Dung beetle (Coleoptera, Scarabaeidae) assemblage of a highly fragmented landscape of Atlantic forest: from small to the largest fragments of northeastern Brazilian region

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

REVISTA

BRASILEIRA

DE

Entomologia

AJournalonInsectDiversityandEvolution

Biology,

Ecology

and

Diversity

Dung

beetle

(Coleoptera,

Scarabaeidae)

assemblage

of

a

highly

fragmented

landscape

of

Atlantic

forest:

from

small

to

the

largest

fragments

of

northeastern

Brazilian

region

Renato

P. Salomão

∗

,

Luciana

Iannuzzi

DepartamentodeZoologia,UniversidadeFederaldePernambuco(UFPE),Recife,PE,Brazil

a

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t

i

c

l

e

i

n

f

o

Articlehistory:

Received21November2014 Accepted2March2015 Availableonline8April2015 AssociateEditor:RodrigoKruger Keywords:

Fragmentation Habitatchange Scarabaeidae

a

b

s

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Humanactivitiesintropicalforestsarethemaincausesofforestfragmentation.Accordingto histori-calfactorindeforestationprocesses,forestremnantsexhibitdifferentsizesandshapes.Theaimofthe presentstudywastoevaluatethedungbeetleassemblageonfragmentsofdifferentdegreeofsizes. Samp-lingwasperformedduringrainyanddryseasonof2010insixfragmentsofAtlanticforest,usingpitfall trapsbaitedwithexcrementandcarrion.Also,weusedtwolargerfragmentsascontrol.Weused Gen-eralLinearModelstodeterminewhetherthefragmentspresenteddistinguisheddungbeetleabundance andrichness.AnalysisofSimilaritiesandNon-MetricMultidimensionalScalingwereusedtodetermine whetherthedungbeetleassemblagewasgroupedaccordingtospeciescomposition.Atotalof3352 individualswerecollectedand19specieswereidentiﬁedinthesixfragmentssampled.Dungbeetle abundanceexhibitedashiftaccordingtofragmentsize;however,richnessdidnotchangeamong frag-mentsevaluated.Also,fragmentssampledandthetwocontrolsexhibiteddistinctspeciescomposition. Thedistinctiononabundanceofdungbeetlesamongfragmentsmayberelatedtodifferentamount ofresourceavailableineachone.Itislikelythatthedungbeetlerichnessdidnotdistinguishamong thedifferentfragmentsduetotheevendistributionofthemammalcommunitiesinthesepatches,and consequentequaldungdiversity.Weconcludethatlargerfragmentsencompasshigherabundanceof dungbeetleanddistinctspecies.However,foraclearerunderstandingofeffectsoffragmentationon dungbeetlesinAtlanticforest,studiesevaluatingnarrowervariationsoflargerfragmentsshouldbe conducted.

Introduction

Theeconomiccyclesofagriculturalandlogginghavebeenthe majorcausesofenvironmentaldegradationforthelast500years inBrazil(Fiszon etal.,2003; Santosetal., 2008).In the north-eastregionofthecountry,thesugarcanemonoculturehasledto hugechangesinnaturalareasoftheAtlanticforest,whichis cur-rentlyalmostcompletelyfragmented(Tabarellietal.,2006).The majorityof theremnants of theAtlanticforest in northeastern Brazilaresmall(<10ha)andirregularinshape(Rantaetal.,1998), althoughthepresentforestremnantsexhibitdifferentsizesand shapes,dependingupontheintensityofthedeforestationprocess, actingaseitherconstraintsorfacilitatorstothenatural

communi-ties(Tabarellietal.,2006).Somefactors,asfragmentsize,history

and disturbanceeffects ofa landscape areimportant structural

∗ Correspondingauthor.

E-mail:renatopsalomao3@hotmail.com(R.P.Salomão).

parameterstotheestablishmentofnaturalcommunitiesover dis-turbedareas(BeversandFlather,1999;Metzger,2000;Cooketal., 2002).Smallfragmentsexperienceahigherintensityofedgeeffect, mainlyduetothesmallercorearea(Rantaetal.,1998),resulting inalesscomplexcommunity(Herrmannetal.,2005).Theedge areaoffragmentsissubjectedtoavarietyofecologicaleffects,such asgreaterlightintensity,lowermoistureandhighertemperature

(Gehlhausenetal.,2000).Theseeffectsaltersoildynamics,suchas

thenitrogencycle(PaulandClark,1996),therebyaffectingforest regenerationandnutrientrecyclingprocesses(Chenetal.,1995;

Hagermanetal.,1999).

Habitat modiﬁcationhasimportant consequences, especially withregardtobiodiversity(Naeemetal.,1999).Sensitivegroups aremorequicklyaffectedbysuchmodiﬁcationsandsufferresource shortagesandareunabletooccupydisturbedareas(Jankielsohn

etal.,2001;HalffterandArellano,2002).Thedungbeetles

repre-sentagroupsensibletohabitatdisturbances,insuchawaythat thediversityoftheirassemblagesareaffectedbyfragment param-eters,asisolationdegree,size,treespeciesrichness andcanopy

http://dx.doi.org/10.1016/j.rbe.2015.03.008

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structure(Nicholsetal.,2007;Díazetal.,2010;Shahabuddin,2010;

Filgueirasetal.,2011).Disturbedhabitatsexhibitaquantitative

impoverishmentofvertebrates,whicharethemainprovidersof resourcesforthedungbeetleassemblage,resultinginan inabil-itytomaintainmorespecializedgroups(AsforaandPontes,2009;

Filgueirasetal.,2009).

Althoughnatural,theseasonalitypresentsanotherinﬂuencing factoroverdungbeetleassemblages(Gill,1991;Hernándezand

Vaz-de-Mello,2009;Nevesetal.,2010).Inthetropics,seasonality

exertsaconsiderableinﬂuenceonthesetoffactorsthatcontribute tothefeedingandnestingofdungbeetles(Gill,1991;Filgueiras etal.,2009).Inthedryseason,foodresources,whichgenerally haveadoughtexture,dryoutquickly,which hamperstheiruse

(Gill,1991).Likewise,thesoilinthisperiodisdrier,thereby

inhib-itingtunnelingactivitiesfortheconstructionofnestsandstorage ofresources(Doube,1991).

Theaimofthepresentstudywastoevaluatehowthedegree ofsizeoffragmentsfromtheAtlanticforestaffectsthedung bee-tleassemblage.Our hypothesisisthat largerfragments areless restrictivetodungbeetlesassemblage.

Materialandmethods Studysite

Thisstudywasconductedinforest fragmentslocatedinthe TrapichesugarprocessingplantlocatedinthecityofSirinhaém (08◦3527 S; 35◦0658 O), state of Pernambuco, Brazil. The regionhasa meanannual precipitation of 2400mm and mean temperatureof 25◦C (Silvaet al.,2010).This regionisinserted in the Pernambuco Endemism Center (“Centro de Endemismo Pernambuco–CEPE”).TheTrapicheplantownsfragmentsofdense ombrophilous forest situated on the topsof hills inferior than 100mabovesealevel.Sixfragmentswithdifferentsizeattributes and separated byat least1km wereselected: Ubaca (8◦3231 S,35◦105W),CantoEscuro(8◦3313S,35◦846W),Matadas

Table1

FragmentsofAtlanticforestsituatedaroundTrapicheproperty,cityofSirinhaém, Pernambuco,andrespectivesize(ha)andsizeclasses.

Fragment Size(ha) Sizeclass Numberonthe map(Fig.1)

Ubaca 8.12 Small 4

MatadasCobras 40.03 Small 1

CantoEscuro 75.80 Small 2

Xanguazinho 100.57 Small 6

Tauá 288.33 Large 3

Xanguá 469.76 Large 5

Cobras(8◦3318S,35◦840 W),Tauá(8◦3315S,35◦923W), Xanguá(8◦3858S,35◦1021W)andXanguazinho(8◦3923S,

35◦1027W)(Fig.1)(Table1).Thefragmentsweregroupedinto

twosizeclassesaccordingtoFilgueirasetal.(2011),asthisstudy presentsalandscapesimilartotheonefoundin Trapiche.Tauá andXanguáwereconsideredthelargefragments,andtheother fourwere consideredsmall.In this way,the smallestfragment wasUbaca,with8ha,andthelargestfragmentwasXanguá,with 469ha.

Additionally,twolargerfragmentsoutsideTrapichewherethe dungbeetleassemblagehasalreadybeensampledwereselectedas control(Filgueirasetal.,2011;Costaetal.,2013).Thesedatawere utilizedtocomparedungbeetleassemblagesoffragmentssampled inTrapicheandlargerfragments,being3500hathefragmentof Coimbra(Filgueirasetal.,2011)and7324hathefragmentofCIMNC

(Costaetal.,2013).ThesefragmentsarelocatedneartoTrapiche

region,presentingasimilarvegetalcomposition,alsosurrounded byasugarcanematrix.Samplingmethodology(trapspacing,type andweightofbaitsused,timeoftrapskeptinﬁeld)appliedonboth fragmentswassimilartothesamplingsoffragmentsofTrapiche. Dungbeetlesampling

Samplingwasperformedin Julyand December 2010, corre-spondingtotherainyanddryseasons,respectively(LAMEPE,2011).

4

1

2

3

5

6

0 10 Kilometers

Studied fragments

Fig.1. MapshowingforestfragmentsevaluatedoftheTrapicheproperty(Oliveira,unpublisheddata);1:MatadasCobas;2:CantoEscuro;3:Tauá;4:Ubaca;5:Xanguá;6: Xanguazinho.Sirinhaém,Pernambuco,Brazil,2010.

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IneachfragmentofTrapichetwosamplingsitesseparatedby150m weredetermined.Eightpitfalltrapswereinstalledpersite, sepa-ratedfromeachotherby20mweredeployed–fourbaitedwith humanexcrement(25gpertrap)andfourbaitedwithcarrion (rot-tenbovinespleen)(25gpertrap).Thetrapconsistedofaplastic bottlemeasuring13cm×15cmwithatotalvolumeof1000mL, andwasﬁlledwith200mLofwaterwithsaltanddetergent.A plas-ticdiskwasplacedoverthetraptoavoidtheaccumulationofleaves, twigsandrainwater.Forty-eighthoursafterdeployment,thedung beetleswereremovedandmountedonentomologicalpins.

Theidentiﬁcationofthedungbeetlescollectedwasdonewith assistanceof the specialist Fernando ZaguryVaz-de-Mello. The specimensweredepositedinthe“Colec¸ãoEntomológicadaUFPE” (CE–UFPE,Brazil).

Dataanalysis

GeneralLinearModels(GLM)wereusedtocomparethe abun-danceandrichnessofdungbeetlespeciesbetweenTrapicheand CIMNCfragments.Abundanceand richnesswerethedependent variables;theTrapicheandCIMNCfragmentswerethecategorical predictorvariables;andfragmentsizeswerethecontinuous pre-dictorvariables.Tocomparesamplesequallybetweentheseareas, weonlyselectedthedatafromtherainyseason,duetothe differ-entsamplingeffortbetweenCIMNCandTrapicheduringthedry season.Eachfragmentwasconsideredonesampleunit.This analy-siswasperformedusingtheSTATISTICA7.0program.Althoughthe samplingmethodologyinCoimbrawassimilartothoserealizedin TrapicheandCIMNC,thenumberoftrapsinstalleddiffered, result-ingindistinctsamplingeffort.Asabundanceandrichnessofdung beetlestendtobeconnectedwithnumberofpitfallsinstalled,we optedtodonotincludeCoimbrainthisanalysistoavoidsampling bias.

Non-Metric Multidimensional Scaling (NMDS) was used to determine overall differences in species composition between Trapiche, CIMNC and Coimbra fragments. Ordination was per-formed for abundance and composition using the Bray–Curtis index. Analysis of Similarities (ANOSIM) was used to test dif-ferences in species composition between the fragments. These analyzeswereperformedusingthePRIMER6.0program.

Results

A total of 3352 dung beetleswere captured and 19 species wereidentiﬁedintheforestfragmentsofTrapiche.Dichotomiusaff. sericeus,CanthonsulcatusandCanthonnigripenniswerethemost abundantspecies,with2648,397and169individuals sampled, respectively(Table2).

Atotalof2210dungbeetlesweresampledintherainyseason and1142weresampledinthedryseason.Twospecieshad pre-dominantdistributionintherainyseason:Dichotomiusaff.sericeus (N=1966;74%oftotal)andCoprophanaeusdardanus(N=56;96% oftotal). C.nigripennis and C. sulcatuswereobtainedmainlyin dryseason(59%and81%oftotal,respectively),particularlywith adry/rainyratioof4.36/1individualsforC.sulcatus(Table2).

FromthesixfragmentssampledinTrapiche,twowere classi-ﬁedaslarge(XanguáandTauá)andtheremainingfourfragments wereclassiﬁedassmall.Atotalof1389individualsfrom11species werecollectedfromthelargefragmentsofTrapiche,withan aver-ageof694dungbeetlesperfragment(Table2).Inthefragmentof Xanguá(thelargestfragmentofTrapiche),wecollected601 indi-vidualsfromsixspecies.Inthesecondlargerfragment,Tauá,we collected1035individualsfromninespecies.Atotalof1716 indi-vidualsfrom16specieswerecollectedfromthesmallfragments, withanaverageof429dungbeetlesperfragment.Therichness exhibitedavariationbetween7and12species,andtheabundance exhibitedavariationbetween255and822individualsinthesmall fragments.

Threespeciesexhibitedawidedistribution,beingcollectedin allfragmentsofTrapiche,alsobeingcollectedinCIMNCand Coim-bra:Dichotomiusaff.sericeus,C.nigripennisandC.dardanus.Onthe otherhand,EurysternushirtelluswascollectedonlyinCIMNCand Coimbra,andC.sulcatuswastheonlyspeciescaughtexclusivelyin Trapiche,occurringinfourofthesixfragments.Thefragmentof CIMNCpresented13exclusivespecies,whileCoimbrapresented

nine(Table3).

The dung beetle abundance showed differenceamong frag-mentsofTrapicheandCIMNC(F=7.54;DF=1;P=0.006).Also,dung beetleabundancewasinﬂuencedbythesizeofthefragmentsof TrapicheandCIMNC(F=7.00;DF=1;P=0.008).However,richness didnotexhibiteddifferencebetweenfragmentsofTrapicheand

Table2

AbundanceofdungbeetlespeciesinsixfragmentsofAtlanticforestontheTrapicheproperty,cityofSirinhaém,Pernambuco,2010.1=Ubaca;2=MatadasCobras;3=Canto Escuro;4=Xanguazinho;5=Tauá;6=Xanguá;R=Rainy;D=Dry.

Taxon Fragmentsandperiods Total

1(8ha) 2(40ha) 3(75ha) 4(100ha) 5(288ha) 6(469ha)

R D R D R D R D R D R D

Ateuchussp.1 1 0 0 0 0 0 2 2 0 0 0 0 5

Ateuchussp.2 0 0 0 0 0 0 2 3 0 0 0 0 2

Canthidiumsp. 0 6 0 0 1 1 7 0 0 0 4 1 23

CanthonchalybaeusBlanchard,1843 0 0 0 0 0 0 1 0 0 0 0 0 1

CanthonnigripennisLansberge,1874 7 27 10 19 12 12 23 11 7 15 9 17 169

Canthonaff.oliveriori(PereiraandMartínez,1956) 0 0 0 0 0 0 0 0 0 1 0 0 1

Canthonsimulans(Martínez,1950) 0 0 0 1 0 0 0 0 0 0 0 0 1

Canthonstaigi(Pereira,1953) 0 0 1 0 1 0 0 0 0 0 0 0 2

CanthonsulcatusLaporte,1840 0 0 36 82 22 109 0 0 14 131 2 1 397

Canthonellaaff.silphoides(Harold,1867) 5 7 0 0 7 2 5 2 0 1 0 0 29

Coprophanaeussp. 0 0 0 0 0 0 0 0 1 0 0 0 1

Coprophanaeusdardanus(MacLeay,1819) 9 0 5 0 6 0 22 2 4 0 10 0 58

Coprophanaeusaff.ensifer(Germar,1824) 0 0 0 0 0 0 1 0 0 0 0 0 1

Coprophanaeuspunctatus(d’Olsouﬁeff,1924) 1 0 0 0 1 0 0 0 1 0 0 0 3

Deltochilumirroratum(Laporte,1840) 0 0 0 1 0 0 0 3 0 3 0 0 7

Dichotomiussp. 0 0 0 0 0 0 1 0 0 0 0 0 1

Dichotomiusdepressicollis(Harold,1867) 0 0 0 0 0 0 0 0 0 0 1 0 1

Dichotomiusaff.sericeus(Harold,1867) 132 68 79 21 391 257 238 49 653 204 473 83 2648

Sylvicanthonsp. 0 0 0 0 0 0 2 0 0 0 0 0 2

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Table3

ListofspeciesofdungbeetlesampledinfragmentsofTrapiche(Tra),CIMNC(Cim) andCoimbra(Coi).

Species Area

AgamopusconvexusBalthasar,1965 Coi CanthonchalybaeusBlanchard,1843 Tra,Cim CanthonnigripennisLansberge,1874 Tra,Cim,Coi CanthonscrutatorBalthasar,1939 Cim

Canthonhistrio(Serville,1828) Cim

CanthonmutabilisLucas,1857 Cim

Canthonaff.oliveriori(Pereira&Martínez,1956) Tra,Cim Canthonsimulans(Martínez,1950) Tra,Cim Canthonsmaragdulus(Fabricius,1781) Coi Canthonstaigi(Pereira,1953) Tra,Cim

CanthonsulcatusLaporte,1840 Tra

Canthonellabarrerai(HalfftereMartínez,1968) Coi Canthonellaaff.silphoides(Harold,1867) Tra,Cim Coprophanaeusacrisius(MacLeay,1819) Cim Coprophanaeuscyanescens(Olsouﬁeff,1924) Cim Coprophanaeusdardanus(MacLeay,1819) Tra,Cim,Coi Coprophanaeustelamon(Erichson,1847) Cim Coprophanaeusaff.ensifer(Germar,1824) Tra,Cim Coprophanaeuspunctatus(d’Olsouﬁeff,1924) Tra,Cim Coprophanaeusbellicosus(Olivier,1789) Coi Deltochilumirroratum(Laporte,1840) Tra,Cim DeltochilumcalcaratumBates,1870 Coi DeltochilumpseudoicarusBalthasar,1939 Cim Dichotomiusdepressicolis(Harold,1867) Tra,Cim,Coi Dichotomiusmormon(Ljungh,1799) Coi Dichotomiusnisus(Olivier,1789) Cim Dichotomiusaff.sericeus(Harold,1867) Tra,Cim,Coi Dichotomiusascanius(Harold,1869) Cim Eurysternuscaribaeus(Herbst,1789) Cim EurysternushirtellusDalman,1824 Cim,Coi

OntheruserosusHarold,1875 Coi

OnthophagusclypeatusBlanchard,1846 Coi OnthophagusranunculusArrow,1913 Cim Pseudocanthonxanthurus(Blanchard,1843) Cim Sylvicanthonfoveiventris(Schmidt,1920) Cim

UroxysbatesiHarold,1868 Coi

CIMNC(F=0.28;DF=1;P=0.597),neitherwasinﬂuencedbythe sizeofthefragments(F=0.29;DF=1;P=0.663).

Whenwe compared the species composition between frag-ments in Trapiche and fragments of CIMNC and Coimbra, we veriﬁeda segregationofthedung beetleassemblage (R:0.875; p:0.03).NMDSshowedthispattern,groupingsamplesfromthe fragmentsofTrapicheapartfromCoimbraandCIMNC,which seg-regatedonefromanother(Fig.2).

2D Stress: 0

Trapiche Coimbra CIMNC

Fig.2.Non-MetricMultidimensionalScaling(NMDS)ordinationoffragmentsof Trapiche,CIMNCandCoimbra,basedondungbeetlespeciescomposition.

Discussion

Onthepresentstudy,theassemblageofdungbeetlewas dom-inatedessentiallybyDichotomiusaff.sericeus.Also,thisspeciesis notablythemostabundantinothertropicalrainforestsof north-easternBrazil,exhibitingcompetitivesuccessintheregion(Endres

etal.,2007;Costaetal.,2009).Thissuccessisprobablyassociated

tolowbiologicalconstrains,asthisspeciesisknowntoexhibita widertrophic habitcompared tootherdungbeetlespeciesthat co-occurswithit, allowingittoovercomeresourcescarcityand competitivebarriers(Salomãoetal.,2014).Althoughnotstudied inD.aff.sericeus,thehighsuccessofdungbeetlespeciesmayalsobe relatedtoasuccessfulbrood,withelevatednumberofeggslaidand highnumberofadultssuccessfullydevelopedfromthem(Halffter

andMatthews,1966;HalffterandEdmonds,1982).However,the

strongdominanceofthis speciesisgeographicallyrestricted,as D.aff.sericeusisreportedtohavelowrepresentativenessinthe dungbeetleassemblagesofotherareasnearthefragmentsstudied herein,suchastherainforestenclavesinthestateofPernambuco andforestremnantstothesouthofthePernambucoEndemism Center(Schifﬂeretal.,2003;Silvaetal.,2007).Animportant fac-torassociatedwiththehighoccurrenceofthisspeciesregardson adaptationtodisturbedhabitats.Humandisturbancesarefound inmostAtlanticforestremnantsintheregionandgenerallylead toareductionintheabundanceofdungbeetlesinforestedareas

(Costaetal.,2009;Filgueirasetal.,2011).However,D.aff.sericeus

populationsarehighlysuccessfulinthesemodiﬁedremnants, dom-inatingthedungbeetleassemblageofforeststhathaveundergone humandisturbanceepisodes(Costaetal.,2009,2013;Filgueiras

etal.,2011).

Dichotomiusaff.sericeusexhibitedahigherabundanceduring therainyseason,withtwo thirds ofthetotal caught duringit. Therainyseasonalsoexertedaninﬂuenceonspeciesofthegenus Coprophanaeus,asthree ofthefourspeciesidentiﬁedwereonly caughtduringthisperiod.Thispatternisinagreementwiththat described in previousstudies ontheseasonality of Neotropical dungbeetles(AndresenandLaurence,2007;Hernándezand

Vaz-de-Mello,2009;Nevesetal.,2010).Intropicalregions,seasonality

isregulatedbytherainyanddryperiodsoftheyear,withlittle ﬂuctuationintemperature(Wolda,1988).Intherainyseason, trop-icalforestshavehighmoisturecontent,allowingthelongeruseof ephemeralresourcesbydungbeetlesforfeedingandbreeding(Gill,

1991;HernándezandVaz-de-Mello,2009).

Differingfromtheresultsusuallyfoundfortropicaldung bee-tles, C.nigripennis and C.sulcatuswereabundantmainlyin the dry season.Dungbeetlesadapted toenvironments andseasons withelevateddroughtstressandlimitedresourceavailabilitytend toexhibittrophicadaptationstostandoutinextremely compet-itive habitats (Ocampo and Philips,2005; Halffterand Halffter, 2009).Thegreaterabundanceofbothspecies inthedry season mayberelatedtothewidertrophicniche,asthesespeciesarenot restrictedtoexcrementandcarrion.Therearerecordsthatspecies ofthegenusCanthonusefruitsofthefamiliesAnnonaceaeand Arecaceae,whicharepresentintheAtlanticforestofnortheastern Brazil(HalffterandHalffter,2009).Also,widertrophicnichecould beanadaptationtothestrongercompetitionthatoccursinepisodes ofscarcerdungavailability,suchasduringthedrierperiodsofthe year.Thisevolutionaladaptationresultsfromtheabsenceoflarge mammalsintheregion(HalffterandMatthews,1966;Halffterand

Halffter,2009).

Althoughourtrappingdesigndidnotfollowthedistance recom-mendedbyLarsenandForsyth(2005)toavoidinterferenceamong traps(atleast50mfromeachother),ourresultspresentedsolid data,astheinterferenceofattractivelythatthetrapscouldcause amongthemwassimilarineachfragmentduetothesamedistance employedin each fragmentsampled.Besidesthat, thedistance

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amongtrapsthatweusedhasalreadybeenprovenrespondwellin anotherstudiesevaluatingdungbeetleassemblagesofAtlantic

for-est(Filgueirasetal.,2011;Costaetal.,2013;Salomãoetal.,2014).

Weverifiedthatthesizeofforestfragmentsexertedaninfluenceon thedungbeetleabundance,confirmingthehypothesisthatlarger fragmentswouldfavorthestructureofdungbeetleassemblage. However,thisresultwasonlyobservedwhentherewasabroad rangeoffragmentssize,whenweincludedfragmentofCIMNC.We believethatfragmentsizevariationsbetween8and470hathat wesampledin Trapichecouldnotexhibitstronginfluenceover dungbeetleabundance.Thisshiftondungbeetleabundancemay beexplained bythetheoryofisland biogeographyproposedby

MacArthurandWilson(1967),whichpointsthatlargeroccupation

areashowsatendencytosupportahigherabundanceanddiversity. Althoughtherearenogreatdistinctiononthedungprovidersof largerforestfragmentsofnortheasternAtlanticforest,these habi-tatsupportshigher abundanceof mammalswhen comparedto smallerones(AsforaandPontes,2009).Asaconsequence,more resourcetodungbeetlesis expectedtobeavailable,allowinga higherabundanceonlargerfragments.

Thesizeoftheforestfragmentsdidnotexertaninﬂuenceon thedungbeetlerichness.Itwasexpectedthatlarger,more con-servedfragments would supporta richer fauna (Nichols et al.,

2007;Filgueirasetal.,2011),sincesuchhabitatssupposedlyhouse

adiversecommunityofresourceproviders.However,mammals, majorprovidersofresourcefordungbeetles,areunableto main-tainstablepopulationsinthemajorityofAtlanticforestremnants inBrazil(AsforaandPontes,2009).Therefore,largerpatchesdo nothaveresourceproviderstosupportdifferentdungbeetlefauna incomparisontosmallerpatches(Harveyetal.,2006;Asforaand

Pontes,2009).Althoughtherewerenotsigniﬁcantdifferenceson

richness,speciescompositionofdungbeetlesshoweda distinc-tionamongthefragmentsof differentsizes.Atlanticforestwas acontinuousregionoftropicalwetforest,however,strongly dis-turbanceandfragmentationepisodescausedanisolationofnative faunaandflora(Rantaetal.,1998;Myersetal.,2000).Duetothe highdiversity,itisexpectedthateachremnantmaintainsa spe-cificfaunalcommunity.C.sulcatus,forexample,wasonlyobtained inthefragmentsofTrapiche,anddidnotoccurinCIMNCand Coim-bra.Thisspeciesisknowntooccurjustinotherisolatedfragments fromsouthernmostregionsofAtlanticforest(Campos,unpublished data).ThesamescenariowasverifiedinfragmentsofCoimbraand CIMNC,insuchwaythateachonepresenteddungbeetlespecies thatdidnotoccurintheotherfragments.Asdungbeetleshavethe capacitytoflylongdistances,itwouldbeexpectedthattheycould movebetweenfragmentsofTrapiche,allowingthespeciesto co-occuronthem(Scholtzetal.,2009).However,asmanydungbeetle speciesfromTropicalrainforesthavestronglimitationstooccupy openunshadedareas,agriculturalmatricesusuallyactsasstrong barriers,insuchawaythatdungbeetlescannottrespassthem(Díaz

etal.,2010;Costaetal.,2013).

Differingfromtheresultsfoundforthemajorityoffragments ofTrapiche,thefragmentofXanguazinho(classiﬁedassmall)had thehigherspeciesrichness(12)andlowestabundance(232 indi-viduals),whichareparametersofwell-balancedhabitats(Novelo

etal.,2007;Nevesetal.,2010).Xanguazinhowasthefragmentwith

greatestdegreeofenvironmentalheterogeneity,asevidencedby thepresenceoflargetreesandwatercourses,therebysupportinga greaterabundanceofmammals(Alves,unpublisheddata)andthe consequentmaintenanceofthedungbeetleassemblage(Andresen

andLaurence,2007).

Thehighdegreeoffragmentationthattropicalforestshavebeen sufferingisreﬂectedinthestabilityoftheecosystems.Sincethe present remnantshave a reduced size and capacity tosupport theenvironment,theassociatedcommunitycontinuouslysuffers simpliﬁcationprocesses (Fahrig,2003).The largestfragment of

Trapicheowns469ha,whichmaynotbeadequatetosupporta sig-niﬁcantportionofAtlanticforest.Comparatively,Coimbraisoneof thelargestpatchesofAtlanticforestinnortheasternBrazil, measur-ing3500ha,inwhich23speciesofdungbeetlehavebeenidentiﬁed

(Filgueirasetal.,2011).Inthepresentstudy,therichestfragment

ofTrapichehad12species.Thisdifferenceinrichnessmaybe asso-ciatedwiththesizeofthefragment,suchthatlargerfragmentscan providehighersortofhabitatandconsequentlyhigherrichness

(Filgueirasetal.,2011).

Basedonthepresentﬁndings,thepatcheslargerthan470ha exhibitedshiftsintheabundanceandspeciescompositionofdung beetles.However,studiesencompassingfragmentsrangingfrom 470haand3500haarenecessaryforanarrowercomprehensionof theinﬂuenceofthisfactorontheAtlanticforest.Withtheclearer understandingof fragmentationeffectsoverdungbeetles,more effectiveconservationstrategiescanbeconductedontheAtlantic forest.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest. Acknowledgments

TheauthorsaregratefultotheadministrationoftheTrapiche sugarprocessingplantforthelogisticalsupportandauthorization forsamplinginthearea;totheBrazilianfosteringagencyCAPES forawardingagraduategrant;toFernandoZaguryVaz-de-Mello forhelpwiththeidentiﬁcationofspecimens;toRichardBoykefor thetranslationofthetext;andtoEvaniafortheassistanceduring theﬁeldwork.

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