Diversity of fruit-feeding butterflies in a mountaintop archipelago of rainforest

20 Pages·2017·22.4 MB·English

RESEARCHARTICLE
Diversity of fruit-feeding butterflies in a
mountaintop archipelago of rainforest
GeanneCarlaNovaisPereira1*,MarcelSerraCoelho1,2,MarinadoValeBeirão1,3,Rodrigo
FagundesBraga4,5,GeraldoWilsonFernandes1
1 UniversidadeFederaldeMinasGerais/EcologiaEvolutiva&Biodiversidade/DBG,ICB/,BeloHorizonte
MG,Brazil,2 UniversidadeEstadualPaulista,InstitutodeBiociências,DepartamentodeBotaˆnica,
Laborato´riodeFenologia,RioClaro,SãoPaulo,Brazil,3 UniversidadeFederaldeOuroPreto,Programade
EcologiadeBiomasTropicais,CampusMorrodoCruzeiro,OuroPreto,MinasGerais,Brazil,4 Universidade
FederaldeLavras,SetordeEcologiaeConservac¸ão,CampusUniversita´rio,Lavras,MinasGerais,Brazil,
5 UniversidadedoEstadodeMinasGerais,UEMG,UnidadeDivino´polis,Divino´polis,MG,Brazil
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a1111111111 *[e-mail]
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a1111111111 Abstract
Weprovidethefirstdescriptionoftheeffectsoflocalvegetationandlandscapestructureon
thefruit-feedingbutterflycommunityofanaturalarchipelagoofmontanerainforestislands
intheSerradoEspinhac¸o,southeasternBrazil.Butterflieswerecollectedwithbaittrapsin
OPENACCESS
elevenforestislandsthroughbothdryandrainyseasonsfortwoconsecutiveyears.The
Citation:PereiraGCN,CoelhoMS,BeirãoMdV,
influenceoflocalandlandscapeparametersandseasonalityonbutterflyspeciesrichness,
BragaRF,FernandesGW(2017)Diversityoffruit-
feedingbutterfliesinamountaintoparchipelagoof abundanceandcompositionwereanalyzed.Wealsoexaminedthepartitioningandde-
rainforest.PLoSONE12(6):e0180007.https://doi. compositionoftemporalandspatialbetadiversity.Fivehundredandtwelvefruit-feeding
org/10.1371/journal.pone.0180007
butterfliesbelongingtothirty-fourspecieswererecorded.Butterflyspeciesrichnessand
Editor:PetrHeneberg,CharlesUniversity,CZECH abundancewerehigheronislandswithgreatercanopyopennessinthedryseason.Onthe
REPUBLIC
otherhand,islandswithgreaterunderstorycoveragehostedhigherspeciesrichnessinthe
Received:January20,2017 rainyseason.Instead,thebutterflyspeciesrichnesswashigherwithlowerunderstorycov-
Accepted:June8,2017 erageinthedryseason.Butterflyabundancewasnotinfluencedbyunderstorycover.The
landscapemetricsofareaandisolationhadnoeffectonspeciesrichnessandabundance.
Published:June30,2017
Thecompositionofbutterflycommunitiesintheforestislandswasnotrandomlystructured.
Copyright:©2017Pereiraetal.Thisisanopen
Thebutterflycommunitiesweredependentonlocalandlandscapeeffects,andthemecha-
accessarticledistributedunderthetermsofthe
CreativeCommonsAttributionLicense,which nismofturnoverwasthemainsourceofvariationinβdiversity.Thepreservationofthis
permitsunrestricteduse,distribution,and mountainrainforestislandcomplexisvitalforthemaintenanceoffruit-feedingbutterflycom-
reproductioninanymedium,providedtheoriginal
munity;oneislanddoesnotreflectthediversityfoundinthewholearchipelago.
authorandsourcearecredited.
DataAvailabilityStatement:Allrelevantdataare
withinthepaper.
Funding:TheauthorsthanktheProgramade
Introduction
PesquisasEcolo´gicasdeLongaDurac¸ão(PELD
Cipo´),theprojectComCerrado,Coordenac¸ãode Mechanismsthatmaintainthestructureofcommunitieshavearousedgreatinterestfromthe
Aperfeic¸oamentodePessoaldeN´ıvelSuperior scientificcommunity[1].Environmentalconditionscanplayapercussiverole,orfilters,facili-
(CAPES),ConselhoNacionaldeDesenvolvimento
tatingorhinderingtheestablishmentofspecies[2,3].Environmentalparameters,indicativeof
Cient´ıficoeTecnolo´gico(CNPq),Fundac¸ãode
environmentalstructure,functionasafilterinthestructuringofcommunities,preventingthe
AmparoàPesquisadeMinasGerais(FAPEMIG),
establishmentofsomespecies[4,5].Thesefilterscanbeglobal(e.g.effectsofclimate),regional
theReservaVelloziaforthefinancialandlogistical
support. (e.g.,effectsoflandscape)andlocal(e.g.,effectsofhabitat).Ecologicalrelationshipsthatare
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Butterfliesinmountaintoprainforestislands
Competinginterests:Theauthorshavedeclared antagonistic(e.g.,predation,herbivory,parasitism,competition)ormutualistic(pollination,
thatnocompetinginterestsexist. facilitation),mayrepresentthemostimportantstructuringmechanismsofbiologicalcommu-
nities,havingthepotentialtoinfluencethedistributionofspeciesalongenvironmentalgradi-
ents[5].
Fruit-feedingbutterfliesareexcellentmodelsfortestinghypothesesregardingtheeffects
ofenvironmentalfiltersintropicalbiologicalcommunities.Theiruseisfacilitatedbythe
availabilityofrelativelysimpleandcheaptrappingmethodsthatpermitreplicationand
standardizationofsamplingforcomparisonsamongdifferentenvironments,besidesbeing
taxonomicallywellknown[6].Amonglocalfactorsthataffecttropicalforestbutterflycommu-
nities,thefrequencyandintensityofclearings,microclimate(e.g.,temperature,windand
rain),luminosity,presenceofhostplantsforcaterpillarsandfoodresourcesforadultsareof
greatrelevance(e.g.[7–9]).Thesefactorsarestronglyrelatedtovegetationstructure[10],
whichisacomponentofessentialhabitatforbutterfliesgivenitsrelationshiptothermoregula-
tionandtheprovisionofrestingandmatinglocations[11,12].Forestbutterflycommunities
arealsoinfluencedbystructuralfactorsofthehabitat,suchastopography,verticalstratifica-
tion,edgeeffect,matrixqualityasdifferentlevelsofdisturbanceorevenmatrixofnatural
grasslands[13–16].Twovariablescanbeeasilymeasuredtocharacterizelocalorhabitatstruc-
ture:opennessofthecanopyandunderstorycover.Canopyopennessisrelatedtothelevelof
humidityandtemperature;themoredenseorclosedthecanopy,thelesssolarincidenceand
themorehumidbecomesthehabitat[8].Often,speciesrichnessandabundanceofinsects
tendtobegreaterinforesthabitatswithmoreopencanopies(e.g.[8,17]),includingbutterflies
[18],howeversomegapsresultedbyanthropicimpactscancauseoppositeeffects[19].The
densityorcoverageofunderstoryvegetationisanotherimportanthabitatvariablethatinflu-
encecommunitystructure.Highdensityofunderstoryvegetationcanhindertheforagingand
reproductiveactivitiesofbutterflies,resultinginadeclineinspeciesrichness(e.g.[20,21]).
Regionalfactorsaffectingbutterflycommunitiesintropicalforestsincludefeaturesofthe
landscapethatinfluencetheentiresystemviaedgeeffects[22].Areaanddegreeofisolationof
forestfragmentsareimportantmetricsforinsectcommunities.Areacaninfluenceresource
abundanceandthestructuralcomplexityofvegetation[10,23–25].Therefore,speciesrichness
canbepositivelycorrelatedwithareaandnegativelywithisolation[26–28].However,this
topicisnotcompletelyunderstoodforinvertebrates.Therearecorrelationsofincreased(e.g.
[23,29,30],decreased(e.g.[31])andabsenceofeffect(e.g.[32,33])betweenspeciesrichnessof
invertebratesandarea.Thespeciesrichnesscandeclinewithincreasedisolationinsimple
landscapesandsmallfragments,butnotincomplexlandscapesandlargefragments[34].Spe-
ciesrichnessisdeterminedbyabalancebetweenareaorisolation,whereinthenumberofspe-
ciestendstobecomeconstantovertimeduetothecontinuousprocessofreplacementof
speciesorturnover[26,35–37].Somebutterflieshavelargethoraxvolumescombinedwith
comparativelyshorterforewinglengthsallowinglongflights.Speciallythosebutterflieswith
adaptivemorphologiespermitforagingflightsunderaregionalscale[24].Itisalsoexpected
thatspeciesrichnessofforestspecialistsincreasewithincreasingconnectivityamongfrag-
ments,aswellaswiththeareaofadjacentforestfragments,asalreadydocumentedforbutter-
flies(see[38]).Largefragmentsorcontinuousareasofforestcanfunctionasacontinentina
source-sinksystemandtheclosestfragmentsassteppingstones(see[39]),facilitatingthe
movementofspeciesamongfragmentsinapossiblemetacommunitydynamic(see[40]).
Localandregionalenvironmentalparametersalsoactsynergisticallytoproduceandmain-
tainpatternsofdiversity,bothinspaceandtime.Habitatstructurealsohasastronginfluence
onpatternsofbetadiversityofarthropods[41].Betadiversityreferstothediversityamong
habitats,andthedifferenceinspeciescompositionamonglocationsorintervalsoftime[42].
Thisdifferencecanbeexplainedbythesubstitutionofspecies(turnover)orthelossofspecies
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Butterfliesinmountaintoprainforestislands
(nesting)dependingontheintensityoflocalandregionalforcesactingonthecommunity
[43].Responsestohabitatheterogeneityvaryamongbutterflysubfamiliesaccordingtothe
foraginghabitatsandadaptations[19].Seasonalityisalsorecognizedasastrongdriverofbut-
terflycommunities.Seasonalityisverydeterminanttoplantphenology,andbutterflycommu-
nitiesfollowthosecirclesofresourcesavailability[44,45].
Naturallyfragmentedlandscapesrepresentanimportantscenariowhereonecanobserve
theforcesthatshapecommunitystructure[33].Althoughwidelystudiedinislands(e.g.
[32,46])andartificiallyfragmentedareas(e.g.[47–51]),therearefewstudiesonbutterfliesin
naturallyfragmentedenvironments[52,53].Itislikelythatdifferentprocessesleadtodifferent
patternsinislandswithnaturalvegetation.Naturalfragmentedforestscanbefoundinthe
highestpoints(above1200metersinelevation)intheEspinhac¸omountainrangeinsoutheast-
ernBrazil,immersedinrupestriangrasslandvegetationmatrix[16].Theseislandsofrainforest
vegetationrequirespecificclimateandsoiltodevelop,beingfoundinerosionvalleys,inloca-
tionswithoutboulders,coveringhills,andformsatruenaturalarchipelagoofforestvegetation
stronglyassociatedwiththeregionsofheadwaters,rivers,creeksandsmallstreams[16,54,55].
Thepatternsofdiversityoffruit-feedingbutterflycommunitieswereanalyzedinanarchi-
pelagoofnaturalislandsofAtlanticrainforestintheEspinhac¸omountainrange,Brazil.Inthis
studywetestedthefollowinghypotheses:i)theopennessofthecanopyhasapositiveeffecton
therichnessandabundanceofbutterflies;ii)thecoverageoftheunderstoryhasanegative
effectontherichnessandabundanceofbutterflies;iii)therichnessandabundanceofbutter-
fliesaregreaterintherainyseasonthaninthedryseason;iv)therichnessandabundanceof
fruit-feedingbutterfliesincreaseswiththesizeofforestislands(e.g.areaandperimeterof
island);v)therichnessandabundanceoffruit-feedingbutterfliesdecreaseswithlevelofisola-
tion;vi)thespeciescompositionoffruit-feedingbutterfliesoftheforestislandsisnotstruc-
turedbychance;vii)thespeciescompositionoffruit-feedingbutterfliesisdependentonboth
local(opennessofcanopyandunderstorycover)andlandscape(areaandisolation)effectsand
seasonality.
Materialsandmethods
Studylocation
ThestudyareawaslocatedinSerradoCipó,municipalityofSantanadoRiacho,MinasGerais,
Brazil(19˚14’19"S43˚31’35"W,Fig1),inthesouthernportionoftheEspinhac¸omountain
range.TheclimateistypeCwb(mesothermalaccordingtotheKo¨ppenclassification)with
humidsummersanddrywinters.Averageannualrainfallrangesfrom1,300to1,600mmand
isconcentratedinthesummer,andaveragetemperaturesarebetween17.4and19.8˚C[56].
Floristically,forestedislandsfoundinSerradoCipóareassociatedwiththeAtlanticForest
domain,withsomeCerradospecies[16].Theelevationofthestudiedislandsvariedfrom1230
to1331metersabovesealevel.Theaverageannualtemperatureoftheregionfor2014and
2015was18.8˚C(datafrommeteorologicalstationsOnsetHOBO1U30data-logger,installed
at1200,1300and1400metersofaltitudeinthestudysite).
Sampling
Sampledesign. Elevenrainforestislandsofdifferentsizeswereselected(Fig1).Three
islandswerelocatedwithintheParqueNacionaldaSerradoCipó(Islands8,9and10)while
theremainderwerelocatedwithinthebufferingparkzonenamedÁreadeProteçãoAmbiental
MorrodaPedreira(hereafterAPA)(Table1)[16].Islandswerechosenconsideringtheirsize
(largeenoughsothatpartcouldbesampledforbutterflies),stateofconservation(preference
forislandswithlowanthropicimpact)andaccessibility(Fig2A,2B,2Cand2D).Thestudied
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Fig1.Mapofthestudyarea,SerradoCipo´,MinasGerais,Brazil(SIGLeebCartografyRapidEyeImage2015).
https://doi.org/10.1371/journal.pone.0180007.g001
islandsvariedinsizefrom12,938m2to358,185m2(Table1).Ineachisland,a50x20mplot
wasestablishedatleast20mfromtheborder,exceptforIslands3,5,8and11,whichwere
closertotheedgeduetotheirsmallsizeandshape(Fig2A).Toobservetheeffectofseasonality
onvariationinbutterflies,twosamplesweremadeperyear,oneduringtherainyseason(Feb-
ruary)andtheotherduringthedryseason(August)forthetwoconsecutiveyearsof2014and
2015.
Butterflycollection. AteachcornerofeachplotaVanSomeren-Rydonbutterflytrap
wasset(n=4traps/island;ntotal=44)(Fig2B).Thetrapsconsistedofa110cmtalland35
cmdiameterfinescreencylinderthatwasclosedatthetop.Thebaseofthetrapconsistedofa
platformonwhicha50mlplasticcupwithbaitwasplaced[57].Trapswerebaitedwithfer-
mentedbananawithsugarcanejuiceataratioof3:1,whichwaspreparedtwodayspriorto
use,andsuspendedbetween70and100cmabovetheground.Butterfliesattractedbythe
smellofthebaitenteredthroughanopeninginthebottomofthecylindertofeed,andwhen
theymovedupwardtheywouldbecometrapped[58].Eachfieldcampaignconsistedoffive
samplingdays,thefirsttosetthetrapsandthefollowingfourtocollectthesampledindividuals
andchangebaitevery24hours.Thetotaleffortwas704days-traps(44trapsx4samplingsx4
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Table1. Area,perimeter,distancetonearestcontinuousforest,distancetoclosestforestisland,altitude,location,andgeographiccoordinatesof
the11forestislandsinSerradoCipo´,Brazil.
Island Area Perimeter Distancetothecontinuous Distancetoclosestforest Altitude Location Coordinates
# (m2) (m) forest(km) island(km) (m)
1 12,938 480 0.88 0.13 1,239 APA S1913’ W4330’
01.97237’’ 28.67035’’
2 84,909 1,807 1.14 0.56 1,235 APA S1911’ W4330’
58.18605’’ 31.58434’’
3 16,316 857 1.4 0.11 1,234 APA S1912’ W4330’
47.65259’’ 46.21099’’
4 169,562 2,836 2.06 0.78 1,269 APA S1913’ W4330’
34.60436’’ 55.97316’’
5 29,716 911 5.47 0.23 1,309 APA S1914’ W4332’
21.24191’’ 26.10892’’
6 113,399 2,220 7.37 0.19 1,317 APA S1915’ W4333’
10.76660’’ 07.45422’’
7 58,653 1,192 7.35 0.1 1,331 APA S1914’ W4333’
40.91360’’ 20.64709’’
8 57,557 1,366 2.49 0.34 1,271 Park S1914’ W4330’
19.32289’’ 45.68173’’
9 358,185 3,685 3.5 0.3 1,230 Park S1915’ W4331’
18.03651’’ 01.00603’’
10 82,375 1,502 6.2 0.21 1,324 Park S1915’ W4332’
34.38313’’ 32.32418’’
11 16,113 675 6.91 0.3 1,273 APA S1914’ W4333’
52.58462’’ 03.19909’’
https://doi.org/10.1371/journal.pone.0180007.t001
samplingdays).Collectedindividualsweresacrificedbythoraciccompressionandplacedin
entomologicalenvelopeswithsamplingdata,includingdate,islandnumberandtrapnumber,
forlateridentification.Inthelaboratory,individualswereidentifiedtothelowestpossibletax-
onomiclevelusingguides[59–61]andthehelpoftaxonomists.Afteridentification,threeindi-
vidualsofeachspecies(wheneverpossible)weremounted,correctlypreparedanddeposited
intheLaboratóriodeEcologiaEvolutiva&Biodiversidade,oftheUniversidadeFederaldeMinas
Gerais.
Canopyopenness. Toevaluatecanopyopennessofislands,hemisphericalphotoswere
takenwithafisheyelensattachedtoaPentaxdigitalcamerafromeachofthefourcornersof
eachplotofeachisland.Thephotosweretakenat1.50mabovethegroundandthenprocessed
fortheproportionofwhiteandblackpixels,whichwereaveragedoverthefourphotostogeta
singlevalueofcanopyopennessforeachisland.Thesedatawerecollectedduringallperiodsof
butterflysamplinginbothseasons.TheimageswereprocessedusingtheRsoftwarepackage
“ReadImages”[62]and“RT4Bio”[63].
Understorycover. Digitalimagesofshrubbyandherbaceousvegetationwereusedto
measuretheinfluenceofunderstoryvegetationcoveronthebutterflycommunity.Thevegeta-
tionwasphotographedatthecornerofeachplotusinga100cmx100cmwhitescreenasa
backdropwiththecamerapositionedatthreemetersfromthescreenandonemeterabovethe
ground[20,64].Fourphotosoftheunderstory,oneineachcardinaldirection,weretakenat
eachcorneroftheplotsforatotalof16photosforeachislandforeachcampaign.Theareasof
thewhitebackdropwerecutfromthephotosandedgesaddedtodefinethepartofthephoto
tobeanalyzedusingthesoftwareGimp2(GnuImageManipulationProgram2.8.14).Very
darkphotoswithpatchesofshadowsorsunwerediscarded.Vegetationcoverisdefinedasthe
ratioofwhiteandblackpixelsinthephotos[20].Theaverageofthevaluesofthephotostaken
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Butterfliesinmountaintoprainforestislands
Fig2. (A)Schematicdrawingof20x50mplotestablishedontheislands(Image@2015CNES/Astrium-Google
EarthPro).(B)VanSomeren-Rydonfrugivorousbutterflytrap.(C):Externalviewoftheislands5.(D)Internalview
oftheisland.
https://doi.org/10.1371/journal.pone.0180007.g002
ateachmeasurementwereusedasavaluefortheunderstorycoverforeachisland.Theimages
wereprocessedusingtheRsoftwarepackage“EBImage”[62].
Landscapeparameters. Thedistanceofeachislandtothecontinuousforestandthedis-
tancetootherislandswereusedasameasureofisolationoftheforestislands[39].Themetrics
ofarea,perimeteranddistancebetweenfragmentswasobtainedwithhelpofthesoftware
FRAGSTATS[65].Aftervectorization,thefilewasconvertedintoaformatcompatibleto
FRAGSTATS(ASCII)[66].Thedistancesbetweenforestislandsweregeneratedfromthe
automateddefinitionoftheanalyzedcentroids.
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Statisticalanalyses
TherichnessestimatorJackknife1wasusedtoestimatespeciesrichness,anonparametric
methodthatutilizesthenumberofrarespeciesthisisfoundinasinglesample(uniques)[67].
Duetothenatureofthedata,twocategoriesofmodelsweredesignedtotestlocal(vegeta-
tionparametersaccordingtoseasonality)andregionalinfluencesonthebutterflycommunity.
AllofthestatisticalanalyseswereperformedusingthesoftwareR[68].
Totesttheeffectofvegetationdependingontheseasonalityonbutterflyspeciesrichness
andabundance,thebutterflycommunityvalueswereusedasresponsevariables(speciesrich-
nessandabundance),whiletheinteractionbetweenvegetationvariables(canopyopenness
andunderstorycoverage)andseasons(dryandrainy)wereusedasexplanatoryvariables.
TheforestedislandswereincludedasrandomfactorsinaGeneralizedLinearMixedModel
(GLMM)[69],usingthe“Poisson”distributionoferrorsforthetwovariables(richnessand
abundance).Theanalysiswasconductedusingthepackage“lme4”[70],withthefunction
“glmer”.Allofthevariablesweretestedtogetherandthenon-significantones(p>0.05)were
removed(stepwise)untiltheminimummodeladequacyisobtained.Thepackage“MuMIn”
[71]wasusedwiththefunction“r.squaredGLMM”[72]toobtainthevalueofR2.Tovisualize
theeffectofthesignificantvariablesusinggraphsweperformedseparateGeneralizedLinear
Models(GLMs).TheGeneralizedLinearModelswereconductedinordertoallowthegraphi-
calinterpretationoftheGeneralizedLinearMixedModelresults.
Totestthehypothesisthatfruit-feedingbutterflyspeciesrichnessandabundanceincreases
withislandsizeanddecreaseswithislandisolation,thebutterflycommunitymetrics(richness
andabundanceofspeciesaccumulatedinallsamplings)wereusedasresponsevariablesand
thevariablesofthelandscape(areaandperimeterofeachisland,distancetotheclosestisland
andtocontinuousforest)wereusedasexplanatoryvariablesinaGeneralizedLinearModel
(GLM)[69]witha“Quasipoisson”distributionoferrorsforbothrichnessandabundance.To
testthediversitybetweentheseason,fruit-feedingbutterflyspeciesrichnessandabundance
persamplewereusedasresponsevariableandtheseasonwereusedasexplanatoryvariablein
aGeneralizedLinearModel(GLM)[69]witha“Quasipoisson”distributionoferrorsforboth
richnessandabundance.
Totestwhatregionalscalemostcontributestothetotalnumberofspeciesinallislandsan
analysisofadditivepartitionofdiversity(β=γ-α)wasused.Thealpha(α)representsthe
diversityofeachisland,thebeta(β)representsdiversitybetweenislands,andthegamma(γ)
representstotaldiversityoftheforestarchipelago.Thepackages“vegan”[73]and“betapart”
[74]wereusedwiththefunctions“adipart”[75],“beta.pair”and“beta.temp”[76].Thediffer-
enceofthediversitybetweentheforestislands(spatialβ)oralongthesamplingtime(temporal
β)canbeduetonestedness(speciesgainorloses)orturnover(speciesreplacementamongthe
forestislandsorsamplingtime)ofspecies.Ananalysisofβpartitionwasmadetotestifthe
temporalandspatialβareduetoturnoverornestedness.Thisanalysiswasmadeusingthe
package“vegan”[73]andresultsinthreeindexes:theSimpsonindex(βSIM)expressesthe
turnover,theSøresenindex(βSOR)expressesthetotalβ,andnestingisexpressedbytheSøre-
senindexminustheSimpsonindex(β )[76].
SNE
Totestthedependenceoflocal,landscapeandseasonaleffectsonbutterflyspeciescomposi-
tion,PermutationalMutlivariateAnalysisofVariance(PERMANOVA)[77]wasperformed
usingthepackage“vegan’[73]andthefunction“adonis”.Forthisanalysis,thebutterflycom-
munitycompositionwasusedastheresponsevariableandthelandscapevariables(perimeter
andareaoftheisland,distancetotheclosestislandandtocontinuousforest),vegetationvari-
ables(canopyopennessandunderstorycoverage)andseasonality(dryandrainy)wereusedas
theexplanatoryvariables.
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Results
Atotalof512fruit-feedingbutterfliesindividualsof34speciesoftheNymphalidaefamily,
belongingtoseventribesandthreesubfamiliesBiblidinae(4individuals),Caraxinae(5indi-
vidual)andSatyrinae(504individuals)werecollected(Table2).Themostabundantspecies
wereGodartianamuscosa(Satyrinae)with189individuals(36.8%),followedbyYphithimoides
straminea(Satyrinae)with69individuals(13.4%)andMoneuptychiasoter(Satyrinae)with44
individuals(8.6%).Ofallthe34species,15weresingletons(representing44.1%ofthespecies).
Noneofthespeciesoccurredonalloftheislands.Speciesrichnessvariedfrom3(Island3)to
18species(Island5)whiletheabundancevariedfrom4(Island6)to100individuals(Island
10)(Table2).BasedontheJacknife1richnessestimator,68.4%ofthespeciespresentwerecol-
lected(estimated49.6species).
Localeffects
Canopyopennessoftheforestislandsvariedfrom7%(island14inthedryseason)to29%
(island10intherainyseason),whiletheaveragecanopyopennesswas12.87%(±4.5SE).The
effectofcanopyopennessonbutterflyrichnessandabundancewasdifferentdependingonthe
season.Canopyopennessdidnotaffecttherichnessandabundanceofbutterfliesintherainy
season.Inthedryseason,richness(p<0.001)andabundance(p<0.001)ofbutterflyspecies
weregreaterinislandswithgreatercanopyopenness(Fig3Aand3B;Table3).
Understorycoveragevariedfrom16%(island9inthedryseason,±0.022SE)to73%
(island10intherainyseason,±0.034SE),whiletheaverageunderstorycoveragewas35.8%
(±0.021SE).Theeffectofunderstorycoverageonbutterflyrichnesswasdependentonthesea-
son(Table3).Intherainyseason,richnessofbutterflieswasgreaterinislandswithhigher
understorycoverage(p=0.03);whileinthedryseason,richnessofbutterflieswasgreaterin
islandswithlowerunderstorycoverage(p=0.02)(Fig3C).Theabundanceofbutterflieswas
notaffectedbytheunderstorycoverageinanyseason(p=0.3)(Fig3D).
Fruit-feedingbutterflyrichnessdidnotvarywithseason(Fig4A).Ofallthe34speciescol-
lected,27specieswerecollectedintherainyseasonand20speciesinthedryseason.Theaver-
agenumberofspeciesofbutterfliesperislandwas3.68(SE=0.83),wherein4.3(SE=0.58)in
therainyseasonand3.04(SE=0.48)inthedryseason.Ofallthe34speciessampled13species
(38.2%)occurredinbothseason,14(41.2%)wereexclusiveoftherainyseasonandseven
(20.6%)ofthedryseason.Therewasnosignificantdifferenceinbutterflyabundancebetween
therainyanddryseasons.Theaverageabundanceofbutterfliesperislandwas11.66(±2.53SE)
individuals,withnosignificantdifferencesbetweenseasonsinthesimplifiedmodel(Fig4B).
Landscapeeffects
Thelandscapemetrics(area,perimeter,distancetoclosestislandandtocontinuousforest)did
notinfluencetherichnessortheabundanceoffruit-feedingbutterfliesoftheforestislandsof
theSerradoCipó(richnessF =2.03;p=0.22;abundance,F =1.71;p=0.28).
3,6 3,6
Speciescomposition
Thepartitioningofdiversityshowedthatα(forestislanddiversity)wasresponsiblefor25.6%
ofthetotaldiversity(averageof8.7species),agreaterdiversitythanexpectedifindividuals
weredistributedatrandom(expected=21.6%;α=7.36;p<0.001;Fig5).Thecontributionof
βdiversitycontribution(diversityamongislands)wasresponsiblefor74.3%ofthetotaldiver-
sity(averageof25.3species)andwaslessthanexpectedbychance(expected=78.3%;β=26.6;
p<0.001).Nevertheless,βdiversitywasthediversityscalethatmostcontributedtothetotal
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Butterfliesinmountaintoprainforestislands
Table2. Frequency,richnessandsingletonsofspeciesoffrugivorousbutterfliescollectedinthearchipelagoofforestislandsinSerradoCipo´,
Brazil. Abundanceofbutterflysubfamilyisshownwithinparentheses.
Species Island# Season Total
1 2 3 4 5 6 7 8 9 10 11 Wet Dry
Biblidinae(4)
TribeBiblidini
Hamadryasferonia(Linnaeus,1758) 1 1 1
TribeCallicorini
Callicoresorana(Godart,[1824]) 1 1 1
TribeCatonephelini
Catonepheleacontius(Linnaeus,1771) 1 1 1
Mysceliaorsis(Drury,1782) 1 1 1
Charaxinae(5)
TribePreponini
Archaeopreponademophoon(Hu¨bner,[1814]) 2 1 3 3
TribeAnaeini
Fountainearyphea(Cramer,1775) 1 1 1
Memphismoruus(Fabr´ıcius,1775) 1 1 1
Satyrinae(503)
TribeBrassolini
Blepolenisbatea(Hu¨bner,[1821]) 1 2 2 3 4 1 13 13
Caligoarisbe(Hu¨bner,[1822]) 13 5 4 1 6 4 33 33
Dasyophthalmarusina(Godart,[1824]) 1 1 1 3 3
Eryphanisautomedon(Cramer,1775) 3 1 3 1 4
Opopterasyme(Hu¨bner,[1821]) 4 4 12 5 25 25
Opsiphanesinvirae(Hu¨bner,[1808]) 1 1 1
TribeSatirini
Carmindagriseldis 1 1 1
Erichthodesnarapa(Schaus,1902) 1 1 1
Forsterinarianecys(Godart,[1824]) 1 10 1 7 5 12
Forsterinariaquantius(Godart,[1824]) 9 1 12 7 10 19 29
Godartianamuscosa(A.Butler,1870) 6 8 6 22 1 23 34 13 65 11 71 118 189
Hermeuptychiasp. 3 9 4 11 5 16
Moneuptychiaitapeva(Freitas,2007) 2 5 1 1 4 5 9
Moneuptychiasoter(A.Butler,1877) 1 1 15 1 20 5 1 11 33 44
Paryphthimoideseous(A.Butler,1867) 1 1 1
Paryphthimoidesphronius(Godart,[1824]) 13 3 16 16
Paryphthimoidespoltys(Prittwitz,1865) 3 1 1 3 2 5
Pharneuptychiasp. 2 1 1 1 3 2 5
Pharneuptychiaphares(Godart,[1824]) 1 1 1
Praepedaliodesphanias(Hewitson,1862) 1 1 1
Yphthimoidesangularis(A.Butler,1867) 1 1 1 9 2 10 4 14
Yphthimoidesmanasses(C.Felder&R.Felder,1867) 1 1 1
Yphthimoidesochracea(A.Butler,1867) 2 1 3 3
Yphthimoidespacta(Weymer,1911) 1 1 1
Yphthimoidesstraminea(A.Butler,1867) 2 1 1 3 35 10 10 7 51 18 69
Yphthimoidesyphthima(C.Felder&R.Felder,1867) 1 1 1 2 1 3
Zischkaiapronophila(Butler,1867) 3 1 2 3
Abundance 8 8 19 35 82 4 78 88 64 100 27 273 239 512
Richness 3 6 9 8 16 4 14 17 13 10 11 27 20 43
Singletons 3 5 1 2 3 1 9 6 15
https://doi.org/10.1371/journal.pone.0180007.t002
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Butterfliesinmountaintoprainforestislands
Fig3.Effectofcanopyopennessandunderstorycoverageonrichnessandabundanceoffrugivorousbutterfliesbyseason(dryand
rainy),basedonsimplifiedgeneralizedlinearmixedmodel(Table3).(A)Richnesswithcanopyopennessinthedryseason—p<0.001;(B)
Abundancewiththecanopyopennessinthedryseason—p<0.001;(C)Richnessofbutterflieswithunderstorycoverageintherainyseason—
p=0.03;(D)Abundanceofbutterflieswithunderstorycoverageinthedryseason—p=0.02.(D)Legend:dryseason—dashedlinesandemptycircles,
rainyseason—solidlinesandfullcircles.
https://doi.org/10.1371/journal.pone.0180007.g003
diversityoftheforestarchipelago(α=25.6%andβ=74.3%).Thedifferenceinbetadiversity
amongislandswascausedmainlybytheprocessofspeciesturnover(75.9%ofβ,β =0.49),
SIM
whiletheprocessesofnestingexplainedonly24.1%ofthebetadiversity(β =0.15).
SNE
Thetemporalpartitionofβindicatedthattheturnoverwasresponsiblefor78.3%ofthe
totalβdiversityamongislandsintime(β =0.518;β =0.406),whilenestingrepresented
SOR SIM
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