazonian tree species NonCommercialLicense4.0(CCBY-NC). 10.1126/sciadv.1500936 HansterSteege,1,2*NigelC.A.Pitman,3,4TimothyJ.Killeen,5WilliamF.Laurance,6CarlosA.Peres,7JuanErnestoGuevara,8,9 Rafael P.Salomão,10 Carolina V.Castilho,11 Iêda Leão Amaral,12 Francisca Dionízia de Almeida Matos,12 Luiz de Souza Coelho,12 William E. Magnusson,13 Oliver L. Phillips,14 Diogenes de Andrade Lima Filho,12 MarcelodeJesusVeigaCarim,15MarianaVictóriaIrume,12MariaPiresMartins,12Jean-FrançoisMolino,16DanielSabatier,16 Florian Wittmann,17 Dairon CárdenasLópez,18 José Renan da Silva Guimarães,15 Abel Monteagudo Mendoza,19 Percy Núñez Vargas,20 Angelo Gilberto Manzatto,21 Neidiane Farias Costa Reis,22 John Terborgh,4 Katia Regina Casula,22 Juan Carlos Montero,12,23 Ted R.Feldpausch,14,24 Euridice N.Honorio Coronado,14,25 Alvaro Javier Duque Montoya,26 Charles Eugene Zartman,12 Bonifacio Mostacedo,27 Rodolfo Vasquez,19 Rafael L.Assis,28 Marcelo Brilhante Medeiros,29 Marcelo Fragomeni Simon,29 Ana Andrade,30 José Luís Camargo,30 Susan G.W. Laurance,6 D Henrique Eduardo Mendonça Nascimento,12 Beatriz S. Marimon,31 Ben-Hur Marimon Jr.,31 Flávia Costa,13 o w Natalia Targhetta,28 Ima Célia Guimarães Vieira,10 Roel Brienen,14 Hernán Castellanos,32 Joost F. Duivenvoorden,33 n HugoF.Mogollón,34MariaTeresaFernandezPiedade,28GerardoA.AymardC.,35JamesA.Comiskey,36GabrielDamasco,8 lo a NállarettDávila,37RooseveltGarcía-Villacorta,38,39PabloRobertoStevensonDiaz,40AlbertoVincentini,13ThaiseEmilio,13,41 de CDaarvoidlinNaeLilel,v44is,A13le,4j2anJudlrioanAaraSuchjoie-Mttui,1r3akParmisci,i4la5 LSuozumzail,a13AArlrfooynos,o45AFleornnsaon,4d3aFAranntucinsceosCDaarlvlmalehioe,r1,343FeLrenaannddraoCVoaelllehoFeSroreuizraa,,1130 d fro m DárioDantasdoAmaral,10RogerioGribel,46BrunoGarciaLuize,47MarceloPetratiPansonato,13EduardoVenticinque,48 h PaulFine,8MarisolToledo,23ChrisBaraloto,49,50CarlosCerón,51JulienEngel,52TerryW.Henkel,53ElianaM.Jimenez,54 ttp PaulMaas,55MariaCristinaPeñuelaMora,56PascalPetronelli,49JuanDavidCardenasRevilla,12MarcosSilveira,57 ://a JulianaStropp,58,59RaquelThomas-Caesar,60TimR.Baker,14DougDaly,61MarcosRíosParedes,62NaaraFerreiradaSilva,28 d v AlfredoFuentes,63PeterMøllerJørgensen,64JochenSchöngart,17MilesR.Silman,65NicolásCastañoArboleda,18 an BrunoBarçanteLadvocatCintra,28FernandoCornejoValverde,66AnthonyDiFiore,67JuanFernandoPhillips,68 ce s TindeR.vanAndel,1PatriciovonHildebrand,69EdelcilioMarquesBarbosa,12LuizCarlosdeMatosBonates,12 .s DeborahdeCastro,28EmanuelledeSousaFarias,70TheranyGonzales,71Jean-LouisGuillaumet,72BruceHoffman,73 cie YadvinderMalhi,74IresPauladeAndradeMiranda,12AdrianaPrieto,75AgustínRudas,75AdemirR.Ruschell,76NatalinoSilva,77 nc e CésarI.A.Vela,78VincentA.Vos,79,80EgléeL.Zent,81StanfordZent,81AngelaCano,40MarceloTrindadeNascimento,82 m AlexandreA.Oliveira,83HirmaRamirez-Angulo,84JoséFerreiraRamos,12RodrigoSierra,85MiltonTirado,85 ag MariaNataliaUmañaMedina,86GeertjevanderHeijden,87EmilioVilanovaTorre,84CorineVriesendorp,3OpheliaWang,88 .o r KennethR.Young,89ClaudiaBaider,83,90HenrikBalslev,91NataliadeCastro,28WilliamFarfan-Rios,65CidFerreira,12 og/ CasimiroMendoza,92,93ItaloMesones,8ArmandoTorres-Lezama,84LigiaEstelaUrregoGiraldo,26DanielVillarroel,45 n RoderickZagt,94MiguelN.Alexiades,95KarinaGarcia-Cabrera,65LionelHernandez,96IsauHuamantupa-Chuquimaco,20 A p WAdileliialzmaFMeillilpikeenSa,9m7pWaaiolt,e9r9PElavliasciHo.sVCauldenercraa,9m8aSuSsaanmdoarvaPla,1n01s,i1n0i2,9L9uDisanViaelleanPzuauellaetGtoa,1m00arFrrae1d9dyRamirezArevalo,101 ril 4, 2 0 1 6 EstimatesofextinctionriskforAmazonianplantandanimalspeciesarerareandnotoftenincorporatedintoland-use policyandconservationplanning.Weoverlayspatialdistributionmodelswithhistoricalandprojecteddeforestationto showthatatleast36%andupto57%ofallAmazoniantreespeciesarelikelytoqualifyasgloballythreatenedunder InternationalUnionforConservationofNature(IUCN)RedListcriteria.Ifconfirmed,theseresultswouldincreasethenum- berofthreatenedplantspeciesonEarthby22%.WeshowthatthetrendsobservedinAmazoniaapplytotreesthrough- outthetropics,andwepredictthatmostoftheworld’s>40,000tropicaltreespeciesnowqualifyasgloballythreatened.A gapanalysissuggeststhatexistingAmazonianprotectedareasandindigenousterritorieswillprotectviablepopulations ofmostthreatenedspeciesiftheseareassuffernofurtherdegradation,highlightingthekeyrolesthatprotectedareas, indigenouspeoples,andimprovedgovernancecanplayinpreventinglarge-scaleextinctionsinthetropicsinthiscentury. INTRODUCTION level, where they include soil erosion (3, 4), diminished ecosystem Amazonian forests have lost ~12% of their original extent and are services (5–8),alteredclimatic patterns (5,7, 9–11), andhabitat degra- projected to lose another 9 to 28% by 2050 (1, 2). The consequences dation.Bycontrast,littleisknownabouthowhistoricalforestlosshas ofongoingforestlossinAmazonia(hereallrainforestsoftheAmazon affectedthepopulationsizesofplantandanimalspeciesinthebasin basinandGuianaShield)arerelativelywellunderstoodattheecosystem andhowongoingdeforestationwillaffectthesepopulationsinthefuture. terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 1of10 RESEARCH ARTICLE Asaresult,theconservationstatusofthe>15,000speciesthatcom- tionalUnionforConservationofNature(IUCN)RedList.Twopre- posetheAmazoniantreeflora—oneofthemostdiverseplantcommu- vious studies have attempted to estimate the extinction threat to nitiesonEarth—remainsunknown.Todate,onlyatinyproportionof Amazonianplantsusingtheory,data,andvegetationmapstomodelre- AmazoniantreespecieshavebeenformallyassessedfortheInterna- ductionsinrangesize,buttheydisagreedonwhethertheproportionof 1BiodiversityDynamics,NaturalisBiodiversityCenter,Darwinbuilding,Darwinweg4,Leiden 97379,FrenchGuiana.50InternationalCenterforTropicalBotany(ICTB),FloridaInternational 2300AA,TheNetherlands.2EcologyandBiodiversityGroup,UtrechtUniversity,Padualaan8, University, 11200SW8thStreet, OE167, Miami, FL33199, USA.51EscueladeBiología Utrecht,Netherlands.3ScienceandEducation,TheFieldMuseum,1400S.LakeShoreDrive, Herbario Alfredo Paredes, Universidad Central, Ap. Postal 17.01.2177, Quito, Pichincha, Chicago,IL60605–2496,USA.4CenterforTropicalConservation,DukeUniversity,Nicholas Ecuador.52UMREcologiedesForêtsdeGuyane,CNRS,KourouCedex,FrenchGuiana. SchooloftheEnvironment, Durham,NC27708, USA. 5Agteca-Amazonica,SantaCruz, 53DepartmentofBiologicalSciences,HumboldtStateUniversity,1HarpstStreet,Arcata,CA Bolivia.6CentreforTropicalEnvironmentalandSustainabilityScience,CollegeofMarine 95521,USA.54GrupodeEcologíadeEcosistemasTerrestresTropicales,UniversidadNacional andEnvironmentalSciences,JamesCookUniversity,Cairns,Queensland4870,Australia. deColombiaSedeAmazonía,Leticia,Amazonas,Colombia.55TaxonomyandSystematics, 7SchoolofEnvironmentalSciences,UniversityofEastAnglia,NorwichNR47TJ,UK. NaturalisBiodiversityCenter,Darwinbuilding,Darwinweg4,Leiden2300AA,TheNeth- 8DepartmentofIntegrativeBiology,UniversityofCalifornia,Berkeley,CA94720–3140, erlands.56UniversidadRegionalAmazónicaIKIAM,Km7viaMuyuna,Tena,Napo,Ecuador. USA.9MuseoEcuatorianodeCienciasNaturales,Av.RíoCocaE6-115eIslaFloreana, 57MuseuUniversitário,UniversidadeFederaldoAcre,RioBranco,AC69915–559,Brazil. Quito,Ecuador.10CoordenaçãodeBotânica,MuseuParaenseEmilioGoeldi,Av.Magalhaes 58Land Resource and Management Unit, Joint Research Centre of the European Barata376,C.P.399,Belém,PA66040–170,Brazil.11EMBRAPA–CentrodePesquisaAgroflorestal Commission,ViaEnricoFermi2749,TP440,Ispra,VAI-21027,Italy.59InstituteofBiological deRoraima,BR174,km8–DistritoIndustrial,BoaVista,RR69301–970,Brazil.12Coordenação andHealthSciences,FederalUniversityofAlagoas,Av.LourivalMeloMota,s/n,Tabuleirodo D deBiodiversidade,InstitutoNacionaldePesquisasdaAmazônia-INPA,Av.AndréAraújo, Martins,Maceio,AL57072–970,Brazil.60IwokramaInternationalProgrammeforRainforest o 2936,Petrópolis,Manaus,AM69060–001,Brazil.13CoordenaçãodePesquisasemEcologia, Conservation,Georgetown,Guyana.61NewYorkBotanicalGarden,2900SouthernBlvd, w InstitutoNacionaldePesquisasdaAmazônia-INPA,Av.AndréAraújo,2936,Petrópolis, Bronx,NewYork,NY10458–5126,USA.62ServiciosdeBiodiversidadEIRL,Iquitos,Loreto, nlo Manaus,AM69060–001,Brazil.14SchoolofGeography,UniversityofLeeds,Woodhouse Peru.63HerbarioNacionaldeBolivia,UniversitarioUMSA,Casilla10077CorreoCentral,La a Lane,LeedsLS29JT,UK.15InstitutodePesquisasCientíficaseTecnológicasdoAmapá-IEPA, Paz,Bolivia.64MissouriBotanicalGarden,P.O.Box299,St.Louis,MO63166–0299,USA. d e Av.FelicianoCoelho,1509.Trem,Macapá,Amapá68901–025,Brazil.16UMRAMAP,Institut 65BiologyDepartmentandCenterforEnergy,EnvironmentandSustainability,WakeForest d de Recherche pour le Développement (IRD), TA 40/PS2, Boulevard de la Lironde, University,1834WakeForestRd,WinstonSalem,NC27106,USA.66AndestoAmazon fr MontpellierCedex534398,France.17Biogeochemistry,MaxPlanckInstituteforChemistry, BiodiversityProgram,MadredeDios,MadredeDios,Peru.67DepartmentofAnthropology, o m Hahn-MeitnerWeg1,Mainz55128,Germany.18HerbarioAmazónicoColombiano,Instituto UniversityofTexasatAustin,SAC5.150,2201SpeedwayStopC3200,Austin,TX78712,USA. SINCHI,Calle20No5,Bogotá,DF44,Colombia.19JardínBotánicodeMissouri,Oxapampa, 68Fundación Puerto Rastrojo, Cra 10 No. 24–76 Oficina 1201, Bogotá, DF, Colombia. h Pasco,Peru.20HerbarioVargas,UniversidadNacionaldeSanAntonioAbaddelCusco,Avenida 69FundaciónEstacióndeBiología,Cra10No.24–76Oficina1201,Bogotá,DF,Colombia. ttp ddeelRaoCnudlôtunriaa,,NRrood7o3v3ia,CBuRs3co64,Csu/nzcKom,Pe9r,5u.-2S1DenetpidaortaAmcreen,tUondire,PBoiortloogViae,lhUon,iRveornsdidôandieaF7e6d.8e2r4a-l 7L0eLôanbiodraastóeriMoardiaeDEecaonloeg,Fiaiocdreuz,DRoueanTçearsezTinraan,s4m76is,sAívderiisandóapoAlims,aMzôannaiaus(,EADMTA6)9,0I5n7st–it0u7t0o, ://a d 027,Brazil.22ProgramadePós-GraduaçãoemDesenvolvimentoRegionaleMeioAmbiente Brazil.71ACEERFoundation,JirónCuscoN°370,PuertoMaldonado,MadredeDios,Peru. v PGDRA,UniversidadeFederaldeRondônia,RodoviaBR364s/nKm9,5-SentidoAcre,Unir, 72DepartementEV,Muséumnationald’histoirenaturelledeParis,16rueBuffon,Paris75005, an Porto Velho, Rondônia 76.824-028, Brazil. 23Instituto Boliviano de Investigacion Forestal, France. 73Amazon Conservation Team, Doekhieweg Oost #24, Paramaribo, Suriname. c UniversidadAutónomaGabrielRenéMoreno,Km9CarreteraalNorte,ElVallecito,FCA- 74EnvironmentalChangeInstitute,OxfordUniversityCentrefortheEnvironment,Dyson es UAGRM,SantaCruz,Bolivia.24CollegeofLifeandEnvironmentalSciences,UniversityofExeter, PerrinsBuilding,SouthParksRoad,Oxford,EnglandOX13QY,UK.75InstitutodeCiencias .s EQxueitñeornEeXs4km4R.J2,.5U,IKq.u2it5oInss,tLitourteotod,ePeIrnuv.e2s6tDigeapcaiortnamesendteoldaeACmieanzcoiansíaFoPreersutaanleas,,UAnv.ivJeorssiédaAd. 7N6aEtmurbarleaps,aUANmALa,zUonniivaeOrsridieandtaNl,aTcriaovn.aDldr.eECnoéalosmPbiniah,eAirpoasrt/andoo,B7e9l4é5m,,BPoAg,oBtára,DziFl.,7C7oUlnoimvebrsiai-. cien NacionaldeColombia,Calle64xCra65,Medellín,Antioquia1027,Colombia.27Facultadde dadeFederalRuraldaAmazônia,Belém,PA,Brazil.78FacultaddeCienciasForestalesyMedio c e Ciencias Agrícolas, Universidad Autónoma Gabriel René Moreno, Santa Cruz, Bolivia. Ambiente,UniversidadNacionaldeSanAntonioAbaddelCusco,SanMartín451,Puerto m 28CoordenaçãodeDinâmicaAmbiental,InstitutoNacionaldePesquisasdaAmazônia- Maldonado,MadredeDios,Peru.79UniversidadAutónomadelBeni,Riberalta,Beni,Bolivia. a INPA, Av. André Araújo, 2936, Petrópolis, Manaus, AM 69060–001, Brazil. 29Prédio da 80RegionalNorteAmazónico,CentrodeInvestigaciónyPromocióndelCampesinado,Ri- g Botânica e Ecologia, Embrapa Recursos Genéticos e Biotecnologia, Parque Estaccao beralta,Beni,Bolivia.81LaboratoryofHumanEcology,InstitutoVenezolanodeInvestiga- .o r Biologica,Av.W5Norte,Brasilia,DF70770–917,Brazil.30ProjetoDinâmicaBiológicade cionesCientíficas-IVIC,Ado20632,Caracas1020A,Venezuela.82LaboratóriodeCiências g FragmentosFlorestais,InstitutoNacionaldePesquisasdaAmazônia-INPA,Av.André Ambientais,UniversidadeEstadualdoNorteFluminense,Av.AlbertoLamego2000,Campos o/ Araújo, 2936, Petrópolis, Manaus, AM 69060–001, Brazil. 31Departamento de Ciências dosGoyatacazes,RJ28013–620,Brazil.83InstitutodeBiociências-Dept.Ecologia,Univer- n Biológicas, Universidade do Estado de Mato Grosso, Nova Xavantina, MT, Brazil. sidadedeSaoPaulo-USP,RuadoMatão,Trav.14,no.321,CidadeUniversitária,SãoPaulo, A 32UniversidadNacionalExperimentaldeGuayana,CalleChile,urbanizChilemex,Puerto SP05508–090,Brazil.84InstitutodeInvestigacionesparaelDesarrolloForestal(INDEFOR), pr Ordaz,Bolivar,Venezuela.33InstituteofBiodiversityandEcosystemDynamics,Universityof UniversidaddelosAndes,ConjuntoForestal,C.P.5101,Mérida,Mérida,Venezuela. il 4 A34mEnsdtearndgaemre,dScSipeenccieepsaCroka9lit0io4,n,A8m53s0teGrdearmen,RNdo.,oSridlveHroSpllarinndg,1M0D9820X9H0,1,TUhSeA.N3e5Pthroegrlaranmdsa. 8B5ioGleoogIyS,,UEnliDveíars3it6y9oyfMElarTyelaléngdr,aCfoo,ll3e°gePiPsoar,kQ,MuiDto2,0P7ic4h2i,nUcShAa,.8E7cDueapdaorrt.m86eDnetpoafrBtimoleongticoafl , 2 0 deCienciasdelAgroyelMar,HerbarioUniversitario(PORT),UNELLEZ-Guanare,Guanare, Sciences,UniversityofWisconsin-Milwaukee,Milwaukee,WI53202,USA.88Environmental 1 Portuguesa3350,Venezuela.36InventoryandMonitoringProgram,NationalParkService, ScienceandPolicy,NorthernArizonaUniversity,Flagstaff,AZ86011,USA.89Geography 6 120ChathamLane,Fredericksburg,VA22405,USA.37BiologiaVegetal,UniversidadeEstadual andtheEnvironment,UniversityofTexasatAustin,305E.23rdStreet,CLAbuilding,Aus- deCampinas,CaixaPostal6109,Campinas,SP13.083-970,Brazil.38InstituteofMolecular tin,TX78712,USA.90AgriculturalServices,MinistryofAgro-IndustryandFoodSecurity, PlantSciences,UniversityofEdinburgh,MayfieldRd,EdinburghEH35LR,UK.39RoyalBotanic TheMauritiusHerbarium,Reduit,Mauritius.91DepartmentofBioscience,AarhusUniver- GardenofEdinburgh,20aInverleithRow,EdinburghEH35LR,UK.40LaboratoriodeEcología sity,Building1540NyMunkegade,AarhusC,AarhusDK-8000,Denmark.92FOMABO, deBosquesTropicalesyPrimatología,UniversidaddelosAndes,Bogotá,DF,Colombia. ManejoForestalenlasTierrasTropicalesdeBolivia,Sacta,Cochabamba,Bolivia.93Escuela 41ComparativePlantandFungalBiology,RoyalBotanicGardens,Kew,Richmond,Surrey deCienciasForestales(ESFOR),UniversidadMayordeSanSimon(UMSS),Sacta,Cochabamba, TW93AB,UK.42ForestEcologyandForestManagementGroup,UniversityofWageningen, Bolivia.94TropenbosInternational,LawickseAllee11POBox232,Wageningen6700AE,The Lumen, building no.100, Droevendaalsesteeg 3, Wageningen 6708 PB, Netherlands. Netherlands.95SchoolofAnthropologyandConservation,UniversityofKent,Marlowe 43CenterforConservationEducationandSustainability,SmithsonianConservationBiology Building,Canterbury,KentCT27NR,UK.96CentrodeInvestigacionesEcológicasdeGuayana, Institute, National Zoological Park, MRC 0705, Washington, DC 20013–7012, USA. UniversidadNacionalExperimentaldeGuayana,CalleChileurbanizChilemex,PuertoOrdaz, 44Ecosistemas,BiodiversidadyConservacióndeEspecies,UniversidadEstatalAmazónica, Bolivar,Venezuela.97ComparativePlantandFungalBiology,RoyalBotanicGardens,Kew, Km.21/2víaaTena(PasoLateral),Puyo,Pastaza,Ecuador.45MuseodeHistoriaNaturalNoel Richmond,SurreyTW93AE,UK.98HerbarioNacionaldelEcuador,UniversidadTécnicadel KempffMercado,UniversidadAutónomaGabrielReneMoreno,AvenidaIrala565Casilla Norte,Quito,Pichincha,Ecuador.99ProgramadePós-GraduaçãoemDesenvolvimento Postal2489,SantaCruz,Bolivia.46DiretoriadePesquisasCientíficas,InstitutodePesquisas RegionaleMeioAmbientePGDRA,UniversidadeFederaldeRondônia,RodoviaBR364 JardimBotânicodoRiodeJaneiro,RiodeJaneiro,RJ,Brazil.47CoordenaçãodeTecnologiae s/nKm9,5-SentidoAcre,Unir,PortoVelho,Rondônia76.824-029,Brazil.100Institutode Inovação,InstitutoNacionaldePesquisasdaAmazônia-INPA,Av.AndréAraújo,2936, BiodiversidadeeFloresta,UniversidadeFederaldoOestedoPará,RuaVeraPaz,Campus Petrópolis, Manaus, AM 69060–001, Brazil. 48Centro de Biociências, Departamento de Tapajós,Santarém,PA68015–110,Brazil.101FacultaddeBiologia,UniversidadNacionalde Ecologia,UniversidadeFederaldoRioGrandedoNorte-UFRN,CampusUniversitário- laAmazoniaPeruana,Pevas5tacdra,Iquitos,Peru.102DepartmentofBiology,Universityof LagoaNova,Natal,RN59072–970,Brazil.49UMREcologiedesForêtsdeGuyane,Institut Missouri,St.Louis,MO63121,USA. Nationalde laRechercheAgronomique (INRA), Campus agronomique, Kourou Cedex *Correspondingauthor.E-mail:[email protected] terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 2of10 RESEARCH ARTICLE threatenedplantspeciesintheAmazonislow(5to9%)(12)ormoderate thecurrencyofstatisticalprobabilityofextinction,weinterpretourresults (20to33%)(13). usingthecriteriaoftheIUCNRedListofThreatenedSpecies,themost Here,webuildonthatworkbyusingaspatiallyexplicitmodeloftree commonlyusedyardstickforspeciesconservationstatus. speciesabundance(14)basedon1485forestinventories(fig.S1)toquan- tifyhowhistoricaldeforestationacrossAmazonia(1,2,15)hasreduced thepopulationsizesof4953relativelycommontreespecies.Weusea RESULTS separatemodeltoestimatepopulationdeclinesforanadditional10,247 rarertreespecies.Forbothmodels,wealsoestimatethepopulationlosses Effects of historical forest loss on tree populations expectedfor2050undertwodeforestationscenarios(1,2)andasktowhat The original lowland forests of Amazonia are estimated to have extentprojectedlossescanbepreventedbyAmazonia’sexistingprotected covered5.74millionkm2(fig.S2),11.4%ofwhichhadbeendeforested areanetwork.Incontrasttopreviousstudies,whichpresentedresultsin by2013(1,2)(figs.S3andS4AandappendixS1).Mostoftheestimated Forest loss Forest loss 1900– Forest loss 1900– 1900–2013 2050 (BAU) 2050 (IGS) D o A D G w n lo a d e Population d declines by fro m region h ttp ://a d v a n c e B E H s.s c ie n c % Threatened e m species by a g degree grid cell .or g o/ n A p r il 4 C F I , 2 A2 0 9% 1 6 A4 22% D1 16% A4 C1 % All Amazonian Not threatened 46% 0% 43% spp. threatened Not threatened D1 Not threatened 64% 14% 75% D1 11% C1 0% Fig.1. EstimatedpopulationdeclinesandthreatstatusofAmazoniantreespeciesunderhistoricaldeforestationandtwoprojecteddeforestation scenarios.Historicaldeforestation(AtoC).Projecteddeforestation(DtoI).Toprow:Percentpopulationlossof4953treespeciesintheentireAmazonandin sixAmazonianregions.Middlerow:PercentspeciesinaDGCestimatedasgloballythreatenedbasedonprojected(includinghistorical)forestloss(IUCNA2 andA4;n=4953).Bottomrow:Proportionofall15,200AmazoniantreespeciesestimatedtobegloballythreatenedbasedonfourdifferentIUCNthreat criteria.BAU:projected(includinghistorical)deforestationthrough2050basedonaBAUscenario(1,2);IGS:projected(includinghistorical)deforestation through2050basedonanIGS(1,2).CristalinoStateParkisthesmallblackpolygoninsoutheasternAmazonia,encircledin(B).CA,CentralAmazonia;GS, GuianaShield;WAS,SouthwesternAmazonia;WAN,NorthwesternAmazonia;SA,SouthernAmazonia;EA,EasternAmazonia;CR,criticallyendangered;EN, endangered;VU,vulnerable. terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 3of10 RESEARCH ARTICLE 3.2×1010individualtreeslosttodate(appendixesS2andS3)werein For common species, mean population declines under the BAU southernandeasternAmazonia(Fig.1A). scenarioareestimatedtobe35%(median,32%),andabsolutedeclines Overlayingthesedeforestationdatawiththeoutputofourspatial rangefrom0to83%(Fig.1D,fig.S4E,andappendixesS2andS3).Un- modelofthedistributionandabundanceof4953relativelycommon dertheBAUscenario,2567(51%)ofallcommonspecieslikelyqualify tree species allowed us to estimate the impact of forest loss on the asthreatenedunderIUCNcriterionA4(Fig.1D).UnderIGS,average Amazonianpopulationsofthesespecies.Forestlossupto2013(figs. lossesarelower,withameanof20%(median,18%)andarangeof0 S3andS4A)causedameandeclineof11%inthenumberofindividuals to 82% (fig. S4F and appendixes S2 and S3); 774 (16%) of common of tree species across Amazonia (median, 6%) (Fig. 1A and fig. S4D) specieslikelyqualifyasthreatened(Fig.1G).Again,theseverestthreat and mean declines of 2 to 32% in individual Amazonian regions. Of is foundin southernandeasternAmazonia(Fig.1G andfig.S4D). 4953commonspecies,342(7.5%)havelostalargeenoughproportion Both scenarios also pose severe threats to rare species. Under the oftheiroriginalpopulations(≥30%)toqualifyasgloballythreatened BAU scenario, 4466 (43%) of all rare species are predicted to lose underIUCNcriterionA2(Fig.1AandappendixS2).Aseparateanal- ≥30%oftheirpopulationby2050(fig.S5BandtableS1),compared ysisperformedtomodelthedistributionandextinctionriskof10,247 to 2590 (25%) of all rare species under IGS (fig. S5C and table S1). raretreespeciesintheAmazonsuggestedthat9%ofthem(atotalof UndertheBAUscenario,rarespeciesareexpectedtobemostseverely 967species)havelostenoughindividualstoqualifyasgloballythreatened hitinsouthernandeasternAmazonia,wherethemedianpopulation underthesamecriterion(fig.S5AandtableS1).Together,theseanaly- loss is 100% and more than 65 and 86% of the species, respectively, D o ses suggest that 9% of all Amazonian tree species likely qualify as have population lossesofmorethan80%(tableS1). w n threatenedasaresultofhistoricalforestlossthrough2013(Fig.1C). Combiningtheanalysesofcommonandrarespeciessuggeststhat lo Adding the 2579rare species thatmayqualifyas threatenedbecause 3364to7033Amazoniantreespecieslikelyqualifyasgloballythreatened a d they have an estimated <1000 individuals (IUCN criterion D1) in- asaresultofacombinationofhistoricalandprojectedforestloss(Fig.1,F e d creases theproportionof all threatenedspecies to 25% (Table 1). andI).Anadditional1657to2151speciesinthedatasetarelikelyto fr o The data in fig. S4 (A and D) suggest a one-to-one relationship qualifyasgloballythreatenedbecausetheyhaveverysmallpopulation m between percent historical forest loss and mean percent loss of indi- sizes(IUCNcriteriaC1andD1).Whenallcriteriaareincluded,wefind h vidualstodate.Consequently,populationlossesofthecommonspecies that36to57%ofAmazoniantreespecieslikelyqualifyasgloballythreat- ttp arehighestinregionswheredeforestationratesarehighest,theso-called ened(Table1). ://a “ArcofDeforestation”insouthernandeasternAmazonia.Thesame d v patternswereobservedfor rare species. Towhatdegreewillprotectedareasandindigenousterritories a n prevent declinesof Amazoniantreepopulations? c e Effects of projected forest loss on tree populations Over the last 50years, Amazonian countries have formalized alarge s .s Werepeatedthe aboveanalyses fortwoscenarios ofprojectedforest networkofprotectedareasandindigenousterritories(fig.S8andap- c ie loss (which include historical loss). The business-as-usual (BAU) pendixS1)thatnowcover52.2%ofthebasin:9%instrictconservation n c scenariomodel(1)estimatesthat,by2050,~40%oftheoriginalAmazon reserves (SCRs) (fig. S9A) and 44.3% in sustainable use and indige- e m forest will be destroyed (figs. S4B and S6 and appendix S1). The nous reserves (SUIRs) (fig. S9B). Our models suggest that all of the a improved governance scenario (IGS) model (1) estimates forest loss 4953 common species are protected to some degree by SCRs and g .o by 2050 at 21% (figs. S4C and S7 and appendix S1). Under these SUIRs (for convenience, we refer to both as protected areas) (fig. S9, r g two scenarios, only 31 to 42% of grid cells maintain >95% forest CandD).Everycommonspeciesisestimatedtohavemorethan5500 o/ cover. As is the case for historical deforestation, future deforestation adultindividualswithinprotectedareas,with23%,onaverage,ofthese n is projected to be most severe in southern and eastern Amazonia individuals occurring in SCRs and 77% in SUIRs. However, Per- A p (34to66%and42to 76%forestcoverloss,respectively). formance is poor in some Amazonian regions. For example, the ril 4 Table1.NumberofAmazoniantreespeciesestimatedtoqualifyasgloballythreatenedunderfourIUCNthreatstatuscriteria.Numbersof , 2 0 threatenedspecies are nonoverlapping (that is,species listedfor C1did notqualify for A4). BAU= projected (including historical) deforestation 1 6 through2050basedonaBAUscenario(1,2);IGS=projected(includinghistorical)deforestationthrough2050basedonanIGS(1,2). Forestloss Forestloss Forestloss 1900–2013 1900–2050(BAU) 1900–2050(IGS) Totalnumberofspecies 15,200 15,200 15,200 Numberofspecieswith>30%observedpopulationdeclinetodate(IUCNA2) 1309 — — Numberofspecieswith>30%projectedpopulationdeclineoverthreegenerations(IUCNA4) — 7033 3364 Numberofspecieswith>10%projectedpopulationdeclineoverthreegenerations — 38 44 and<10,000individuals(IUCNC1) Numberofspecieswith<1000individuals(IUCND1) 2505 1619 2107 Totalnumberofthreatenedspecies 3814 8690 5515 Percentageofallspeciesthreatened 25 57 36 terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 4of10 RESEARCH ARTICLE scarcityofSCRsincentralandeasternAmazoniameansthat,onav- most of the species thatlikely qualify as threatened in the regionre- erage,only2%ofindividualsofcommonspeciesintheseregionsare main absent from global and national red lists. For example, of the in SCRs (fig. S9, C and D). Our simulation models also suggest that 2567commonspeciesthatqualifyasthreatenedunderourBAUanal- 580ofthe10,247rarespecieshavemorethan70%oftheirindividuals ysis,only351(14%)hadpreviouslybeenassessedusingIUCNcriteria inSCRs(fig.S10AandtableS2),comparedto4005inSUIRs. and only 6% are listed as threatened. Adding all of our threatened Preventingdeforestationwithinprotectedareasbetweennowand Amazonian tree species to the IUCN Red List would increase the 2050couldsignificantlyreducethenumberofthreatenedAmazonian number of globally threatened plants on Earth by 22% and the treespeciesbecauseboth2050deforestationscenariosassumesignifi- number of globally threatened tree species by 36%. cantdeforestationwithinprotectedareas(figs.S11toS13):one-thirdof We are aware, however, that our results are too preliminary to projectedBAUdeforestationand16%ofprojectedIGSdeforestation.If constitutearedlistforAmazoniantrees.Red-listingthesespecieswill thedeforestationthatisprojectedtooccurwithinprotectedareasunder requirecase-by-caseassessmentsbytheIUCN/SpeciesSurvivalCom- theBAUscenarioandIGSisnotfactoredin,thenumberofcommon missionGlobalTreeSpecialistGroupandcountry-levelteams,taking speciesthatlikelyqualifyasthreatenedunderIUCNcriterionA4will intoaccountotherdatasourcesandthreatcriteria.Whatweshowhere fallby29to44%.Forexample,63%ofwildBrazilnuttrees(Bertholletia are the size, urgency, and feasibility of this task. A recent Brazilian excelsa)areexpectedtobelostby2050undertheBAUscenario.Under effort to evaluate the threat status of 4617 plant species in Brazil re- amodifiedIGSthatallowsfornodeforestationwithinprotectedareas, portedaper-species costof ~US$50(19). This suggests thatindivid- D o thispercentagedropsto32%,andB.excelsanolongerqualifiesasen- uallyassessingthenamedspeciesthatwesuspecttobethreatenedand w n dangered(appendixS2). making their threat status visible to the conservation community lo wouldcost<US$1,000,000. a d e d DISCUSSION Most tropical tree species may be globally threatened fro Despite strong spatial clustering in both deforestation scenarios and m Ouranalysessuggestthathistoricalandongoingforestlossmaycause speciesdistributions, our analyses reveal asimplerule of thumbthat h populationdeclinesof>30%inone-quartertoone-halfofallAmazonian worksatbothregionalandbasinwidescales: n%forestlossyieldsan ttp tree species by 2050. These declines affect species in all Amazonian averageof~n%populationloss(Fig.1andfig.S4,AandD).Thisim- ://a regions,includingiconicAmazoniantreessuchasBrazilnut(B.excelsa), pliesthattreespeciesinotherforestbiomesoftropicalSouthAmerica d v wildpopulationsofmajorfoodcropssuchascacao(Theobromacacao; havelostmuchlargerproportionsoftheirpopulationthaninthecore a n 50%populationdeclinewiththeBAUscenario)andaçaipalm(Euterpe closed-canopyAmazonianmoistforest:forexample,theAtlanticforest c e oleracea; 72% decline with the BAU scenario), and 167 of the 227 (84 to 88% forest loss) (22), the Cerrado (53%) (23), the Caatinga s .s hyperdominanttaxathataccountforhalfofallAmazoniantrees(14). (37%)(23),anddryforests ingeneral(>60%)(24). c ie Althoughthesedeclinescomprisebothhistoricalpopulationlossesand GiventhatAfricahaslost~55%ofitstropicalforestsandAsiahas n c populationlossesprojectedtooccurinthefuture,theycouldbeusedto lost~35%,mostlysince1900(25),ouranalysessuggestthatmosttree e m classifythesespeciesasthreatenednowunderIUCNcriterionA4b. species in the Old World tropics have lost more than 30% of their a ThousandsofotherAmazoniantreespeciesarelikelytoqualifyas individualsoverthelast150yearsandthusqualifyasgloballythreat- g .o globallythreatenedbecausetheyhaveverysmallpopulations(Table1). enedunderIUCNcriterionA4.Inturn,because>90%ofalltreespe- r g Although our methods and results are preliminary (see the Supple- ciesonEartharetropical(26),treesmaydeservetojoincycads(63%), o/ mentaryMaterials),thestatisticalindependencethatwefindbetween amphibians (41%), and corals (33%) on the list of groups with the n theestimatedpopulationsizeofaspeciesanditsfractionaldeclinein highest proportions of globallythreatenedspecies. A p nbluemabsesrasm(fpigli.nSg14im)psuroggveesst.sthattheprimaryfindingswillremainsta- withAlathnoimugahlsmanadnycot-roocpciucarlwtriethe sthpoecuiseasnhdasvoefssypmecbiieostiocfrneolantiaornbsohriepasl ril 4 plants,highratesofthreatcannotbeinferredfor theseorganismsin , 2 0 A 22% increase in the global red list for plants thesamewaybecauseoftheirmuchshorterlifespans.Birdetal.(27) 1 6 OurestimatesofthethreatstatusofallAmazoniantreespeciesconstitute comparedestimatedrangemapsofAmazonianbirdspecieswithmaps thelargestthreatassessmentevercarriedout.Infact,thenumberofspe- ofprojecteddeforestationacrossthreebirdgenerationsandfoundthat ciesassessedinouranalyses(15,200)isnearlyaslargeasthenumber only5.5to18.8%ofspeciesqualifiedasthreatenedunderIUCNcrite- ofall plantspecies evaluated bytheIUCN overits50-yearhistory rion A4. Three bird generations in their model averaged 14.8 years, (19,738)[Table3bintheIUCNRedList(16)].Ifthe194countries comparedto150yearsinourtreemodel. thathaveadoptedtheGlobalStrategyforPlantConservationareto meettarget2(“Apreliminaryassessmentoftheconservationstatusof Linkingforestloss, speciesthreat status, andprotectedareas all known plant species” by 2020), it will require large scaling-up managementin theAmazon approachessuchastheonedescribedhere[seealsoMilleretal.(17)]. Heavy forest clearing in southern and eastern Amazonia has put an SuchapproachesareurgentlyneededforSouthAmerica’stropical especially high proportion of tree species at risk of extinction (Fig. flora. Over the last 10 years, only 1275 plant species from tropical 1A).IntheworsthitareasoftheArcofDeforestation,athirdoftree SouthAmericawereaddedtotheIUCNRedList,despitestrongev- species have already lost >30% of their population to deforestation, idencethatthenumbershouldbeatleastanorderofmagnitudehigher and more than half likely qualify as globally threatened based on (18–21). In general, our results provide strong support to predictions projected(andhistorical)forestloss (Fig. 1B). that at least one in four plant species in the South American tropics Bylinkingspatialtrendsinforestlosstotrendsinthepopulation now deserve listing as globally threatened (20). They also show that sizesofindividualAmazonianplantspeciesinthisway,modelssuch terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 5of10 RESEARCH ARTICLE asoursshouldsoonmakeitpossibletotranslateremotesensing–based ThetotalnumberoftreesinAmazoniawith≥10cmdiameterat dataonAmazoniandeforestationintosite-specificandspecies-specific breastheightwas estimatedas in our previous study (14) but with a guidanceforconservationmanagers.Itwillalsobepossibletomodel largersubsetofplots(1625)andatthe1-degreegridcell(DGC)level. howindividualspecieswillbeaffectedbyinfrastructureprojects(28) Weconstructedalocallyweighted(loess)regressionmodelfortreeden- suchasmajorhydroelectricdams(29),degazettingofprotectedareas sity(stems/ha)onthebasisoftheobservedtreedensityin1625plots, (30),andotherdriversofAmazonianforestloss.Thiscouldhavese- withlatitude,longitude,andtheirinteractionasindependentvariables. riousimplicationsforlarge-scaledevelopmentprojects,whicharein- Thespanwassetat0.5toyieldarelativelysmoothaverage.Themodel creasinglyrequiredtoprotectIUCN-listedtaxaandtheirhabitat[for was used to estimate the average tree density in each DGC (D , DGC example, Performance Standard 6. Biodiversity Conservation and stems/ha) (fig. S15). This average density per hectare was then multi- Sustainable Management of Natural Resources (31)]. pliedbythetotalforestedareaofeachDGCtoobtainthetotalnumber Thesemodelscanalsogeneratepredictionsaboutwhichplantspe- oftreesintheDGC.Thetotalnumberoftreesestimatedwas3.2×1011. cies occur in which protected areas and, thus, to what extent these Thisis17.9%lowerthantheestimateinourpreviousstudy(14)because speciesareprotectedandwhere.Forexample,floristicsurveysatCris- thisnumbercorrectsfortheactuallowlandforestcoverineachDGC. talino State Park, in one of Brazil’s most severely deforested regions, haverecordedatleast551treespecies(32).AppendixS4listsanother Modeled population sizes and species distributions: 766speciesthathaveahighprobabilityofoccurringatCristalinoState Common species D o Parkaccordingtoourmodelandshowsthatasmanyas1214ofthe Analysesoftreespeciescompositionwereperformedwithasubset w 1317speciesknownorexpectedfromCristalinoStateParklikelyqualify of 1560 plots in which all 775,532 free-standing trees ≥10 cm di- nlo asgloballythreatenedundertheBAUscenario.Similaranalysescould ameteratbreastheighthadbeenidentifiedwithavalidnameatthe a d help ensure that Amazonian protected areas with especially high species (86.0%), genus (97.2%), or family (99.0%) level before our e d numbersofgloballythreatenedtreespeciesreceivethelevelofprotec- study. Most plots (1282) measured exactly 1 ha, 392 were smaller fr o tionandfundingthey merit. (0.25to0.99),91werelarger(1.01to4),and4wereplotlesssamples m Manypracticalandscientificobstaclesstandinthewayofastable, (point-centeredquarter)forwhichthenumberoftreeswasequivalent h comprehensive red list for Amazonian tree species (see the Supple- tothattypicallyfoundin0.5to1ha.Mostissuesofspeciesidentification ttp mentaryMaterials).Wehaveshowninthisstudythatsuchalistwill andnomenclaturewerehandledasinourpreviousstudy(14),butthere ://a includeseveralthousandspecies,manyofwhicharenowconsidered weresomeexceptions.Specieswitha“cf.”identificationwereaccepted d v common, and will include a very large majority of the tree species asbelongingtothenamedspecies,whereasthosewith“aff.”weretabu- a n occurringintheAmazon’sworsthitregions.AsAmazonianforestloss latedatthegenuslevel.Alldataassociatedwithnamesthatwereclear- c e continues,newapproachessuchasthesewillbeneededtohelpguide lywrong(forexample,thoseofsmallherbs)weredisregarded. s .s management away from BAU scenarios and ensure a long-term fu- Although we assume identification error to be within acceptable c turefortheworld’srichesttreeflora.Indeed,sustainingtherecent limits for common species [see discussion in our previous paper ien historicaltrendofreducedAmazoniandeforestationthrough2050will (14)],weretainedonlyplotsinwhich≥60%ofindividualswereiden- ce m keepasmanytreespeciesfrombecomingcriticallyendangeredasthere tifiedtospecies(1480plots)(fig.S16).Thenumberoftreesbelonging a are critically endangeredplant species onthe IUCN RedListtoday. toeachspeciesintheDGCwasestimatedasfollows.Abundancesof g .o allvalidspecieswereconvertedintorelativeabundancesforeachplot: r g RAi=ni/N,whereniisthenumberofindividualsofspeciesiandNis o/ MATERIALS AND METHODS thetotalnumberoftreesintheplot(includingunidentifiedtrees)(14). n Foreachofthe4953specieswithavalidnameinthe1485plots,we A p ATomoavzeorlnaiyasnpabtiaasledamtaaopndeforestation,protectedareas,andtreespe- caopnoswtreurctoefd2a,naimnvaexrimseudmistnanucmebwereiogfhtpilnogts(IuDseWd)fomroeadcehlfloorcaRlAesi,tiwmitah- ril 4 cies distribution and abundance, we first made a base map of Ama- tionof150,andamaximumdistanceparameterof4°.Wedidnotuse , 2 0 zonia. The borders of the base map were the same as those in our aLOESSmodel(14)becausethishadtheundesirableeffectofpredicting 1 6 previous study (14). We gridded this landscape into 0.1-degree grid verysmalloccurrencesofspeciesfarfromlocalitieswherethespecies cells(01DGCs)(33)andeliminatedall01DGCsthatweremorethan wasactuallyrecorded.Forasimilarreason,weusedacutoffof4°with 50%water(33),nonforestvegetationsuchasopenwetlandsorsavannahs IDWmodelingbecause,otherwise,specieswouldhaveverylowden- (1),orelevationsof>500m(34).Thisreducedthetotalareaby17%. sities over the entire Amazon. These adjustments have a significant We then quantified the area of all individual 01DGCs, which varies effect on the ranges of species [that is, ranges here are smaller than with latitude because of distance from the equator (~124 km2 at the inourpreviousstudy(14)]butanegligibleeffectontheirtotalnumber equator, ~106 km2 at 14°S, and ~120 km2 at 8°N). The final forest ofindividuals.ThenumberofindividualsofspeciesiinagivenDGC mapconsistsof46,98601DGCsor5.79millionkm2(fig.S1). wasthensimplythetotalnumberoftreesintheDGCmultipliedbythe fractionofthespeciesi.Althoughweusedaslightlydifferentapproach Tree density and a slightly larger data set compared to those in our previous study OurtreeinventorydatacomefromtheAmazonTreeDiversityNet- (14),ourresultsare verysimilar tothe results of thatstudy. work (ATDN) (14). The methods we used to estimate tree density, abundance,anddistributionaresimilartothoseusedinourprevious Modeled population sizes and species distributions: study(14)butarebasedon>20%moretreeplotsthaninthatstudy. Rare species TheATDNnowcomprises1766(1-ha)treeinventoryplotsscattered ToestimatethetotalnumberoftreespeciespresentinAmazonia,we throughoutAmazonia(fig.S1). extrapolatedtherank-abundancedistributionofthe4953namedspecies terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 6of10 RESEARCH ARTICLE as in our previous study (14).This yieldedan additional10,247spe- Forrarespecies,theproportionofthenumberofindividualsofa cies, for a total of 15,200 estimated tree species in Amazonia. For givenrarespecieslostinagivenDGCwasquantifiedastheproportion shorthand,inthispaper,werefertothe4953namedspeciesas“com- ofthatDGCclassifiedasdeforested.Rarespeciesinheavilydeforested monspecies”andtothe10,247othertaxaas“rarespecies.” DGCsthusshowamuchhigherlossthanthoseinlessdisturbedDGCs, Becauseourtreeplotdatacannottellushowtheseveryrarespecies andthoseinintactDGCshadzerolosses.Thedegreetowhichrarespe- aredistributed,wecarriedoutaseparatemodelingexercisetoestimate cies’distributionsoverlapwithprotectedareaswasestimatedinthe the degree to which their ranges overlap with deforestation or pro- samefashion.AllanalyseswerecarriedoutwithRsoftware(38). tectedareas.Indoingthis,wereliedontwosimplifyingassumptions: (i)theserarespecieshavesmallcirculargeographicrangeswhosesizes arecorrelatedtotheir populationsizes (13)and(ii)thesespecies are SUPPLEMENTARY MATERIALS not randomly distributed across the Amazon but instead are more likelytooccurinDGCswithhigheroveralltreediversity.Thisstrat- Supplementarymaterialforthisarticleisavailableathttp://advances.sciencemag.org/cgi/ ificationisconsistentwiththetheoreticalnotionthatthereisaone-to-one content/full/1/10/e1500936/DC1 relationshipbetweenFisher’sa atlargesamplesizesandrarespecies UseoftheIUCNthreatcriteria (inlargesamples,thenumberofsingletonsactuallyequalsFisher’sa, Caveatsregardingdeforestationscenarios Caveatsregardingpopulationmodels the number of doubletons equals ~a/2, andthe number of tripletons D Caveatsregardingtheinteractionbetweentreespeciespopulationsandforestloss o equals~a/3…)(35).Toestimatehowmanyrarespeciesoccurineach Fig.S1.MapofAmazoniashowingthelocationofthe1485ATDNplotsthatcontributeddata w DGC,wemadeanupdatedmapoftreediversity(Fisher’sa)inAmazonia tothisreport. nlo (36)at0.1°resolutionandusedthismaptostratifythepositionofrare Fig.S2.MapoflowlandforestsintheAmazon. a d species. For each rare species, a DGC was chosen randomly, with a Fig.S3.TotaldeforestationoftheAmazonby2013. e d probability proportional to the DGC’s Fisher’s a. Range size was FFiigg..SS45..DDeeffoorreessttaattiioonnaannddttrreeeeppooppuullaattiioonnddeecclliinneessionftrhareeAsmpeaczioens.intheAmazon. fro calculated for all 10,247 species as in the study of Hubbell et al. TableS1.DeforestationandtreepopulationdeclinesofrarespeciesintheAmazon. m (13).Eachcircularrangewasoverlainondeforestationandprotected Fig.S6.Projected(includinghistorical)deforestationintheAmazonby2050intheBAU h area maps (pixels at 0.1° resolution). The fraction of the population scenario. ttp intersecting these maps was then calculated as the number of pixels FFiigg..SS78..PPrroojteecctteedd(ainrecalusdainngdhinisdtiogreicnaolu)sdeteforrrietostraietisoinnitnhethAemAamzoazno.nby2050intheIGS. ://a of deforestation (or protected area) divided by the total number of d Fig.S9.HowmuchoftheAmazonisprotectedandhowmanyindividualtreesdoprotected v pixels of forest within that circular section. This was repeated 500 areasprotect? an times to provide themeanexpectationandconfidencelimits. Fig.S10.Rarespeciesinprotectedareasandindigenousterritories. c e TableS2.Rarespeciesinprotectedareasandindigenousterritories. s Fig.S11.ProtectedareasandindigenousterritoriesintheAmazonwithdeforestation .s Protected areas and deforestation c accordingtoBAUscenario2050. ie Spatial data and categories of Amazonian protected areas were Fig.S12.ProtectedareasandindigenousterritoriesintheAmazonwithdeforestation n c gatheredfromtheWorldDatabaseofProtectedAreas(37)andupdated accordingtoIGS2050. e with individual country park service sources (for example, http:// Fig.S13.HowmuchforestlosshastakenplaceandwilltakeplaceinAmazonianprotected m geo.sernanp.gob.pe/geoserver)and—forindigenousterritoriesofGuyana, areas? ag Peru, and Bolivia—with data from Red Amazónica de Información Finig(.AS)1B4A.DUescclienneairniorealnadtiv(eB)pIoGpSu.lationsizeshowsnorelationshipwithoriginalpopulationsize .org Socioambiental Georeferenciada (http://raisg.socioambiental.org/). Fig.S15.InterpolatedstemdensityfortheAmazon. o/ WedidnotincludeindigenousterritoriesfromSuriname,Venezuela, Fig.S16.InterpolatedidentificationlevelofplotsintheAmazon. n and Ecuador because these areas are not yet officially designated. Fig.S17.ProjectedandobserveddeforestationinAmazoniafrom2002to2013. A p PSUroItResct(eIdUCarNeacsatweegroericelsasVsiftioedVaIIsaSnCdRasll(oIUthCerNtycpaetes)go(traiebsleIaS3t)o.WIVh)eorer TAapbpleenSd3ix.IUS1C.NDacatatebgyorDieGsC,d.esignations,andconversionintoSCRs(1)andSUIRs(2). ril 4 thedataindicatedanoverlapbetweenSCRsandSUIRs,theoverlapwas AppendixS2.Databyspecies. , 2 AppendixS3.Dataofindividualsbyregion. 0 designatedas SCR. AppendixS4.TreespeciesestimatedtooccurinCristalinoStateParkinBrazilbutnotyet 16 Historical deforestation up to 2013 was based on data from recordedthere(32)andtheirestimatedthreatstatusaccordingtohistoricalandprojected Soares-Filhoetal.(1,2)andHansenetal.(15).Toestimateprojected deforestation. 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H.terSteege,I.Welch,R.J.Zagt,Long-termeffectoftimberharvestingintheBartica rg N.D.Cardozo,C.I.Czimczik,T.R.Feldpausch,M.A.Freitas,E.Gloor,N.Higuchi,E.Jiménez, Triangle,CentralGuyana.For.Ecol.Manage.170,127–144(2002). o/ G.Lloyd,P.Meir,C.Mendoza,A.Morel,D.A.Neill,D.Nepstad,S.Patiño,M.C.Peñuela, 81. J.Grogan,A.G.Blundell,R.M.Landis,A.Youatt,R.E.Gullison,M.Martinez,R.Kómetter, n A.Prieto,F.Ramírez,M.Schwarz,J.Silva,M.Silveira,A.S.Thomas,H.terSteege,J.Stropp, M.Lentini,R.E.Rice,Over‐harvestingdrivenbyconsumerdemandleadstopopulation A R.Vásquez,P.Zelazowski,E.A.Dávila,S.Andelman,A.Andrade,K.-J.Chao,T.Erwin,A.DiFiore, decline:Big‐leafmahoganyinSouthAmerica.Conserv.Lett.3,12–20(2010). p r EHse..nHRsoaitnmivoíirrtieyozo-CAf.,ntHgh.ueKloAe,emAlian.zgRo,unTd.arJas.i,KnRiflo.leSreeanslat,.mWSãc.ioFe,.nLNcae.uS3ria2lvn3ac,,e1J,.3AT4.e4Pr–.b1Co3rru4g7zh,,(N2A.0.C0T.9oA)r..rPesit-mLeazna,mP.aN,D.Vroaurggahst, 82. JCU.oKMm,a2mr0ke1,r4Ac)i..aCl.TNimewbetornT,rSee.OSlpdeficeields,(MBo.Rtaivneicrs,GTahredeInntserCnoantisoenravlaTtiiomnbeInrtTerrandaet:ioAnWalo,rRkiicnhgmLiostnodf, il 4, 2 0 57. P.M.Brando,J.K.Balch,D.C.Nepstad,D.C.Morton,F.E.Putz,M.T.Coe,D.Silvério, 83. W.F.Laurance,H.E.M.Nascimento,S.G.Laurance,A.C.Andrade,P.M.Fearnside,J.E.L.Ribeiro, 1 M.N.Macedo,E.A.Davidson,C.C.Nóbrega,A.Alencar,B.S.Soares-Filho,Abruptincreasesin R.L.Capretz,Rainforestfragmentationandtheproliferationofsuccessionaltrees.Ecology 6 Amazoniantreemortalityduetodrought–fireinteractions.Proc.Natl.Acad.Sci.U.S.A.111, 87469–482(2006). 6347–6352(2014). 58. J.Brodie,E.Post,W.F.Laurance,Climatechangeandtropicalbiodiversity:Anewfocus. Acknowledgments:Thisreportistheresultoftheworkofhundredsofdifferentscientistsand TrendsEcol.Evol.27,145–150(2012). researchinstitutionsintheAmazonoverthelast80years.Withouttheirhardwork,thisanalysis 59. A.Lima,T.S.F.Silva,L.E.OliveiraeCruzdeAragão,R.M.deFeitas,M.Adami,A.R.Formaggio, wouldhavebeenimpossible.Funding:ThisworkwassupportedbyAlbertaMennegaStichting; Y.E.Shimabukuro,Landuseandlandcoverchangesdeterminethespatialrelationship ALCOASuriname;AmazonConservationAssociation;BancodelaRepública;CELOSSuriname; betweenfireanddeforestationintheBrazilianAmazon.Appl.Geogr.34,239–246 CAPES(PNPG);ConselhoNacionaldeDesenvovimentoCientíficoeTecnológicoofBrazil(CNPq) (2012). ProjectsCENBAM,PELD(558069/2009-6),PRONEX-FAPEAM(1600/2006),ÁreasÚmidas,MAUA; 60. F.Tierra,Ampliaciónresponsabledelafronteraagrícola.PropuestasparaPoliticasPúblicas, PELD(403792/2012-6),PPBio,PVE004/2012,Universal(479599/2008-4),andUniversal307807- No.1(Tierra,LaPaz,Bolivia,2014);http://ftierra.org/index.php?option=com_mtree&task= 2009-6;FAPEAMprojectsDCR/2006,HidrovegwithFAPESP,andPRONEXwithCNPq;FAPESP; att_download&link_id=53&cf_id=43 Colciencias;CONICIT;DukeUniversity;Ecopetrol;FEPIM044/2003;TheFieldMuseum;Conservation 61. Cambio(Cambio,PeriodicodeestadoplurinacionaldeBolivia,2014);www.cambio.bo/ International/DC(TEAM/InstitutoNacionaldePesquisasdaAmazôniaManaus),GordonandBetty ?q=bolivia-proyecta-ampliar-su-frontera-agr%C3%ADcola-10-millones-de-hect%C3%A1reas MooreFoundation;GuyanaForestryCommission;Investissementd’AvenirgrantoftheFrenchANR 62. J.L.DammertB.(IniciativaparalaConservaciónenlaAmazoníaAndina(ICAA),United (CEBA:ANR-10-LABX-0025);IVIC;MargaretMeeAmazonTrust;Miquelfonds;MCTI–MuseuPara- StatesAgencyforInternationalDevelopment(USAID)/InternationalResourcesGroup enseEmílioGoeldi–Proc.407232/2013-3–PVE-MEC/MCTI/CAPES/CNPq;NationalGeographicSoci- (IRG),SociedadPeruanadeDerechoAmbiental(SPDA),CorporacióndeGestiónyDerecho ety(7754-04and8047-06toP.M.J.;6679-99,7435-03,and8481-08toT.W.H.);NSF-0726797toK.R.Y.; Ambiental(ECOLEX),SocialImpact(SI),PatrimonioNatural(PN)yConservationStrategyFund NSFDissertationImprovement;NetherlandsFoundationfortheAdvancementofTropicalResearch (CSF),2013),vol.2015;www.amazonia-andina.org/amazonia-activa/biblioteca/publicaciones/ WOTRO(grantsWB85-335andW84-581);PrimateConservationInc.;ProgrammeEcosystèmes cambio-uso-suelos-agricultura-gran-escala-amazonia-andina. Tropicaux(FrenchMinistryofEcologyandSustainableDevelopment);ShellProspectingand terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 9of10 RESEARCH ARTICLE DevelopmentPeru;SmithsonianInstitution’sBiologicalDiversityoftheGuianaShieldProgram; O.L.Phillips,D.deAndradeLimaFilho,M.deJesusVeigaCarim,M.V.Irume,M.P.Martins, StichtinghetvanEeden-fonds;TheBodyShop;TheMinistryoftheEnvironmentofEcuador; J.-F.Molino,D.Sabatier,F.Wittmann,D.C.López,J.R.daSilvaGuimarães,A.M.Mendoza, TROBIT;TropenbosInternational;U.S.NationalScienceFoundation(NSF-0743457andNSF- P.N.Vargas,A.G.Manzatto,N.F.C.Reis,J.Terborgh,K.R.Casula,J.C.Montero,T.R.Feldpausch, 0101775toP.M.J.;NSF-0918591toT.W.H.);USAID;VarietyWoodsGuyana;Wenner-GrenFoundation; E.N.HonorioCoronado,A.J.D.Montoya,C.E.Zartman,B.Mostacedo,R.Vasquez,R.L.Assis, WWF-Brazil;WWF-Guianas;XIIémeContratdePlanEtatRégion-Guyane(FrenchGovernment M.B.Medeiros,M.F.Simon,A.Andrade,J.L.Camargo,S.G.W.Laurance,H.E.M.Nascimento, andEuropeanUnion)andgrantstoRAINFORfromtheEuropeanUnion,UKNaturalEnvironment B.S.Marimon,B.-H.MarimonJr.,F.Costa,N.Targhetta,I.C.G.Vieira,R.Brienen,H.Castellanos, ResearchCouncil,andtheGordonandBettyMooreFoundation.WethankD.Zappiforprovidingthe J.F.Duivenvoorden,H.F.Mogollón,M.T.F.Piedade,G.A.AymardC.,J.A.Comiskey,G.Damasco, CristalinoStateParkchecklist.O.L.P.wassupportedbyaEuropeanResearchCouncilAdvancedGrant N.Dávila,R.García-Villacorta,P.R.S.Diaz,A.Vincentini,T.Emilio,C.Levis,J.Schietti,P.Souza, andaRoyalSocietyWolfsonResearchMeritAward.Authorcontributions:H.t.S.andN.C.A.P.con- A.Alonso,F.Dallmeier,L.V.Ferreira,D.Neill,A.Araujo-Murakami,L.Arroyo,F.A.Carvalho, ceivedthestudyanddesignedtheanalyses.H.t.S.carriedoutmostanalyses.H.t.S.,N.C.A.P.,T.J.K., F.C.Souza,D.D.doAmaral,R.Gribel,B.G.Luize,M.P.Pansonato,E.Venticinque,P.Fine, W.F.L.,C.A.P.,andJ.E.G.wrotethemanuscript.Alloftheotherauthorscontributeddata,discussed M.Toledo,C.Baraloto,C.Cerón,J.Engel,T.W.Henkel,E.M.Jimenez,P.Maas,M.C.P.Mora, furtheranalyses,andcommentedonvariousversionsofthemanuscript.Thisiscontribution679of P.Petronelli,J.D.C.Revilla,M.Silveira,J.Stropp,R.Thomas-Caesar,T.R.Baker,D.Daly, thetechnicalseriesoftheBDFFP(INPA/STRI).Competinginterests:Theauthorsdeclarethatthey M.R.Paredes,N.F.daSilva,A.Fuentes,P.M.Jørgensen,J.Schöngart,M.R.Silman,N.C.Arboleda, havenocompetinginterests.Dataandmaterialsavailability:Alldataneededtoevaluatethe B.B.L.Cintra,F.C.Valverde,A.DiFiore,J.F.Phillips,T.R.vanAndel,P.vonHildebrand, conclusionsinthepaperarepresentinthepaperand/ortheSupplementaryMaterialsinappen- E.M.Barbosa,L.C.deMatosBonates,D.deCastro,E.deSousaFarias,T.Gonzales,J.-L.Guillaumet, dixS1andS5.Additionaldatarelatedtothispapermayberequestedfromtheauthors. B.Hoffman,Y.Malhi,I.P.deAndradeMiranda,A.Prieto,A.Rudas,A.R.Ruschell,N.Silva, C.I.A.Vela,V.A.Vos,E.L.Zent,S.Zent,A.Cano,M.T.Nascimento,A.A.Oliveira,H.Ramirez-Angulo, Submitted15July2015 J.F.Ramos,R.Sierra,M.Tirado,M.N.U.Medina,G.vanderHeijden,E.V.Torre,C.Vriesendorp, Accepted7October2015 O.Wang,K.R.Young,C.Baider,H.Balslev,N.deCastro,W.Farfan-Rios,C.Ferreira, D Published20November2015 C.Mendoza,I.Mesones,A.Torres-Lezama,L.E.U.Giraldo,D.Villarroel,R.Zagt,M.N.Alexiades, o w 10.1126/sciadv.1500936 K.Garcia-Cabrera,L.Hernandez,I.Huamantupa-Chuquimaco,W.Milliken,W.P.Cuenca, n S.Pansini,D.Pauletto,F.R.Arevalo,A.F.Sampaio,E.H.ValderramaSandoval,L.V.Gamarra, lo Citation:H.terSteege,N.C.A.Pitman,T.J.Killeen,W.F.Laurance,C.A.Peres,J.E.Guevara, Estimatingtheglobalconservationstatusofmorethan15,000Amazoniantreespecies. a d R.P.Salomão,C.V.Castilho,I.L.Amaral,F.D.deAlmeidaMatos,L.deSouzaCoelho,W.E.Magnusson, Sci.Adv.1,e1500936(2015). e d fr o m h ttp ://a d v a n c e s .s c ie n c e m a g .o r g o/ n A p r il 4 , 2 0 1 6 terSteegeetal.Sci.Adv.2015;1:e1500936 20November2015 10of10

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9Museo Ecuatoriano de Ciencias Naturales, Av. Río Coca E6-115 e Isla 28Coordenação de Dinâmica Ambiental, Instituto Nacional de Pesquisas da .. threatened species are nonoverlapping (that is, species listed for C1 did not .. ly wrong (for example, those of small herbs) were disregarded.
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