Effects of changes in the riparian forest on the butterfly community (Insecta: Lepidoptera) in Cerrado areas

REVISTA

BRASILEIRA

DE

Entomologia

AJournalonInsectDiversityandEvolution

w w w . r b e n t o m o l o g i a . c o m

Biology,

Ecology

and

Diversity

Effects

of

changes

in

the

riparian

forest

on

the

butterfly

community

(Insecta:

Lepidoptera)

in

Cerrado

areas

Helena

S.R.

Cabette

a

_,

_Jaqueline

_R.

_Souza

a

_,

_Yulie

_Shimano

b

_,

_Leandro

_Juen

c,∗

a_{UniversidadedoEstadodeMatoGrosso,DepartamentodeCiênciasBiológicas,NovaXavantina,MT,Brazil} b_{MuseuParaenseEmílioGoeldi,Belém,PA,Brazil}

c_{UniversidadeFederaldoPará,InstitutodeCiênciasBiológicas,LaboratóriodeEcologiaeConservac¸ão,Belém,PA,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received5May2016 Accepted17October2016 Availableonline3November2016 AssociateEditor:HéctorVargas Keywords: Conservation Environmentalchanges Integrity Riparianvegetation

a

b

s

t

r

a

c

t

Preservedriparianvegetationusuallyhasgreaterenvironmentalcomplexitythantheriparianvegetation

modifiedbyhumanactions.Thesesystemsmayhaveagreateravailabilityanddiversityoffoodresources

forthespecies.Ourobjectivewastoevaluatetheeffectofchangesonthestructureoftheriparianforest

onspeciesrichness,betadiversityandcompositionofbutterflyspeciesintheCerradoofMatoGrosso.

Wetestedthehypothesesthat:(i)higherspeciesrichnessand(ii)betadiversitywouldberecordedin

morepreservedenvironments;and(iii)speciescompositionwouldbemorehomogeneousindisturbed

habitats.Forhypothesistesting,theriparianvegetationofeightstreamsweresampledinfourperiodsof

theyearinafixedtransectof100malongtheshores.Therichnessofbutterflyspeciesislowerindisturbed

thaninpreservedareas.However,speciesrichnessisnotaffectedbyhabitatintegrity.Betadiversity

differedamongsites,suchthatpreservedsiteshavegreaterbetadiversity,showinggreatervariationin

speciescomposition.Inaddition,betadiversitywaspositivelyaffectedbyenvironmentalheterogeneity.

Atotalof23ofthe84speciessampledoccurredonlyinthechangedenvironment,42wereexclusive

topreservedsitesand19occurredinbothenvironments.Theenvironmentalchangecausedbyriparian

forestremovaldrasticallyaffectsthebutterflycommunity.Therefore,riparianvegetationisextremely

importantforbutterflypreservationintheCerradoandmaybeatruebiodiversityoasis,especiallyduring

thedryperiods,whenthebiomeundergoeswaterstressandresourcesupplyismorelimited.

©2016SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen

accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Riparianforestisdefinedastheforestvegetationestablished

alongtheshores ofmediumtolargerivers.Thisvegetationhas

importantfeaturesandresourcesforthesurvivalofanimal

commu-nities(RibeiroandWalter,1998,2001),providinghighhumidity,

temperaturesthat are cooler and more stablethan that of the

surrounding landscape, low light incidence and abundant food

resources (Brown, 2000). In addition, riparian forests are also

ecological corridors for wildlife, connect different habitat

frag-mentsandeffectivelyincreasepercolationinthelandscapescale

(Metzger, 2010).The density of animal species in the riparian

forestsindryerregionsandseasonsmayleadtoanintensebiotic

pressureamongthepopulationspresent,leadingtogenetic

diversi-ficationandevolution,andconsequentlytoahighspeciesrichness

(Brown,2000).

∗ Correspondingauthor.

E-mail:[email protected](L.Juen).

Naturalhabitatshavebeendrasticallyreducedand/ormodified

byintensehumanactivities,whichhave causedonlyfew

vege-tationremnants topersist. Theprimarycause ofthedecline of

speciesdiversityinriparianforestishabitatloss.Forest

fragmen-tationincreaseswiththelossoforiginalhabitatandhasitssize

reduced,consequently,theisolationofhabitatpatchesincreases.

Changesintheuseoftheriparianvegetation,aswellasthe

vari-ationintheintensityofusemaycausethelossofsomespecific

environmentalconditionsorresourcesthatareimportantforthe

species.Suchlossmaythusreduceabundance,causelocal

extinc-tionofmoresensitivespeciesorinsomecasesfavortheinputand

theestablishmentofgeneralistorinvasivespecies(Barrellaetal.,

2000).

TheCerradoisoneoftheBrazilianbiomesthathavemost

suf-feredtheeffectsofanthropization.Thisbiomehashighlevelsof

endemism(Rodrigues,2005;Camargo,2001;Pinheiro,2008)for

severalgroups,inadditionahighspeciesdiversity.Anexampleis

thebutterflyfauna,whichconsistsonagroupwithhighspecies

richness,extremelydependentonspecificresources(plants)and

highlyfaithfultomicrohabitats(BrownandFreitas,2002;Freitas

http://dx.doi.org/10.1016/j.rbe.2016.10.004

0085-5626/©2016SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

et al., 2003). Butterflies are especially dependent on specific

resourcesassociatedwithenvironmentswithhighhumidityand

abundantfoodresources(Brown,1992,2000;Camargo,2001).

Butterflies respond quickly to environmental and climatic

changesarerelativelyeasytomonitor,anditscommunity

struc-tureiseasilyassessed(Brown,1992;BrownandFreitas,1999,2000;

Raimundoetal.,2003;Uehara-Pradoetal.,2009).Theseinsectsare

involvedinmanyinteractionsinthesurroundingenvironment,for

example,pollinationandpredation(Bogianietal.,2012).

There-fore,butterfliesare important forthe functioningof ecosystem

servicesand are goodmodels for ecologicalstudies. Given this

scenario,ourobjectivewastoevaluatetheeffectoftheriparian

forestchangesonspecies richness,betadiversity and

composi-tionofbutterflyspeciesinsavannahareasofMatoGrosso,Brazil.

Therefore,wetestedthehypothesesthat:(i)higherspecies

rich-nessand(ii)betadiversitywouldberecordedinmorepreserved

environments,and(iii)speciescompositionwouldbemore

homo-geneousindisturbedhabitats.Preservedsiteshavewiderriparian

forestandthereforemayprovidegreateravailabilityanddiversity

offoodresources.Weassumethatenvironmentalconditionssuch

astemperatureandhumidityinpreservedareasaremorefavorable

forbutterflies,incontrasttotheobservedwhenthevegetationis

removed(highersunlightinput,hightemperatures,droughtstress

andlossofspecificmicrohabitats).Thereductionorelimination

ofresourcesand/orspecificmicrohabitatswouldleadtothelocal

extinctionofspecialistspecies,favoringthepersistenceof

gener-alistspecies.

Materialandmethods

OurstudywascarriedoutintwostreamsthatdrainfromtheLeft

BankofthePindaíbaRiver.Thisriverisatributaryintherightbank

oftheMiddleMortesRiver,locatedattheSouthwestregionofthe

stateofMatoGrosso,andrunsthroughthemunicipalitiesofBarra

doGarc¸as,Araguaiana,CocalinhoandNovaXavantina.Theregional

climateisAwaccordingtoKöppen,withtwowell-defined

sea-sons–dryfromMaytoOctoberandrainyfromNovembertoApril

(Peeletal.,2007).Theaverageannualrainfallrangesfrom1500to

1800mmandthetemperaturefrom18.9and33.7◦C(INMET,2009).

Themainsoilusechangesarederivedfrombeefcattlebreeding

activitiesandextensiveagriculture.

52º35’0”W 52º30’0”W 52º25’0”W 52º20’0”W 52º15’0”W 52º10’0”W 52º5’0”W 52º0’0”W 51º55’0”W 14º45’0” 14º50’0” CRCV4 CRCV3 CRCV1 CRCV2 CRM2 CRM1 CRM3 N CRM4 14º55’0” 15º0’0”S 15º5’0”S 14º45’0”S 14º50’0”S 14º55’0”S 15º0’0”S 15º5’0”S 51º55’0”W 52º0’0”W 52º5’0”W 52º10’0”W 52º15’0”W 52º20’0”W 52º25’0”W 52º30’0”W 52º35’0”W 0 3500 7000 14 000 21 000 28 000 Meters

Fig.1. ButterflysamplingsitesatthePindaíbaRiverBasin,MT–Brazil;(CVS1,CVS2,CVS3,CVS4=Caveirastream(1stto4thorder);MS1,MS2,MS3andMS4=Mata Stream(1stto4thorder).

Table1

ButterflysamplingsitesintheRiparianForest,ordersofstreams,codes,geographical coordinatesandHabitatIntegrityIndex(HII);PindaíbaRiverBasin,MT,2007–2008. Streams Orders Codes Coordinates HII Caveira 1st CVS1 S14◦₅₉_06.0_W50◦₂₀_29.0 _0.6 2nd CVS2 S14◦₅₉_53.4_W52◦₁₈_17.5 _0.5 3rd CVS3 S14◦₅₇_28.7_W52◦₁₃_43.9 _0.7 4th CVS4 S14◦₄₉_47.7_W52◦₀₃_16.4 _0.6 Mata 1st MS1 S14◦2951.7W52◦2842.6 1.0 2nd MS2 S14◦5925.2W52◦2757.7 0.9 3rd MS 3 S14◦₅₉_59.0_W52◦₂₆_29.0 _0.8 4th MS4 S14◦₀₁_37.0_W52◦₂₆_29.0 _0.9

ThesampleswerecollectedattheshoresoftheMata(MS)and

Caveira(CVS) Streams,in 1st,2nd,3rdand 4thorder segments

(accordingtotheclassificationof Strahler,1957)withdifferent

riparianforest conservationlevels (eightsampling sites; Fig.1,

Table1).TheMataStreamstillholdsmostofitsriparianforestonce

itislocatedinasharprelief,whiletheCaveiraStream(locatedin

amildrelief)isconsideredidealforagricultureand agricultural

mechanizationactivities,andthushasmostofitsmarginal

veg-etationchangedorremovedanddamsestablishedfortheuseof

livestock.Thesampleswerecollectedintwoseasons,ineach

sea-sonwecollectedtwice:dryperiod (Augustof2007andMayof

2008)andrainyperiod(Novemberof2007andJanuaryof2008).

Sampleswerecollectedusingdipnets,withthesamplingeffort

ofonepersoncollectingperhour,coveringfixed100-msegments

alongbothbanks.Eachsite(orderofthestreams)was

invento-riedalwaysbetween9a.m.and 4p.m.The specimens collected

werekilledwithfingerpressureinthechest,storedinproperly

labeledentomologicalenvelopesandtakentothelaboratorytobe

assembled,identifiedandpreserveddry.

Thespecies wereidentified usingspecialized literature (e.g.,

Brown,1992;Uehara-Pradoetal.,2004;D’Abrera,1994)andby

comparisonwithspecimensstoredattheZoobotanicalCollection

“JamesAlexanderRatter”oftheUniversidadedoEstadodeMato

Grosso,NovaXavantinacampus.Thespeciesidentifiedunderwent

confirmationofataxonomistexpertintheorder,whennecessary.

ThetaxonomicclassificationfollowedLamas(2004).

The conservationstatus of thesites sampled wasevaluated

usingthe HabitatIntegrity Index(HII) (Nessimianetal., 2008).

The HII is a protocol consisting of 12 items that assess

envi-ronmental conditions, suchas: useof the landadjacent tothe

riparianvegetation,riparianforestwidthandpreservationstate,

state of the riparian vegetation within a 10m range, internal

structure ofthe stream(e.g.,sediment and retentions). TheHII

rangesfrom 0 to1, where higher values indicate

environmen-talpreservation.TheHIIdataobtainedwerecategorizedintotwo

conservationcategories:disturbedhabitats(HII<0.65>0.50)and

preservedenvironments(HII>0.82).Disturbedhabitatswere

cate-gorizedbyloss/replacementoforiginalvegetationatleastinoneof

themarginsandflowchangedbythepresenceofdams.Preserved

habitatwerecategorizedbywell-preservedareas,andifhadhuman

influence,isbeyondtheriparianzone.

Statisticalanalyses

Therichness,compositionandbetadiversitypatternswere

eval-uated bytwoapproaches:consideringtheconservationmetrics

(HIIvalues)ascategoricalvariables(conserved/altered)todetect

morerobustpatterns,andasquantitativevariablestofind

sub-tlerpatternsofchangeintheassemblyofstructure.Weusedthese

twometricsintendedtoreachpeoplewiththeoreticaland

scien-tificinterestsandthoserelatedtopublicpolicyandenvironmental

monitoring.Theobservedspeciesrichnessisoftenimprecisedue

tothedifficultyinsamplingallspeciesofagivensite.Therefore,we

usedtherichnessestimatedbythenonparametricjackknife

esti-mator,usingthesoftwareEstimateSWin7.5.0(Colwell,2005).This

techniqueyieldsmoreaccuratevaluesofspeciesrichnessofagiven

community(Krebs,1999;WaltherandMorand,1998),andprovides

aconfidenceintervalthatenablesstatisticalcomparisonsbetween

twoormoresampledregions.Weusedtheinferencebyconfidence

intervaltocomparerichnessamongsites,whereatreatmentisonly

considereddifferentfromtheotherwhentheconfidenceinterval

ofagroupdoesnotoverlapthemeanoftheother.

Betadiversitywasestimatedforeachsitesampled.Therelative

abundanceofeachspecieswasdeterminedforeachsiteaddingall

samplingtimes.Betadiversitywascomparedamongthestreams

sampled,separatedbystationwhichwereconsideredreplicasin

hypothesistesting.Theapproachisbasedonthedissimilarity

mea-sureestimatedusingtheJaccardquantitativeindex(Chaoetal.,

2005).Thequantitativeindexwasused,measuredthedifferences

inspeciescomposition,andiscalculatedusingthetotalrelative

abundanceofspeciesineachsampledarea.AccordingtoChaoetal.

(2005),thequantitativeindexisthebestbetadiversityestimator

onceitisnotdependentonspeciesrichness,andismoreaccurate

evenfordatawithsmallsamplesizes.Thisindexconsidersspecies

abundance,aswellasanestimationofthespeciesthatwere

proba-blynotsampled.HigherJaccardindexvaluescorrespondtohigher

turnoverrates(moredifferentspeciescompositionamongsites).

Themean abundanceandbeta diversityvalues (among

pre-servedandalteredstreams)werecomparedusingtheStudent’s

t test(Zar,1999).Theassumptionsof homogeneityandnormal

distributionwerealwaysevaluatedbeforeconductingtheanalyses.

Weusedaprincipalcoordinatesanalysis(PCoA)withthe

Jac-cardquantitativeindextosummarizethestructureandcommunity

compositiondata.ThePCoAisamethodusedtoexploreand

visu-alizesimilaritiesordifferencesinthedatausingasimilaritymatrix.

The datawere logtransformed(log (x+1))to remove the

out-liereffectandensurehomogeneityofvariances.APermutational

MultivariateAnalysisofvariance(PERMANOVA)(Anderson,2001)

wasusedtotestfordifferencesinspeciescompositionbetween

preservedandalteredareas.ThePERMANOVAusesrandom

permu-tations(999)basedontheBray–Curtissimilaritymatrix.Weused

linearregressionstoevaluatetheeffectofenvironmentalintegrity

(HIIvalues),ontheestimatedspeciesrichnessandonbetadiversity

(Zar,1999).ALinearregressionbetweentheHIIvaluesandthefirst

axisofthePCoAwasusedtoevaluatetherelationshipbetweenHII

andspeciescomposition.

Results

Environmentaldescription

ThefoursegmentssampledattheriparianforestoftheCaveira

stream(1stto4thorder–streamwidthinthesegmentsranged

from140to1720cmanddepthfrom13to163cm)hadthe

low-estHIIvalues(0.52–0.65).Thesegmentssampledattheshoresof

theMatastream(streamwidthinthesegmentsrangedfrom263

to486cmanddepthfrom33to40cm)yieldedhigherHIIvalues

(0.82–0.96).

Communityoverview

A total of 245 butterflies were recorded in 32h of

samp-ling, comprising five families, 63 genera, 84 observed and

133±22.91estimated species(mean±confidence interval).The

family Nymphalidae was the most well represented, with 29

speciessampled,followedbyHesperiidae(25species),Riodinidae

140 Estimated b u tterfly r ichness Estimated b u tterfly r ichness Samples number Preserved-MS Altered-CVS

A

B

r2_{=0.124; p=0.180; y=7.3397+14 045∗x} IHH 28 26 24 22 20 18 16 14 12 10 8 6 0.50 0.55 0.60 0.65 0.70 0.75 0.80 0.85 0.90 0.95 1.00 120 100 80 60 40 20 0 –20 16 31 46 61 76 91 106 121 136 151 166

Fig.2.RelationshipbetweenenvironmentalintegrityandbutterflyspeciesrichnessinpreservedandalteredstreamatthePindaíbaRiverbasin,MT,Brazil.(A)Species accumulationcurveand(B)linearregression.

ThemostabundantspecieswereHermeuptychiahermes

(Fabri-cius,1775)(10.9%),Euremaelathea(Cramer,1777)(7.9%),Pyrgus

orcus(Stoll,1780)(7.9%),andDoxocopaagathina(Cramer,1777)

(6.4%).45specieswererepresentedbyonlyoneindividualinthe

samples(AppendixA).

Environmentalintegrityandthebutterflycommunity

Speciesrichness(hypothesisI)

Weobservedadifferencebetweentheestimatedspecies

rich-ness(conserved=105.74±25.62;altered=69.84±20.21;Fig.2A)

when analyzing the categorical metrics of conservation status

(alteredandconserved).Still,thespeciesaccumulationcurveofthe

preservedenvironmentshasasteeperslopethanthecurveofthe

alteredsites,whichstabilizeswithasmallernumberofsites(the

preservedsiteshadonaverage35speciesmorethatthealtered

sites).However,weobservedthattheestimatedspeciesrichness

wasnot affectedbytheconservationlevel (r2_{=0.124,p=0.180)}

whenweusedthequantitativehabitatintegritymetric(individual

HIIvalues)toseeksubtlerstructurepatterns(Fig.2B).

Betadiversity(hypothesisII)

Thebetadiversityvaluesdifferedbetweenthepreservedand

alteredsites(t=2.771,gl=4,p=0.015).Thebetadiversityvalueof

preservedsiteswas0.07higherthanthatofalteredsites,

show-ingahigherturnoveramongpreservedsitesthanamongaltered

sites.Therewasalsoapositiveeffectoftheintegrityindexonbeta

diversity(r2_{=0.319,p=0.022)(Fig.3).}

Speciescomposition(hypothesisIII)

We recordeddifferences betweenthepreserved and altered

treatmentswhenorderingthesampledsiteswithrespecttothe

conservationcategory(Fig.4A),whichwasalsoconfirmedbythe

PERMANOVA (F=2.306; R2_{=0.141; p<0.001). The altered sites}

weremoreclusteredintheordinationspace(graph), indicating

amorehomogeneousspeciescompositionandalargesimilarity

amongaltered sites,corroboratingourthirdhypothesis. Onthe

otherhand,thepreservedsiteshadawiderturnover,which

indi-catesmorepronouncedfaunaheterogeneitywhencomparedwith

alteredsites.Atotalof23ofthe84speciessampledoccurredonly

inalteredenvironments,42wereexclusivetopreservedsitesand

19occurredinbothstreamcategories.Thehabitatintegrity

mea-suredbytheHIIwasalsopositivelyrelatedwiththefirstaxisof

thePCoA,whichsummarizesthevariationofspeciescomposition

amongthesampledsites(r2_{=0.521,p=0.002)(Fig.4B).}

0.98 _r2 =0.319; p=0.022; y=6914+0.2311∗x 0.96 0.94 0.92 0.90 0.88 0.86 0.84 0.82

Butterfly beta div

e rsity IHH 0.80 0.78 0.76 0.50 0.55 0.60 0.65 0.70 0.75 0.80 0.85 0.90 0.95 1.00

Fig.3. Relationshipbetweenbetadiversityofbutterflyspeciesinpreservedand alteredstreamsandtheHabitatIntegrityIndex(HII),ofthePindaíbaRiverbasin, MT–Brazil.

Discussion

TheCerrado biome hasheterogeneous landscapeswith

sev-eral plantformations and is a habitat withthe conditions and

resourcesrequiredforthesurvivalofalargevarietyofbutterflies

that occurin this environment (Emery et al., 2006). The

high-estspeciesrichnessoftheCerradobiomeoccursinhumidareas,

suchas riparianforests, oncesuchareasprovideresourcesthat

arerarerorabsentinthemoreopenadjacentsystems(e.g.,less

humidandrichsoil)(Brown,2000).Thespeciesofthesubfamily

Ithomiinae, for example, needenvironments withnutrient rich

soilsandabundantwatertodevelop,andarefaithfultotheir

micro-habitasduetoitsspecificrequirements(Brown,1992;Brownand

Freitas,2000,2002).Therefore,theenvironmentalspecificitiesof

theriparianforestarea(meetingspecificbiologicalrequirements)

couldexplainthediversityofspeciesrecordedinourstudy.Ina

recentstudy,Queiroz-Santosetal.(2016) producedthe

histori-calsurveysofspeciesofbutterfliesrecordedforMatoGrosso,and

mentionedarichnessbetween51and100speciesintheregion,

indicatingthatourdataisrepresentativefortheregionalfauna.

ThestateofMatoGrossoispotentiallyhighlybiodiversebecause

threeofthemainBrazilianbiomesarepresentwithinitsborders:

Amazontropicalrainforest,CerradoandPantanal.However,little

informationisavailableonthemagnitudeoftheirbiodiversity.The

greaterspeciesrichnessrecordedinpreservedareasmayalsobe

0.5 600 500 400 300 200 100 0 0.4 0.4 0.5 0.6 0.7 r2=0,521, p=0.002, y=–410.87+779.37∗x 0.8 0.9 1.0 0.3 0.3 0.2 0.2 0.1 0.1 0.0 0.0 –0.1 –0.1 –0.2 Preserved PCoA 2 (14.50%) PCoA Axis 1 PCoA 1 (19.37%)

A

B

IHH Altered –0.2 –0.3 –0.3 –0.4 –0.4 –0.5 –0.5

Fig.4.(A)Ordinationofthesampledsitesinregardstobutterflycompositionandabundanceand(B)relationshipbetweenbetadiversityofbutterfliesandtheHabitat IntegrityIndex(HII),PindaíbaRiverbasin,MT–Brazil.

intheriparianforest.Naturalriparianzonesaresomeofthemost

diverse,dynamic,andcomplexbiophysicalhabitatsonthe

terres-trialportionoftheplanet(Naimanetal.,1993),riparianforests

actasrefugesinadjacentareasand,insomecases,ascorridors

formigrationanddispersal(NaimanandDécamps,1997).

There-fore,somevegetationtypeswouldbemoreimportantthanothers

forconservationalpurposes.Theauthorsgroupedthelocalitiesfor

phytophysiognomy,andverifiedthatriparianandCerradãofauna

weresimilarandformadistinctgroupfromthosewithopencrown

(savannas).Theysuggestthatthetypeofvegetationistheoneofthe

mostimportantfactorsdeterminingassembliesofArctiidaein

Cer-rado.Ontheotherhand,FerroandRomanovski(2012)compared

forestborderandGrasslandareasinRioGrandedoSul,andfound

Grasslandmostrich,probablybecauseofnectarsupplyavailablein

herbaceousofthearea.

Inthisstudy,itislikelythatspeciesspecifictoeachmicrohabitat

exist.Suchspecieswouldhaveahigherspecializationinmore

het-erogeneousandpreservedriparianforestenvironmentstooccupy

uniquesuitablenichespreferredforpopulationmaintenance.

ThelackofrelationshipbetweenHII,andcompositionand

rich-nesswhenusingquantitativevariablesmaybeaconsequenceof

thehighflightcapacity andmigrationofsomebutterflyspecies

(Marinietal.,2009;ShahabuddinandTerborgh,1999;Veddeler

etal.,2005).AnexampleisthespeciesDanausplexippus(Linnaeus,

1758),whichcanflyoverabout3000km,migratinginsearchof

areaswithmilderenvironmentalconditionschangingperiodand

flywaytoavoidunfavorableclimaticeventsofthatparticularyear

(Milleretal.,2012).Ahighflightcapacitymayenabletheorganisms

originallyfromaltered sitestoentertheriparianforestseeking

otherresources,andmayallowthespeciestoseekenvironmental

characteristics more similarto theirniche. Therefore, the

real-izednichewouldbewiderforspecieswithhigherflight/migration

capacity.However,Komonenetal.(2004)provedthatmore

spe-cialistbutterflyspecieshavelowermobilityandrarelyleavethe

habitatlocationwherethefoodsupplyforthelarvalstageislocated

whereas less specialist species mayhave higher mobility. Still,

whentheincreasedlanduseresultsinahomogeneouslandscape,

thealteredareabecomesthehabitatofspecieswithhighermobility

(generalistspecies)(Dormannetal.,2007).Therefore,thespecialist

specieswouldberestrictedtovegetationpatchesandstrong

habi-tatchangesmaycauselocalextinction,oncefragmentationand

habitatmodificationwouldcreatedispersalbarriers.

Wemayconsiderthisdivergencebetweentheresultsobtained

fromcategoricalandquantitativechangestobeanindicationthat

speciesrichnessmaynotbeagoodmetrictoassesshabitatquality,

especiallygiventhatbetadiversityandspeciescompositionwere

influencedbythesamechangesintheriparianforestthatwere

consideredintestingspeciesrichness.Speciesrichnessmaynotbe

agoodparametertostudytheeffectsofenvironmentalchangeson

butterflies,onceitconsidersonlythenumberofspeciesregardless

oftheidentityorecologicalroleofthespeciesenteringor

leav-ingthecommunity.Thespeciesrichnessofalteredenvironments

maybesimilartothatofpristineenvironments,oncerichnessmay

remainhighduetotheentranceofgeneralistinsteadofspecialist

specieswithlowconservationvalue.Notethatspecialistspecies

mayoccurinseveraltypesofenvironments.Ontheotherhand,

betadiversityandspeciescompositionhaveprovedtobeeffective

tocapturingsubtlecommunitychanges.

The hypothesis that beta diversity of butterflies would be

higherinpreservedenvironmentswascorroborated.Thepreserved

areasofourstudyhavehigherenvironmentalheterogeneitythan

altered,andpossiblyallowthecoexistenceofspecieswith

differ-entrequirements,enablinggreaterhabitatsharingwhichinturn

leadstogreaterbetadiversity.Theseenvironments,whenaltered

bynativevegetationremoval,receivedgrazingorextensive

mono-culture,gettingsimplerandmorehomogeneous.Insuchcontext,

fewspeciesmanagetosurvive,usuallythosewithfewer

environ-mentaldemandsandwiderniches,leadingtoadecreaseinregional

betadiversity.However,thispatternisnotalwaysobserved.The

highmigrationcapacityofbutterfliestendstohomogenizethe

spa-tialscaleeffectandlimitthecompositionvariationpatterns(Marini

et al.,2009).Therestrictions ofspecialist species tothehumid

areasoftheCerradobiomemayhaveeffectivelycontributedtosuch

result.

BetadiversitywaspositivelyrelatedwithHII,showingthat

pre-servedsiteshaveahighervariationinspeciescompositionthanthe

alteredsites,whichinfact,wasexpected.Ourresultssupportthe

studycarriedoutbyEkroosetal.(2010),whostatethatagricultural

intensificationreducesthebetadiversityofbutterflies,regardless

ofitslocationintheriverbasin.Wealsobelievethatthenumber

ofrarespecies(42exclusivetopreservedsitesand19toaltered

sites)contributedeffectivelytotheobservedbetadiversity

varia-tion,oncethelandscape-scalebetadiversitymeasuresaremore

affectedby rarespecies than thealphadiversity. Thespecialist

speciesarepreciselythosethatmostsuffertheeffectsoflandscape

changes(Marinietal.,2009).

Likewise,the hypothesis that species composition would be

more homogeneousin altered environmentswas corroborated.

Thisresultisprobablyaconsequenceofthegreaterlightinputin

alteredsites,whichcausesgreaterwaterstressandlossof

spe-cificmicrohabitats,withtheeliminationofspecialistspeciesand

alteredsitesreduceshumidityandcontributestohigher

temper-atureoscillation,whichcanpreventtheoccurrenceofstenotopic

butterflies.

The restoration of butterfly communities in an area that

underwent natural a disturbance is rapid and complex.

How-ever,mostbutterfly species disappear altogetherin profoundly

changed,anthropizedorpollutedenvironments,leavingfew

resis-tant,adaptableorcolonizingspeciesabletoreachhighpopulation

densities(BrownandFreitas,1999).Inaddition,bothalphaandbeta

diversityreducemorequicklywhennaturalvegetationissmaller

than40%,increasingthenegativeeffectsonthebutterflydiversity

(Ekroosetal.,2010).

Thelittlevegetationpresent in disturbedhabitats mayhave

providedadifferentmicrohabitatforthespecies.However,these

smallvegetationpatchesmaynotaccommodatethelocalfauna

foralongtime,duetoincreasedsusceptibilitytostochastic

pro-cesses. Therefore, the alteration of riparian vegetation directly

affectsthediversityandcompositionofbutterflyspeciesofthe

Cer-rado.Theconservationoftheriparianforestisthereforeessential

fortheconservationoftheaquaticfaunaaswellasforthe

terres-trialfauna,aswedemonstrated.Thus,itisextremelyimportant

thattheriparianvegetationnotbealteredbysoiluseactivities.

Ontheotherhand,deforestedareasshouldbereforestedseeking

therestorationofecosystemservices,enablinggeneflowamong

sites.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

WethankFAPEMATforthefinancialsupportgrantedforthe

executionoftheproject“Análisedaconservac¸ãodemicrobacias

hidrográficasdoRioPindaíba:uma visãomultidisciplinar”

(pro-cessnumber0907/2006);AndréVictorLucciFreitas–UNICAMP

fortheidentificationandconfirmationofsomespecies;andRafael

Dell’Erba,forthehelpinidentifyingthematerial.Wealsothank

allthemembersoftheLaboratoryofEntomology,UNEMAT–Nova

XavantinafortheirsupportandhelpinthisstudyandCNPqforthe

scholarshipgrantedtoLJ(process303252/2013-8).

AppendixA.

ListoftheLepidoptera(butterflies)speciesfoundattheCaveira

(CVS)andMata(MS)streams,MT–Brazil,August/2007–May/2008

[1–4=orderofthestreams].

Species Family CVS1st CVS2nd CVS3rd CVS4th MS1st MS2nd MS3rd MS4th Total

Adelphaiphiclus(Linnaeus,1758) Nymphalidae – 1 – – 1 – – – 2

AdelphathesprotiaFelder&Felder,1867 Nymphalidae – – – – – – – 1 1

Agunaalbistriaalbistria(Plötz,1880) Hesperiidae – – – – – 1 – – 1

Agunasp. Hesperiidae – – – – 1 – – – 1

Anartiajatrophaejatrophae(Linnaeus,1763) Nymphalidae – 5 – 1 – – – – 6

Antigonuserosus(Hübner,1812) Hesperiidae – – – – 1 – 1 – 2

Aphrissastatira(Cramer,1777) Pieridae – 1 1 1 3 – – – 6

Aricoriscampestris(H.Bates,1868) Riodinidae 4 2 1 1 – – – – 8

Aricorissp. Riodinidae – – 1 – – – – – 1

Autochtonneis(Geyer,1832) Hesperiidae – – – – – 1 – – 1

Brevioleriaaeliaplisthenes(R.F.d’Almeida, 1958)

Nymphalidae – – – – 1 – – – 1

Brevioleriasebaemyra(Haensch,1905) Nymphalidae – – – – 4 – – – 4

CaligoillioneusButler,1870 Nymphalidae – – – – 1 – – – 1

Caligoteucer(Linnaeus,1758) Nymphalidae – – – – 1 – – – 1

Calopsilalucianus(Fabricius,1793) Riodinidae – – – – – – – 1 1

Calycopisbellera(Hewitson,1877) Lycaenidae 1 – – – – – – – 1

Calycopissp. Lycaenidae – – 1 – – – – – 1

Cariaplutargus(H.Bates,1868) Riodinidae – – – – 1 – – – 1

ChamaelimnastircisC.Felder&R.Felder,1865 Riodinidae – – 1 – – – – – 1

Chioidescatiluscatilus(Cramer,1779) Hesperiidae – – – – – – 1 – 1

Chorineaamazonamazon(Saunders,1859) Riodinidae – – – – – 1 1 – 2

Coeruleuptychiabrixus(Godart,[1824]) Nymphalidae – – – – – – 1 – 1

Detritivoracuiaba(Harvey&Hall,2002) Riodinidae 1 – 2 – – 2 – – 5 Diaethriaclymenameridionalis(Bates,1864) Nymphalidae – – – – – – 1 1 2

DoxocopaagathinaCramer,1777 Nymphalidae – – – – 1 14 – 2 17

EueidesvibiliaunifasciatusA.Butler,1873 Nymphalidae – – – – 1 – – – 1

EunicasydoniaGodart,1824 Nymphalidae 1 – – – – – – – 1

Euremaalbula(Cramer,1775) Pieridae – – – – – – 1 1 2

Euremadeva(Doubleday,1847) Pieridae – – – – – 1 – – 1

Euremaelathea(Cramer,1777) Pieridae 5 4 4 5 1 – 1 1 21

EurybiaelvinaemidiataStichel,1915 Nymphalidae – – – – 1 – – – 1

Eurybiasp. Nymphalidae – – – – 1 – – – 1

Evenussatyroides(Hewitson,1865) Nymphalidae – – – – – – 1 – 1

Exoplisiacadmeis(Hewitson,1866) Riodinidae – – – 1 – – – – 1

Gorgythionbeggabegga(Prittwitz,1868) Hesperiidae 1 – – – 1 – – – 2

Gorgythionsp. Hesperiidae – – – – – 3 – – 3

Hamadryasarete(Doubleday,1847) Nymphalidae – – – – – – 1 – 1

Heliasphaloenoidespalpalis (Latreille,[1824])

Nymphalidae – – – – 1 – – – 1

Heliconiuseratophyllis(Fabricius,1775) Nymphalidae – – 1 – 2 1 1 2 7

HeliconiusmelpomenenannaStichel,1899 Nymphalidae – – – – – – – 1 1

Heliconiussarathamar(Rübner[1806]) Nymphalidae – – – – 1 1 – – 2

Species Family CVS1st CVS2nd CVS3rd CVS4th MS1st MS2nd MS3rd MS4th Total

Hemiargushannohanno(Stoll,1790) Lycaenidae – 2 2 6 – – 2 2 14

Hermeuptychiahermes(Fabricius,1775) Nymphalidae 8 1 5 – – – – 8 22

Hesperiidaesp1. Hesperiidae – – – – – 1 – – 1

Hesperiidaesp2. Hesperiidae 1 – – – – – – – 1

Hesperiidaesp3. Hesperiidae – – – – 1 – – – 1

Hyphilariaparthenis(Westwood,1851) Riodinidae – – – 1 – – 1 – 2

Hypolerialavinia(Hewitson,[1855]) Nymphalidae – – – – 1 – – – 1

Junoniaevarete(Cramer,1779) Nymphalidae 1 – – 1 – – – – 2

LentoaptaEvans,1955 Hesperiidae – – – – – 1 – – 1

Libytheanacarinenta(Cramer,1777) Nymphalidae – – – – – 2 – – 2

Mechanitispolymniacasabranca Nymphalidae – – – – – 1 – – 1

Melanissmithiaesmithiae(Westwood,1851) Riodinidae – – 1 – – – – 1 2

MesosemiasynnephisStichel,1924 Riodinidae 1 – – – – – – – 1

MorphohelenorCramer,1776 Nymphalidae – – – – 2 – 1 – 3

Morphomenelaus(Linnaeus,1758) Nymphalidae – – – – 2 – – – 2

Nymphidiumcaricaecaricae(Linnaeus,1758) Riodinidae – – 2 – – – – 1 3 NymphidiumlisimonepiplateaA.Butler,1867 Riodinidae – – 1 – – – – 1 2

NymphidiumniveaTalbot,1928 Riodinidae – – 3 2 – – – – 5

OuleosfredericuscandangusMielke,1968 Hesperiidae – 1 – – 1 – – – 2

Panoquinasp. Hesperiidae – – – – – – 1 – 1

Parcellaamarynthina(C.Felder&R.Felder, 1865)

Riodinidae – – 1 – – – – – 1

PareuptychiahesionidesForster,1964 Nymphalidae – – 1 – – 1 – – 2

Pelliciasp. Hesperiidae – 1 – – – – – – 1

Phoebissennaesennae(Linnaeus,1758) Pieridae – – 1 – – – – – 1

Politesvibexcatilina(Plötz,1886) Hesperiidae – – 1 – – – – – 1

Pompeiuspompeius(Latreille,[1824]) Hesperiidae 2 – – – – – – 1 3

Pyrgusorcus(Stoll,1780) Hesperiidae 4 3 4 7 1 – – 2 21

PyrisitianiseCramer,[1775] Pieridae – – 2 1 – 1 – 1 5

PythonidesherenniusherenniusGeyer,[1838] Hesperiidae – – – – – – 1 – 1

Quadruscerialis(Stol,1782 Hesperiidae – 1 – – – – – – 1

Stalachtisphlegiaphlegetontia(Perty,1833).) Lycaenidae – – 1 1 – – 2 – 4

Synargisaxenus(Hewitson,1876) Riodinidae – – – – – 1 – – 1

Synargiscalyce(C.Felder&R.Felder,1862) Riodinidae – – 1 – – – – – 1

Taygetisecho(Cramer,1775 Nymphalidae – – 1 – – – – – 1

Tegosaclaudina(Eschscholtz,1821) Nymphalidae – – – – – – 2 1 3

Thoonsp. Hesperiidae – – – – – – – 1 1

TithoreaharmoniaCramer,1777 Nymphalidae – – – – 1 1 – – 2

Urbanusdorantesdorantes(Stoll,1790) Hesperiidae – – 1 – – – – – 1

Urbanussimplicius(Stoll,1790) Hesperiidae 1 2 – – – – – – 3

Violaviolella(Mobille,1897) Hesperiidae – – – 1 – – – – 1

Yphthimoidesaffins(Butler,1867) Nymphalidae – – 1 – 1 – – – 2

Zaretisitys(Cramer,[1777]) Nymphalidae – – – – – – 1 – 1

Total 31 25 43 29 34 34 21 29 246

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