Bait traps remain attractive to euglossine bees even after two weeks: a report from Brazilian Atlantic forest

REVISTA

BRASILEIRA

DE

Entomologia

Short

Communication

Bait

traps

remain

attractive

to

euglossine

bees

even

after

two

weeks:

a

report

from

Brazilian

Atlantic

forest

Judson

Albino

Coswosk

_,

_Elaine

_Della

_Giustina

_Soares

_,

_Luiz

_R.R.

_Faria

a_{UniversidadeFederaldoEspíritoSanto(UFES),CentroUniversitárioNortedoEspíritoSanto(CEUNES),DepartamentodeCiênciasAgráriaseBiológicas,SãoMateus,ES,Brazil} b_{UniversidadeFederaldaIntegracãoLatino-Americana(UNILA),InstitutoLatino-AmericanodeCiênciasdaVidaedaNatureza,FozdoIguac¸u,PR,Brazil}

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r

t

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c

l

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n

f

o

Received13July2018 Accepted3November2018 Availableonline16November2018 AssociateEditor:EduardoAlmeida Keywords: Euglossina Euglossini Orchidbee Survey Assessment

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Baittrapsareeffectiveandcommonlyusedmethodinthestudiesoforchidbees.Importantquestionsin thecontextofthismethod,includingthoserelatedtobaitdispersion,howlongbaitsremainattractive, thedistancefromwhichmalesaresupposedtobeattractedtoluresandsoon,arestillopensubjects.Data ontheattractivenessofbaittrapsthathaveremainedinthefieldduringtwoweeksinalargeAtlantic forestpreservearepresented.Fourmainresultsemergefromthedata:(i)theabundanceofspecimens collectedperdaydecreasedinalltheattractantsasthetrapswereleftonthefield;(ii)despitethis decrease,theabsolutenumberofindividualscollectedaftereightandfifteendaysisremarkably,mostly ineugenolandvanillinbaits;(iii)thevastmajorityofspecies,22of25,wasalreadycollectedonthefirst sampleday;(iv)aconsistentvariationintherelativeabundanceofindividualscollectedineachscent ascollectionsweremade.Weurgethatbaittrapsshouldnotbeleftinthefieldbeyondwhatisstrictly necessarysincethereisarealpossibilityofcollectingasignificantnumberofindividualsasthesetraps remainavailable.

©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Orchid bees (Hymenoptera, Apidae, Euglossina) have been regardedasaneffectivemodelforstudyingseveralecological ques-tions(e.g.NemésioandSilveira,2006).Oneofthemainreasons behindthispracticeisthepossibilityofattractingeuglossinemales tosyntheticcompoundsthatmimictheresourcestheygatherfrom naturalsources(Dodsonetal.,1969).Itseemscrystalclearthere isanoverallmethodologyfor collectingorchidbees,buta sim-pleanalysisofpaperspresentinglocalsurveysofeuglossinebees revealsthatthewayattractantsareusedisquitevariablefromone studytoanother,regarding,forinstance,thenumberofusedscents, theselectedscents,thedistancebaitsareplacedfromtheground andaparteachother,ifbaitsareofferedintrapsorhungfordirect capturebyinsectnetsandsoon(Nemésio,2012;Fariaetal.,2015). Bait trapping euglossine bees is itself a rather controversial issue.Activesampling(i.e.samplingeuglossinebeesthroughinsect nets)is regarded tocollect significantlymore bee species than passivesampling(throughbaittraps)andleadstosignificantly dif-ferentspeciescomposition(NemésioandVasconcelos,2014).On theotherhand,itisundeniablethatthislattermethodincreases percapitasamplingeffort,particularlywhenlargeareasormany sitesare surveyedsimultaneously(Mattozoetal., 2011)and/or

∗ Correspondingauthor.

E-mail:luiz.faria@unila.edu.br(L.R.Faria).

whenrobustsamplingdesignsarerequiredintermsofreplication (SydneyandGonc¸alves,2015).

Instudieswherebaittrapsareemployedforattractingmales,for instance,thesetrapsaresometimesofferedtobeesduringagiven periodofasingleday(e.g.Bezerraand Martins,2001;Ramalho etal., 2009), ortraps areleftin thefieldovernight(e.g.Botsch etal.,2017;Coswosketal.,2018)andevenlonger(e.g.3–4days;

Storck-Tononetal.,2009;KnollandPenatti,2012).Replenishing ofchemicalsonthebaitsisalsoacommonconcernineuglossine assessments(seee.g.SofiaandSuzuki,2004;NemésioandSilveira, 2006;Silveiraetal.,2011).Thispracticeisregardedtobeawayof tryingtoensurethatcompoundswithdifferentvolatilityprofiles couldbeevenlyavailabletomales(e.g.Uehara-PradoandGarófalo, 2006),sincealcohol-basedscentswoulddispersefasterthan oil-basedscents(seeNemésio,2012).Nemésio(2012)presentedand extensivelydiscussedsomemethodologicalconcernsinecological studieswithorchidbees,includingthoserelatedtobaitdispersion, distancefromwhichmalesaresupposedtobeattractedtolures andsoon.Themainconclusiononecandrawfromthevast con-troversypresentedbyNemésio(2012)isthatwedonotentirely understandhowbaitswork.Inparticular,onekeyaspecthastodo withthedurationoftheattractivenessofthesebaitstomalesor howlongbaittrapsshouldbeofferedtobeesforsufficientsample, althoughasuggestionthatthisperiodmaybeaslongas multi-pleweeks wasgiven by Roubik(1993). However,two relevant

https://doi.org/10.1016/j.rbe.2018.11.001

0085-5626/©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

2 J.A.Coswosketal./RevistaBrasileiradeEntomologia63(2019)1–5

questionsshouldbestressed:(i)Roubik(1993)presented infor-mationonlyontheattractivenessofcineole,whilewepresentdata onsevencompounds;and,moreover,(ii)Roubik(1993)reported theuseof8–15mLofcineolepertrap,whilewejustutilized cot-tonswabssoakedwithagivenaromaticcompound(seemethods below).

Thisshortcommunicationaimsatpresentingsomegeneraldata ontheattractivenessofbaittrapsthatwereleftinthefieldduring twoweeksinalargeAtlanticforestpreserve.

Fieldwork was carried out at Reserva Natural Vale (RNV), a large remnant of Brazilian Atlantic forest, encompassing ca. 22,700hainthemunicipalitiesofLinhares,JaguaréandSooretama (19◦06–19◦18S and 39◦45–40◦19W), northern Espírito Santo state,Brazil(LopesandMello-Silva,2014).ReservaNaturalVale, togetherwithReservaBiológicaSooretama(ca.24,000ha),areby farrecognized(Amorim,1984)asthelastTabuleiroforestmassifin northernEspíritoSanto(reviewedbySilva,2014).Amongthefour naturalvegetationtypesfoundintheregion,MataAlta(tallforest), whichpresentsathickcanopylayerreachingupto40m,occupies ca.70%ofthetotalareaoftheReservaNaturalVale(Peixotoetal., 2008).Baitswereinstalledinthisphysiognomy.

Atotalof175baittraps(35trapsforeachofthefollowingseven attractants:benzylacetate,␤-ionone,eucalyptol,eugenol,methyl salicylate, methyl trans-cinnamateand vanillin) wasoffered to beesalonganedge-interiortransectwithinthefragment.Complete descriptionofbaittrapsandexperimentaldesignmaybefound elsewhere(Coswosketal.,2018).Itisimportanttohighlightthat attractantswerenotreplenishedafterthetrapswereplacedinthe field.TrapswereinstalledinearlyDecember2012,andsamples werecarriedoutone(sample1),eight(sample2)andfifteen (sam-ple3)daysaftertheirinstallation.Inthisway,sample2wascarried outsevendaysaftersample1andsample3wascarriedoutseven daysaftersample2(fourteendaysaftersample1).Beesluredwere gentlyremovedfromtraps,transferredto70%ethanol,andpinned. Maleswereidentified withhelpof taxonomickeys(Rebêloand Moure,1996;FariaandMelo,2007,2012;Nemésio,2009)andby comparisonwithspecimenspreviouslyidentified.Taxonomy fol-lowsMoureetal.(2012).Alltheindividualsaredepositedinthe “Colec¸ãoZoológicaNorteCapixaba”(CZNC),CentroUniversitário NortedoEspírito Santo,UniversidadeFederaldo EspíritoSanto, SãoMateus,Brazil.

Atotalof3114malesof25specieswascollectedatthethree moments (sample1: 683; sample 2:1648; and sample 3:783 specimens)(Table1).Fourmain resultsarehighlighted: (i)the abundanceofspecimenscollectedperday(sample1:theabsolute numberofindividualscollectedafterthefirstday;sample2and 3:thenumberofindividualsdividedbythesevendaysbetween samples1and2andsamples2and3)decreasedinallthe attrac-tantsasthetrapswereleftonthefield(Fig.1A);(ii)despitethis decrease,theabsolutenumberofindividualscollectedaftereight andfifteendaysisremarkable,mostlyineugenolandvanillinbaits (Fig.1B);(iii)thevastmajorityofspecies,22of25,wasalready col-lectedonthefirstsample(Fig.1C);(iv)thereisanotablevariation intherelativeabundanceofindividualscollectedineachscentas thecollectionsweremade(Fig.1D).

Regardingthe decrease in attractiveness of the compounds, whatcouldbeinferredbythedeclineinthenumberofmales col-lectedperday,theabruptdropineucalyptolattractivenessafterthe firstsampleisremarkable.Thiscompoundisthemostemployed byorchidbeeresearchers,atleastinBrazil(Fariaetal.,2015),and isregardedtobethemostattractivecompoundwithrespecttothe numberofspeciescollected(Rebêlo,2001).Theevidencepresented heresupportsthestatementthatusingeucalyptolbaitedtrapsfor alongperiodoftime,withoutreplenishment,seemstobe inef-fectivesinceitisahighlyvolatilecompound.Ontheotherhand, thedecreasewasmuchlesspronouncedineugenolandvanillin

baits,twootherwidelyusedcompounds(Fariaetal.,2015),that keepattractingareasonablenumberofmalesperdayevenafter twoweeks.Inthespecificcaseofvanillin,thisbaitbecomesmore attractiveasalcoholevaporatesandthecompoundcrystallizes,so thatbaitreplenishmentwouldnotbedesirableatfirst(Coswosk, pers.obs.).

Thesetwobaitscouldthenbeemployedinsamplingdesigns wheretheavailability ofbaittraps inthefield forlongperiods isuseful,forinstanceinstudieswherepopulationsizesoffocal speciesthatareknowntobeattracttothesecompoundsare esti-mated.Intensivesamplingschemesforsomerarespeciescouldalso besettled,improvingthechancesofcollectingthem.Somerare orchidbeesofseasonalgenusEufriesea,forinstance,areknownto beattractedtoeugenolandvanillinbaits(e.g.Eufriesea brasiliano-rum(Friese,1899),seeNemésio,2009).

Thesedecisionsshouldobviouslyconsidertheriskof collect-ingseveralspecimensofthemostabundantspeciesandshouldbe definedinacost-effectivecontext.Afterall,wehavetokeepin mindthatthenumberofbeescollectedinsamples2and3(2431 specimens)isquitehigh.Whenweconsiderthatthedeclineof populationsofforestdependenteuglossinespeciesisarealmatter (e.g.Nemésio,2013),withthepossibilityofbecomingevenworse (Faleiroetal.,2018),andthatdataontheconservationstatusof a largenumber of speciesis deficient (see Nemésio,2009), we reallyshouldconsidertherealneedofcollectingandsacrificing euglossinemales(seeNemésio,2012).

Theresultspresentedherealsogivesupporttothestatement thatmosteuglossinespeciesareexpectedtobeinventoriedinthe firstsamplingdays.Somestudiessuggestthatshort-term inten-sivesamplinghasbeendemonstratedtobeusefulincharacterizing thelocalfaunasofEuglossina,bothinAtlanticareaswherealarge regionalspeciespoolisfound(e.g.Nemésio,2010)andinCerrado, whereeuglossinerichnessisnotthathigh(e.g.Tostaetal.,2017). However,itshouldbestressedthattheresultspresentedhere,and alsobyNemésio(2010)andTostaetal.(2017)wereobtainedduring therainyseason.AssuggestedbyNemésio(2016),rapidinventories shouldbecarriedoutduringtherainyseasonwhentheoverall com-munitycomposition,includingthoseinthehighlyseasonalgenus Eufriesea,arelikelytobesampled.Obviously,anassessmentaims atcollectingtheentirelocalfauna,sothelackofrecordsforthree speciesinthefirstdaymatters.Whenitisassumedthatsurveying allspeciesisavirtuallyimpossibletask(e.g.Nilssonetal.,2001) andthatallsamplingmethodshaveinherentandusuallyunknown samplingbiasesthatfavorthedetectionofsomespeciesbutnot others(GotelliandColwell,2011),thefactthat22of25species weresampledinjustonedayisoutstanding.

Theavailabilityofdataoneuglossinerichnessandcomposition fromlong-termstudiesisa bottleneckfor conductingextensive comparativestudies,e.g.onbiogeography(e.g.Aguiaretal.,2014) of thesebees. Asthe resultsof short-termassessments appear increasinglyrobust,dataassociatedwithorchidbeedistribution andseasonalitywillgreatlyincreaseandcomparativestudieson euglossineassemblageswillsurelythrive.

Finally,evenconsideringtheresultspresentedherecomefrom aregionwhereeuglossinebeesareabundantandspeciose,weurge thatbaittrapsshouldnotbeleftinthefieldbeyondwhatisstrictly necessary,eveninplaceswhereorchidbeesarenotthatspeciose and/orabundant,sincethereisarealpossibilityofcollectinga sig-nificantnumberofindividualsasthesetrapsremainavailableto males.

Contributors

Allauthorsconceived theresearchandwent tofieldto per-formtheexperiments.Thelastauthorwroteafirstversionofthe

J.A. Coswosk et al. / Revista Brasileira de Entomologia 63 (2019) 1–5 3

Abundanceofeuglossinespeciescollectedinsevendifferentattractantsoverthreeconsecutivesamples(one,eightandfifteendays)attheReserveNaturalVale,northernEspíritoSantostate,Brazil(BA:benzylacetate;BI: ␤-ionone;EC:eucalyptol;EG:eugenol;MC:methyltrans-cinnamate;MS:methylsalicylate;VN:vanillin).

Species Sample1 Total Sample2 Total Sample3 Total Totalby

species

BA BI EC EG MC MS VN BA BI EC EG MC MS VN BA BI EC EG MC MS VN

Eulaemacingulata(Fabricius,1804) 68 42 0 24 1 0 69 204 108 222 0 153 0 23 260 766 6 159 0 184 0 0 188 537 1507

Euglossacordata(Linnaeus,1758) 0 14 157 8 45 0 0 224 11 46 4 142 241 0 0 444 0 3 0 80 3 0 0 86 754

EulaemanigritaLepeletier,1841 0 0 45 0 0 0 24 69 0 0 0 0 0 3 207 210 0 0 0 0 0 0 93 93 372

EuglossasecurigeraDressler,1982 0 1 4 10 0 1 0 16 1 0 0 81 11 0 0 93 0 0 0 32 0 0 0 32 141

EuglossaiopoecilaDressler,1982 0 0 3 11 1 0 12 27 0 0 0 17 0 0 10 27 0 0 0 19 0 0 4 23 77

EuglossaignitaSmith,1874 4 0 6 5 10 6 0 31 13 0 0 5 8 6 0 32 0 0 0 0 0 0 0 0 63

EuglossafimbriataMoure,1968 0 4 10 2 1 0 0 17 3 24 0 5 0 0 0 32 0 0 0 2 0 0 0 2 51

EuglossagaianiiDressler,1982 1 22 1 0 0 0 0 24 0 0 0 2 0 0 0 2 0 0 0 0 0 0 0 0 26

Eulaemaniveofasciata(Friese,1899) 0 0 0 0 2 5 0 7 2 0 0 0 0 12 0 14 0 0 0 0 0 0 0 0 21

EuglossacognataMoure,1970 0 0 0 1 0 7 0 8 0 0 0 1 0 5 1 7 0 0 0 0 0 0 0 0 15

EuglossaimperialisCockerell,1922 0 0 0 1 0 8 0 9 0 0 0 1 0 5 0 6 0 0 0 0 0 0 0 0 15

EulaemaatleticanaNemésio,2009 2 2 2 0 0 2 1 9 0 4 0 0 0 2 0 6 0 0 0 0 0 0 0 0 15

Exaeretesmaragdina(Guérin,1844) 1 0 3 2 1 0 0 7 1 0 0 0 0 1 0 2 0 0 1 2 0 0 0 3 12

EuglossaadiastolaHinojosa-Dìaz, Nemésio&Engel,2012

0 0 1 2 0 1 0 4 0 0 0 1 0 0 1 2 0 0 0 3 0 0 0 3 9

EuglossabotocudaFaria&Melo,2012 0 0 5 0 0 4 0 9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 9

EuglossamarianaeNemésio,2011 0 0 9 0 0 0 0 9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 9

Eufrieseadentilabris(Mocsáry,1897) 0 0 0 0 0 0 2 2 0 0 0 0 0 0 2 2 0 0 0 0 0 0 0 0 4

EuglossapleostictaDressler,1982 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 2 0 0 0 2 0 0 0 2 4

Eufrieseasurinamensis(Linnaeus,1758) 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2 2

ExaeretesalsaiNemésio,2011 0 0 0 0 0 2 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2

Exaeretefrontalis(Guérin,1844) 0 0 1 1 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2

EufrieseaatlanticaNemésio,2008 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

EuglossaaviculaDressler,1982 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 1

EuglossaleucotrichaRebêlo&Moure, 1996

0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

EuglossamilenaeBembé,2007 0 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

Total(scent/sample) 76 85 247 68 62 36 109 139 296 4 410 260 57 482 6 162 1 324 3 0 287 3114

4 J.A.Coswosketal./RevistaBrasileiradeEntomologia63(2019)1–5 250 200 150 100 50 0 500 400 300 200 100 0 25 20 15 10 5 0 1.00 0.75 0.50 0.25 0.00 BA BI EC EG MC MS VN BA BI EC EG MC MS VN BA BI EC EG MC MS VN T 3 2 1

a

b

c

d

Fig.1.VariationinthenumberofindividualsandspeciescollectedinRNV accord-ingtotheattractivebaitandeachperformedsample.a:abundanceofspecimens collectedperdayineachsample;b:absolutenumberofspecimenscollectedin eachsample;c:accumulatednumberofspeciesaftersamples(a–c:sample1,black; sample2,gray;sample3,white;BA:benzylacetate;BI:␤-ionone;EC:eucalyptol; EG:eugenol;MC:methyltrans-cinnamate;MS:methylsalicylate;VN:vanillin;T: totalpersample);d:relativeabundanceofspecimenscollectedineachscent(EC, black;EG,darkgray;VN,gray;BI,lightgray;BA+MC+MS:white;numbersrefer sequentiallytofirst,secondandthirdcollections).

paperandallauthorscontributedequallyreviewingcriticallythe manuscriptforimportantintellectualcontent.Allauthorsapproved thefinalversionofthismanuscript.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

WeareindebtedtoMariaCecíliaMartinsKierulffforgivingus allthesupportwithinherreachduringthefieldworkatReserva NaturalVale.WealsoacknowledgeValeandReservaNaturalVale administrationforprovidingthepermissiontoperformthisstudy and for all the facilities during the fieldwork. CEUNES/UFES is acknowledgedforprovidingtransportduringafieldtrip.Frederico FalcãoSalles(UFES)isacknowledgedforallhishelpwith field-work.WeacknowledgeAntonioJoséCamillodeAguiar(UnB)for importantdiscussionsonfieldcollectionoforchidbees.Wethank SISBIO/ICMBioforthecollectingpermit(#21803).

References

Aguiar,W.M.,Melo,G.A.R.,Gaglianone,M.C.,2014.Doesforestphisiognomyaffect thestructureoforchidbee(Hymenoptera,Apidae,Euglossini)communities? AstudyintheAtlanticforestofRiodeJaneirostate,Brazil.Sociobiology61, 68–77.

Amorim,H.B.,1984.FlorestasnativasdosestadosdoRiodeJaneiroeEspíritoSanto. InventárioFlorestalNacional.InstitutoBrasileirodoDesenvolvimento Florestal-IBDF,Brasília.

Bezerra,C.P.,Martins,C.F.,2001.DiversidadedeEuglossinae(Hymenoptera, Api-dae)emdoisfragmentosdeMataAtlânticalocalizadosnaregiãourbanadeJoão Pessoa,Paraíba,Brasil.Rev.Bras.Zool.18,823–835.

Botsch, J.C., Walter, S.T., Karubian, J., González, N., Dobbs, E.K., Brosi, B.J., 2017. Impactsof forest fragmentationonorchid bee (Hymenoptera: Api-dae:Euglossini)communitiesintheChocóbiodiversityhotspotofnorthwest Ecuador.J.InsectConserv.21,633–643.

Coswosk,J.A.,Ferreira,R.A.,Soares,E.D.G.,Faria,L.R.R.,2018.Responsesof euglos-sinebees(Hymenoptera, ApidaeEuglossina)to anedge-forest gradientin alarge TabuleiroForest remnant ineastern Brazil.Neotrop. Entomol.47, 447–456.

Dodson,C.H.,Dressler,R.L.,Hills,H.G.,Williams,N.H.,1969.Biologicallyactive com-poundsinorchidfragrances.Science164,1243–1249.

Faleiro,F.V.,Nemésio,A.,Loyola,R.,2018.Climatechangelikelytoreduceorchidbee abundanceeveninclimaticsuitablesites.Glob.ChangeBiol.24,2272–2283. Faria,L.R.R.,Melo,G.A.R.,2007.SpeciesofEuglossa(Glossura)intheBrazilianAtlantic

forest,withtaxonomicnotesonEuglossastellfeldiMoure(HymenopteraApidae, Euglossina).Rev.Bras.Entomol.51,275–284.

Faria,L.R.R.,Melo,G.A.R.,2012.SpeciesofEuglossaoftheanalisgroupintheAtlantic forest(Hymenoptera,Apidae).Zoologia29,349–374.

Faria,L.R.R.,Sydney,N.V.,Gonc¸alves,R.B.,2015.HowBrazilianresearchershavebeen samplingorchidbees?In:Aguiar,A.J.C.,Gonc¸alves,R.B.G.,Ramos,K.S.(Orgs.), EnsaiossobreasabelhasdaregiãoNeotropical:homenagemaos80anosde DanunciaUrban.EditoraUFPR,Curitiba,pp.307–346.

Gotelli,N.J.,Colwell,R.K.,2011.Estimatingspeciesrichness.In:Magurran,A.E., McGill,B.J.(Eds.),BiologicalDiversity:FrontiersinMeasuringBiodiversity. OxfordUniversityPress,NewYork,pp.39–54.

Knoll,F.R.N.,Penatti,N.C.,2012.Habitatfragmentationeffectsontheorchidbee communitiesinremnantforestsofsoutheasternBrazil.Neotrop.Entomol.41, 355–365.

Lopes,J.C.,Mello-Silva,R.,2014.AnnonaceaedaReservaNaturalVale,Linhares, EspíritoSanto.Rodriguésia65,599–635.

Mattozo,V.C.,Faria,L.R.R.,Melo,G.A.R.,2011.Orchidbees(Hymenoptera:Apidae) inthecoastalforestsofsouthernBrazil:diversity,efficiencyofsampling meth-odsandcomparisonwithotherAtlanticforestsurveys.Pap.AvulsosZool.51, 505–515.

Moure,J.S.,Melo,G.A.R.,Faria,L.R.R.,2012.EuglossiniLatreille,1802.In:Moure,J.S., Urban,D.,Melo,G.A.R.(Eds.),CatalogueofBees(Hymenoptera,Apoidea)inthe NeotropicalRegion–OnlineVersion.,http://www.moure.cria.org.br/catalogue (accessed10.02.18).

Nemésio,A.,2009.Orchidbees(Hymenoptera:Apidae)oftheBrazilianAtlantic Forest.Zootaxa2041,1–242.

Nemésio,A.,2010.Theorchid-beefauna(Hymenoptera:Apidae)ofaforestremnant innortheasternBrazil,withnewgeographicrecordsandanidentificationkeyto theknownspeciesoftheAtlanticForestofnortheasternBrazil.Zootaxa2656, 55–66.

Nemésio,A.,2012.Methodologicalconcernsandchallengesinecologicalstudies withorchidbees(Hymenoptera:Apidae:Euglossina).Biosci.J.28,118–135. Nemésio,A.,2013.Areorchidbeesatrisk?Firstcomparativesurveysuggests

declin-ingpopulationsofforestdependentspecies.Braz.J.Biol.73,367–374. Nemésio,A.,2016.Orchidbees(HymenopteraApidae)fromtheBrazilian

savanna-like‘Cerrado’:howtoadequatelysurveyunderlowpopulationdensities, North-West.J.Zool.12,230–238.

Nemésio,A.,Silveira,F.A.,2006.Edgeeffectsontheorchid-beefauna(Hymenoptera: Apidae)atalargeremnantofAtlanticForestinsoutheasternBrazil.Neotrop. Entomol.35,313–323.

Nemésio,A.,Vasconcelos,H.L.,2014.Effectivenessoftwosamplingprotocolsto surveyorchidbees(Hymenoptera:Apidae)intheNeotropics.J.InsectConserv. 18,197–202.

Nilsson,S.G.,Hedin,J.,Niklasson,M.,2001.BiodiversityanditsassessmentinBoreal andNemoralforests.Scand.J.ForestRes.3,10–26.

Peixoto,A.L.,Silva,I.M.,Pereira,O.J.,Simonelli,M.,Jesus,R.M.,Rolim,S.G.,2008. TabuleiroforestsnorthoftheRioDoce:theirrepresentationintheValedoRio DoceNaturalReserve,EspíritoSantoBrazil.In:Thomas,W.W.(Ed.),TheAtlantic CoastalForestofNortheasternBrazil.TheNewYorkBotanicalGardenPress,New York,pp.319–350.

Ramalho,A.V.,Gaglianone,M.C.,Oliveira,M.L.,2009. Comunidadesdeabelhas Euglossina(HymenopteraApidae)emfragmentosdeMataAtlânticanoSudeste doBrasil.Rev.Bras.Entomol.53,95–101.

Rebêlo,J.M.M.,2001.Histórianaturaldaseuglossíneas.Asabelhasdasorquídeas. Lithograf,SãoLuís.

Rebêlo,J.M.M.,Moure,J.S.,1996[1995].AsespéciesdeEuglossaLatreilledonordeste deSãoPaulo(Apidae,Euglossinae).Rev.Bras.Zool.12,445–466.

Roubik,D.W.,1993.Tropicalpollinatorsinthecanopyandunderstory:fielddata andtheoryforstratum“preferences”.J.InsectBehav.6,659–673.

Silva,A.G.,2014.AimportânciadaReservaNaturalValeparaaconservac¸ãodas florestastropicaisnativasdoNortedoEspíritoSantoBrasil.NaturezaOnline12, 206–211.

Silveira,G.C.,Nascimento,A.M.,Sofia,S.H.,Augusto,S.C.,2011.Diversityofthe euglossinebeecommunity(HymenopteraApidae)ofanAtlanticForestremnant insoutheasternBrazil.Rev.Bras.Entomol.55,109–115.

Sofia,S.H.,Suzuki,K.M.,2004. ComunidadesdemachosdeabelhasEuglossina (Hymenoptera:Apidae)emfragmentosflorestaisnosuldoBrasil.Neotrop. Entomol.33,693–702.

Storck-Tonon, D., Morato, E.F., Oliveira, M.L., 2009. Fauna de Euglossina (Hymenoptera:Apidae)daAmazôniaSul-Ocidental,AcreBrazil.ActaAmaz.39, 693–706.

Sydney, N.V., Gonc¸alves, R.B., 2015. Is the capture success of orchid bees (HymenopteraApoidea)influencedbydifferentbaitedtrapdesigns?Acase studyfromsouthernBrazil.Rev.Bras.Entomol.59,32–36.

Tosta,T.H.A.,Silveira,G.C.,Schiavini,I.,Sofia,S.H.,Augusto,S.C.,2017.Using short-termsurveysandmark-recapturetoestimatediversityandpopulationsize oforchidbeesinforestformationsoftheBraziliansavanna.J.Nat.Hist.51, 391–403.

Uehara-Prado,M.,Garófalo, C.A.,2006.Small-scaleelevational variationinthe abundanceofEufrieseaviolacea(Blanchard)(Hymenoptera:Apidae).Neotrop. Entomol.35,446–451.