ww w . r b e n t o m o l o g i a . c o m
REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolutionSystematics,
Morphology
and
Biogeography
Sexual
behavior
of
the
digger
wasp
Sphex
ingens
Smith
(Hymenoptera,
Sphecidae)
Carlos
Alberto
S.
Souza
a,∗,
Fábio
Prezoto
a,
Mauro
Sérgio
C.S.
Lima
b,
Jonas
Pederassi
caLaboratóriodeEcologiaComportamentaleBioacústica,UniversidadeFederaldeJuizdeFora(UFJF),JuizdeFora,MG,Brazil bUniversidadeFederaldoPiauí(UFPI),Floriano,PI,Brazil
cMuseuNacional,DepartamentodeVertebrados,UniversidadeFederaldoRiodeJaneiro(UFRJ),RiodeJaneiro,RJ,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received17September2014 Accepted11February2015 Availableonline9April2015 AssociateEditor:KevinWilliams Keywords: Copulation Coercivecopulation Breedingseason PraiadoAventureiro Solitarywasp
a
b
s
t
r
a
c
t
Aspecies’matingsystemdependsonitsspatialdistributionandtemporalavailabilityofmating opportu-nities,aswellasontheresourcesthatcreatetheseopportunities.Inaddition,formanyspecies,courtship isdrivenbyspecificbehaviorsthatprecedeandfollowcopulation.AlthoughSphexingensisa taxono-micallywellknownspeciesofdiggerwasp,itsecologyandbehaviorremainpoorlyknown.Hence,we analyzedpatternsandtrendsofsexualbehavior,inordertounderstandwhethercourtshipcanpersist inapolygamousmatingsystem.WemonitoredbyvideowasppopulationsinIlhaGrande,southeastern Brazil.Basedontheobservedbehaviors,wecalculatedstochasticprobabilitieswithaMarkovchainto inferonbehavioraltrends.Werecordedfourbehavioralphasesbasedon19,196behavioralactsobserved in224copulationattempts.Therewerenosignificantdifferencesincommonbehavioralactsbetween malesandfemales.Thecopulationpatterns,conflicts,andtrendsobservedinS.ingensclearlyshowthe influenceofsexualselectioninitspromiscuousmatingsystem.
©2015SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Allrightsreserved.
Introduction
Inseveralanimalspecies,matingsystemsareaffectedbyfood availabilityanddistribution,breedingsites,andpotentialpartners. Thecourtshipandcopulationphasesareobservedinmostmating events.Currently,there isconsensusontheconflictsofinterest betweensexesduringmating,andsexualselectionisanimportant mechanisminthechoiceofanidealpartner.
Amonghymenopterans,thespheciformcomplex(Ampulicidae, Crabronidae,andSphecidaesensu Melo,1999)comprises wasps thatareusuallysolitaryandhaveabroadbehavioral repertoire, especiallyintermsofreproductiveandnestingbehaviors(Evans andO’Neill,1978;Amarante,1999;Melo,2000;AlcockandKemp, 2005).Males increasetheirreproductivesuccessthrough adap-tivestrategiesorspecialization(Evans,1966;Alcock,1975;Kroiss etal.,2010),whereasfemalesincreasetheirreproductivesuccess throughmultiplemating(Melo,2000)orbychangingandsharing nestsafterthechoiceofapartnerwithbetterattributesorabilities. ThediggerwaspSphexingens Smith1856isa largesphecid, whichisusuallyblackandwhosegasterandlegsvaryfrompartially
∗ Correspondingauthor.
E-mail:seteorus@yahoo.com.br(C.A.S.Souza).
tocompletelyred(BohartandMenke,1976).Ithasbeenrecorded intheBrazilianstatesofBahia,EspíritoSanto,RiodeJaneiro,and SãoPaulo(Amarante,2002).
TheecologyandthebehaviorofS.ingensinBrazilwerestudied byPiliackasetal.(2007)andBuys(2009),respectively.Although thesestudiescompriseshort-termpreliminaryassessmentsand casualobservations,theyarestillconsideredpioneeringinBrazil, asfewscientistshavetriedtounderstandthenaturalhistoryofS. ingens.
Thegreatestchallengesofadetailedstudyontheecologyand behaviorofa wildpopulationofS.ingens aretheseasonalityof its breeding and its restricted distribution. However, the poor information available ontheecology and behavior of S.ingens, inparticularintermsofitssexualbehaviordeservesmore atten-tion,forinstance,onthetypeofmating,phasesandactsofmating repertoire,sexualbehaviortrends,influenceofthecourtshipinthe processofmateselectionandselectioncriteriaoffemales.
PreliminaryobservationsindicatethattheS.ingensmating sys-temispolygamous,andtheselectionofpartnersdoesnotoccur throughthecourtshipbehavior.For thisreason,weasked:how extensivelydoescourtshipbehaviorcoexistinapolygamous mat-ing system? Hence,the present study aimedat describing and analyzingthematingpatternsand trendsofthediggerwaspS. ingens,aimingatadvancingtheknowledgeofitsnestingdynamics. http://dx.doi.org/10.1016/j.rbe.2015.03.005
Materialsandmethods
Studyareaandsamplingdesign.IlhaGrande,a coastalisland, islocatedinthemunicipalityofAngradosReis,stateofRio de Janeiro,southeasternBrazil.Itisafragmentofthecoastalmassif witharuggedrelief,andhasapproximately19,300ha.Its predom-inantvegetationtypeismontaneandsubmontaneforest(Veloso etal.,1991).ThePraiadoSulStateBiologicalReserve(RBEPS) cov-ers18.6%(3.600ha:23◦10S–44◦17W)ofIlhaGrande’sarea,and harborsinnearlyallitsareaacontinuouscomplexofAtlantic For-est,whichcomprisesforestenvironments(sensustricto),restinga forests,mangroves,lagoons,shrubbyrestingas,rockyshores,and thebeaches Meros,Aventureiro, Demo,Sul, and Leste (FEEMA, 2008).
Wedelimitedtransectsabovethehightidelineandinforedune areasonAventureiroBeachtofindnestingsites.Whenwefound anestingsitewedelimitedthearea.Ineachnestingsite,we cap-turedmalesandfemales,markedtheirmesoscutumwithcolored non-toxicpaint(Martins,1993),andreleasedthemforindividual identificationandbehavioralanalysis.
We daily monitored in copulo pairs formed randomly with exchangeofindividuals,usingadigitalcamcorderanda chronome-ter.Thesamplingefforttotaled131hofobservation,comprisingthe firstfortnightofJanuary2010andthefirstandsecondfortnights ofJanuary2011.However,only50hwereselectedforanalysis,i.e., 45hofobservationincludingallrecordedcopulationsplus5hof observationusedtointerpretthematingbehaviorofthespecies.
Atfirst,inordertointerpretthebehaviorsweusedthead libi-tum method(Altmann, 1974), which is based onthebehaviors thatprecede, trigger,and endcopulation attempts,whereas for quantitativeobservationsweusedthesequencesamplingmethod (Altmann,1974).Theseproceduresallowedtheconstructionofa flowchartwiththeobservedbehaviors,inordertosupportthe analysisand theconstructionofanotherflow chartonthe con-ditional probabilitiesof occurrence and formation of stochastic processes(GottmanandRoy,1990).
All procedures of the present study complied with the guidelines of the permit for scientific research #002/2011 issued by the Directorate of Biodiversity and Protected Areas (INEA-RJ). The captured specimens were deposited as vouch-ers in the Natural History Collection of the Federal University of Piauí (CHNUFPI: Hymenoptera Collection), campus Amil-car Ferreira Sobral: CHNUFPI(HYM)0002, CHNUFPI(HYM)0003, CHNUFPI(HYM)0004,andCHNUFPI(HYM)0005.
Statisticalanalysis
Wetransformedtheabsolutefrequenciesofthebehavioralacts thatcomposethebehavioralstatesintorelativefrequencies.We submittedthe frequency of behavioral acts(state) common to malesandfemalestoachi-squaredtestandlogarithmizedthem toreducethevariation of frequencieswhenever necessary.We modeledtherelativefrequenciesofbehavioralstateswithaPoisson distributionandaMarkovchain,inordertoestimateconditional probabilitiesand formationof stochasticprocesses. We ranthe analysisusinganadd-infor MicrosoftExcel® developed bythe OperationResearchGroupoftheUniversityofTexas.Wesubmitted thecomparisonbetweenthePoissondistributionandtheMarkov chaintoaKolmogorov–Smirnovtest(p<0.01).Allstatistical anal-ysesweremadeusingfreesoftware.
Results
Weanalyzed224copulationattemptsin137randomlyformed pairs with interchange of males and females. The behavioral
0.0 1.0 0.1 F requency (Log) Behavioral categories Male Female
Pre-copulation Copulation Post-copulation
WIFA CONN SUCC UNSU PERM DISP
ANCO 10.0 100.0
Fig.1.Comparativefluctuationbetweenthelogarithmizedandnon-significant fre-quency(x2=16.622,df=n−1,p<0.01)ofthecommonbehavioralactsofSphex
ingensSmith1856(Hymenoptera,Sphecidae).Thecommonbehavioralactswere: antennation(ANCO),wingfanning(WIFA),connubium/strictcopulation(CONN), genital clasping/successful copulation(SUCC), nogenital clasping/unsuccessful copulation(UNSU),permanenceofmalesinthenestingarena(PERM),and disper-sion/malesleavethenestingarena(DISP).
repertoire was divided in four phases: identification, pre-copulation,copulation,and post-copulation,based ona total of 19,196behavioralactsdistributedin24sexualbehaviors(Table1). Femalematingbehaviorwascomposedofnineexclusive behav-iors(2319 behavioralacts, 12.0%),whereasmalesshowedeight exclusivebehaviors(940behavioralacts,4.8%).Sevenbehaviors werecommontobothsexes(15,937behavioralacts,83.0%),but there was no difference between sexes (x2=16.622, df=n−1, p<0.01)(Fig.1).Themostfrequentmatingphasesinbothsexes werepre-copulationandcopulation,andbehavioralactsrelatedto communicationweresignificantandrecurrentinthesephases. Descriptionofthesexualbehaviorbasedontheobservedbehavior
The identification phase consisted of visual recognition and male assault against females (n=155), which were engaged in activitiesintheirnestsorwereseizedwhileflyingoverthe nes-tingsite.Allapproachesrecordedwereaggressive,precedingthe attemptofimmobilization,corroboratingtheexistenceofcoercive copulation.Thesuccessin immobilizationoffemaleswas80.0% (n=124)amongallapproachattempts(Fig.2).In18.7%ofthecases themalescouldnotimmobilizethefemalesorwererejectedbefore anyattempt,asthefemaleswerealwaysaggressive.
The beginning of pre-copulation is characterized by males mountingfemales,followedbyintensivecommunication, culmi-natingintheextrusionoftheaedeagusbeforeitsintromissioninthe female’sgenitalopening.Insomecasesmalesrubbedtheaedeagus laterallyonthefemales’gasterbeforetheintromission,whereas femaleshinderedthecopulationbycurvingtheirgaster.
In the copulation phase, receptive females positioned their gasterparalleltothesubstrateforaedeagusintromission. Contrac-tionandbendingmovementsdirectedthegenitalclasptoassure reproductivesuccess.Femalesshowedself-cleaningbehavior dur-inggenitalclasping(Fig.3),andthenwerestimulatedtoadopta disengagementbehavior.
Inpost-copulation,malescleanedtheirgenitalsaftertheywere disengaged.Weobservedbothdispersalandpermanencebehavior innestingarenasafterdisengagementinthepost-copulationphase inmalesandfemales.Mostfemalesremainedinthenestingarena (84.8%)andonlyafewdispersed(15.1%),whereasmalesshowed theoppositebehaviorwithhigherdispersal(73.2%)than perma-nence(26.7%)innestingarenas.Weobservedamongmalesthat remainedinthenestingarenaaftereffectivecopulationadecrease inmotoractivitiesreflectedinlowantennamobilityandwing fan-ning,characterizingarecoveryperiodof124.10±39.30sbeforea newcopulationattempt.
Table1
SexualbehaviorrecordedformaleandfemalediggerwaspsSphexingens(Smith1856)(Hymenoptera,Sphecidae).
Behavioralacts Abbreviation Description
Recognitionandassault REAS Malesrecognizevisuallyfemalesandmovetowardsthem.
Immobilization IMOB Malesassaultfemalesdirectlyforacopulationattempt.Malesusuallyimmobilize
femalesusingthefirstpairofappendages.
Aggressivedisplay1 DIS1 Behavioralactcharacterizedbypartiallyopenedmandiblesandverticalinclinationof thebodyonthelastappendages.
Confrontation CONF BehavioralactassociatedwithDIS1,characterizedbyaggressivenessand
advancementoffemalesagainstmales.Itisusuallytriggeredbylateralorfrontal immobilizationattempts.
Rejection REJE Behavioralactcharacterizedbytherefusalofthepartnerduringlateralorfrontal
immobilizationattempts.Thisactwasalsoobservedwhenamaleunderwentmany unsuccessfulcopulationattempts.
Mount MOUN Recurrentbehavioralactafterasuccessfulimmobilization.Malesremainontopof
femalestobeginthepre-copulationsequence.
Extrusion EXTR Extrusionoftheaedeagusfortheintromissioninthegenitalsoffemales.
Rubbing RUBB Tolaterallyrubtheaedeagusonthefemale’sgasterbeforegenitalintromission.
Curvatureofthegaster CUGA Femalesbendtheirgasteringeneraltopreventtheaccessofmalestothefemale’s genitalopening.
Antennation ANCO Antennacommunication.
Wingfanning WIFA Wingfanningcommunication.
Aedeagusintromission AEIN Aedeagusintromissioninthefemale’sgenitalopening.
Aggressivedisplay2 DIS2 Behavioralactcharacterizedbypartiallyopenedmandiblesandintenseantenna
vibration.
Swayingbodymovements SWAY Unsociablebehavioralactcharacterizedbyswayingbodymovementsintheattempt todislodgethemale.
Drumming DRUM Consistsinknockingseveraltimesthefirstpairofappendagesagainstthesubstrate.
Connubium CONN Sexualactivitymarkedbycopulationdynamicscomposedofgastercontractionand
bendingmovements.
Unsuccessfulcopulation UNSU Nogenitalclaspingoccursafterconnubium,characterizinganunsuccessfulcopulation attempt.
Permanenceofmount PEMO Permanenceofmalesinthemountpositiontobeginanewcopulationattempt.
Genitalcleaning GECL Malescleantheirgenitalsusingthethirdpairofappendages.
Genitalclasping SUCC Genitalclaspingcharacterizingthecopulationsuccessofthemale.Malesclasped
duringcopulationbendtheirbodiesverticallyonthelastpairofappendages,andmay twisttheirgasterlaterallyormaintainthemselvesindorsaldecubitus.
Genitaldisengagement DISE Behavioralactsofreleaseaftergenitalclasping.Femalesshovemalesusingthethird pairofambulatorialappendages,dragthemontheground,ormakeflightattempts.
Self-cleaning SECL Usuallyperformedbythefemaleduringthegenitalclasping,comprisingthecleaning
ofantennaeandfirstambulatorialpairofappendages.
Permanence PERM Malesremaininthenestingarena.
Dispersion DISP Malesflyawayfromthenestingarena.
Sexualbehavior:behavioraltrends
Theconditionalprobabilitiesoftransitiondifferedsignificantly
betweenthe Poisson distribution model and theMarkov chain
(Dmax=0.240,df=n−1,p<0.01:Kolmogorov–Smirnov),sothatthe
vectorsoflimitingprobabilitieswerebuiltaccordingtotheMarkov
chain.ThepredictionsderivedfromtheMarkovchaincorroborated
theobservationthatthebehaviorsexhibitedduringmating
dif-feredbetweenmalesandfemalesintermsofobservedtransition
ofbehavior.However,sexualbehaviorsrecordedinloco(observed
behavior)infemales,suchaseyeandantennacleaningwiththeir
firstpairofambulatoriallegsduringgenitalclasp,draggingonthe
ground,andtheattemptofflightwithclaspedmales,were
consid-eredirrelevantand,hence,excludedfromtheanalysis.
TheresultsexpressedbythediagramoftheMarkovchain
high-lightedthatthebehavioraltransitionsincommunicationincluding
theantennation(7.9%)andwingfanning(21.4%)behaviorsduring
pre-copulationandcopulationhaveweakinfluenceonthemating
behaviorofS.ingens.
Thetransitionoftheagonisticbehaviorsdisplayedbyfemales
during the identification (aggressive display 1: 10.3%,
con-frontation: 33.3%, and rejection: 33.0%), and copulation phases
(aggressive display 2: 24.5%, swaying body movements: 31.1%,
drumming:64.3%,andrejection:45.9%)indicateastrongtrendto
Fig.2. Sequenceofthephaseofidentificationandpre-copulation:(A)immobilizationattemptsbymaleswhilethefemaleissupplyingitsnestwithprey,(B)efficient immobilizationofthefemaleandmountinthenestingarea,(C)aedeagusextrusion.Femaleshowsamixedbehaviorofreceptiveness(lastpairsofappendagesup)and aggressiveness(partiallyopenedmandibles).
Fig.3. Sequenceofthecopulationphase:(A)beginningofaedeagusintromission.Copulationduringnestdigging–femalecarryingaclodofsand.(B)Connubium,gaster’s contractionmovements.(C)Connubium,gaster’sbendingmovements.(D)Successfulcopulation–claspingofclaspingorgans.Malewiththebodyverticallyinclinedand femaleself-cleaning.
Photoby:JonasPederassi.
selectmales.Anothertrendpointedoutbytheanalysiswasthe
attemptof malestoremainmounted onfemales (47.9%) when
copulationattemptswereunsuccessful(Fig.4).
Discussion
InthediggerwaspS.ingens,eventhoughmalesand females showedcommonbehavioralactsduringmating,differencesinthe frequency and diversity of these acts indicate different energy investmentbetweensexes.Historically,thedescriptionofmating eventsinhymenopteransischaracterizedbydifferenteffortsand methods,whichhindercomparisons.
However, although a behavioral similarity among species betweencopulation and mating phaseshas beendescribed for some hymenopteran species, such as Mormoniella vitripennis Walker (Barrass, 1960, 1961), Campoletis sonorensis Cameron (Vinson,1976)BrachymeriaintermediaNees(LeonardandRingo, 1978),ApantelesglomeratusLinnaeus(Tagawaetal.,1985), Asco-gasterreticulatusWatanabe(Kainoh,1986),EdithamagnificaPerty (Martins, 1993), NasoniavitripennisWalker(AssemandWerren, 1994),andRubricanasutaChrist(PimentaandMartins,1999),the detailsofthebehaviorofS.ingens,aswellasthevariationin behav-ioralacts,theirsequence,time,andfrequencydifferfromthoseof otherwaspspecies.
TheconfrontationandrejectionbehaviorsrecordedinS.ingens werecommonandpresentinallmatingphasesbetweenmalesand females.AccordingtoCorderoandEberhard(2003)pre-copulatory confrontationsindicatetheexistenceofconflictsbetweensexes andsexualselection,whichfavorsmanipulativemalesincoercive copulations.Theresistanceoffemalestotheantagonisticbehavior ofmalesmayselectindividualsaccordingtotheircapacityof indi-vidualmanipulation(signalingvigorandfitness)inclaspingthe femaleasittriestogetridofthemale(AllenandSimmons,1996).
InS.ingenscoercivecopulationisanalternativestrategyofmales inresponsetotheconstantaggressivenessoffemales,asthelatter usethiscriteriontoselectpartners.
InS.ingensfemales,thelargernumberofcopulationattemptsin relationtothephaseofnestconstruction(diggingthetunnelor sup-plychamber)reflectsahighenergyinvestment,whichmakesthem moreevidentintheirrespectivearenasandnests,andjustifiesthe trendofremaininginthenestafteracopulationattempt, regard-lessoftheresult.Evansetal.(1976),Jangetal.(1996),andMelo (2000)consensuallyaffirmedthatmosttimeandenergyoffemales ofthefamilySphecidaeisinvestedinmaternalcareintheformof constructionandprovisionofnestsduringtheirreproductivelife.
MaleS.ingenswereabletocopulaterepeatedlywithfemales inthenestingsiteatanyphaseofnestbuilding.Thisresultsinan intensivedailycopulationactivitythatinvolvesarelevant invest-mentoftimeandinpartcorroboratesthestudiesbyGenaro(1998) onthespeciesSphexjamaicencisDrury.Inseveralinsectspeciesthe occurrenceofmultiplecopulationssuggeststheexistenceofcryptic femalechoice(Ebehard,1996),spermcompetition(Parker,1970), reductioninthefemale’sspermathecaorthatoneorfew copula-tionsarenotenoughforthefemalestoobtainenoughspermfora maximumproductionofoffspring(Ridley,1990),andeven physi-ologicaldeficienciesinthereproductivesystemofmales(Martins etal.,2004).
Severalstudiesreportedthatthecourtshipandcopulationof manyhymenopteransconsistofmovementsofwings,legs, anten-nae, and mouthparts of males (Barrass, 1960, 1961; Mathews, 1975;Vinson,1976;LeonardandRingo,1978;Tagawaetal.,1985; Kainoh,1986;Martins,1993;AssemandWerren,1994;Pimenta and Martins, 1999). The sequence of these movements varies accordinglybetweenspeciesandisrepeatedbyareceptivefemale (Mayr, 1973;Assem, 1986).Althoughthesestudies suggestthe existenceofvisualstimulithatprecedemount,wedidnotobserve
1st phase: Identification REAS IMOB DYS1 CONF REJE MOUN EXTR RUBB CUGA ANCO DYS2 SWAY DRUM AIEN CONN UNSU SECL DISE PERM Symbols or <1% 1 ~ 5% 5 ~ 10% >10% <1% 1 ~ 10% 10 ~ 20% 20 ~ 30% 30 ~ 40% >40% DISP SUCC GECL PEMO WIFA 2nd phase: Pre-copulation 3rd phase: Copulation 4th phase: Pos-copulation
Fig.4.DiagramrepresentingtheMarkovchainforthesexualbehaviorrepertoireofthewaspSphexingensSmith1856(Hymenoptera,Sphecidae).Symbolsrepresentsexes. Symbolsizeandlinethicknessrepresentthefrequencyofoccurrenceofeachbehavior.Arrowheadsrepresentthetransitionfromonebehaviortothenextandarrowthickness representsthefrequencyclass.
anypre-copulationgesturalbehaviorinS.ingens.Thelackofthese behaviorsinS.ingensresultsfromtheinfluenceofthepromiscuous matingsystemandfromthewayfemalesselecttheirpartners.
Presumably,theenergyspentinintersexualcommunicationin S.ingensdoesnotsupportthatthisbehaviorinfluencescourtship, butwouldrepresenttheexchangeofstimuliusedinconspecific recognition,assuggestedbyMayr(1973),orgeneralexcitement signals.However,morespecifictestsontheperformanceof anten-nationanditsinfluenceonthesuccessfulandunsuccessfulmating couldclarifythefunctionofthisbehavior.Furthermore,itis possi-blethatinS.ingenspheromonesaretheonlyexpressionsoffemale receptivity,asweobservedmalestryingtocopulatewithpreyleft byfemalesattheentranceofnests.Thisbehaviorwasalsoobserved
instudieswithotherspeciescarriedoutinthelaboratory(Barrass, 1960,1961;Mathews,1975;Vinson,1976).
OtheraspectsofsexualbehaviorofS.ingens,thatwouldexpand theunderstandingofitsreproductivebehavior,refertothe adjust-ments,disputesandstrategiesadoptedbymalestoincreasetheir reproductive success. Apparently, preliminarytests on the col-lectedspecimenssuggestthattherearesizedifferencesbetween thetwosexes,aswellbetweenmaleswithterritorialandpatrol behavior.Therefore,differencesinsizeandbehaviorcould influ-enceindividualfitness,withconsequencestotheresultsofmating disputes,andinthefrequencyofthereproductivesuccess.
Ouranalysiscorroboratesthatthematingsystemandfemale aggressivenessresultinlowsexualselectivityandadecreasein
courtshipeffortbymales,and,hence,favor themaintenance of coercivecopulation.Theyalsosuggestthattheabilityofmalesto manipulatethefemalesduringcopulationisthemainrequirement forasuccessfulcopulation.Hence,thedecreaseincourtshipeffort bymalesisanalternativestrategytoenergy-demandingstrategies basedonelaboratedcourtshipdisplays,consideringthewaythat copulationsoccur,numberof copulationattempts observedand constantconfrontationwithrivalmalesinthepresentstudy.The escalationoffemaleaggressivenessisanantagonisticsexual selec-tioncriteriondifferentfromclassicformsfoundintheliterature intermsofassessmentofattributesorcourtshiprites.Inaddition, althoughcoercivecopulationisnotanexclusivestrategyamong insects,itisrareinsolitarywasps,inparticularsphecids.
Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgments
WethanktheINEA-RJteamforthehelpinthepresentstudy. RogérioP.Martins(UFMG)supportedourstudyandprovidedus withimportantliterature.SérvioT.P.Amaranteidentifiedthefirst specimenscaptured.Mr.Waldomiro(camping7)atAventureiro Beachwasverykindtousandprovideduswithroomtodevelopthe presentstudy.Wealsothankthereviewersfortheirsuggestions.
References
Alcock, J., 1975. Territorial behavior by males of Philantus multimaculatus (Hymenoptera:Sphecidae)withareviewofterritorialityinmaleSphecids. Anim.Behav.23,889–895.
Alcock,J.,Kemp,D.J.,2005.Thescramblecompetitionmatingsystemofthesphecid waspPalmodespraestans(Kohl).J.Nat.Hist.39,2809–2814.
Allen,G.F.,Simmons,L.W.,1996.Coercivemating,fluctuatingasymmetryandmale matingsuccessinthedungflySepsiscynipsea.Anim.Behav.52,737–741.
Altmann,J.,1974.Observationalstudyofbehavior:samplingmethods.Behaviour 49,227–267.
Amarante,S.T.P.1999.Sphecidae,in:Brandão,C.R.F.,Cancello,E.M.(Eds.). Inver-tebrados Terrestres. Biodiversidade do Estado de São Paulo. Síntese do conhecimentoaofinaldoséculoXX,in:Joly,C.A.,Bicudo,C.E.M.(orgs.).FAPESP, SãoPaulo,5,pp.183–192.
Amarante,S.T.P.,2002.AsynonymiccatalogoftheNeotropicalCrabronidaeand Sphecidae(Hymenoptera:Apoidea).Arq.Zool.37,1–139.
Assem,J.vanden,1986.Matingbehaviorinparasitcwasps.In:Waage,J.,Greathead, D.(Eds.),Insectparasitoids.Academic,NewYork,pp.125–157.
Assem,J.vanden,Werren,J.H.,1994.Acomparisonofthecourtshipandmating behavioroftreespeciesofNasonia(Hymenoptera:Pteromalidae).J.InsectBehav. 7,53–66.
Barrass,R., 1960. Thecourtship behavior of Mormoniellavitripennis (Walker) (Hymenoptera:Pteromalidae).Behaviour15,185–209.
Barrass,R.,1961.AquantitativestudyofthebehaviorofthemaleMormoniella vitripennis(Walker)(Hymenoptera:Pteromalidae)–towardstwoconstant stim-ulussituations.Behaviour18,288–311.
Bohart,R.M.,Menke,A.S.,1976.SphecidWaspsoftheWorld.UniversityofCalifornia Press,Berkeley.
Buys,S.C.,2009.Sphecidae(Hymenoptera:Apoidea)ofRiodeJaneiroState (South-easternBrazil):inventoryofspeciesandnotesonbiologyanddistribution.Arq. Mus.Nac.RiodeJaneiro67,275–282.
Cordero,C.,Eberhard,W.G.,2003.Femalechoiceofsexuallyantagonisticmale adap-tations:acriticalreviewofsomecurrentresearch.J.Evol.Biol.16,1–6.
Ebehard,W.G.,1996.FemaleControl:SexualSelectionbyCrypticFemaleChoice. PrincetonUniversityPress,Princeton.
Evans,H.E.,1966.TheComparativeEthologyandEvolutionoftheSandWasps. HarvardUniversityPress,Cambridge.
Evans,H.E.,Matthews,R.W.,Alcock,J.,Fritz,M.A.,1976.Notesonthenestsandprey oftwosubspeciesofCercerisrufimanaTaschenberg(Hymenoptera:Sphecidae: Cercerini).J.Kans.Entomol.Soc.49,126–132.
Evans,H.E.,O’Neill,K.M.,1978.Alternativematingstrategiesindiggerwasp Philan-thuszebratusCresson.Proc.Natl.Acad.Sci.U.S.A.75,1901–1903.
FEEMA,2008.Fundac¸ãoEstadualdeEngenhariaeMeioAmbiente,Availableat:
http://www.inea.rj.gov.br/(accessed14.03.15).
Genaro,J.A.,1998.ComportamientodeSphexjamaicensisdurantelanidificacióny notassobreS.mandibularesyS.cubensis(Hymenoptera:Sphecidae).Caribb.J. Sci.34,238–242.
Gottman, J.M., Roy, A.K., 1990. Sequential Analysis: A Guide for Behavioral Researchers.CambridgeUniversityPress,NewYork.
Jang,Y.,Wuellner,C.T.,Scott,C.S.,1996.Floatingandfidelityinnestvisitationby Crawfordapisluctuosa(Hymenoptera:Colletidae).J.InsectBehav.9,493–504.
Kainoh,Y.,1986.MatingbehaviorofAscogasterreticulatusWatanabe(Hymenoptera: Braconidae),anegg-larvalparasitoidofthesmallerteatortrixmoth,Adoxophyes sp(Lepidoptera:Tortricidae)I.Dielpatternsofemergenceandmating,andsome conditionsformating.Appl.Ent.Zool.21,1–7.
Kroiss,J.,Lechner,K.,Strohm,E.,2010.Maleterritorialityandmatingsystemin theEuropeanbeewolfPhilanthustriangulumF(Hymenoptera:Crabronidae): evidencefora“hotspot”lekpolygyny.J.Ethol.28,295–304.
Leonard,S.H.,Ringo,J.M.,1978.Analysisofmalecourtshippatternsandmating behaviorofBrachymeriaintermedia.Ann.Entomol.Soc.Amer.71,817–826.
Martins,G.F.,Serrão,J.E.,Furieri,K.S.,2004.NotesonthespermathecaofVespidae andSphecidae(Hymenoptera).Sociobiology45,119–127.
Martins,R.P.,1993.ThebiologyofEdithamagnifica(Perty,1834)(Hymenoptera Sphecidae).Trop.Zool.6,109–123.
Mathews,R.W.,1975.Courtshipinparasiticwasps.In:Price,P.W.(Ed.),Evolutionary StrategiesofParasiticInsectsandMites.PlenumPress,NewYork,pp.66–86.
Mayr,E.,1973.AnimalSpeciesandEvolution.HarvardUniversityPress,Cambridge.
Melo,G.A.R.,1999.Phylogeneticrelationshipsandclassificationofthemajor lin-eagesofApoidea(Hymenoptera),withemphasisonthecrabronidwaps.Sci. Pap.Nat.Hist.Mus.Univ.Kans.14,1–55.
Melo, G.A.R., 2000. Comportamento social em vespas da família Sphecidae (Hymenoptera,Apoidea).In:Martins,R.P.,Lewinsohn,T.M.,Barbeiros,M.S. (Eds.),EcologiaeComportamentodeInsetos.OecologiaBrasiliensis,vol.VIII. PPGE-UFRJ,RiodeJaneiro,pp.85–130.
Parker,G.A.,1970.Spermcompetitionanditsevolutionaryconsequencesinthe insects.Biol.Rev.45,525–567.
Pimenta,H.R.,Martins,R.P.,1999.Thenaturalhistoryoftheneotropicalsandwasp Rubricanasuta(Christ1791)(HymenopteraSphecidae)inBrazil.Trop.Zool.12, 273–288.
Piliackas,J.M.,Meira,F.V.,Suhogusoff,V.G.,Rossi,P.G.,Badio,A.A.,2007.Estudosobre acapacidadereprodutivadapopulac¸ãodeSphexingensSmith(Hymenoptera, Sphecidae) em período reprodutivono ParqueEstadual daIlha Anchieta, Ubatuba,SP,Brasil.Publicac¸õesAvulsasdoInstitutoPauBrasildeHistória Nat-ural10,73–80.
Ridley,M.,1990.Thecontrolandfrequencyofmatingininsects.Funct.Ecol.4,75–84.
Tagawa,J.,Asano,S.,Ohtsubo,T.,Kamomae,M.,Gotoh,T.,1985.Influenceofageon thematingbehaviourofthebraconidwaspApantelesglomeratusL.Appl.Ent. Zool.20,227–230.
Veloso,H.P.,RangelFilho,A.L.R.,Lima,J.C.A.,1991.Classificac¸ãodaVegetac¸ão Brasileira:AdaptadaaumSistemaUniversal.IBGE,DepartamentodeRecursos NaturaiseEstudosAmbientais,RiodeJaneiro.
Vinson,S.B.,1976.Hostselectionbyinsectparasitoids.Ann.Rev.Entomol.21, 109–133.
