First report of two species of scarab beetles (Coleoptera, Scarabaeidae) inside nests of Azteca cf. chartifex Forel (Hymenoptera, Formicidae) in Brazilian Amazonian Rainforest

RevistaBrasileiradeEntomologia60 (2016)359–361

REVISTA

BRASILEIRA

DE

Entomologia

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

Short

Communication

First

report

of

two

species

of

scarab

beetles

(Coleoptera,

Scarabaeidae)

inside

nests

of

Azteca

cf.

chartifex

Forel

(Hymenoptera,

Formicidae)

in

Brazilian

Amazonian

Rainforest

João

Rafael

Alves-Oliveira

_,

_Diego

_Matheus

_de

_Mello

_Mendes

_,

_Douglas

_de

_Campos

_,

Alberto

Moreira

da

Silva-Neto

_,

_José

_Wellington

_de

_Morais

_,

_Paschoal

_Coelho

_Grossi

a_{InstitutoNacionaldePesquisasdaAmazônia,Coordenac¸ãodeBiodiversidade,Manaus,AM,Brazil}

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

a

r

t

i

c

l

e

i

n

f

o

Received7June2016 Accepted29July2016 Availableonline10August2016 AssociateEditor:AdrianaMarvaldi Keywords: CentralAmazonia Flowerchafer Myrmecophily Rhinocerosbeetle

a

b

s

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Wereportforthefirsttimetheoccurrenceoftwospeciesofscarabbeetles,PhileuruscarinatusdeclivisPrell, 1914(Scarabaeidae:Dynastinae)andCyclidiuselongatus(Olivier,1789)(Cetoniinae:Cremastocheilini) insidenestsofAztecacf.chartifexForel,1896,aneotropicalarborealantspecies.Thisreportindicatesthat thesetwobeetlespeciesareassociated,atleastasinquilines,tothisantspecies,althoughthenatureof thisrelationshipremainsunclear.

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

Nestbuildingsocialinsectscreatesahabitatthatcontainsawide rangeofresources.Itmayserveasanalimentarysource,sincetheir inhabitantscanbepreyeduponoreventhenestitselfcanbeeaten. Itcanalsoserveasshelter,functioningasaphysicaldefenseagainst theweatherand predators.Forthis reason,thenestsbecomea resourcethatcanbeexploitedbyotheranimals(Hölldoblerand Wilson,1990).In ordertopreventfrominvaders,theantshave severaldefensemechanismstoprotectthenest,suchasa com-plexchemicalrecognitionsystemamongstmembersofthesame colonyandavarietyofchemicalalarmsignals(VanderMeerand Morel,1998).Nevertheless,severalanimalsdenominated myrme-cophilesliveinsideorclosetoantnests(Rettenmeyeretal.,2010), manyofwhichexploitsthechemicalrecognitionsystemoftheants (Lenoiretal.,2011).Thecomplexityoftheinteractionsbetween myrmecophilesandants,plusthelackofgeneralknowledgeabout thenatureofmostofthemmakesitdifficulttocategorizethem (Mynhardt,2013).

AntsfromAztecaForel,1878genusareneotropical,arboreal, characterizedbytheirbigcartonnests(Longino,2007).Azteca char-tifexForel,1896isaterritoriallydominantant(Dejeanetal.,2009), thataggressively defendsits territorybothintraspecifically and interspecifically(Dejeanetal.,2007;BlüthgenandStork,2007).

∗ Correspondingauthor.

E-mail:jraoliveira.bio@gmail.com(J.R.Alves-Oliveira).

Theyconstructlargenests,onheightsthatcanreachupto2m fromtheground level andare frequent inwetforests (Longino, 2007).

Amongstthemyrmecophilesinsects,Coleopteraisoneofthe mostdiverse,withatleast33familiesreportedlyinteractingwith ants(Parker,2016),althoughthereisnobehavioraldataforatleast 15ofthem(Mynhardt,2013).Thebeetleshavedifferentstrategies tosurpassthedefensemechanismsofitshosts,suchas chemi-calmimicrybyproductionoracquisitionofspecifichydrocarbons fromtheirhosts(VanderMeerandWojcik,1982),morphological mimicry(AkreandRettenmeywer,1967),secretionofdefensiveor attractivecompounds(Geiselhardtetal.,2007)ormorphological defenses,suchasreducedappendages(RatcliffeandMicó,2001).

SpecimenswerecollectedinSeptemberandOctober2014,in ReservaFlorestalAdolfoDucke,northofManauscity,Amazonas, Brazil.Thisisa“Terra-Firme”wetforest,withanaverageannual temperatureof 26◦C. The annualrainfallvaries from1.750mm to2.500mm(Marques-Filhoetal.,1981).FourAztecacf.chartifex nestswithsizesrangingfrom1mto1.5mwerecollectedin differ-enttrees.Nestswerelocatedataheightof1–2mfromtheground level.

Nests weresectionedbyitslower third(Figs. 1–3), toallow thecolonyrecovery.Theremovedportionwasthenplacedinside aplasticbagandtakentoafreezer,tokilltheinsects. Thenthe nestpiecewasexaminedmanuallyatthelaboratory“Laboratório deFaunadeSolo–InstitutoNacionaldePesquisadaAmazônia”, http://dx.doi.org/10.1016/j.rbe.2016.07.003

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

360 J.R.Alves-Oliveiraetal./RevistaBrasileiradeEntomologia60(2016)359–361

1

4

5

6

7

2

3

Figs.1–7.Aztecacf.chartifexnestanditsassociatedmyrmecophilebeetles.1,Nest,sectionedatitsthirdlowerpart,whichwassearchedformyrmecophiles.2,Upcloseview ofuppernestpart,withnosightoflargegalleries.3,Largegalleryonthecollectednestpiece,inwhichonebeetlewasfound.4,Phileuruscarinatusdeclivis,dorsalview.5, Phileuruscarinatusdeclivis,ventralview.6,Cyclidiuselongatus,dorsalview.7,Cyclidiuselongatus,ventralview.

withastereomicroscopeandfeatherweighttweezerstofindthe myrmecophiles.

Collected specimens were deposited in the following col-lections: INPA (Colec¸ão Entomológica do Instituto Nacional de PesquisasnaAmazônia,Manaus,Amazonas–MárciodeOliveira) andCERPE(Colec¸ãoEntomológicadaUniversidadeFederalRural dePernambuco,Recife,Pernambuco–PaschoalC.Grossi).

Twelve specimens of the Scarabaeidae Phileurus carinatus declivisPrell, 1914(Dynastinae,Phileurini)(Figs. 4and 5)were found, beingpresentin allsampled nests,withthequantityof specimensfoundvaryingbetweentwo andfourspecimensin a singlenest.Therewasnoexternalopeningsinthenests,which indi-catestheantsreconstructsthedamagedstructureafterthebeetle entrance,oreventhatthelarvaeofthisspeciesdevelopsinsidethe nest.Thegalleriesbuiltbythebeetlesaredeep,withanextension superiorto40cm, allowingustoinferthatthebeetlesarewell adaptedtothecontactwiththeants.

Specimensexamined. 9♂e3♀ – BRASIL, Amazonas,Manaus, ReservaDucke,20.ix.2014,trilhadoigarapédoAcará,interiorde ninhode Aztecacf.chartifex, (A.M.Silva-Neto,D.M.M.Mendes, D.Campos&J.R.Oliveiraleg.)(2♂e1♀);idem,trilhaaoladodos alojamentosdabasesede,21.ix.2014,(3♂e1♀); idem,trilhade saídadareserva,21.ix.2014,(2♂);idem,trilhadoigarapédoAcará, 05.x.2014,(2♂e1♀)(CERPE,INPA).

OnlyonemalespecimenoftheCetoniinaeCyclidiuselongatus (Olivier,1789)(Cetoniinae,Chremastocheilini)(Figs.6and7)was foundinsideanestofA.cf.chartifex,insimilarconditionstothe previousspecies.

Specimenexamined.1♂–BRASIL,Amazonas,Manaus,Reserva Ducke,20.ix.2014,trilhadoigarapédoAcará,interiordeninhode Aztecacf.chartifex,(A.M.Silva-Neto,D.M.M.Mendes,D.Campos& J.R.Oliveiraleg.)(CERPE).

Therearefewpublications aboutthelifestories ofPhileurus species,althoughitisknownthatbothlarvaeandadultscanbe foundinsidedeadtreetrunks,ofwhichtheypossiblyfeedatlarvae stage(Ritcher,1966;Morelli,1991;Lamant-Voirin,1995;Ratcliffe andMorón,1997;Dechambre,1998);orpreyonotherlarvaeat adultstage(RatcliffeandMorón,1997;McCleve,2007).Thistaxon wasrecentlyreviewedbyGrossiandSaltin(2014)andhaditsstatus confirmed,apparentlybelongingtoAmazonpopulations,with dis-tributionextendingtoareasthatpreviouslyhadconnectionwith theAmazonforest.Untilnowmyrmecophilywasonlyregisteredfor thePhileurusgenusbyDeloya(1988),tothespeciesPhileurusvagus (Olivier,1789)inMexico,asaninquilineofAttamexicana(Smith, 1858),agroupofantsfarlessaggressivethanthosebelongingto thegenusAzteca.

For Cetoniinae there are 52 records of new world species associatedin somewaywithants,but this isthefirst recordof

J.R.Alves-Oliveiraetal./RevistaBrasileiradeEntomologia60(2016)359–361 361

myrmecophilyforthegenusCyclidius,aswellasthefirstrecordofa CetoniinaemyrmecophileforAztecaants(Pukeretal.,2015). Cyclid-iusisthelargestneotropicalgenusinthetriberegardingtobody size,andhassixspeciestodate.Althoughitshabitsareunknown, morphologicalevidencespointedthattheywereassociatedwith social insects,due tothereductionof itsappendages,an adap-tationshownbyotherscarabaeoidsthatlivesintermiteandant nests(RatcliffeandMicó,2001).Itstribe,Cremastocheilini,have thehighestnumberofspeciesassociatedwithants,with31species distributedintwogenerainneotropicregion(Pukeretal.,2015). Cremastocheillusspecies,themoststudiedgenusofmyrmecophile inthistribepreyonantlarvaewhilearetreatedindifferentlyby theants(CazierandMortenson,1965).Morphologicaladaptations, suchasthickenedintegument,retractileantennaeandconcealed mouthparts protects them from antattacks, as well as defen-sivesecretionsfromtheanalopeningwhendisturbed(Alpertand Ritcher,1975).

SomeColeopteraareabletocapturehydrocarbonsfromthe cuti-cleoftheiranthosts,beingacceptedbythecolony(e.g.Vander Meerand Wojcik,1982; Talarico etal.,2009).BothP.carinatus declivisandC.elongatushavebristlesthat eitherareorfunction astrichomes,whichcanpossiblyexudatecompoundsattractiveto ants.Somethingsimilarcouldbeoccurringwiththosetwospecies beingreportedasAztecamyrmecophiles.

Comprehensivesamplings,includingAztecanestsfrom differ-entspeciesandlocalitiesareneededtobedone,toverifyifmore speciesfromthegeneraPhileurusandCyclidiusareAzteca myrme-cophiles.In addition,we needtoknowtowhich extentthelife cyclesofthosebeetlesareassociatedwiththeants.Observations ofmyrmecophilesaredifficult.Formostcasesitisonlypossible toinferabouttheirbehavior throughtheirmorphological char-acteristics.Howthosespeciesavoidantsdefensesystemremains unanswered.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

J.R.A.O, D.M.M.M, D.C, A.M.S.N and J.W.M thanks Instituto NacionaldePesquisasdaAmazônia(INPA),forcontinuousresearch support.

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