Ground-Vegetation Clutter Affects Phyllostomid Bat Assemblage Structure in Lowland Amazonian ...

16 Pages·2015·1.31 MB·English

RESEARCHARTICLE
Ground-Vegetation Clutter Affects
Phyllostomid Bat Assemblage Structure in
Lowland Amazonian Forest
RodrigoMarciente,PauloEstefanoD.Bobrowiec*,WilliamE.Magnusson
InstitutoNacionaldePesquisasdaAmazônia,CoordenaçãodeBiodiversidade,Manaus,Amazonas,Brazil
* [email protected]
a11111
Abstract
Vegetationclutterisalimitingfactorforbatsthatforageneargroundlevel,andmaydeter-
minethedistributionofspeciesandguilds.However,manystudiesthatevaluatedtheef-
fectsofvegetationclutteronbatshaveusedqualitativedescriptionsratherthandirect
OPENACCESS
measurementsofvegetationdensity.Moreover,fewstudieshaveevaluatedtheeffectof
Citation:MarcienteR,BobrowiecPED,Magnusson vegetationclutteronaregionalscale.Here,weevaluatetheinfluenceofthephysicalob-
WE(2015)Ground-VegetationClutterAffects structionofvegetationonphyllostomid-batassemblagesalonga520kmtransectincontin-
PhyllostomidBatAssemblageStructureinLowland
uousAmazonianforest.Wesampledbatsusingmistnetsineightlocalitiesduring80nights
AmazonianForest.PLoSONE10(6):e0129560.
doi:10.1371/journal.pone.0129560 (3840net-hours)andestimatedtheground-vegetationdensitywithdigitalphotographs.The
totalnumberofspecies,numberofanimalivorousspecies,totalnumberoffrugivorousspe-
AcademicEditor:DaniloRusso,Universitàdegli
StudidiNapoliFedericoII,ITALY cies,numberofunderstoryfrugivorousspecies,andabundanceofcanopyfrugivorousbats
werenegativelyassociatedwithvegetationclutter.Thebatassemblagesshowedanested
Received:January2,2015
structureinrelationtodegreeofclutter,withanimalivorousandunderstoryfrugivorousbats
Accepted:May10,2015
distributedthroughoutthevegetation-cluttergradient,whilecanopyfrugivoreswererestrict-
Published:June12,2015 edtositeswithmoreopenvegetation.Thespeciesdistributionalongthegradientofvegeta-
Copyright:©2015Marcienteetal.Thisisanopen tionclutterwasnotcloselyassociatedwithwingmorphology,butaspectratioandwingload
accessarticledistributedunderthetermsofthe differedbetweenfrugivoresandanimalivores.Vegetationstructureplaysanimportantrole
CreativeCommonsAttributionLicense,whichpermits
instructuringassemblagesofthebatsattheregionalscalebyincreasingbetadiversitybe-
unrestricteduse,distribution,andreproductioninany
medium,providedtheoriginalauthorandsourceare tweensites.Differencesinforagingstrategyanddietoftheguildsseemtohavecontributed
credited. moretothespatialdistributionofbatsthanthewingcharacteristicsofthespeciesalone.
DataAvailabilityStatement:Thedataandmetadata
aredepositedinthepublicrepositoryofthePPBio
(http://ppbio.inpa.gov.br/repositorio/dados).Toaccess
thedatausethekeywords"morcegos","BR-319",
and"clutter".
Introduction
Funding:ProgramadePesquisaemBiodiversidade
(PPBio),NationalInstituteforScience,Technology Thestructureandcompositionofbatassemblagesismostlydeterminedbyvegetationfeatures
andInnovationforAmazonianBiodiversity(INCT- [1,2].Inparticular,physicalobstructionoftheforestcreatedbytrunks,branchesandleaves
CENBAM),InstitutoNacionaldePesquisasda
stronglyeffectshabitatusebyforagingbatsdirectlybecauselocomotioninclutteredspacesre-
Amazônia(INPA),BatConservationInternational,
quiresgreaterflightmaneuverability[3,4].Siteswithverydensevegetationreduceforagingeffi-
FundaçãodeAmparoàPesquisadoAmazonas
ciencybylimitingthemovementofspeciesanduseofecholocationtodetectobstaclesand
(FAPEAM),andInstitutoChicoMendesde
ConservaçãodaBiodiversidade(ICMBio)ofHumaitá potentialprey[5–9].
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 1/16
EffectofVegetationClutterinBats
havefundedfieldwork.RMwassupportedbya PhyllostomidbatsarecommonlycapturedintheunderstoryofNeotropicalforestsand
fellowshipfromConselhoNacionalde mostspeciesarefrugivores,nectarivores,orgleaninganimalivores[10].Theseguildsforage
DesenvolvimentoCientíficoeTecnológico(CNPq
inhighlyclutteredsitesandcollectfood(fruits,nectar,insects,andsmallvertebrates)
132573/2010-5)andFundaçãoAmazônicade
veryclosetovegetation[11].Inthissituation,batsneedspecificsensoryandmorphological
DefesadaBiosfera(FDB)andPEDBbya
CoordenaçãodeAperfeiçoamentodePessoalde adaptationstoflyinrestrictedspacewherefoodechoesmaybehiddenbyclutter
NívelSuperior(CAPES)post-doctoralscholarship echoes[12].
(02499/09-6). ForbatsofthefamilyPhyllostomidae,foragingstrategiesandwingmorphologyhavebeen
CompetingInterests:Theauthorshavedeclared suggestedtobethemainfactorsassociatedwiththeabilitytouseclutteredenvironments[8,
thatnocompetinginterestsexist. 12].Thedifferentforagingstrategiesshouldreflectdifferentuseofspacebybatspeciesand
guilds,andthusmaydeterminetheorganizationofbatassemblages.Gleaninganimalivores
capturetheirpreyfromambush(sit-and-waitbehavior)anddependonthesoundgenerated
bypreyforlocalizethesitewithprey[12–14].Becausetheirwingsareshort,withalargesur-
faceareaandroundedtips,gleaninganimalivoreshaveverymaneuverableflightandcanoccu-
pysiteswithdensevegetation[8].However,siteswithhighlyclutteredvegetationhinder
obstacleavoidanceandmaylimitpreyperceptionbyecholocation[13–15].Frugivorousand
nectarivorousbatstendtobelessagileinnarrowspaces,buttheirlongnarrowwingsallowa
slowerandefficientflight.
Foragingstrategiesvarybetweencanopyandunderstorybats[16–18].Canopyfrugivores
forageontreesthatareusuallypatchilydistributedandproduceagreatquantityoffruitsfora
relativelyshortperiod.Thesebatsspendmostofthenighttravelinglongdistancesbetween
areasinsearchoftreeswithripefruits.Moreopenareasfacilitateflightintotheforest[19–21].
Understoryfrugivoresconsumefruitsonshrubsandsmalltreeswithmorelocalizeddistribu-
tion,whichproducefewerripefruitspernight,butwithproductionextendingoverweeksor
months.Thesespecieshaveshorterflightswithinasmallarea.
Processesthatoccuronasmallspatialscalemayplayanimportantroleinstructuringas-
semblagesatwiderscales[22].Microhabitatcharacteristics(e.g.,canopyheight,foliagestruc-
ture)areknowntoinfluencetropicalandtemperatebatensemblesatintermediatetolocal
scales[23–28].Thephysicalobstructionofvegetationimposeslimitationsonmobilityand
fooddetectionbybats,changingthenumberandtypeofbatspeciesthatcancoexistonalocal
scale.Therefore,itseemsreasonablethatvegetationcluttermayalsoincreasebetadiversitybe-
tweensitesatregionalscales.
Althoughvegetationclutterisknowntoexertastronginfluenceontheabundanceandspe-
ciescompositionofbats[1,2,4,29–31],manystudiesusedqualitativedescriptionsofvegetation
clutter(e.g.edge,open,structurallycomplexvs.simple),ratherthandirectmeasurementsof
vegetationdensity,andfewstudieshaveevaluatedtheeffectofvegetationclutterataregional
scale[28].Inthisstudy,weevaluatetheinfluenceofthephysicalobstructionofvegetationon
Phyllostomid-batassemblagesataregionalscale,coveringa520kmtransectinCentralAma-
zonia.Wehypothesizedthatvegetationstructure,consideredausefulpredictorofthedistribu-
tionofPhyllostomidbatsatthelocalscale,alsoinfluencesbatassemblagesataregionalscale.
Wealsoassessedwingmorphologyofthespeciestotesttherelationshipbetweenspeciesdistri-
butionalongthegradientofvegetationclutterandwingmorphology(aspectratioandwing
load)ofthespecies.Weexpectedthatchangesinassemblagecompositionwouldbemediated
mainlybydecreaseinabundanceandnumberofspeciesinclutteredvegetation.Becauseofthe
differentforagingstrategyoftheguilds,wealsopredictedthatspecieswouldbedistributedina
nestedpatternalongthegradientofvegetationclutterataregionalscale,withanimalivorous
andunderstoryfrugivorousbatspresentinbothopenanddensevegetationandcanopyfrugi-
voresrestrictedtomoreopenvegetation.
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 2/16
EffectofVegetationClutterinBats
Methods
EthicsStatement
WefollowedtheguidelinesapprovedbytheAmericanSocietyofMammalogistsinourproce-
dures[32].Allcapturedbatswerehandledbyexperiencedaninvestigator.Capturedbatswere
keptinclothbagsindividuallyfortheminimumpossibletimeandwerereleasedattheplace
wheretheywerecaptured.VoucherspecimenswerecollectedanddepositedintheMammal
CollectionoftheInstitutoNacionaldePesquisasdaAmazônia(INPA6418-INPA6726).Bat
capturesandhandlingwereinaccordancewithBrazilianconservationandanimalwelfare
laws,andwasundertakenunderscientificlicensesfromtheInstitutoChicoMendesdeConser-
vaçãodaBiodiversidade—ICMBio(Permitnumbers25781–1and25799–2).
StudyareaandSamplingDesign
Batassemblagesweresampledalonga520-kmsectionoftheBR-319highwaythatconnects
themunicipalitiesofManausandHumaitá,betweenthePurusandMadeiraRiversinCentral
Amazonia(Fig1).Thevegetationisclassifiedasdensetropicallowlandforestinthenorthern
partoftheBR-319highwayandopentropicallowlandforestsinthesouthernpart,near
Humaitá[33].Inthecentralpartoftheinterfluve,themaximumannualrainfallisaround
2800mm,whileinthenorthernandsouthernparts,nearManausandHumaitá,themaximum
annualrainfallisaround2400mm.Thenumberofdrymonths(precipitationbelow100mm)
peryearvariesfromtwotofourmonths[34].
Batswerecapturedin80permanentplotsdistributedineightsamplingmodulesthatare
partoftheBrazilianBiodiversityResearchProgram(PPBio;http://ppbio.inpa.gov.br).The
moduleswereinstalledatintervalsrangingfrom40to60kmalongtheBR-319highway
(Fig1).Eachmoduleconsistsoftwo5kmparalleltrails,withtenplotsdistributedat1kmin-
tervals,followingtheRAPELDsamplingdesign[35,36].Eachplotwas250mlongandfol-
lowedthealtitudinalterraincontourinordertominimizevariationintopographyandsoil
properties,andconsequently,variationinthevegetationtypewithineachplot[35].
BatCaptures
BatswerecapturedbetweenOctoberandNovember2010andbetweenJuneandNovember
2011,duringthedryseason.Weusedeightmistnets(12×3m,19mmmesh,Ecotone,Poland)
installedatgroundlevelalongthecenterlineofeachplot.Netsremainedopenfrom18:00to
00:00handwerecheckedatintervalsof30–45minutes.Eachplotwassampledforonenight,
totaling10capturenightsand480mist-nethours(mnh)effortpermodule(onemnhdenotes
one12-mnetopenfor1h).Nightswithfullmoonorstrongrainswerenotsampledinorderto
minimizepotentialbiasincapturesuccess.
Batswereidentified,measuredandweighedbeforerelease.Weidentifiedbatsusingkeysof
LimandEngstrom[37]andGardner[38],supportedbybatdescriptionsofCharles-Domi-
niqueetal.[39]andSimmonsetal.[40].IndividualsofthegenusCarolliaweregroupedas
Carolliaspp.becauseitwasnotpossibletodistinguishC.perspicillataandC.brevicaudabased
onexternalcharactersmeasuredinthefield.Thesespecieshavethesameforagingstrategyand
arefrugivores[41–43].Basedontheirhabitattype,foragingmode,andecholocationbehavior
reportedintheliterature[12,16,30,43,44],specieswerecategorizedintosixfeedingguilds:clut-
tered-spacepassive-gleaningforagers(includinggleaninginsectivoresandcarnivores;hereafter
denotedgleaninganimalivores),cluttered-spacepassive/active-gleaningforagers(canopyfrugi-
vores,understoryfrugivores,andnectarivores),edge-spaceaerialforagers,andedge-space
trawlingforagers.
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EffectofVegetationClutterinBats
Fig1.Mapofthestudyareashowingtheeightsamplingmodulesalongthe520-kmsectionoftheBR-319highway,CentralAmazonia.
doi:10.1371/journal.pone.0129560.g001
VegetationClutter
Weestimatedthedensityofunderstoryvegetationusingdigitalphotographs,adaptedfrom
Marsdenetal.[45].Awhiteclothmountedina3×3maluminumframewasplaced8mfrom
thecentrallineoftheplotandpositionedperpendiculartoadigitalcamera(S1Fig).Were-
cordedonephotographforeachmistnet,totalingeightphotographsperplotand80
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 4/16
EffectofVegetationClutterinBats
photographspermodule.Wetransformedthephotosintoblack-and-whiteimagesusingSide-
look1.1.01program[46],sothatblackareasrepresentedvegetation.Thevegetationclutterof
eachmodulewasestimatedastheaveragepercentageofareacoveredbyvegetation(trunks,
branches,twigs,andleaves)inthe80photographs.
DataAnalysis
WeonlyanalyzeddataonbatsofthefamilyPhyllostomidaesincespeciesfromotherfamilies
arenotadequatelysampledwithmistnets[11].Onlyfrugivores,gleaninganimalivores,and
nectarivoresoccurinthefamily.Weevaluatedinventorycompletenesswithsample-basedrar-
efactioncurvesbasedonspeciesabundancerandomized1000times[47].Inaddition,weesti-
matethespeciesrichnessusingtheJackknife1estimatorandcomparedittotheobserved
numberofspeciestoestimatethepercentageofinventorycompleteness.Rarefactioncurves
andJackknife1estimatorwerecalculatedwithEstimateSsoftware9.1.0[48].
AnordinationbyNon-metricMultidimensionalScaling(NMDS)wasusedtoreducethedi-
mensionalityofthespecies-occurrencedata(presence-absence)inthemodulestooneordina-
tionaxis[49].ThedissimilaritybetweenpairsofmoduleswascalculatedusingtheSørensen
index.WecalculatedtheNMDSstressasameasureofgoodnessoffittoindicatehowwellthe
ordinationpreservestheoriginaldistancerelationshipsamongthesamples[49].Stress
values<0.2arerecommended[49].Weusedgeneralizedlinearmodels(GLM)toevaluatethe
effectofvegetationclutteronthetotalnumberofspeciesandabundance,numberofspecies
andabundanceoftheallfrugivorous,canopyfrugivorous,understoryfrugivorous,andanimal-
ivorousbats,andbatspeciescomposition(summarizedbythesingleNMDSaxis).Theover
dispersionoftheresidualsintheGLMmodelswascontrolledusingaquasi-GLMregression
modelforrichnessandabundanceofspeciesandguilds[50].
Thespeciesdistributioninrelationtodifferencesinvegetationclutterbetweenmoduleswas
evaluatedbydirect-gradientanalysis(Fig2).Inthisanalysis,themoduleswereorderedinrela-
tiontothegradientinvegetationclutter.Thespecieswereorderedbytheaveragenumberof
capturesweightPedbyvegetationclutterofeachmodule,accordingtothefor-
mula:Rank¼ð ½n (cid:2)clutter(cid:3)Þ=N,wherenijrepresentthenumberofcapturesofthespecies
ij j i
iinthemodulej,clutter istheaveragevegetationcluttervalueinmodulej,andN isthetotal
j i
numberofcapturesofthespeciesi.Highervaluesrepresentspeciescapturedinmoduleswith
moreclutteredvegetation.Therankvaluesofthespeciesabundanceweightedbythevegetation
clutteroftheanimalivorousandallfrugivorousspecieswerecomparedwithattest,anddiffer-
encesamonganimalivorous,canopy-frugivorous,andunderstory-frugivorousspecieswere
comparedusinganAnalysisofVariance(ANOVA)followedbyapost-hocTukeytest.
Weevaluatedwhetherthestructureofthebatassemblagesgeneratedbydirect-gradient
analysisshowedanestedpatternofspeciesdistributionamongmodules.Nestednessoccurs
whensiteswithlowerspeciesrichnesstendtoharborsubsetsofspeciespresentinrichersites.
WeappliedthemetricNODF(NestednessMetricBasedonOverlapandDecreasingFill;[51])
withalgorithmSIM2[52]thatislesspronetotypeIerrorinanalysisofstandardized"sample
lists"ofspeciescollectedinrapidecologicalsamplingwithminorcontributionofrarespecies.
NODFisconsideredarobustmetricforstudieswithlownumbersofspecies,andtoinsensitive
toshapeandsizeofthedatamatrix[51].Weusedanullmodeltoevaluatewhetherthestruc-
tureofthebatassemblagesgeneratedbydirect-gradientanalysisdiffersfromarandomdistri-
butionofspecies[53].Theprobabilitywasbasedon10000randomizations.AstheNODF
metricisdependentonthearrangementofcolumnsandrowstoallowtestinghypotheseson
thecausesofnestedness,positionsofspeciesandmodulesinthenullmodelwererestrictedto
thoseofthedirectgradientanalysis(Fig2)inwhichbatspecieswerecolumnsandmodules
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 5/16
EffectofVegetationClutterinBats
Fig2.Relationshipbetweenbatabundanceandthegradientofvegetationclutter.Thehorizontalorderofthesamplingmoduleswasbasedonthe
gradientinvegetationclutter.Theverticalorderofspecieswasbasedontheaveragenumberofcapturesweightedbyvegetationclutterofeachmodule,as
indicatedbyrankvalues.Specieswithhigherrankvaluesareplacednearthetopofthegraph.Blacksquaresrepresentgleaninganimalivorousbats,white
squarescanopyfrugivores,greysquaresunderstoryfrugivores,andhatchedsquaresthenectarivore.
doi:10.1371/journal.pone.0129560.g002
wererows.TheNODFcvaluequantifiesthenestedstructureofthemodulesinrelationto
vegetationclutter.
Toevaluatewhetherthespeciesdistributionalongthegradientofvegetationclutterwasas-
sociatedwithwingmorphology,werelatedtherankvaluesofthespeciesabundanceweighted
bythevegetationclutterwithwingcharacteristics(aspectratioandwingload)usingaquasi-
GLMmodel.Highvaluesofaspectratioandwingloadindicatespecieswithfasterflightand
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 6/16
EffectofVegetationClutterinBats
lowermaneuverability[8].AspectratioandrelativewingloadwereobtainedfromMarinello
andBernard[54]forbatsofCentralAmazonia.AspectratioandwingloadofVampyressa
brockiwerenotfoundintheliteratureandthespecieswasexcludedfromtheanalysis.
Thenectarivoreswerenotincludedintheanalysisbecauseofthelownumberofcaptures
andspecies.Wecomparedaspectratioandwingloadbetweenanimalivorousandallfrugivo-
rousspecieswithattest,andbetweenanimalivorous,canopyfrugivorous,andunderstory
frugivorousspeciesusinganAnalysisofVariance(ANOVA)followedbyapost-hoc
Tukeytest.
Geographicalautocorrelationofspeciesabundancebetweenpairsofmodulesmayviolate
statisticalassumptionsofanalysesandleadtoinappropriateconclusionsinstudiesthatcorre-
latespeciesdistributionwithenvironmentalfactors[55].Wetestedthespatialautocorrelation
intheresidualsoftheGLMtestsusingMoran'sIstatistics.Thedistanceclasseswereadjusted
tointervalsof40km(minimumdistancebetweenmodules)andusedanequalnumberof
modulesforeachdistanceclass.Moran'sIstatisticwastestedforsignificanceusing1000per-
mutations.WedidnotdetectautocorrelationintheresidualsoftheGLMtests,indicatingthat
theresponsevariablesofthemoduleswerespatiallyindependent.
AnalyseswerecarriedoutwiththeRsoftwareversion3.1.1[56].TheNMDSordinationand
nullmodeltotestthesignificanceofthenestednesspatternwereundertakenintheRpackage
‘vegan’[57].ThenullmodelwasgeneratedwiththeoecosimufunctionandNMDSwiththe
metaMDSfunction.SpatialautocorrelationanalyseswereperformedinSAMsoftwarev.4.0
[58].ThedataandmetadataaredepositedinthepublicrepositoryofthePPBio(http://ppbio.
inpa.gov.br/repositorio/dados).Toaccessthedatausethekeywords"morcegos","BR-319",
and"clutter".
Results
After3840mnh(80nightsofsampling),wecaptured512batsof27speciesfromfourfamilies
(Emballonuridae,Phyllostomidae,Vespertilionidae,andThyropteridae)(Table1).Phyllosto-
midbatsaccountedformost(98.2%)captures(Table1).Mostspecies(12)werefrugivoresand
theyaccountedformostcaptures(n=413),followedbygleaninganimalivores(10speciesand
70captures)andnectarivores(1speciesand19captures).Amongthefrugivorousbats,the
threeunderstoryspeciesaccountedfor328ofthecaptures,whilethecanopyfrugivoresac-
countedfor86capturesdistributedinninespecies(Table1).Thenumberofphyllostomidspe-
ciesrecordedineachmodulerangedfrom8to16(11.8±3.2,mean±SD)andthenumberof
capturespermodulerangedfrom13to137bats(62.9±46.3).Theninespecieswithmorethan
10individualscapturedaccountedfor89%ofallcaptures.Lophostomasilvicolumwastheonly
speciescapturedinallmodules,andArtibeusconcolor,Chrotopterusauritus,Rhinophylla
fischerae,andVampyriscusbrockiwereeachcapturedinonlyonemodule.Carolliaspp.andR.
pumiliowerethetaxamostcapturedandrepresented34%and33%ofallcapturedindividuals,
respectively(Table1).Species-accumulationcurvesandspecies-richnessestimator(S2Fig)in-
dicatedahighlevel(80%)ofinventorycompleteness.
Groundvegetationclutterofthemodulesrangedfrom52.9±14.4%to73±12.8%(Fig2).
Vegetationclutter(Fig3)wasnegativelyassociatedwiththetotalnumberofbatspecies(GLM,
r2=0.82,t=-5.12,P=0.002),numberofanimalivorousspecies(GLM,r2=0.57,t=-2.84,
P=0.030),numberoffrugivorousspecies(GLM,r2=0.60,t=-2.98,P=0.025),numberofun-
derstoryfrugivorousspecies(GLM,r2=0.79,t=-4.76,P=0.003),andabundanceofcanopy
frugivorousbats(GLM,r2=0.55,t=-2.55,P=0.044).Abundanceofallspecies,allfrugivores,
andunderstoryfrugivoresandnumberofcanopyfrugivorousspecieswerenotsignificantly
influencedbyvegetationclutter(P>0.084,r2<0.40).TheNMDSordinationaxis(Fig3)
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 7/16
EffectofVegetationClutterinBats
Table1. BatscapturedineightmodulesalongtheBR-319highway,CentralAmazonia,Brazil.
Taxon Captures Range Modules Guilds
Emballonuridae
Saccopteryxbilineata 1 0–1 1 Edgespaceaerialforager
Phyllostomidae
Carollinae
Carolliaspp. 167 0–86 6 Clutteredspacepassive/activegleaningforager—understoryfrugivore
Rhinophyllafischerae 1 0–1 1 Clutteredspacepassive/activegleaningforager—understoryfrugivore
Rhinophyllapumilio 160 3–33 8 Clutteredspacepassive/activegleaningforager—understoryfrugivore
Lonchophyllinae
Lonchophyllathomasi 19 0–7 7 Clutteredspacepassive/activegleaningforager—nectarivore
Phyllostominae
Chrotopterusauritus 1 0–1 1 Clutteredspacepassivegleaningforager
Lophostomabrasiliense 2 0–1 1 Clutteredspacepassivegleaningforager
Lophostomasilvicolum 13 1–3 8 Clutteredspacepassivegleaningforager
Micronycterismegalotis 6 0–2 5 Clutteredspacepassivegleaningforager
Mimoncrenulatum 6 0–2 4 Clutteredspacepassivegleaningforager
Phyllodermastenops 4 0–1 4 Clutteredspacepassivegleaningforager
Phyllostomuselongatus 13 0–4 5 Clutteredspacepassivegleaningforager
Tonatiasaurophilla 8 0–2 5 Clutteredspacepassivegleaningforager
Trachopscirrhosus 15 0–5 5 Clutteredspacepassivegleaningforager
Trinycterisnicefori 2 0–2 1 Clutteredspacepassivegleaningforager
Stenodermatinae
Artibeusconcolor 1 0–1 1 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Artibeusgnomus 18 0–7 5 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Artibeuslituratus 4 0–2 3 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Artibeusobscurus 31 0–18 7 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Artibeusplanirostris 12 0–6 3 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Mesophyllamacconnelli 6 0–3 2 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Urodermabilobatum 4 0–2 3 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Vampyriscusbidens 9 0–3 6 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Vampyriscusbrocki 1 0–1 1 Clutteredspacepassive/activegleaningforager—canopyfrugivore
Vespertilionidae
Myotissp. 3 0–2 2 Edgespacetrawlingforager
Thyropteridae
Thyropteradiscifera 1 0–1 1 Edgespaceaerialforager
Thyropteratricolor 4 0–2 3 Edgespaceaerialforager
Total 512 13–137
doi:10.1371/journal.pone.0129560.t001
explained76%ofthetotalvariation(NMDSstress=0.17)andwasassociatedwithvegetation
clutter(GLM,r2=0.79,t=-4.72,P=0.003).
BatassemblagesoftheBR-319highway(Fig2)showedanestedstructure(NODFc,
Fill=51%,nestednessdegree=67.25,Z=2.63,P=0.008).Thespeciescompositioninmodules
withmoreclutteredunderstoryrepresentedasubsetofthespeciesinthemoduleswithmore
openvegetation.Themodulewithmostopenvegetation(53%clutter)hadtwiceasmanyspe-
ciesasthemoduleswithdensestvegetation(>70%clutter).Onlythreespecies(Trinycteris
nicefori,Lophostomabrasiliense,andVampyriscusbidens)inmoduleswithhighclutterwere
notcapturedinthemoduleswithmoreopenvegetation.Asvegetationclutterdecreased,more
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 8/16
EffectofVegetationClutterinBats
Fig3.Relationshipsbetweenvegetationclutterand(A)numberofbatspecies,(B)bat-speciescompositionsummarizedbythefirstaxisofa
NMDSanalysis,(C)numberofgleaninganimalivorousspecies,(D)numberoffrugivorousspecies,(E)numberofunderstoryfrugivorousspecies,
and(F)abundanceofcanopyfrugivores.
doi:10.1371/journal.pone.0129560.g003
specieswereaddedtothebatassemblages,especiallycanopyfrugivorousbats,suchasMeso-
phyllamacconelli,V.brocki,A.concolor,A.gnomus,A.obscures,andA.planirostris(Fig2).The
rankvaluesofabundanceweightedbythevegetationclutter(Fig2)oftheanimalivoreswas
greaterthanforfrugivorousbats(ttest,t=3.08,P=0.007).Animalivorousbatsalsohada
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 9/16
EffectofVegetationClutterinBats
Fig4.Relationshipbetweenrankvalues(meannumberofcapturesweightedbyvegetationclutterofeachmodule)andwingmorphology(wing
loadandaspectratio)of21batspeciescapturedalongtheBR-319highway,CentralAmazonia.
doi:10.1371/journal.pone.0129560.g004
rankvaluegreaterthancanopyfrugivores(ANOVA,F=4.70,P=0.022,Tukeytest,P=0.024;
Fig2),butnotsignificantlydifferentfromunderstoryfrugivores(Tukeytest,P=0.16).Rank
valuesdidnotdifferbetweencanopyandunderstoryfrugivorousbats(Tukeytest,P=0.99).
Thisindicatesthatanimalivorousandunderstoryfrugivorousbatsweremoreabundantand
havehigheroccurrencealongthevegetationcluttergradient,whilecanopyfrugivorousbats
werelargelyrestrictedtomoduleswithmoreopenvegetation(Fig2).Nevertheless,therank
values(Fig4)werenotcorrelatedwithmeanaspectratio(GLM,r2=0.17,t=-0.61,P=0.55)
orwingload(GLM,r2=0.11,t=0.92,P=0.37).Theaspectratio(ttest,t=2.79,P=0.018)
andwingload(ttest,t=5.68,P<0.0001)ofthespeciescapturedwerehigherforfrugivores
thanforgleaninganimalivores.Wingloadofthecanopyandunderstoryfrugivoreswashigher
thanforgleaninganimalivores(ANOVA,F=15.68,P<0.0001),whileaspectratiodiffered
onlybetweenunderstoryfrugivoresandanimalivores(ANOVA,F=4.17,P=0.033).Wing
characteristicsdidnotdiffersignificantlybetweencanopyandunderstoryfrugivores(Tukey
test,P>0.88).
Discussion
Ground-vegetationclutterinfluencedthestructureofbatassemblagesataregionalscaleinour
studyareainCentralAmazonia.Thedecreaseinthetotalnumberofspeciesandguildsin
densevegetationwasresponsibleformostofthedifferenceinbat-speciescompositionbetween
modules.Overall,thenumberofspeciesinthemoduleswithmoreclutteredvegetation
(>72%)washalfthatofthemoduleswithmoreopenvegetation(<55.6%).Reductioninthe
numberofbatspeciesinsiteswithclutteredvegetationhasalsobeendocumentedinother
PLOSONE|DOI:10.1371/journal.pone.0129560 June12,2015 10/16