Flight patterns and sex ratio of beetles of the subfamily Dynastinae (Coleoptera, Melolonthidae)

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

Flight

patterns

and

sex

ratio

of

beetles

of

the

subfamily

Dynastinae

(Coleoptera,

Melolonthidae)

Larissa

Simões

Corrêa

de

Albuquerque

a,∗

_,

_Paschoal

_Coelho

_Grossi

b

_,

_Luciana

_Iannuzzi

a

a_{UniversidadeFederaldePernambuco,DepartamentodeZoologia,Recife,PE,Brazil}

b_{UniversidadeFederalRuraldePernambuco,DepartamentodeAgronomia/Protec¸ãodePlantas,Recife,PE,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received8July2015 Accepted24March2016 Availableonline13May2016 AssociateEditor:RodrigoKrüger Keywords:

BrazilianAtlanticforest Cyclocephalini Lighttrap Nocturnalbeetles

a

b

s

t

r

a

c

t

DynastinaeisoneofthemostrepresentativesubfamiliesofMelolonthidae(Scarabaeoidea)andhas

considerableecologicalimportanceduemainlytointeractionswithplantsofthefamiliesAraceaeand

Annonaceae.Thisrelationshiphasledtotheevolutionofnocturnalactivitypatterns,whichareinfluenced

byenvironmentalconditions.Inthepresentstudy,abioticfactorswereinvestigatedtocomprehendthe

influenceontheflightpatternsandidentifythesexratioofbeetlesfromthissubfamily.Astudywas

con-ductedatCampodeInstruc¸ãoMarechalNewtonCavalcantiinnortheasternBrazilbetweenDecember

2010andNovember2011.ThirteenspeciesofDynastinaewereidentified,mostofwhichwerefromthe

genusCyclocephala.Abundanceandrichnessweregreaterinthedryseason.Sixspeciesexhibitedpeak

flightactivityatspecificperiodsofthenight.MorefemalesthanmaleswererecordedforCyclocephala

distinctaandC.paraguayensis.Thepresentfindingssuggestthatrainfallreducestheflightactivityof

thesebeetlesanddifferenttimeschedulesmayberelatedtomatingbehavior,foragingbehaviorandthe

avoidanceofinterspecificresourcecompetition.

©2016SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen

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

Introduction

Dynastinae is one of the most remarkable subfamilies of

MelolonthidaesensuEndrödi(1966).Beetlesofthissubfamilyoccur innearlyallmajorbiogeographicregionsandaremostlyfoundin thetropics,especiallytheNeotropics(Ratcliffe,2003).Adultsfeed ondecomposedfruits,algae,plantsroots(obtainingnutritive liq-uids),leaves,flowersandpollen(JacksonandKlein,2006;Ritcher, 1958).NearlyallDynastinaeadultsareeithernocturnalor crepus-cular(Ratcliffe,2003;Riehs,2006;RatcliffeandCave,2009).Diurnal activitycorrespondstotheintervaloftimeusedforforagingand matingandisdefinedbythepresenceofsunlight(Pianka,1973; Ma ˜nosaetal.,2004;Hernández,2007;González-Mayaetal.,2009). Ingeneral,peakactivityinspeciesisregulatedbydifferentfactors (Hernández,2007,2002;FeerandPincebourne,2005;Gilletetal., 2010;Gerberetal.,2012).Predatorsandfoodsources,forinstance, actasregulatorsofpeakactivity,leadingtoadaptationsthatresult inthesuccessandsurvivaloforganisms(Pianka,1973;Dawkings andKrebs,1979;Overdorff,1988;Gill,1991;González-Mayaetal., 2009;HalffterandHalffter,2009;Valeraetal.,2011).

∗ Correspondingauthor.

E-mail:larissa.sca@hotmail.com(L.S.C.d.Albuquerque).

Nocturnalorcrepuscularhabitsareassociatedwithanthophilia, especially forCyclocephalini (Endrödi, 1985;Gottsberger,1999, 1986;MaiaandSchlindwein,2006;Maiaetal.,2012,2010).The pol-linationofmanytropicalfruittreesthathavenightanthesis,suchas Annonaspp.(Annonaceae),palms(Arecaceae)andaroids(Araceae), isdependentonpollinatingbeetles,especiallyspeciesofthegenera CyclocephalaLatreilleandErioscelisBurmeister,whichensurethe reproductivesuccessofthesetrees(Endrödi,1985;Gottsberger, 1986,1999;Silberbauer-Gottsbergeretal.,2003;García-Robledo etal.,2004;Croat,2004;Maiaand Schlindwein,2006;Ratcliffe, 2008,2003;Maiaetal.,2012,2010).

Intropicalrainforests,insectspecies areinfluencedbybiotic andabioticoscillations(EmmelandLeck,1970;Wolda,1989;Nair, 2007).Rainfall,foodsourcesandpredatorsexertaninfluenceon theabundanceoftropicalinsects(Wolda,1988,1978).Favorable environmentalconditionsfacilitatethegrowth,reproductionand activityoftheseorganisms(Tauberetal.,1986;Wolda,1988).

Environmentalconditions alsoexertaninfluenceonthesex

ratioofinsects(Hamilton,1967).Inresponsetovariationsin envi-ronmentalconditions,thesexratiooftheoffspringvariesdueto changesinfitness(WestandSheldon,2002).Dependingon

off-spring competitionof one sexwithanother and theparents, a

tendencytoproducetheothersexoccurstoavoidtheeffectoflocal resourcecompetition(Taylor,1994;Julliard,2000).Inpoor-quality

http://dx.doi.org/10.1016/j.rbe.2016.03.002

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

environments,parentalindividualsmayincreasefitnessbybiasing theiroffspringmoretowardadispersingsex(Julliard,2000).

Despite theimportanceof beetlesof thesubfamily Dynasti-naeaspollinatorsand theirroleinmaintaininghealthyedaphic ecosystems,fewstudieshaveaddressedthebiodiversityand nat-uralhistoryofthesebeetles,especiallyintheAtlanticRainforest northoftheSãoFranciscoRiverBasininnortheasternBrazil.Thus, theaimofthepresentstudywastodeterminetheeffectsof rain-fallofbeetlecommunitiesofthesubfamilyDynastinaeandidentify nocturnalflightactivityandthesexratioofthespeciescollected.

Thehypotheses are thatdifferences in abundanceand richness

occurbetweenthedry andrainyseasons;peakflightactivityis relatedtoforagingbehaviorandthesexratiodenotessimilar pro-portionsofmalesandfemales.

Materialandmethods

Studysite

This study was conducted in the municipality of Abreu e

Lima(stateofPernanbuco,northeasternBrazil)attheCampode Instruc¸ãoMarechal NewtonCavalcanti (CIMNC – 7◦4949.39S, 35◦610.20W), which is a military site located in the

Aldeia-Beberibe Environmental Protection Area, covering 30,000ha

(SEMAS,2012)(Fig.1A–C).TheCIMNCislocated40kmNWofthe coastandhasatotalof7324ha(Andradeetal.,2005;Lucena,2009). Vegetationconsistsofopentropicalrainforestandsemi-deciduous forest,comprisingsecondaryforestwitha fewremnantsof pri-maryforest(Andradeetal.,2005;Lucena,2009;IBGE,2012).This sitewasformerlyasugarcanemillthatwasintensivelyexploited untiltheestablishmentoftheCIMNCin1944(Andradeetal.,2005; Lucena,2009;Guimarãesetal.,2012).Itiscurrentlypreservedby theBrazilianArmy(Lucena,2009).

Abiocticdata

Dailyand monthly rainfall indices from 2010to 2011were

obtainedfromhydro-meteorologicalmonitoringunitofthe Labo-ratóriodeMeteorologiadePernambuco(ITEP/HIDROMET,2012).

Historical mean rainfall and monthly mean temperature were

obtainedfromtheAbreueLimaStation(ITEP/HIDROMET,2012).

Other temperature and humidity data were obtained at the

samplingpointusingadigitalthermohygrometer.Readingswere takenonthesamplingdaybetween5:00pmand5:00am. Consider-ingthehistoricalprecipitationindex,therainyseasonwasdefined asspanningfromMarchtoAugust(ITEP/HIDROMET,2012). Insectsampling

Beetles ofthesubfamily Dynastinaewere collectedmonthly

fromDecember2010toNovember2011,exceptApril2011,dueto intenserainfallthatpreventedaccesstothecollectionsite. Samp-linglasted12handwasperformedevery30days.Thesamplesite wasestablishedatadistanceof30mfromtheedgeoftheremnant oftheAtlanticrainforest.

Alight trapwasinstalledtoattract beetlesfrom5:00pm to 5:00amthefollowingday.Blacklight(250W)andmixedmercury vaporbulbs(250W)weredeployedonoppositesidesofawhite sheetmeasuring2.3m×2.0m, stretchedat thecollectionpoint (Fig.2A–C). Thebeetleswerecollectedmanuallyastheylanded ontheilluminatedsheet.

A C B 2.3m 2.3m 2.0m

Fig.2. Lighttrapmodelusedforbeetlesampling:(A)Blacklightbulb.(B)Mixed mercurybulb.(C)Lightsupport.

Fig.1. Mapshowingsamplingsite:(A)PernambucoStaterepresentedinblack.(B)BlackdotrepresentingCampodeInstruc¸ãoMarechalNewtonCavalcanti,AbreueLima, Pernambuco,Brazil.(C)BlackdotrepresentingsamplingsiteatMarechalNewtonCavalcanti,AbreueLima,Pernambuco,Brazil.

Table1

TotalandrelativeabundanceofnocturnalspeciesofDynastinae(Coleoptera,Melolonthidae)atCampodeInstruc¸ãoMarechalNewtonCavalcantioveroneyearofcollection (2010–2011).

Tribe Species Abundance Relativeabundance(%)

Cyclocephalini CyclocephalacearaeHöhne,1923 19 4.2

Cyclocephalini CyclocephaladistinctaBurmeister,1847 266 58.3

Cyclocephalini CyclocephalaparaguayensisArrow,1913 63 13.8

Cyclocephalini CyclocephalavestitaHöhne,1923 2 0.4

Cyclocephalini Dyscinetusdubius(Olivier,1789) 27 6

Cyclocephalini Dyscinetusrugifrons(Burmeister,1847) 10 2.2

Cyclocephalini Chalepidessp. 1 0.2

Cyclocephalini Stenocratesholomelanus(Germar,1824) 28 6.1

Pentodontini Eutheolahumilis(Burmeister,1847) 1 0.2

Pentodontini Tomarusebenus(DeGeer,1774) 10 2.2

Pentodontini Ligyrus(Ligyrus)cuniculus(Fabricius,1801) 27 6

Oryctini Strategusvalidus(Fabricius,1775) 1 0.2

Oryctini Coelosisbicornis(Leske,1779) 1 0.2

Total 456 100

Foreachhourofcollection,akillingjar(polypropylenejarwith ethylacetate) wasusedtorecord offlight period. Thesamples weretakentolaboratoryofTaxonomiaeEcologiadeInsetosofthe UniversidadeFederaldePernambucofortaxonomicidentification. Abioticdata,abundance,richnessand flightperiodwerepooled forthesubsequentanalyses.Voucherspecimensweredepositedin Colec¸ãoEntomológicadaUFPE(CE-UFPE).

Dataanalysis

TheabundanceandrichnessofthespeciesofDynastinae sam-pledinthedryandrainyseasonswerecomparedusingone-way ANOVAtestwiththeaidoftheSTATISTICA7.0program(StatSoft, 2004),withsignificancelevelsetat5%(p<0.05).Tukey’stestwas

employedfortheposthocevaluations.Abundanceandrichness

valuesweretransformedtoLOG+1.Forthedeterminationofsex ratios,differencesbetweenmalesandfemalesweretestedusing thechi-square(2_{)testforeachspecieswiththeaidofthe} BioEs-tat5.0program(InstitutoMamirauá,2007).Spearmancorrelation analysiswasperformed,withR3.1.1 program,betweenrainfall andthemostabundantspeciesfound(RDevelopmentCoreTeam, 2014).Circularstatisticswereperformedfortheflightperiodwith

theaidoftheORIANAprogram,consideringthemostabundant

species(n≥10)(KovachComputingServices,2004).

Results

Atotalof456specimensofDynastinaebelonging13species, eightgeneraandfourtribeswerecollected.Themost representa-tivetribewasCyclocephalini,witheightspecies (approximately

62% of total richness) and 416 specimens (approximately 91%

of total abundance) (Table 1), followed by Pentodontini (three speciesand38specimens)andOryctini(twospeciesandtwo spec-imens).CyclocephalaLatreillewasthemostabundantandrichest genus,accountingforapproximately31%ofthespeciesrecorded. Cyclocephaladistincta Burmeistercontributedtothemajority of

specimens (approximately 58%), followed by C. paraguayensis

Arrow,whichwasthesecondmostabundantspecies.

Significantdifferences in abundance were foundamong the

samplingmonths(F=4.75;df=10;p<0.001).Theposthoctests revealedgreaterabundanceinthedryseason.Likewise,richness valuesweresignificantlyhigher(F=3.95;df=10;p<0.001)inthe dryseason.

RainfallcausedgreatereffectinCyclocephalinibeetles,when comparedtoPentodontini (Fig.3A–C). Speciesfromboth tribes

hadgreater abundanceduringthedryseasonand beginning of

rainyseason,howeverPentodontinihadhigherabundancesinthe

30

A

B

C

25 20 15 Ab undance (Mean ± SE) Ab undance (Mean ± SE) Rainf a ll (mm) 10 5 0 3.0 2.5 2.0 1.5 1.0 0.5 0.0 700 600 500 400 300 200 100 0

Dec/10 Feb/11 May/11 July/11 Sep/11 Nov/11

Fig.3.RainfalleffectinthemostabundanttribesofDynastinae(Melolonthidae), duringoneyearofcollectionusinglighttrapatCampodeInstruc¸ãoMarechal New-tonCavalcanti,AbreueLima,PE,Brazil:(A)MeanabundanceofCyclocephalini beetles,recordedmonthly,betweenDecember2010andNovember2011(except April2011). (B) Meanabundance of Pentodontinibeetles,recorded monthly, betweenDecember2010andNovember2011(exceptApril2011).(C)Rainfall, recordedmonthly,betweenDecember2010andNovember2011(exceptApril 2011).

A

B

C

D

E

F

00:00 18:00 06:00 18:00 12.5 100 75 50 06:00 25 50 75 100 125 00:00 12:00 12:00 12:00 00:00 00:00 8 6 4 2 12:00 12:00 12:00 00:00 20 15 10 5 5 10 15 20 18:00 06:00 18:005 06:00 5 4 3 2 1 4 3 2 00:00 10 8 6 4 2 2 4 6 8 10 18:00 06:00 18:00 8 6 4 2 06:00 12.5 10 7.5 5 2.5 12.5 10 7.5 5 2.5

Fig.4.Circularhistogramshowingpeakflightactivityof:(A)Cyclocephalacearae;(B)C.distincta;(C)Dyscinetusdubius;(D)Stenocratesholomelanus;(E)C.paraguayensis; (F)Ligyrus(Ligyrus)cuniculus,duringoneyearofcollectionusinglighttrapatCampodeInstruc¸ãoMarechalNewtonCavalcanti,AbreueLima,PE,Brazil.Blackline=mean vectorandconfidenceinterval.

beginningandbyendoftherainyseason,thenanabruptdecrease

in the beginning of the dry season.On theother hand,

Cyclo-cephalini had a decrease of abundance after the beginning of

therainyseason,maintainingthatuntilthebeginningofthedry season.

Regardingflightperiod,sixspecies,whichwerethemost abun-dant,weredividedintwogroups.Thefirstgroupexhibitedflight activityfrom6:00to8:00pmandincludedCyclocephalacearae,C. distinctaandDyscinetusdubius,withsignificantpeakflight activ-ityat 6:35pm(r=0.919;p<0.001)(Fig.4A),7:27pm (r=0.818; p<0.001) (Fig. 4B) and 7:19pm (r=0.67; p<0.001) (Fig. 4C), respectively.Thesecondgroupexhibitedflightactivityfrom8:00

to10:00pm and includedStenocrates holomelanus,Cyclocephala paraguayensisandLigyrus(Ligyrus)cuniculus,withsignificantpeak flightat8:44pm(r=0.698,p<0.001)(Fig.4D),9:32pm(r=0.895, p<0.001)(Fig.4E)and9:37pm(r=0.67,p<0.001)(Fig.4F), respec-tively.The2 _{resultsrevealedthatthesexratioofCyclocephala} distinctaandC.paraguayensisdifferedsignificantly,withfemales occurringingreaterabundancethanmales(Table2).

Regardingthefourmostabundantspecies,justLigyrus(Ligyrus) cuniculus, had sex ratio positively influenced by rainfall (0.68, p=0.01) (Fig. 5A), unlike Cyclocephala distincta (−0.1, p=0.75) (Fig.5B),C. paraguayensis(0.21,p=0.52)(Fig.5C),and Tomarus ebenus(0.32,p=0.33)(Fig.5D).

5.0

A

C

B

D

4.0 3.0 2.0 1.0 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 3.0 2.5 2.0 1.5 1.0 0.5 0.0 2.2 2.0 1.8 1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

Fig.5.Spearmancorrelationbetweensexratioandrainfallof:(A)Cyclocephaladistincta;(B)C.paraguayensis;(C)Tomarusebenus;(D)L.(Ligyrus)cuniculus.

Table2

SexratioofnocturnalspeciesofDynastinae(Coleoptera,Melolonthidae)atCampo deInstruc¸ãoMarechalNewton Cavalcanti,during overone yearofcollection (2010–2011).

Species Females Males 2 _p

CyclocephalacearaeHöhne,1923 14 5 4.26 0.066 CyclocephaladistinctaBurmeister,1847 176 90 27.80 <0.001 CyclocephalaparaguayensisArrow,1913 50 12 23.29 <0.001 Dyscinetusdubius(Olivier,1789) 10 10 0 1 Stenocratesholomelanus(Germar,1824) 13 10 0.39 0.676 Ligyrus(Ligyrus)cuniculus(Fabricius,1801) 9 13 0.72 0.522

Discussion

ThepresentfindingsindicatethattheactivityoftheDynastinae communityinnortheasternBrazilisinfluencedbyrainfallandthat somespecieshavespecificperiodsofflight.Furthermore,thegroup ofspeciesbelongingtheCyclocephalinitribewaspredominant.

Cyclocephalini,themostrepresentativeinthepresentstudy,is adiversetribeintheNeotropicalregion.Thisgrouphasalsobeen veryrepresentative insurveys ofDynastinae beetlesconducted intheAmazonregion(AndreazzeandFonseca,1998;Andreazze, 2001;Andreazze and Motta, 2002)and hasalso beenrecorded inagro-ecosystemsnearremnantsoftheAtlanticRainforestsas wellasotherrainforests,withsomespeciesconsidered agricul-turalpestsduetothefactthatthesebeetlesfeedonrootsystems (Morón, 2001; Pereira and Salvadori, 2006; García-Lópezet al., 2012,2010).C.distinctawasthemostabundantamongthespecies ofthistriberecordedherein.Thismaybeexplainedbyits adap-tationtoenvironmentaldisturbancesandtheexploitationofnew trophicniches,asobservedforotherspeciesofthisgenusinthe Amazon(AndreazzeandFonseca,1998).C.distinctaiswidely dis-tributedthroughoutSouthAmerica(Endrödi,1985).

For Cyclocephalini, and Cyclocephala cearae especially, the

present findings are congruent with emissions of floral scents

fromTaccarum ulei Engl. & K. Krause (Araceae), as the species hasbeen identified as a pollinator of this plant species (Maia etal.,2013).Suchnocturnalhabits,andperiodofactivity,maybe

associated with the cantharophilous pollination of species of

Araceae and Annonaceae, which provide special chambers and

exudates for feedingand mating(Maia and Schlindwein,2006;

Cavalcanteetal.,2009;Maiaetal.,2010,2013).Duetothis rela-tionship,somegroupshaveevolvedflightperiodsthataresimilar tothefloweringtimeoftheirpreferentialhostplants(Maiaand Schlindwein,2006;Maiaetal.,2010).Theconsiderableabundance ofC.distinctainthepresentstudymaybeexplainedbyvisitations totheflowersofplantsofthegenusAttaleaKunth(Araceae)found intheCIMNC(Voeks,2002;Lucena,2009),inwhichthisspecies matesandforages.

Onlytwospeciesinthepresentstudyexhibitedagreater abun-danceoffemalesthanmales,differingfromtheexpected1:1ratio.

Females are known to spend more time foraging and looking

foridealovipositionsites,whichmayexplainthis phenomenon (Bedford,1975).

TheAtlanticrainforest, especiallyin northeastern Brazil,has beensufferingfromhumanactionsoverthepast516yearsthat haveresultedinhomogenizationofthesystem(Lôboetal.,2011). Thus,somespeciesofDynastinaespeciesmayrespondtothis situ-ationthroughfemaledispersal.Anotherpossibilityistheadversity causedbyhighmoisturecontentinthesoilintherainyseason. AsseeninPhyllophagacrinita(Burmeister,1855)(Melolonthidae: Melolonthinae)(GaylorandFrankie,1979),Cyclocephaladistincta

femalesmayremainabovegroundundersuchconditions.

How-ever,thisisnotthepatternforC.immaculata(Olivier,1789)(=C. luridaBland,1863),forwhichmoremalesthanfemaleshavebeen recorded in thefield (Potter, 1980), which is likely due tothe differentperceptionofthelightbetweensexes(Potter,1980). Nev-ertheless,Neiswander(1938) foundthat naturalpopulations of speciesofCyclocephalahaveasexratioof1:1.

Conclusion

Basedonthepresentfindings,weconsiderthattheDynastinae communityisinfluencedbytherainfall.Furthermore,fightactivity hastemporalsegregationforsomespeciesofthesubfamily.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

TheauthorsaregratefultotheBrazilianArmyandtheCampo deInstruc¸ãoMarechal NewtonCavalcanti forallowingthe

exe-cution of the project and offering accommodations. Thisstudy

wassupportedbytheBrazilianfosteringagenciesCoordenac¸ãode Aperfeic¸oamentodePessoaldeNívelSuperior(CAPES)andConselho Nacional deDesenvolvimento Científicoe Tecnológico(CNPq). We alsothankRichardBoikefortheEnglishimprovement,W.Rafael Souzaforthesupportwiththeimages,andBrunoK.C.Filgueiras forreviewingtheanalysis.

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