Spatial variation of dung beetle assemblages associated with forest structure in remnants of southern Brazilian Atlantic Forest

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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

Spatial

variation

of

dung

beetle

assemblages

associated

with

forest

structure

in

remnants

of

southern

Brazilian

Atlantic

Forest

Pedro

Giovâni

da

Silva

∗

,

Malva

Isabel

Medina

Hernández

ProgramadePós-Graduac¸ãoemEcologia,DepartamentodeEcologiaeZoologia,UniversidadeFederaldeSantaCatarina,Florianópolis,SC,Brazil

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t

i

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l

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i

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f

o

Articlehistory:

Received6September2015 Accepted4November2015 Availableonline30November2015 AssociateEditor:RodrigoKrüger Keywords: Betadiversity Speciescomposition Speciesdiversity Spatialdistribution Tropicalforest

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TheBrazilianAtlanticForestisoneoftheworld’sbiodiversityhotspots,andiscurrentlyhighly frag-mentedanddisturbedduetohumanactivities.VariationinenvironmentalconditionsintheAtlantic Forestcaninﬂuencethedistributionofspecies,whichmayshowassociationswithsomeenvironmental features.Dungbeetles(Coleoptera:Scarabaeinae)areinsectsthatactinnutrientcyclingviaorganic mat-terdecompositionandhavebeenusedformonitoringenvironmentalchanges.Theaimofthisstudyisto identifyassociationsbetweenthespatialdistributionofdungbeetlespeciesandAtlanticForeststructure. Thespatialdistributionofsomedungbeetlespecieswasassociatedwithstructuralforestfeatures.The numberofspeciesamongthesamplingsitesrangedwidely,andfewspecieswerefoundinallremnant areas.Principalcoordinatesanalysisindicatedthatspeciescomposition,abundanceandbiomassshowed aspatiallystructureddistribution,andtheseresultswerecorroboratedbypermutationalmultivariate analysisofvariance.Theindicatorvalueindexandredundancyanalysisshowedanassociationofseveral dungbeetlespecieswithsomeexplanatoryenvironmentalvariablesrelatedtoAtlanticForeststructure. Thisworkdemonstratedtheexistenceofaspatiallystructureddistributionofdungbeetles,with signiﬁ-cantassociationsbetweenseveralspeciesandforeststructureinAtlanticForestremnantsfromSouthern Brazil.

Introduction

Tropicalforestshostmostoftheearth’sbiodiversity,and pro-vide severalbenefitstohumanbeings throughtheprovisionof economicgoodsandecosystemservices(Gardneretal.,2009).In contrast,themaintenanceofbiodiversityandecosystemprocesses associated with it depend on effective conservation initiatives, whicharemajorchallengestoconservationistsanddecision mak-ers(Gardneretal.,2009;Randsetal.,2010;Tabarellietal.,2010). There are many barriers tothe creation of effective conserva-tionpolicydecisions,includinglack ofestablishedconservation practicestailoredtodifferentlocalconditions,apaucityofbasic informationonspeciesabundance,distributionandconservation status,andperhapsmostimportantly,thepotentiallylarge num-berofunknownspecies(Pimmetal.,2014).Suchshortcomingsin ourknowledgeaboutspeciesidentityandlocalorregional distribu-tionarereferredtoasLinneanandWallaceanshortfalls(Whittaker etal.,2005).Someofthesegapscanbefilledbyconnecting impor-tantissuessuchasthefulfillmentofbasicstudies(e.g.associations

∗ Correspondingauthor.

E-mail:[email protected](P.G.daSilva).

betweenspeciesandenvironmentalconditions)inorderto con-tributetotheknowledgeonspeciesdistributionandalsotothe potentialtodiscovernewspecies.Furthermore,thesestudiescan bring newinformationonspatialdistributionof species associ-atedwiththevariationinenvironmentalconditions,whichmay betakenintoconsiderationinplanningconservationinitiatives.

InBrazil,AtlanticForesthostsalargepartofthebiodiversity ofSouthAmericanrainforests(Myersetal.,2000;Tabarellietal., 2005)andwasthesecondlargestrainforesttypeinSouthAmerica, coveringabout150millionhectaresoftheBraziliancoast, north-eastern Argentina and southeastern Paraguay (Tabarelli et al., 2005;Ribeiroetal.,2009;VieiraandGardner,2012).Historically, theBraziliancoasthasalwayshadthehighesthumanpopulation and industrial concentration and, thus, the Atlantic Forest has beenaffectedbythegrowthanddevelopmentofthecountryover thelast ﬁvecenturies (Dean, 1996), mainlyin thelastcentury. The Atlantic Forest is currently themost endangered Brazilian ecosystem in terms of biodiversity conservation (Myers et al., 2000).Recentstudiesindicate thatonly12%of itsoriginalarea remains,much ofitfragmentedwithahighdegreeofisolation, andmostinanintermediatestateofregeneration(Ribeiroetal., 2009).Regardless,thefragmentsareusuallyofdifferentsizesand existinaheterogeneousmatrix,consistingmainlyofareasbeing

http://dx.doi.org/10.1016/j.rbe.2015.11.001

0085-5626/© 2015 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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usedforvariousagricultureandforestrypurposes.Thesefeatures maketheAtlanticForestaveryheterogeneousecosystem,housing specieswithdifferentenvironmentalrequirements(Aleixo,1999). Thestudyof thediversity-environmentalheterogeneity rela-tionshipoforganismsthathavekeyecologicalfunctionsandcan beusedasecologicalindicators,suchasdungbeetles(Coleoptera: Scarabaeidae:Scarabaeinae),isafirststeptosupportbiodiversity conservationinitiativesandmanagementofecosystemprocesses intropicalforests.Dungbeetlesaredetritus-feedinginsectsthat aidinorganicmatterdecompositionandnutrientcycling(Halffter andMatthews,1966;HanskiandCambefort,1991;Simmonsand Ridsdill-Smith,2011)byburyingandconsumingportionsoffeces, animal carcasses and rotting plant matter,thereby makingthe nutrientsinthesematerialsavailabletotheecosystemonceagain (Nicholsetal.,2008).Theseinsectsconstructtunnelsinthesoil, increasingaerationandwaterinfiltration.Theyalsoburyeggsof cattleparasites(e.g.,fliesandnematodes)andsecondarilydisperse fruitseedspreviouslyconsumedbymammalsonwhichtheyfeed (AndresenandFeer,2005;Nicholsetal.,2008).

Dungbeetleshavebeenusedasatoolformonitoring environ-mentalchangesin tropicalforestsbecausetheyaresensitiveto fragmentation,disturbanceandhabitatloss(Klein,1989;Halffter andFavila,1993;Davisetal.,2001;Nicholsetal.,2007;Gardner etal.,2008b;Korasakietal.,2013;Viegasetal.,2014)andbecause theyrespond positively to increased restoration time in tropi-cal forests (Davis et al., 2003; Audino et al., 2014; Bett et al., 2014;Hernándezetal.,2014).However,fewstudieshave identi-ﬁedimportantassociationsbetweendungbeetlespeciesandsmall changesinforestfeatures(e.g.HernándezandVaz-de-Mello,2009; CamposandHernández,2013;daSilvaandHernández,2014).Most studiesinvestigatetheScarabaeinaecommunityresponse when thereisaclearenvironmentalchange,suchasforestvs.open habi-tats(Lopesetal.,2011;Costaetal.,2013;Silvaetal.,2014),forest vs.monocultures(Gardneretal.,2008b;Barlowetal.,2010),or dis-tinctvegetationformations(AlmeidaandLouzada,2009;daSilva etal.,2013).

Changesinenvironmentalconditionsinsmallspatialextents maybekeydriversofcompositionalandstructuraldifferencesin dungbeetlecommunitiesintropicalforests(Feer,2013;daSilva

andHernández,2014,2015a;MedinaandLopes,2014).Changes indungbeetlecommunitiesaffecttheirecologicalfunctions,and hence proper ecosystem functioning (Vulinec, 2002; Andresen, 2003;Horgan,2005;Sladeetal.,2007;Gardneretal.,2008b;Kunz and Krell,2011;Sladeet al.,2011;Braga etal.,2012,2013).In addition,thesebeetlesarecorrelatedwithothertaxa,particularly mammalianfauna(Barlowetal.,2007;Culotetal.,2013).Thus, theevaluation of the spatial distributionof dung beetle fauna, whichcombineseaseofidentiﬁcationandlow-costand standard-izedsamplingmethods(Gardneretal.,2008a),maycontributeto researchconcerningeffectiveness ofconservation management, especiallyinaheterogeneousenvironmentastheAtlanticForest.

Theaimofthisstudywastodeterminewhethersmall differ-encesinforeststructureaffectthelocaldistributionofScarabaeinae dungbeetlesinremnantsofAtlanticForestinsouthernBrazil.We predictthatdungbeetlefaunawillshowspatialdifferencesin rela-tiontostructuralfeaturesoftheAtlanticForest.

Materialandmethods

Studyarea

Thestudywasperformedinfourlarge,non-contiguousareasof AtlanticForestinSantaCatarinastate,southernBrazil(Fig.1).Two areasarelocatedontheIslandofSantaCatarina:PeriLagoon Munic-ipalPark(PER,27◦42and27◦46S;48◦32and48◦30W,areaofca 75km2₎_and_Permanent_Protection_Areas_of_Ratones_(RAT,₂₇◦₃₀

and27◦32S;48◦30and48◦27W,areaofca73km2_),_both_located

inFlorianópoliscity.Othertwoareasarelocatedonthemainland neartheBrazilianAtlanticcoast:AnhatomirimEnvironmental Pro-tectionArea(ANH,27◦22and27◦26S;48◦35and48◦33W,areaof ca56km2₎_located_in_Governador_Celso_Ramos_city,_and_Permanent

ProtectionAreasofItapema(ITA,27◦02and27◦05S;48◦38and 48◦35W,areaofca175km2₎_located_in_Itapema_city._The_Island_of

SantaCatarinaisapproximately54km(north–southlength)with amaximumwidthof18km,withatotalareaof424.4km2_._The

distancebetweentheislandandmainlandvaries,withaminimum distanceof500mandmaximumaround10km.Despitethe con-versionofforestforagricultural,livestockandforestryactivities,

Fig.1. MapoftheAtlanticForestremnantswheredungbeetlesweresampledduringJanuaryandFebruary2012.AnhatomirimEnvironmentalProtectionAreainGovernador CelsoRamoscity;PermanentProtectionAreasofItapemacity;PeriLagoonMunicipalParkinFlorianópoliscity;PermanentProtectionAreasofRatonesinFlorianópoliscity.

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thestateofSantaCatarinainsouthernBrazilstillcontainsthethird highestAtlanticForestareaamongthestates,with17%ofits origi-nalcover;italsocontainsthethirdlargestAtlanticForestremnant (Ribeiroetal.,2009).Regardless,thefragmentsareusuallyof differ-entsizesandexistinaheterogeneousmatrix,consistingmainlyof areasbeingusedforvariousagricultureandforestrypurposes.Over thedecadestherehavebeenseveralconﬂictsofinterestregarding theseareas,primarilyrelatedtoillegaloccupationandlackofpublic administrationoversight.

Allsampledareascontaindenseombrophilousforest(Veloso etal.,1991)withintheAtlanticForestbiome,withvegetationin differentstagesof succession.AccordingtotheKöppen classiﬁ-cation (Peel et al., 2007) the climateis Cfa, humid subtropical (mesothermal)withhotsummers(average25◦C),nodryseason andwelldistributedrainfallthroughouttheyearaveragingaround 1500mmannually(Velosoetal.,1991).Thealtitudeofthesampled sitesrangedbetween28and265masl.Thedistancebetweenthe protectedareasrangedbetween13.5and71km,andthedistance amongsamplingsiteswithinareasvariedbetween500mtoseveral kilometers(ca6km).

Dungbeetlesampling

Dungbeetlesweresampledateachofthefourstudyareasatﬁve differentsamplingsitesperarealocatedonhillsidesnearrivers. Baitedpitfalltrapswereusedforsamplingdungbeetles.Each sam-plingsiteconsistedof10trapsdistributedinpairs,witheachpair spaced 50mapart. A minimumdistance of 50mdecreasesthe riskofinﬂuenceofothersetsoftrapsonsamplingofdung bee-tles(LarsenandForsyth,2005).Ourworkwascarriedoutbefore thenewtrapspacingproposedbydaSilvaandHernández(2015b)

wheretheyfoundthat100maremoreappropriatetoreduce inter-ference between baited pitfall traps in sampling dung beetles. Paired trapswere spaced 5–10m apart.Each pairof trapswas consideredasamplingunit,andalltrapsremainedintheﬁeldfor 48h.

Thetrapsconsistedofplasticcontainers(15cmdiam.×20cm depth)buriedwiththeiredgelevelwiththeground.Arainguard wasplacedabovethetrapstopreventtrapoverflowandto sup-portthebait.Trapscontainedasolutionofwaterand detergent (300mL)forcatchingfallenbeetles.Trapscontainedtwodifferent baittypes,includinghumanfecesandrottingflesh(30g)(i.e.,to attractcoprophagousandnecrophagousspecies,respectively).The baitswereindividuallywrappedinthinclothandtiedinthecentral portionoftherainguard.Allbeetlescollectedweresorted,mounted onentomologicalpinsanddriedinanoven(60◦Cfor72h)then weighed.Theywereidentifiedbyexperts(FernandoVaz-de-Mello andDavidEdmonds)anddepositedintheEntomologicalCollection oftheCentrodeCiênciasBiológicasattheUniversidadeFederalde SantaCatarina,Brazil.Thesamplingswereperformedduringthe summerof2012(JanuaryandFebruary).Thisperiodis character-izedbyhighregionaltemperatures,aswellasbeingtheperiodof greatestdungbeetleabundanceinsouthernBrazil(Hernándezand Vaz-de-Mello,2009;daSilvaetal.,2013).

Foreststructure

Foreach area,foreststructure wasdescribedby15 environ-mentalvariables,whichweretestedforinfluenceondungbeetle distribution.Variationintreefeatures,suchasdensity,heightand canopycover,canchangemicroclimaticconditionsthatmayaffect dungbeetles(Feer,2008,2013).Furthermore,thephysical struc-tureoftheforestfloor,suchasincreasedleaflitter,canaffectthe nestingactivitiesofsomeguildsofdung beetles(Nicholsetal., 2013).Measurementofvariableswasperformedusingtheadapted point-centeredquartermethod(CottamandCurtis,1956).Briefly,

aplasticcrosswasplacedinthecenterofeachpairoftraps(i.e.,at eachsamplingpoint),dividingthesamplingpointintofour quad-rants(northwest,southwest,southeastandnortheast).Tree,shrub andsoilenvironmentalvariablesweremeasuredineachquadrant asfollows:(A)circumferenceatbreastheightwhendiameterat breastheight[DBH]>5cm,(B)height,(C)topdiameterand(D) dis-tancefromthenearesttreetothecenterofcross,(E–H)repeated same measuresfor shrubs when circumferenceat ankle height whenDBH<5cmandwithaminimumheightof1m,(I)landslope, (J)altitude,(K)canopycover,(L)percentageofleaflittercover,(M) green(vegetationupto1mheight)cover,(N)exposedsoil,and(O) heightofleaflitter.Additionalinformationonthemethodsused andenvironmentalmeasurescanbefoundinAppendicesAandB.

Dataanalysis

The samplingeffortwasverifiedby smoothed species accu-mulationcurvesusingdataofthenumberofindividualsforeach samplingsiteandarea.Thedatawereextrapolatedtwotimesin relationtothenumberofsamplespersite(Colwelletal.,2012). Speciesrichnesswascomparedgraphicallybetweensamplingsites andareasusingtherarefactionmethod.Theestimatedspecies rich-nesswasobtainedbyusingChao1estimator(anditsconfidence interval)thatittakesintoaccounttheabundanceofspecies.We usedtheEstimateS9.1programfortheseanalyses(Colwell,2013). Weperformedaprincipalcoordinatesanalysis(PCoA)tomap thesimilaritybetweensitesregardingtocomposition(presence data),andassemblagestructurebasedonabundanceandbiomass ofdungbeetleassemblages,andalsoregardingtoenvironmental conditions.TheseanalyseswerebasedonBray–Curtis dissimilar-ity,andabundanceandbiomassdataweresquareroottransformed prior toanalysis.A permutationalmultivariate analysisof vari-ance (PERMANOVA) wasusedto testfor significantdifferences indungbeetleassemblagesandenvironmentalvariablesbetween samplingareas.PCoAandPERMANOVAwereperformedinR3.1.1 program(RCoreTeam,2014)and Primer6withPERMANOVA+ package(ClarkeandWarwick,2005;Andersonetal.,2008), respec-tively.WeusedMantelteststocorrelatedungbeetledissimilarity matrices(composition,abundanceandbiomass)withthe environ-mentaldissimilaritymatrix.BioticdatawerebasedonBray–Curtis dissimilaritywhileabioticdatawerebasedonEuclideandistance. TheseanalyseswerecomputedinR3.1.1program(RCoreTeam, 2014)usingveganpackage(Oksanenetal.,2013)with999 permu-tations.

TheMultivariateRegressionTreeanalysis(De’ath,2002)was usedtoidentifyhabitattypesthatweresimilarinenvironmental conditionsandindungbeetlespeciescomposition.Asetofclusters wereconstructedbyrepeatedbinarysplitsoftheenvironmental dataset(15environmentalvariables)toproducenodesas homoge-neousaspossiblewithrespecttothedungbeetleabundanceand biomass(species-by-sitesdataset)asresponsevariables.Wekept allenvironmentalvariablesafterthecollinearitybetweenthemhas beentested(seeAppendixA).MRTanalysiswascomputedinR3.1.1 program(RCoreTeam,2014)usingthemvpartpackage(De’ath, 2006).

TheIndicatorValueIndex–IndVal(DufrêneandLegendre,1997) wasusedtoassess possibleassociations ofdung beetlespecies withfeatures of samplingareasidentified byMRT analysis(De Cáceresand Legendre, 2009).TheIndVal methodcombines the degreeofspecificityofanecologicalstatus,presentingthe percent-ageofoccurrenceandsignificanceforeachspeciesindependently (McGeoch et al.,2002).Thisanalysis wasperformed in R3.1.1 program(RCoreTeam,2014)usingtheindicspeciespackage(De Cáceres,2013)with999permutations,usingdatafordungbeetle abundance.

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Fig.2. Principalcoordinatesanalysis(PCoA)ofdungbeetlespeciesbasedonBray–CurtissimilarityandenvironmentalvariablesbasedonEuclideandistance.Theanalysis wasperformedusingpresence–absence(a),abundance(b)andbiomass(c)dataofdungbeetles,and15environmentalvariables(d).ANH:AnhatomirimEnvironmental ProtectionArea;ITA:PermanentProtectionAreasofItapema;PER:PeriLagoonMunicipalPark;RAT:PermanentProtectionAreasofRatones.

Redundancy analysis (RDA) was used to verify the linear relationship betweendung beetle abundanceand biomass and forest structure. Abundance and biomass data were Hellinger-transformedpriortotheanalysisinordertoeliminatethedisparity between values (Legendre and Gallagher, 2001). The Pearson correlationcoefﬁcientwasusedtocorrelatetheRDA-axesand envi-ronmentalvariables.

Results

Wecollectedatotalof3004Scarabaeinaebeetlesbelongingto 21species(AppendixC).Mostextrapolatedspeciesaccumulation curves(exceptforsiteAofPeri,siteEofRatones,andRatonesas whole)reachedtheasymptote(AppendixD).Similarpatternswere foundforspeciesaccumulationcurvesforeacharea,which demon-stratesthesuccessinsamplingdungbeetleassemblages(Appendix D).Therareﬁedspeciesrichnessshoweddifferencesinthe num-berofspeciesbetweensitesandareassampled(AppendixE).This differencewasgreaterforITAandPER.Accordingtothespecies richnessestimatorChao1,basedontheabundance,therewerean estimatedcaptureofspeciesrichnessbetween70%and100%for thesamplingsites(AppendixE),withaveragesabove88.2%ineach ofthefourareas.

Dichotomiussericeus(Harold,1867),Canthonrutilanscyanescens Harold, 1868,and Canthidium aff. trinodosum (Boheman, 1858) werethemostabundantspecies,representing71percentofthe totalindividualscaptured(AppendixC).Onlyeightspecies(38.1%) werefoundinallfourareas.Thenumberofspeciespersiteranged between5and14.Onlyonespeciesoccurredinallsamplingsites(C. rutilanscyanescens).Threespeciesweresampledinatleast19sites (DeltochilummorbillosumBurmeister,1848,Deltochilummulticolor Balthasar,1939,andD.sericeus).Fivespecieswereresponsiblefor

92.8%ofthetotaldungbeetlebiomass(D.sericeus,Coprophanaeus saphirinus(Sturm,1826),C.rutilanscyanescens,D.multicolorandD. morbillosum)(AppendixC).

In general,PCoA analysesexplained more than 58% of total variation in dung beetle assemblages. According to the PCoA speciescomposition(presence–absence),speciesabundanceand speciesbiomassshowedaspatialdistributionaccordingtothe for-estareas sampled(Fig.2a–c). Thedissimilarityvalues between sites within thesame area were higher for dung beetle abun-danceandbiomass(Table1).PERMANOVAresultsconﬁrmedthe differencesvisually observedfor composition (Pseudo-F=3.199; p=0.001), abundance (Pseudo-F=4.053; p=0.001) and biomass (Pseudo-F=3.138; p=0.001). PCoA analysis explained 94.5% of totalvariationinenvironmentalvariables(Fig.2d).PERMANOVA resultsshowedthattherearedifferencesinenvironmental con-ditionsbetweenthem(Pseudo-F=3.083;p=0.001).Manteltests showedthatonlydissimilaritybetweendungbeetle abundance andenvironmentalvariablesamongsiteswasassociated(Mantel test=0.299;p=0.010).

MultivariateRegressionTreeanalysisusingenvironmental vari-ablesaspredictorssplitthedungbeetleabundancedistribution intofourgroups,whichexplained66.2%ofthevariation(Fig.3a). Theenvironmentalvariablesthatshowedhighersimilarityofdung Table1

Meandissimilarityofdungbeetledatasetsbetweensiteswithinthesamearea. DissimilaritywasbasedonBray–Curtis.Standarddeviationisinparenthesis.

Composition Abundance Biomass Anhatomirim 16.3(6.8)% 44.5(12.3)% 41.7(16.0)% Itapema 35.3(18.9)% 54.4(12.9)% 60.2(21.9)% Peri 29.1(9.4)% 46.3(14.6)% 45.6(16.7)% Ratones 17.5(3.8)% 33.2(10.9)% 25.1(10.1)%

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Fig.3. MultivariateRegressionTree(MRT)analysisofthedungbeetleabundance(a)andbiomasswithenvironmentalvariablesaspredictorvariables.Environmental variables:A,basalareaoftrees;I,landslope;J,altitude;N,heightofleaflitter;O,canopycover.SpeciesnamesareabbreviatedandcanbefoundinlegendofFig.4andin AppendixC.Barchartsattheterminalleavesoftheregressiontreerepresentspeciesabundancemeans.Theorderofbarsineachbarchartarethesameandfollowsthe sequenceofnamesshowedatleft.

beetle composition based on abundancewere altitude, canopy cover (insiteswithlower altitudes)andbasal areaof trees(in siteswithloweraltitudesandhighercanopycover).Forbiomass, MRTanalysisalsosplitthedungbeetlebiomassdistributioninto fourgroups,whichexplained74.6%ofthevariation(Fig.3b).The environmentalvariablesthatshowedhighersimilarityofdung bee-tlecompositionbasedonbiomasswereheightofleaflitter,land slope(insiteswithlowerheightofleaflitter)andaltitude(insites withhigherheightofleaflitter).ThePrincipalComponent Analy-sisresultingfromMRTanalysesforabundanceandbiomasscanbe foundinAppendixF.

Severaldungbeetlesspeciesweresigniﬁcantlyassociatedwith someenvironmentalfeature,accordingtotheresultsofthe Ind-Valanalysis(Table2).Sevenspecieswereassociatedtositeswith highervaluesofaltitude,whichoccurredmainlyinRatonesand Peri.OnlyParacanthonaff.rosinaeBalthasar,1942wasassociated tositeswithlowervaluesofbasalareaoftrees,whichoccurred mainlyinPeri.

Redundancyanalysisconstrained27%ofthedungbeetle abun-danceinrelationtotheexplanatoryvariables(Fig.4a).Theﬁrstand

secondcanonicalaxesweresigniﬁcantandaccountedfor67.7%of theconstrainedvariance.Theﬁrstaxis(RDA1,F=13.982;p=0.001) accountedfor44.8%ofthevariance,andwaspositivelycorrelated with leaf litter height(r=0.46), green cover (r=0.38) and dis-tanceofshrubs(r=0.26);itwasnegativelycorrelatedwithaltitude (r=−0.82),shrubheight(r=−0.20)andshrubbasalarea(r=−0.20). Thesecondaxis(RDA2,F=7.167;p=0.001)accountedfor22.9%of

Table2

IndValanalysesofdungbeetlespecieswithsigniﬁcantassociationswithsome envi-ronmentalfeatures(seeMultivariateRegressionTreeanalysisforvalues).

IndVal p-Value Environmentalfeature Canthidiumaff.trinodosum 0.971 0.003 Higheraltitudes Canthonluctuosus 0.837 0.022 Higheraltitudes Deltochilumbrasiliense 0.985 0.001 Higheraltitudes Deltochilummorbillosum 0.858 0.045 Higheraltitudes Deltochilumrubripenne 0.934 0.003 Higheraltitudes Dichotomiussericeus 0.876 0.043 Higheraltitudes Paracanthonaff.rosinae 0.939 0.011 Lowerbasalareaoftrees Uroxyssp.1 0.990 0.001 Higheraltitudes

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Fig.4.Redundancyanalysisordinationfordungbeetleabundance(a)andbiomass (b)constrainedbyenvironmentalvariables.Triplotwithexplanatoryvariables, speciesandsamples:sp.1:Bdelyrusbraziliensis;sp.2:Canthidiumaff.trinodosum; sp.3:Canthonluctuosus;sp.4:Canthonrutilanscyanescens;sp.5:Canthonellaaff. instriata;sp.6:Coprophanaeusdardanus;sp.7:Coprophanaeussaphirinus;sp.8: Del-tochilumbrasiliense;sp.9:Deltochilumfurcatum;sp.10:Deltochilummorbillosum; sp.11:Deltochilummulticolor;sp.12:Deltochilumrubripenne;sp.13:Dichotomius sericeus;sp.14:Dichotomiusquadrinodosus;sp.15:Dichotomiussp.;sp.16: Eurys-ternuscyanescens;sp.17:Eurysternusparallelus;sp.18:Paracanthonaff.rosinae;sp. 19:Phanaeussplendidulus;sp.20:Uroxyssp.1;sp.21:Uroxyssp.2;A:basalareaof firsttree;B:heightoffirsttree;C:topdiameteroffirsttree;D:distancetofirsttree; E:basalareaoffirstshrub;F:heightoffirstshrub;G:topdiameteroffirstshrub;H: distancetofirstshrub;I:landslope;J:altitude;K:leaflittercover;L:greencover;M: exposedsoil;N:heightofleaflitter;O:canopycover;1–25:ANHsamplingpoints; 26–50:ITAsamplingpoints;51–75:PERsamplingpoints;76–100:RATsampling points.

thevariance,andwaspositivelycorrelatedwithleaflitterheight (r=0.42),altitude(r=0.41),landslope(r=0.38),distanceofshrubs (r=0.37),canopycover(r=0.34)anddistanceoftrees(r=0.20);it wasnegativelycorrelatedwithtreeheight(r=−0.42),shrubheight (r=−0.30)andtreebasalarea(r=−0.24).

Redundancyanalisysondungbeetlebiomassconstrined27.5% oftotalvarianceinrelationtotheexplanatoryvariables(Fig.4b). Thefirstandsecondcanonicalaxesweresignificantandaccounted for 76.3% of the constrained variance. The first axis (RDA1, F=13.281; p=0.001) accounted for 41.6% of the variance, and

waspositivelycorrelatedwithtreeheight(r=0.44),shrubheight (r=0.27)andpercentageofexposedsoil(r=0.20);itwasnegativelly correlatedwithshrubdistance(r=−0.44),landslope(r=−0.26), percentageofgreencover(r=−0.31),heightofleaflitter(r=−0.64), andcanopycover(r=−0.26).Thesecondaxis(RDA2,F=11.082; p=0.001)accountedfor34.7%ofthevariance,andwaspositively correlatedwithlandslope(r=0.31)andaltitude(r=0.88).

Analysesof speciesdistributionplots (Fig.4a)indicated that abundanceofC.aff.trinodosumandUroxyssp.1wereassociatedto siteswithhigheraltitudevaluesandlowergreen(vegetation)cover values.C.rutilanscyanescenswasassociatedtositeswithlower alti-tudevalues,small-sizedtrees,higherleaflitterheightandgreen (vegetation)covervalues.C.saphirinuswasassociatedtositeswith highersizedtrees,canopycoverandlandslopevalues.D.multicolor wasassociated tositeswithhighervaluesofgreen(vegetation) coverandleaflitterheight,whileD.morbillosumwasassociated tositeswithhigheraltitudeandwide-crownedshrubs.D.sericeus wasassociatedtositeswithhighersizedtreesandlowervalues ofleaflitterheight.Analyzingthebiomass(Fig.4b),C.saphirinus wasassociatedtositeswithhigheraltitude,landslopeandcanopy cover.D.morbillosumwasassociatedtositeswithhigherleaflitter height,greencoveranddistanceofshrubs,whileD.sericeusshowed anoppositepattern.

Discussion

Theresultsindicatesigniﬁcantdifferencesinspeciesrichness, assemblagestructure basedonabundanceandbiomass,as well as in the composition of dung beetles between remnant sites ofthe AtlanticForest,and that thesedifferencesare associated withthedistributionofenvironmentalcharacteristicsofremnants alongthespatialgradientstudied.Wealsofoundthatabundance andbiomassofdungbeetlesresponddifferentlyto environmen-talvariation,whichisrelatedtodifferencesinspeciescomposition betweensampledsites,asdemonstratedbyPCoAanalysis.

Differenthistoricalprocessesofanthropogenicoccupationand landusemayhaveproducedtheseassociations.However,several othermechanismsandprocessesmaybeassociatedwithpatterns ofspeciesdistribution(speciesrichness,composition,abundance andbiomass)duetoisolationandfragmentationofareasandthe mainland-islandlandscape(daSilvaandHernández,2014),aswell asdifferences incurrent humanactivityamongareas and neu-tralprocesses.Furthermore,dungbeetlesareverydependenton mammalsasamainfoodresource(Culotetal.,2013),and mam-malpopulationscanalsobenegativelyaffectedbyfragmentation (Canaleetal.,2012;Santos-Filhoetal.,2012),aswellasby human-drivendefaunationthatoccurredontheIslandofSantaCatarina (Graipeletal.,2001).Historically,sealeveloftheAtlanticOcean waslowerand theislandand mainlandwereunited duringthe lasticeage(∼10,000–100,000yearsago),whichprobablyenabled migration of speciesbetween theareasof themainland tothe island(Kleinetal.,2006).Withtheincreaseinsealevel(∼10,000 yearsago)andurbanization(inthelastcentury),severalareasof forestsbecamefragmentedandisolated,acommonscenarioin cur-rentAtlanticForestareas(Tabarellietal.,2005;Kleinetal.,2006; Ribeiroetal.,2009).Theselargefragmentsnowactas“islands”, withisolatedcommunitiesandlowdispersalandcolonizationrates (Mayetal.,2013),especiallyoforganismsthatareseverelyaffected byforestfragmentationandhabitatloss.Thesecharacteristicscan adverselyaffect thelong-term conservationof biodiversity and relatedecologicalprocesses.

Inadditiontothehistoricalprocesses,theIndValandRDA analy-sesofdungbeetlespeciesdistributionindicatedthatseveralspecies showedsomedegreeofassociationwithenvironmental character-isticsofforeststructureamongareas.C.aff.trinodosum,Canthon

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luctuosusHarold,1868,Deltochilumbrasiliense(Castelnau,1840),D. morbillosum,Deltochilumrubripenne(Gory,1831),D.sericeusand Uroxyssp.1wereassociatedtositeswithhigheraltitudevalues (IndVal),whileC.rutilanscyanescensshowedanoppositeresponse (RDA).Altituderangedbetween28and265maslamongsites,a commonfeatureofthesouthernBrazilianAtlanticForest(Ribeiro etal.,2009).Altitudeisanimportantfeaturefordungbeetle distri-butionashighlightedbyEscobaret al.(2005)intheColombian Andes. However,we expectedthat altitudein our studymight beaproxythatrepresentsanenvironmentalvariablewedidnot measure,suchassoiltype,soilpenetrability,soiltexture,orother variabledescribing soilcondition,which inﬂuencesdungbeetle distributioninoursampledareas.Thesesoilconditions maybe relatedtoagreaterorlesserdistancefromthesamplingsiteto thesea.

Ourresults(RDA)alsoshowedthatC.saphirinuswasassociated tositeswithgreatertrees,canopycover,landslopeandaltitude.D. multicolorwasassociatedtositeswithgreatergreen(vegetation) coverandleaflitterheight.D.morbillosumwasalsoassociatedto siteswithhigherleaflitterheight,greencoverandwide-crowned shrubs.D.sericeuswasassociatedtositeswithlargersizedtrees and lowervalues ofleaflitter height,green cover anddistance ofshrubs.HernándezandVaz-de-Mello(2009)andCamposand Hernández(2013)alsoshowedthatsomeofthesefeatures(sizeand distanceoftreesandshrubs,percentageofleaflitter,greencover andexposedsoil)werealsoimportantdeterminantsofdungbeetle distributioninAtlanticForestareasinSãoPauloandSantaCatarina, respectively.Increasedleaflitterisexpectedtoaffectnegatively thenestingactivitiesofsomerollerspecies(Nicholsetal.,2013), butourresutsdidnotexplicitlyshowsuchassociation.However, heightofleaflitterwashighlightedasanimportant environmen-talconditionforthedistributionofdung beetlebiomassin our study.Dungbeetlespeciesassociatedtositeswithhigherorsmaller sizedtreesorshrubsmaybeaffectedbyrelatedmicroclimatic vari-ation(Feer,2008),which mayinﬂuencereproductiveaspectsof species(MartínezandVásquez,1995).Differencesin environmen-talcharacteristicsacrossstudysitesandareasmayrepresentthe degreeofchange,orthestatusofsuccessionoftheforeststructure inAtlanticForestremnants.Ingeneral,thedistributionofdung beetlesalong differentenvironmentalcharacteristicsmayshow discreteassociationswithparticularbiotypeswithinthelandscape (Davisetal.,2001;Viegasetal.,2014),andevidencesuggeststhat speciesrichness,abundanceandbiomassarenegativelyimpacted indisturbedhabitats(Gardneretal.,2008b).Theseenvironmental characteristicsarealsoexpectedtoaffectthedistributionofsome mammalianspecies(Culotetal.,2013)and,therefore,theintakeof foodresourcesfordungbeetles.

Differencesin environmental conditions (e.g. habitat distur-bance)indirectlyaffecttheecologicalfunctionsofdungbeetlesby affectingtheircommunityattributes(e.g.speciesrichness, abun-dance and biomass) (Braga et al., 2013). Several studies have highlightedtherelationshipbetweencommunity attributesand ecologicalfunctions(Andresen,2002;Bangetal.,2005;Sladeetal., 2007). In addition, some species may have their demographic dynamicsalteredbypoorenvironmentalconditions.Therefore, dif-ferencesindungbeetledistributionacrossdifferentspatialextents associatedwithdifferencesinenvironmentalconditionsmaybe affectingtheecologicalfunctions,aswellascommunitystructure, evenwithinthesamefragmentofforest.Thedifferencesin envi-ronmentalconditionsfoundwithinthesamefragmentreﬂectthe currentstageoftheAtlanticForest:isolatedandsmallfragments composedbysecond-growthforestsinearlytomediumstagesof succession(Metzgeretal.,2009).

Thisworkdemonstratedtheexistenceofsigniﬁcantassociations betweenseveralspeciesof dungbeetlesand theenvironmental structureofBrazilianAtlanticForestremnantsatlocalandregional

scale.Speciescompositionandstructurebasedonabundanceand biomass of dung beetleassemblages werealso associated with structuralfeaturesofthestudiedhabitats.Thisresultrevealsthe importanceofspatialdistributionoftheseareasforthe mainte-nanceandconservationofdungbeetlespecies,aswellasforthe responseofthesespecies toenvironmentalchanges.Weexpect thatprovidingbasicinformationonspeciesdistributionand com-munitystructuremaybeusefulintheevaluationandmonitoring oftheprotectedBrazilianAtlanticForestremnants.

Thespatialdistributionandtheoccurrenceofspatially struc-turedenvironmentalcharacteristicsofAtlanticForestremnantscan hostahighgammadiversityofdungbeetles.Becausetheseinsects showresponsessimilartoseveralothertaxa(Barlowetal.,2007; Culotetal.,2013),weexpectthattheremnantsinthisstudy con-tributetothemaintenanceofwildlifeofseveraltaxonomicgroups oforganisms.We knowthatboth themammalcommunityand environmentalheterogeneity inﬂuencethedistribution ofdung beetleassemblages.Knowingtherelativeimportanceofthesetwo factorsisademandforfuturestudiesonfactorsinﬂuencingthe spatialdistributionofdungbeetles.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest.

Acknowledgments

Wethankallwhocontributedtothisstudyinanyway.Wethank CoordenaçãodeAperfeiçoamentodePessoaldeNívelSuperiorfor thescholarshiptoPGSandforresearchfunding(Process001/2010 MEC/CAPES/PNPD, “Biodiversidade de artrópodes terrestres e aquáticosemdiferentesgradientesambientaisdaMataAtlântica doestadodeSantaCatarina”).WethanktheConselhoNacionalde DesenvolvimentoCientíficoeTecnológicofortheresearchgrant toMIMH(ResearchProductivity/PQ/2010,Process303800/2010-0, Project“ComportamentodebesourosScarabaeinaeesuafunção nociclodedecomposiçãodamatériaorgânica”),andtheInstituto ChicoMendesdeConservaçãodaBiodiversidadeforpermissionto collectspecimens(permit#32333-3).

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.rbe.2015.11.001.

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