Poor Prospects for Avian Biodiversity in Amazonian Oil Palm

17 Pages·2015·3.57 MB·English

RESEARCHARTICLE
Poor Prospects for Avian Biodiversity in
Amazonian Oil Palm
AlexanderC.Lees1*,NárgilaG.Moura1☯,ArleteSilvadeAlmeida1,2☯,ImaC.G.Vieira1,2
1 MuseuParaenseEmílioGoeldi,Belém,PA,Brazil,2 ProgramadePós-GraduaçãoemCiências
Ambientais,UniversidadeFederaldoPará/MuseuParaenseEmílioGoeldi,Belém—Pará,Brazil
☯Theseauthorscontributedequallytothiswork.
* [email protected]
Abstract
Expansionofoilpalmplantationsacrossthehumidtropicshasprecipitatedmassivelossof
tropicalforesthabitatsandtheirassociatedspeciosebiotas.Oilpalmplantationmonocul-
tureshavebeenidentifiedasanemergingthreattoAmazonianbiodiversity,butthereare
noquantitativestudiesexploringtheimpactoftheseplantationsonthebiome’sbiota.Un-
derstandingtheseimpactsisextremelyimportantgiventherapidprojectedexpansionofoil
OPENACCESS
palmcultivationinthebasin.Hereweinvestigatethebiodiversityvalueofoilpalmplanta-
Citation:LeesAC,MouraNG,deAlmeidaAS,Vieira tionsincomparisonwithotherdominantregionalland-usesinEasternAmazonia.Wecar-
ICG(2015)PoorProspectsforAvianBiodiversityin
riedoutbirdsurveysinoilpalmplantationsofvaryingages,primaryandsecondaryforests,
AmazonianOilPalm.PLoSONE10(5):e0122432.
andcattlepastures.Wefoundthatoilpalmplantationsretainedimpoverishedaviancom-
doi:10.1371/journal.pone.0122432
munitieswithasimilarspeciescompositiontopasturesandagrarianland-usesanddidnot
AcademicEditor:ClintonNJenkins,Institutode
offerhabitatformostforest-associatedspecies,includingrestrictedrangespeciesandspe-
PesquisasEcológicas,BRAZIL
ciesofconservationconcern.Ontheotherhand,theforeststhattheoilpalmcompaniesare
Received:November21,2014
legallyobligedtoprotecthostedarelativelyspecies-richcommunityincludingseveralglob-
Accepted:February11,2015
ally-threatenedbirdspecies.Weconsideroilpalmtobenolessdetrimentaltoregionalbio-
Published:May8,2015 diversitythanotheragriculturalland-usesandthatpoliticalpressureexertedbylarge
Copyright:©2015Leesetal.Thisisanopen landownerstoallowoilpalmtocountasasubstitutefornativeforestvegetationinprivate
accessarticledistributedunderthetermsofthe landholdingswithforestrestorationdeficitswouldhavedireconsequencesforregional
CreativeCommonsAttributionLicense,whichpermits
biodiversity.
unrestricteduse,distribution,andreproductioninany
medium,providedtheoriginalauthorandsourceare
credited.
DataAvailabilityStatement:Allrelevantdataare
withinthepaperanditsSupportingInformationfiles.
Introduction
Funding:WearegratefultotheInstitutoNacionalde
Globallythedemandforfood,animalfeed,andfuelcontinuestoincreaseatunprecedented
CiênciaeTecnologia,BiodiversidadeeUsodaTerra
naAmazônia(CNPqgrant574008/2008-0),for rates,yetlandavailableforagricultureisshrinkinginmanypartsoftheworld[1],[2].World
financialsupport;CNPqfortheSciencewithout fooddemandisforecasttomorethandoubleby2050[1],broughtaboutbothbyagrowing
BordersProgram’sFellowshiptoACLandfora humanpopulationandevenmorerapidrisesinmeatconsumption[3].Togetherwiththerap-
postdoctoralfellowshipgranttoNGM,aswellasa idlygrowingbiofuelmarket[4]–[6],theyrepresentoneofthemostpervasivethreatstotropical
CNPqforResearchProductivitygrant(CNPq
biodiversity,drivingconversionofnaturalecosystems[1],[7],[8].Oilpalm(Elaeisspp.)plan-
306368/2013-7)toICGV.Thefundershadnorolein
tationsarenowadominanttropicalland-useoccupyingover16millionhectares[9].Itisesti-
studydesign,datacollectionandanalysis,decisionto
publish,orpreparationofthemanuscript. matedthat74%ofglobalpalmoilusageisforfoodproductsand24%forindustrialpurposes,
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 1/17
BirdsinAmazonianOilPalmPlantations
CompetingInterests:Theauthorshavedeclared thelatterpredominantlyforbiodiesel[10].ProductionisespeciallyprevalentinIndo-Malaysia
thatnocompetinginterestsexist. (80%oftheglobaltotal),butplantationacreageisalsoincreasingrapidlyintheAfro-andNeo-
tropics[11],[12].Thisrapidexpansionislikelytocontinuefordecadesgivenbothhighprofit-
abilityandhighdemand.Proponentsofpalmoilemphasizethatitsmainalternatives,
includingsoy,sunflower,andcanolaoils,haveproductionefficienciesjust10–20%ashighas
palmoil(onaper-hectarebasis)andwouldthereforerequiremuchlargerareasofcultivated
landtohaveasimilarbenefit[13],moreover,theindustryisalsohighlylucrativeandcouldpo-
tentiallycreatethousandsofnewjobsandraiseregionalstandardsofliving.
Althoughwidelyflaggedasagreenfuel,fromclimate-changeandbiodiversityperspectives,
suchadvantagesarediminishedshouldpalmoilproductioncontributeeitherdirectlyorindi-
rectlytodeforestation[10],[11].Thishasproventobethecaseinmanypartsoftheworld,
whereexpansionhascomeattheexpenseofbothundisturbedandloggedprimaryforest[8],
[12],[14]despitethehighbiodiversityvalueassociatedwithevendegradedprimaryforests
[15].Thislossisalsopartiallyduetoplantationownersusingtimberrevenues(fromprimary
forests)toprovideset-upcostsforplantationestablishmentandmaintenance[14].Thusthe
questionofhowtomakeoilpalmamoreenvironmentallyfriendlycropbecomesofcritical
conservationimportance[16–18].Asmitigationmeasures,insitupracticestoenhancelocal
biodiversity;suchasproductionofoilpalmbeneathshadetrees,diverseagro-forestryonplan-
tationboundaries,andmaintenanceofforestpatcheswithinplantationshavebeenproposed
[18–21].Significantenvironmentalprogresshasalsobeenmadeundertheauspicesofthe
RoundtableonSustainablePalmOil(RSPO)certificationprogram[22],aresultofmanyofthe
largestpalmoilproducersdesiretoimplementenvironmentally-friendlymanagement.
TheBraziliangovernmentisplanningalargeincreaseinbiofuelproductionoverthenext
decade,drivenbyinternalandexternalmarketdemand(ethanol),aswellasbygovernment-
enforcedblending(biodiesel)[23–25].MuchofthisexpansionisforecastfortheeasternAma-
zonianstateofParáwherethepalmoilacreagedoubledbetween2004and2010[25].Bastos
etal.[26]suggestedthatupto80%ofthestatewouldbesuitableforoilpalmcultivation,with
degradedlands(suchasabandonedcattlepasture,andminingareas)likelytohostmuchofthe
growthinproduction.TheEnvironmentalCouncilofParáState(COEMA)recentlypasseda
resolution[27]thatpermitsthedesignationofoilpalmasa‘low-impact’land-usethatmay
substitutenativeforestvegetationinthelegally-mandatedpermanentprotectionareas(áreas
depreservaçãopermanente)‘APPs’andlegalreserves(reservaslegais)‘RLs’requiredofsmall-
holderpropertiesoflessthan20ha.Withthisprecedentthereisnowapowerfulrurallobbyar-
guingforthisdispensationtobeavailabletoalllandowners,irrespectiveofpropertysize[28],
asareplacementforregeneratingforestvegetation.GiventhattheforestsoftheAmazonbasin,
representingabout41%oftheworld'sremainingtropicalrainforestarealreadysubjecttode-
forestationratesfluctuatingaroundhalfamillionhectaresperyear[29],thisexpansioninto
Amazoniarequirescarefulappraisalofthepotentialimpactsofoilpalmmonoculturesonthe
region’srichbiodiversity.Suchimpactshavebeenheavilystudiedinsouth-eastAsia,where
evenwildlife-friendlymanagementtechniqueshavefailedtoconservespeciesofconservation
concerne.g.[30],buttherearenosuchquantitativestudiesfromAmazonia.Decisionsabout
howtobalancelandrequirementsforagriculturebiofuelsandbiodiversityconservationwill
thushaveprofoundeffectsontheconservationofAmazonianbiodiversity,aswellaseconomic
developmentandpovertyalleviation[31].
Hereweevaluatethevalueofoilpalmplantationsforavianbiodiversityinrelationtoother
localland-uses(primaryandsecondaryforestsandcattlepastures)locatedinthe145,000km2
BelémAreaofEndemism(hereafterBelémAE),aregionofeasternAmazoniadelimitedbythe
eastbankoftheTocantinsriverandthewesternbiogeographiclimitofAmazonianterrafirme
forestsinwesternMaranhãostate[32].TotalforestlossintheBelémAEhasreachedatleast
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 2/17
BirdsinAmazonianOilPalmPlantations
75%oftheoriginalextentandfurtherextensiveforestlossandconcomitantglobalextinctions
areforecastifeffectiveforestconservationpoliciesarenotenforced[33],[34].Weinvestigate
theavianbiodiversityvalueofoilpalmlandscapesintermsofplantationage,treespeciesrich-
nessanddistancetosourcehabitatsandcomparethesevalueswiththoseofland-usesinthe
surroundinglandscapematrix(pastoralsystems,primaryandsecondaryforests).
MaterialsandMethods
StudyRegion
ThisstudytookplaceinthemunicipalitiesofMoju,TailândiaandAcarálocatedcirca120km
southofBeléminParástate.Meanannualtemperatureis26.6°C,meanannualprecipitationis
circa2,500mm[35]andlocalsoilsarehighlyweatheredacidoxisols[36].Forestcanopy
heightsaretypicallyintherangeof25–35mandtheunderstoreyisdominatedbyplantsfrom
thefamiliesLecythidaceae,Violaceae,Sapotaceae,Burseraceae,MoraceaeandLeguminosae
[37].Therearealsosmallpatchesofnaturalopenvegetationenclaves—campinaformationson
whitesandsoilswhichhaveaverydistinctbiodiversity[38].Bytheyear2010,forestcoverin
TailândiaandMojuhadbeenreducedby45%to4,989km2muchofwhichisdegradedprima-
ryorregeneratingsecondaryforest(Fig1and[29]).Thesetwomunicipalitiesformpartofthe
oilpalm‘pole’ofMoju-Acará-Tailândia,where124,700haofoilpalmhadbeenplantedby
2009,predictedtoincreaseto370,500haby2014[39].
Datacollection
Weselectedthreestudyregionsoccupiedbydifferentoilpalmproducers,asfollows:Ubá
(1,008km2)inthenorthofthemunicipalityofMojuincludingthesourceoftherioUbá;Ara-
uai(952km2)locatedinthecentreofthemunicipalityincludingthesourceoftherioArauai;
andfinallyMamorana(680km2)locatedatthesouthernextremeofthemunicipalityincluding
thesourceoftherioMamorana(forfurtherdetailssee[40]).Between15–17300mtransects
wereallocatedtoeachregion,distributedusingastratified-randomsamplingdesign(wherea
standarddensityoftransects(1per400ha)wasdistributedinproportiontothepercentage
coveroftotalforestandproductionareas)acrosseachregiontoincreasethelikelihoodthat
theywouldcaptureimportantinternalheterogeneitiesinforestand/orproductionsystems.To
reducethedependencybetweentransectswithineachregion,transectswereseparatedbya
minimumdistanceof1.5km.Wealsoavoidedplacingtransectswithin200mofanyother
land-usetocontrolforpotentialedgeeffects.
Intotalwesampled50transects,17inprimaryforest,4insecondaryforests—foreststhat
developedaftercompletedeforestation[41]ofdifferentages(5,7,15&20yearsold),15invar-
iable-ageoilpalmplantations(1,3,4,12,14,23,24&25yearsold),12incattlepastureandone
incampinavegetation(althoughthelatterwasnotusedinlateranalysesexceptFig.CinS1
File).Designationofsecondaryforestandplantationageswasdonethroughvisualinspection
ofa20yeartime-seriesofLandsatimagesforeachtransect,calibratedbyinterviewswithlocal
farmers.Allprimaryforestsiteshadbeensubjecttohistoricselectiveloggingeventsbutnone
havebeenburnedinthelastfiveyears.Allfieldworktookplaceonprivatelandsandlandown-
ersineachregionwerevisitedpriortoanyfieldworktointroducetheprojectandsecureper-
missionsforsurveys.Land-useclassificationwasundertakenusingArcGis9.3andEnvi4.5
usingbothunsupervised(ISODATA)andsupervised(MaxVer)classificationprotocols(ISO-
DATA)[40].TheISODATA(InteractiveSelf-organizingDataAnalysis)methodwasusedto
determineland-useclassespriortofieldworkandemployedminimumEuclideandistance
measurements(inmultidimensionalspace)toidentifyspectralclustersfromtheimageandas-
signaclasstoeachpixel.Onreturningfromthefieldwithourground-truthedmeasurements
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 3/17
BirdsinAmazonianOilPalmPlantations
Fig1.Mapofthestudyregiondepicting(a)thethreeareasstudiedwiththemunicipalityofMojuandland-usetypes;thedistribution(b)of
transectsacrossonestudyarea(Arauai)anditsland-uses;andc)transectdesigndepictingvegetativesamplingplotsandsub-parcelsandthe
positionofpointcountstations.
doi:10.1371/journal.pone.0122432.g001
weperformedasupervisedMaxVer(MaximumLikelihoodClassification)analysiswhichas-
signstheprobabilityofeachpixeltopre-definedclasses(basedonourground-truthing),as-
signingpixelstotheclasswiththehighestprobability.Toassessclassificationaccuracyweused
Cohen’sKappastatistic[42],whichprovidesanindicationoftheclassificationagreementbe-
tweentheclassifiedandtheground-truthedmapsthatisnotattributabletochance.Theremote
sensinganalysiswasperformedusinggeoreferenceddatawithLandsatTM-5(ThematicMap-
per)imageswith30mspatialresolutionfromtheyear2010.
Tosamplethebirdcommunitywelocatedthreepointcount(PC)stationsineachtransect
at0,150and300m.Atotalof288PCswereconductedbetweenthethreeregions.We(ACL&
NGM)carriedouttworepetitionsofthree15minute,75mfixedradiusPCspertransect,re-
cordingallspeciesseenorheard.Repetitionsensuredthattemporalvariationinavianvocalac-
tivitywasminimized,andPCswererecordedusingsolidstaterecorders.Theavifaunalsurveys
werecomplementedwithsamplingofwoodyplantsandvegetativestructuretoseehowhabitat
structuralcharacteristicsandbotanicdiversitymightinfluenceavianspeciesrichness.These
surveystargetedtreesandlianasandpalmsabove2cmDBH(DiameteratBreastHeight)and
wereconductedin10x250mplots,subdividedinto10x(10x15m)parcelsfollowingthepro-
tocolsofGardneretal.[43].Allindividualswereidentifiedtospeciesormorphospeciesbyex-
pertparabotanists(NelsonRosaandCarlosAlbertoSantos).Plantspecieswhichdefiedfield
identificationwerecollectedanddepositedintheherbariumoftheMuseuParaenseEmílio
Goeldiforlateridentification.Togeneratebiomassestimates(asMg.ha-1)weusedallometric
equationsforallplantspecieswithDBH(cid:1)2cm.
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 4/17
BirdsinAmazonianOilPalmPlantations
WeusedtheequationsofChaveetal.[44]forhumidforesttreespecies:
ðAGBÞest¼p (cid:3)expð(cid:4)1:499 þ2:1481 (cid:3)lnðDBHÞ þ0:207 (cid:3)ðlnðDBHÞÞ2 (cid:4)0:0281
(cid:3) ðlnðDBHÞÞ3
where:AGB=abovegroundbiomassforallspecieswithDBH(cid:1)2cm;p=wooddensity
(g/cm-3);andDBH=diameteratbreastheight(cm).Weusedagenera-specificequation
forpalmsinthegenusCecropia,thatofNelsonetal.[45]:
DW¼expð(cid:4)2:5118 þ2:4257 (cid:3)lnðDBHÞÞ
whereDW=estimatedbiomassofCercropiasp.trees.Finallytogenerateestimatesofthebio-
massofoilpalmElaeisguineensisweusedtheage-specificformulaofCorley&Tinker[46]:
Bt¼p (cid:3)ðr (cid:3) Z2Þ(cid:3)100(cid:3)h (cid:3)r
whereBt=estimatedbiomass(kg)ofElaeisguineensis;r=radius(cm)ofthepalm’strunk;
Z=diameterofthepalmbase(aconstant—0.777),ρ=height(m)ofthetrunkandρ=trunk
density(Kg/m3)whichiscalculatedusingtheformula:
Id(cid:3)0:0076þ0:083
r¼
1000
WhereIdistheageoftheoilpalminyears.
Dataanalyses
Weanalysedtheresponsesoftotalspeciesrichnessaswellasrichnessandturnoverforthesub-
setof‘primaryforest-associatedbirds’(hereaftertermed‘forestbirds’).Theseforestbirdsrep-
resentthecoreavifaunaofundisturbedterrafirmeforestsbutnotnecessarilybirdsrestrictedto
thosehabitats,assomecoreprimaryforestspeciesalsooccurinhuman-modifiedforestand
non-foresthabitats(e.g.Blue-grayTanagerTangaraepiscopusandBananaquitCoerebafla-
veola).Thesecategorizationswerebasedonpreviouslypublishedclassificationofbirdsfrom
theregione.g.[47]and[48].OurtaxonomyfollowsthechecklistofBrazilianbirdscompiled
bytheComitêBrasileirodeRegistrosOrnitológicos[49].
Tocomparesamplingintensityandavianresponsesbetweendifferentland-usesweused
sample-basedrarefactioncurves,with95%confidenceintervalscalculatedusingthe‘specac-
cum’tool,includedintheveganpackageoftheRsoftware[50].Comparisonsbetweenspecies
richnessineachland-usetypeweremadeusingaone-wayANOVAtestwithintervalsfollowed
byaTukeypost-hoctesttocheckforsignificantpairwisedifferences.Toexploreunivariaterela-
tionshipsbetweenforestcoverandforestbirdspeciesrichnessweperformedlinearregressions
usingpercentageoftotalforestcover(primaryandold(>15years)secondaryforestscombined
ina1kmbuffer),thepercentageofprimaryforestcoverina1kmbufferaroundthecentroid
ofeachtransect(tostandardisesamplingunitsize)anddistancetothenearestprimaryforest
aspredictorvariablesforavianspeciesrichness.
Toassesstherelativeimportanceofdifferentenvironmentalvariablesonbirdspeciesrich-
nesswefirstassessedforvariablecolinearityusingPearsoncorrelationbetweenthevariables,
edgedistance,treespeciesrichness,plantsbiomassandpercentageofprimaryforestcoverex-
cludingvariableswithanunacceptably-highdegreeofcolinearity(r(cid:1)0.7).Wethenusedgen-
eralizedlinearmodels(GLMs)withaGaussiandistributionandaloglinkfunctionandmodel
averagingusingAICcweights[51]togeneratesubsetsoftopmodelsanduncovertherelative
importanceofdifferentvariables.AlltheseanalysisweredoneusingRversion2.15.1[50]with
the‘glmulti’and‘MuMin’packages.
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 5/17
BirdsinAmazonianOilPalmPlantations
Toassessthevariationinspeciescompositionbetweenland-usesystemsanddifferentpri-
maryforestdisturbanceclassesweproducednon-metricmulti-dimensionalscalingordina-
tions(nMDS[52])usingtheSorensensimilaritymatrixforspeciespresence-absencedata.To
assessthestatisticalsignificanceofdifferencesinassemblagecompositionbetweendifferent
land-usetypesandforestdegradationclassesweconductedaone-wayPERMANOVAwhich
usespseudo-Fvaluestocompareamong-grouptowithin-groupsimilarityandassessessignifi-
cancebypermutation.AllmultivariateassemblageanalyseswerecarriedoutinPrimerv.6
(PRIMER-ELtd,Plymouth,UK,[53]).Tofacilitatecomparisontoalargersampleofdifferent
land-useswecomparedourdatafromMoju-Tailândia-Acaráwithdatafromanextensivein-
ventoryoftheneighbouringmunicipalityofParagominas[41].Thisinventoryusedthesame
transectselectionandaviansamplingprotocolsandhasthesamesourceavifauna[54],[55]as
thepresentstudyandwasconductedbythesamefieldornithologists(ACL&NGM).Intotal
weusedaviandatafrom187transects—97inprimaryforest,25insecondaryforest,53incattle
pastureand12frommechanisedagriculture(soybeanfieldsinthiscase).Weinvestigatedrela-
tivecontributionofindividualspeciestotheoveralldissimilarityusingthesimilaritypercent-
agesroutine-SIMPER[50].Owingtohistoriclegacyeffectsoflandpurchasing(with
smallholderpropertiestypicallyclosertoforestborders),oilpalmplantationswereonaverage
situatedfartherfromprimaryforestborders(mean=972m,SD=267m,range545–1424m)
thancattlepastures(mean=510m,SD=150m,range216–719m).Tocontrolforthispoten-
tialbiasofleakageofforestspecieswecomparedoilpalmforestbirdrichnesswithforestbird
richnessfromcattlepastures(n=23mean=1009m,SD=382m,range554–2069m)inPara-
gominassituatedover550mfromthenearestprimaryforestborderandassessedthesignifi-
canceofdifferenceswithapairedt-testusingR.
Finally,weusedaglobalphylogenyofbirds[56]tovisuallycomparethephylogeneticstruc-
tureofthemostspecioseavianclades(familieswith>8species)betweenthedominantregion-
alland-uses(primaryforest,pastureandoilpalm).Theresultingcircularphylogramswere
visualizedandeditedusingtheFigTreev1.4.1software(http://tree.bio.ed.ac.uk/software/
figtree/)todocumentnon-randomextinctionprocesses.
Results
Regionalland-useclassification
Acrossthe2,588km2studyregionourremote-sensinganalysisidentifiedsevendiscreteland-use
types:varyingly-degradedprimaryforest:40.2%(1041km2),secondaryforest:9.0%(234.9km2),
campinaformations:2.8%(71.8km2),oilpalmplantations:8.3%(214.9km2),cattlepasture:
39.2%(1016km2),openwater:0.3%(9.0km2)andcloud/shadow:0.01%(0.15km2).Thesere-
sultswereassociatedwithaKappacoefficientof0.85(withaglobalaccuracyof89%ofthepixels
correctlyclassified).FollowingMonserudandLeemans[57]Kappastatisticsvalues,from0.7to
0.85representverygoodagreementbetweenimages.
Speciesrichnessbetweenland-usetypes
Werecorded3,090detectionsof249birdspecies,ofwhich1982wereforest-associatedspecies
(forafulllistseeTableAinS1File).Thespeciesaccumulationcurvesindicatedthatsurveysin
mostland-usetypeswerenearasymptotic(FigAinS1File).Werecordedmeanspeciesrichness
pertransectof50.1inprimaryforest(SD=13.2,n=16,totalrichness=211,range=24–69,),
33.25insecondaryforest(SD=2.3,n=4,totalrichness=68,range=30–36),30.0incattlepas-
ture(SD=7.9,n=12,totalrichness=100,range=17–41),and16.3inoilpalmplantation
(SD=6.9,n=15,totalrichness=69,range=6–28).Thesedifferencesinspeciesrichnessweresig-
nificantbetweenallland-usetypesconsideringthewholeavifaunalcommunity(Fig2A,F=32;
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 6/17
BirdsinAmazonianOilPalmPlantations
Fig2.Boxplotscomparingavianspeciesrichnessbetweenland-usetypes,usingtheentireavianassemblage(A)andjustforest-associatedbirds
(B).Non-significantpairwisedifferencesbetweenland-usetypesareindicatedbythepresenceofthesameletter(accordingtoaTukeytest95%).
doi:10.1371/journal.pone.0122432.g002
df=43;N=4;P<0.01)andforforest-associatedbirds(Fig2B,F=46;df=43;N=4;P<0.01),
withtheexceptionofthosebetweenpastureandsecondaryforestsforwhichthemeandifferences
richnesspertransectwasstatisticallynon-significant(Fig2).Thedifferenceinforestbirdspecies
richnesswasnotsignificantbetweenoilpalmandcattlepastures(mean=4.34,SD=2.19,n=23)
situatedover500mfromthenearestprimaryforestinParagominas(unpairedt-test,t=1.7;
df=36;P=0.09,Fig.C,inS1File).Wefoundthatavianspecieswasstatisticallydifferentbetween
old(>11years,n=6,meanspeciesrichness:10.2)andyoung(<10years,n=8,meanspecies
richness:21.5)oilpalmtransectsforboththeentireaviancommunity(F=29.4;df=13;P<0.01)
andforest-associatedbirdsonly(F=18.7;df=13;P<0.01).Furthermore,aviancommunitiesin
oilpalmplantationsofvaryingagesunderwentaviancommunitysuccessionresultingindifferent
communitystructureandrichnessbetweenplantationsofdifferentages(FigC,inS1File).Re-
centlyplantedstands((cid:5)1–2years)hadaverylowvegetativebiomassandweremostlyoccupied
bybirdstypicalofcattlepastures(ornaturalsavannahenclaves—see[38])suchasPale-breasted
SpinetailsSynallaxisalbescensandRed-breastedBlackbirdsSturnellamilitaris.Plantationsof(cid:5)5
yearshadamoresignificantbiomasscomparablewithyoungsecondaryforests,buthadasimilar
communitystructure,albeitincludingsomespeciesmoretypicalofedge/secondaryforestsuchas
ReddishHermitPhaethornisruber,GreatAntshrikeTarabamajorandWhite-fringedAntwren
Formicivoragrisea.
Environmentaldeterminantsofspeciesrichness
Wefoundasignificantpositiveandbroadlylinearrelationshipbetweentherichnessofallbird
speciesandtreebiomass(adj.R2=0.49,p<0.001)whichstrengthenedwhenonlyforestasso-
ciatedbirdswereincludedinthemodel(Fig3,adj.R2=0.70,P<0.001).Weuncoveredasig-
nificantnegativerelationshipbetweendistancetoforestedgeandspeciesrichness(adj.R2=
0.56,P<0.001)whichwasmarginallymoresignificantwhenonlyforestbirdswereretained
(Fig3,adj.R2=0.56,P<0.001).TheGLMsrevealedthattreerichnesswasthemostimportant
predictorvariableinfluencingrichnessforthewholecommunity(Fig4andTableBinS1File)
followedbydistancetotheforestborder,forestcoverandvegetativebiomassforthewhole
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 7/17
BirdsinAmazonianOilPalmPlantations
Fig3.Linearregressionsbetweenrichnessofforestbirdspeciesanda)treebiomassandb)distancetothenearestprimaryforestborder.
doi:10.1371/journal.pone.0122432.g003
community,whilstforforestassociatedbirdsthemostimportantpredictorvariablesweretree
speciesrichness,biomass,distancetotheforestborderandforestcover.Thetopmodelresults
showedthat,consideringthewholeaviancommunity,fourmodelshadlowΔAICc(<2),with
thebestmodelincludingdistancetoborderandtreerichness.Consideringonlyforest-associat-
edbirdstwomodelshadlowΔAICcwiththebestretainingonlytreespeciesrichness(TableB
inS1File).
Fig4.Relativeimportanceofenvironmentalvariablesinexplainingtotalavianspeciesrichness(A)andforest-associatedbirdrichness(B).Signs
indicatethedirectionoftheeffectofeachvariable.Theexplanatoryvariablesincludedistancetotheforestborder(border),treespeciesrichness,forest
cover(%ofprimaryforestcover)andbiomassoftrees(biomass).
doi:10.1371/journal.pone.0122432.g004
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 8/17
BirdsinAmazonianOilPalmPlantations
Aviancommunitystructureacrossland-usetypes
Avianspeciescompositionchangedconsistentlyandsignificantlyalongagradientofhuman
impactsbetweenprimaryforests,secondaryforests,cattlepasturesandoilpalmplantations
Fig5,TableCinS1File,PERMANOVA,Pseudo-F=8.1725,P<0.001).Allspeciesassem-
blagesweresignificantlydifferentfromeachother(P<0.001)withtheexceptionofpastures
andplantationsforwhichP=0.573.Communitystructureinprimaryforests,secondaryfor-
estsandcattlepasturewasbroadlysimilartothatfoundintheneighbouringmunicipalityof
Paragominas(Fig5)indicatinglowspeciesturnoverbetweenthemunicipalitiesandemphasis-
ingthegeneralizabilityoftheresultsacrosstheBelémAE.Eachland-usetypeplayedhostto
characteristicassemblagesofspecieswhoserelativedominancecontributedtocommunitydis-
similarity(Table1),withcommunitiesintheoilpalmplantationssharingmorespecieswith
cattlepasturesthantheydidwithforesthabitats.Thephylograms(Fig6)indicatethatland-use
mediatedlocalextinctionswerenon-random,withgreatestlossesofspeciesoccurringfromthe
diverseradiationofsuboscinepasserines(antbirds,tyrantflycatchers,ovenbirdsandwood-
creepers)forwhichfewspeciespersistedincattlepasturesoroilpalmplantations.Therewas
someturnoverofspecies,withwaterbirdssuchascrakesandrailsanddiversegranivorousos-
cinepasserinestypicalofopenareascolonisingthepasturesandoilpalmplantations(Fig6.
TableAinS1File).
Occurrenceofthreatenedandendemicspecies
Mostofthebirdspecies(96%)wedetectedareclassifiedasLeastConcernbyBirdLifeInterna-
tional[58]withtheexceptionofninespeciesinthethreatcategoriesEndangered(EN),Vulner-
able(VU)andNearThreatened(NT).Thesewereasfollows:White-crestedGuanPenelope
pileata(VU);RuddyPigeonPatagioenassubvinacea(VU);GoldenParakeetGuarubaguar-
ouba(VU);White-belliedParrotPionitesleucogaster(EN);PearlyParakeetPyrrhuralepida
Fig5.NMDSplotsofcommunitystructureoftheaviancommunityinMoju(polygonswithheavyblack
borders)andParagominas(narrowborders),primaryforesttransectsarerepresentedbydarkgreen
squares,secondaryforestsbylightgreensquares,orangecirclesarecattlepastures,greycirclesare
mechanisedagricultureandtrianglesareoilpalmplantations(darkred=15–20yearsold,lighterred
0–6yearsold).
doi:10.1371/journal.pone.0122432.g005
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 9/17
BirdsinAmazonianOilPalmPlantations
Table1. Thetop-ranked15birdspeciesineachland-usetypewhichcontributedtothedissimilarityofspeciescompositionbetweenoilpalmplan-
tations,cattlepastures,secondaryforestsandprimaryforests.
OilPalm Pasture
Latinbinomial Av.Abund Contrib% Cumu.% Latinbinomial Av.Abund Contrib% Cumu.%
Formicivoragrisea1 1 20.7 20.7 Myiophobusfasciatus2 0.92 7.54 7.54
Tyrannusmelancholicus 0.8 11.89 32.59 Tangaraepiscopus 0.92 7.54 15.09
Ramphoceluscarbo4 0.67 8.33 40.92 Tyrannusmelancholicus 0.92 7.54 22.63
Tangarapalmarum 0.53 5.48 46.41 Troglodytesmusculus2 0.85 6.4 29.03
Myiophobusfasciatus2 0.6 5.19 51.6 Elaeniaflavogaster 0.85 5.97 35
Troglodytesmusculus2 0.53 4.76 56.36 Phaeomyiasmurina 0.85 5.97 40.97
Pitangussulphuratus 0.47 3.79 60.15 Ramphoceluscarbo4 0.85 5.41 46.38
Turdusleucomelas 0.4 3.48 63.62 Synallaxisalbescens2 0.69 4.14 50.52
Phaethornisruber3 0.4 3 66.63 Tangarapalmarum 0.69 4.06 54.58
Sturnellamilitaris2 0.47 2.93 69.56 Volatiniajacarina2 0.69 3.93 58.51
Volatiniajacarina2 0.47 2.93 72.49 Sturnellamilitaris2 0.62 3.64 62.15
Prognechalybea3 0.4 2.68 75.17 Formicivoragrisea 0.62 2.82 64.97
Synallaxisalbescens2 0.4 2.11 77.28 Prognechalybea3 0.54 2.27 67.24
Crotophagaani 0.4 2.02 79.3 Tachyphonusrufus 0.54 2.26 69.5
Amazonaamazonica 0.33 1.78 81.09 Myiarchustyrannulus 0.54 2.17 71.67
SecondaryForest PrimaryForest
Latinbinomial Av.Abund Contrib% Cumu.% Latinbinomial Av.Abund Contrib% Cumu.%
Coerebaflaveola2 1 6.11 6.11 Cercomacracinerascens 1 4.54 4.54
Formicivoragrisea 1 6.11 12.22 Lophotriccusgaleatus 1 4.54 9.09
Phaethornisruber3 1 6.11 18.34 Phaethornisruber3 0.93 4.04 13.13
Pheugopediusgenibarbis 1 6.11 24.45 Myrmotherulaaxillaris2 0.93 3.97 17.1
Prognechalybea2 1 6.11 30.56 Pyriglenaleuconota2 0.93 3.94 21.03
Pyriglenaleuconota2 1 6.11 36.67 Glyphorynchusspirurus 0.87 3.32 24.36
Ramphoceluscarbo4 1 6.11 42.78 Myiopagisgaimardii2 0.8 2.97 27.33
Thamnophilusamazonicus 1 6.11 48.89 Pheugopediusgenibarbis 0.8 2.78 30.11
Amazonaamazonica 0.75 3.14 52.04 Ramphoceluscarbo4 0.8 2.78 32.88
Manacusmanacus 0.75 3.14 55.18 Thamnomanescaesius 0.8 2.62 35.5
Patagioenasspeciosa 0.75 3.14 58.32 Isleriahauxwelli 0.73 2.25 37.75
Saltatormaximus 0.75 3.14 61.46 Coerebaflaveola2 0.73 2.22 39.97
Lophotriccusgaleatus 0.75 3.08 64.53 Zimmeriusgracilipes 0.73 2.15 42.12
Myiopagisgaimardii2 0.75 3.08 67.61 Thamnophilusamazonicus 0.67 2.11 44.23
Myrmotherulaaxillaris2 0.75 3.08 70.69 Ramphastosvitellinus 0.67 1.89 46.12
Numberedsuperscriptsrefertothenumberofotherhabitatsinwhichspecieswerealsotop-rankedcontributorstospeciessimilarity.
doi:10.1371/journal.pone.0122432.t001
(VU);VulturineParrotPyriliavulturina(VU);(Eastern)Red-neckedAracariPteroglossus
bitorquatus(EN);Red-billedToucanRamphastostucanus(VU);Channel-billedToucanRam-
phastosvitellinus(EN)(asArielToucanRamphastosariel)andLong-tailedWoodcreeperDeco-
nychuralongicauda(NT).Allthesespecieswereconfinedtoprimaryforests;withthe
exceptionofasingleRed-neckedAracariphotographedinanarborescentpasture[59]andone
recordofChannel-billedToucanfromasecondaryforesttransect(TableAinS1File).Inaddi-
tionwefoundafurtherfourspecieswhicharenarrowlyendemictotheBelémAE(andafur-
therfourhighly-differentiatedendemicsubspecieslikelytobesubjecttofuturetaxonomic
upgradestospeciesstatus[60–62])andsixotherspeciesthatarerestrictedtosouth-east
PLOSONE|DOI:10.1371/journal.pone.0122432 May8,2015 10/17