Species richness and activity pattern of bees (Hymenoptera, Apidae) in the restinga area of Lençóis Maranhenses National Park, Barreirinhas, Maranhão, Brazil

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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

Species

richness

and

activity

pattern

of

bees

(Hymenoptera,

Apidae)

in

the

restinga

area

of

Lenc¸

óis

Maranhenses

National

Park,

Barreirinhas,

Maranhão,

Brazil

Luana

Fontoura

Gostinski

a

_,

_Gracy

_Chrisley

_Alencar

_Carvalho

b

_,

_Márcia

_Maria

_Correa

_Rêgo

c

_,

Patrícia

Maia

Correia

de

Albuquerque

a,c,∗

a_Universidade_Federal_do_Maranhão,_Programa_de_{Pós-Graduaç}_ão_em_Rede_de_{Biodiversidade}_e_{Biotecnologia}_da_Amazônia_Legal,_São_Luís,_MA,_Brazil b_Universidade_Federal_do_Maranhão,_Programa_de_{Pós-Graduaç}_ão_em_{Biodiversidade}_e_Conservaç_ão,_São_Luís,_MA,_Brazil

c_Universidade_Federal_do_Maranhão,_Departamento_de_Biologia,_Laboratório_de_Estudos_sobre_Abelhas,_São_Luís,_MA,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received14April2016 Accepted26August2016 Availableonline9September2016 AssociateEditor:MariaCristinaGaglianone

Keywords: Annualactivity Apoidea Beediversity Coastalregion Neotropical

a

b

s

t

r

a

c

t

TheApidaecommunitystructurewasstudiedinavegetatedareaofcoastaldunesinLenc¸óis Maran-hensesNationalPark.CollectionswereperformedmonthlyfromAugust2009toJuly2010.Thecollection methodsincludedtheuseofentomologicalnetsonﬂowersandMoeriketraps.Intotal,1211individuals belongingto59specieswerecollected.Thepatternofabundanceandrichnesswassimilartothosefound inMaranhãoandothercoastalareasofnortheasternBrazil.Thebeeswerepresentthroughouttheyear, withanincreaseinthenumberofindividualsduringtherainyseason.Constantanddominantspecies includedTrigonasp.gr.fulviventris,Apismellifera,Plebeiaalvarengai,Centrisaenea,Xylocopacearensis,and Centriscaxiensis.

Introduction

Theexuberance and uniqueness of thelandscape of Lençóis MaranhensesNationalPark(ParqueNacionaldosLençóis Maran-henses–PNLM),representedbydunefieldssurroundedbylakes, beaches,mangroves,andrestingas(sandycoastalplains)andthe highleveloflocalbiodiversityjustifiedthecreationoftheProtected

AreaofPNLM in1981(Silva andSilvaFilho, 2008).Toimprove

theunderstandingofthisecosystem,speciesinventorieshavebeen performedatPNLM.Amongthebees,severalspeciesofCentrisand Euglossawererecordedusingtrapnests(Ramosetal.,2006).Amore completelistof14of speciesoforchidbees(Euglossa,Eulaema, andEufriesea)wasobtainedbybaitingwitharomaticfragrances

(Silvaetal.,2009).Inacasestudyofmuricipollinators(Byrsonima

crassifolia(L.)Rich,Malpighiaceae),21speciesofCentridiniwere identiﬁed(Rêgoetal.,2006).Althoughthesestudiesyieldedﬁrst assessmentsofsomespeciesrichbeetaxa,theknowledgeregarding thebeespeciesremainedfragmentarybecauseoftheselectivityof thesamplingmethodsused.

∗ Correspondingauthor.

E-mail:patemaia@gmail.com(P.M.Albuquerque).

Sakagamietal.(1967)proposedthestandardizationof

samp-ling,withthecollectionofbeesonﬂowersusingentomological nets,thus providingdataonlocaldiversity,relative abundance, habitatpreference,andassociatedplants.Thismethodallows com-parisonsamongvariousecosystems,enablingeasiertocompare patternsinthestructure ofbeecommunitiesintheNeotropical region(AguiarandZanella,2005).Othermethodsofcollectingbees arescentbaiting,whichistypicallyaimedatattractingEuglossini males(NemésioandSilveira,2007),theuseoftrapnests(Gazola

andGarófalo,2009),andmorerecently,samplingwithcoloured

traysandbowls(Gonc¸alvesandOliveira,2013).Withouttheuse ofcomplementarymethods,20%or8%ofthebeespecieswould nothavebeenrecordedinrecentinventoriesinSantaCatarinain southernBrazil(Krug andAlves-dos-Santos,2008;Kamkeetal., 2011,respectively).

AsreportedbyVianaandKleinert(2005),despitethevariety ofmethods,littleisknownregardingthebeefaunaofthecoastal ecosystemsofBrazil.Mostsurveysofbeesinrestingaareashave focussedonthesouthernregionofthecountry,includingstudies inParaná(Laroca,1974;Zanella,1991;Schwartz-FilhoandLaroca, 1999),SantaCatarina(Mouga,2004;Kamkeetal.,2011),andRio GrandedoSul(Alves-dos-Santos,1999).Amongthestudies con-ductedinthenortheasternregion,wecanciteVianaandKleinert

(2005),Silvaetal.(2015)andMoreiraetal.(2016)inBahiaand

http://dx.doi.org/10.1016/j.rbe.2016.08.004

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Madeira-da-SilvaandMartins(2003)inParaíba.Gottsbergeretal.

(1988)studiedpollinatingbeesinthedunevegetationonSãoLuís

Island(northernBrazil) andfoundthatnineoutofthe10plant speciesstudiedweremelittophilous,andinspiteoftheadverse conditionsandthestrongwind,18beespecieswerereportedas ﬂowervisitors.Inaddition,thestudiesofAlbuquerque(1998)and

Oliveiraet al.(2010)were conductedatthe samelocation and

resultedininventoriesof36and31beespecies,respectively. Thepresent studyaimstoevaluate, usingdifferentsampling methods,thespeciesrichness,and diversityofbeesinPNLMto describetheiractivitypattern,andtocomparethesimilaritieswith othercoastalenvironmentsofnortheasternBrazil.

Materialandmethods

Studyarea

Thisstudywasconductedinarestingaareameasuring200ha located at the edge of PNLM in the municipality of Barreirin-has(2◦4322.5S–42◦4950W),Maranhão,Brazil.Accordingtothe

Köppen(1948)classiﬁcation,theregionalclimateistheAwtype,

whichisatropicalclimatewithhightemperaturesandtwo well-deﬁnedseasons, dry(July–December)and rainy(January–June), withapproximately1800mmofrainfall(Maranhão,2002).

ThePNLMvegetationcoversanareaof453.28km2_,_405.16_km2

(89%)ofwhichareclassiﬁedasrestinga.Therearealsomangroves, riparianforests, and cerradosthat cover a smallportion ofthe totalarea(Ibama,2003).Accordingtostudiesconductedthrough thePNLMManagementPlan(Ibama, 2003),therestinga of this regionis composedofmelittophilous plants that belongtothe familiesLythraceae,Malpighiaceae,Turneraceae,Asteraceae,and Ochnaceae.

Sampling

Thecollectionswereperformedbytwocollectorsataninterval of25–30daysover12 months(August2009–July2010)ontwo consecutivedays:from12:00to18:00honthefirstdayandfrom 6:00to12:00honthesecondday,foratotalof288hofsampling. Thebeeswerecollectedinentomologicalnets(whiletheinsects wereeitherflyingorvisiting flowers)usingthemethodologyof

Sakagamietal.(1967).Tosample45,000m2_,_a₄₅₀_m_transect_was

walkedataslowpacebythetwocollectorssimultaneously,and eachbeethatwasobservedfeedingonaﬂowerwithina50mstrip oneachsideoftheobserverswascollected.

Inaddition,bowltraps(Moeriketraps,15cmwide,5cmhigh, 300ml ofwater and dropsof dishwashing)wereused simulta-neously(Grundeletal.,2011).Bowlshaddifferentcolours(yellow, blue,green,orwhite)andweredeployedmonthlyfor48h,fora totalof 576hof sampling(in10 groupsof fourbowlseach) in thesame areawhere beeswerenetted.Thebowlswereplaced ontheground(ﬁvegroups)oronpoles(1mhigh,ﬁvegroups)at 5mintervalswithinterspersedcolours.Thecollectedinsectswere preservedandstoredin70%ethanol.

ThebeesweremountedonpinsanddepositedintheBee Collec-tionoftheLaboratoryofBeeStudies(LEACOL/UniversidadeFederal doMaranhão–UFMA).Theywereidentiﬁedtothemorphospecies levelwiththeaidoftaxonomickeys(Silveiraetal.,2002), and tospecieslevelbycomparisonwiththereferencecollection,and withtheassistanceoftaxonomists.Moreover,wereusedMoure

etal.(2012a,b)toconﬁrmthedistributionofspecies.Tocompare

thesedatawiththoseofpreviousstudies,weconsidered corbicu-late(Apini,Meliponini,andEuglossini)andnon-corbiculateApinae (asanalysed by Gonc¸alves and Melo,2005; Milet-Pinheiro and

Schlindwein,2008).

Temperature and air humiditydatawere obtainedfromthe GeoenvironmentalCentreofMaranhãoStateUniversity,usingthe UrbanoSantosstationlocatedapproximately85kmfromthe col-lectionsite.TheWeatherForecastsandClimateStudiesCentrein theNortheastRegion(CPTEC,2010)providedrainfalldata.

Dataanalysis

TheShannon–Wienerindexwasappliedtocalculatethespecies diversity, and Pielou’s index was used to calculate the area equitability.ThecalculationswereperformedusingPAST (Paleon-tologicalStatistics2.00)(Hammeretal.,2001).

Foreach speciessampledbynetting, thedominance(D)and constancy(C)werecalculatedaccordingtoBodenheimer(1955). Fordominance,D=(abundanceofspeciesi/totalabundance)×100. If D>5%, then the species was considered dominant (D); if 2.5%<D<5%,thenthespecieswasconsideredaccessory(A);and ifD<2.4%,thenthespecieswasconsideredoccasional(OC).

Constancyisthepercentageofindividualspresent,calculated asC=P×100/N,wherePisthenumberofsamplescontainingthe species,andNisthetotalnumberofsamples.Thebeescollectedin 12hofnettingpermonthwereconsideredonesample.IfC>50%, thenthespecieswasconsideredconstant(W);if25%<C<50%,then thespecieswasconsideredaccessory(Y);andifC<25%,thenthe specieswasconsideredaccidental(Z)(Silveira-Netoetal.,1976).

TheMorisitaindexwasappliedtoanalysethesimilaritywith beecommunitiesequivalenttotherestingaofPNLM,suchasthe restingaofCabedelo,Paraíba(Madeira-da-SilvaandMartins,2003), AbaetédunesandSalvador,Bahia(VianaandKleinert,2005;Silva etal.,2015),Panaquatirabeach(SãoJosédeRibamar),Maranhão

(Oliveiraet al.,2010), andSãoMarcosbeach(SãoLuís),

Maran-hão(Albuquerque,1998),usingPAST.TheMorisitaindexwasonly

appliedtothebee speciescollectedwithnets,theprimary col-lectingmethodusedinthosestudies.

Todeterminetherepresentativenessofthecommunity sam-pledwithbothmethods,aspeciesaccumulationcurve(collector curve)aswellasrichnessestimatorsChao1andJackknife1were generatedusingBioDiversityProVersion2(Mcaleeceetal.,1997).

Results

Speciesrichnessanddiversity

A total of 1211 individuals belonging to 59 species of the Apoideawerecollectedusingentomologicalnetsandbowltraps in the restinga of thePNLM (Tables 1 and 2).The descending orderofrichness persubfamilywasasfollows:non-corbiculate Apinae (24 spp.)>Megachilinae (14 spp.)>corbiculate Apinae (13 spp.)>Halictinae (6 spp.)>Andreninae (2 spp.). The abun-dance per subfamily was as follows: corbiculate Apinae (644 individuals)>non-corbiculateApinae(384ind.)>Andreninae(133 ind.)>Megachilinae(33ind.)>Halictinae(17ind.).

ThetribeMegachilinicontained20%ofthespecies,followedby Centridini(18%),Xylocopini(17%),Meliponini(12%),andEuglossini (8%).ThemostspeciesrichgenerawereMegachile(12spp.),Centris (10spp.),Ceratina,Xylocopa(5spp.each),andDialictus(3spp.)

(Table 1).Elevenbee species wereobtainedonlythrough bowl

traps.ThesubfamilyAndreninae,representedbyCallonychium (Cal-lonychium)brasiliense(Ducke,1907)andC.(Callonychium)sp.,were exclusivelycollectedwiththismethodandrepresented60.5%of theindividualscollectedinthebowltraps.Atotalof218beesof 19specieswerecollectedwithbowltraps.Inthebluebowlsall19 speciesand56.4%oftheindividualswerecaptured(Table1).

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Table1

Compositionandnumberofbees(Hymenoptera,Apidae)oftherestingaareaofthePNLMcapturedbydifferentmethods.Samplingmethods:nets(entomologicalnets)and bowltraps(Ye:yellow,Wh:white,Bl:blue,Gr:green)wereusedinthisstudy;chemicalbaits,trapnests(numberofemergingindividuals)andByrsonimacrassifoliaﬂower visitors(numberofbeespecimenscollectedat)wereusedinothersurveysinthesamestudyarea.

Species Net Bowltraps Chemicalbaits

Silvaetal. (2009) Trapnest Ramosetal. (2006) Muricivisitors Rêgoetal. (2006) Ye Wh Bl Gr Andreninae–Calliopsini

Callonychium(Callonychium)brasiliense(Ducke,1907) 27 26 52 1 Callonychium(Callonychium)sp. 11 16 Apinae–Apini

ApismelliferaLinnaeus,1758 170 1 1 1

Apinae–Euglossini

Eufrieseanigrescens(Friese,1923) 85

Eufrieseaornata(Mocsáry,1896) 56

Eufrieseasp.1 1

Eufrieseasp.2 1

Eufrieseasuperba(Hoffmannesegg,1817) 3 Eufrieseasurinamensis(Linnaeus,1758) 16

Euglossa(Euglossa)cordataLinnaeus,1758 1 88 18 Euglossa(Euglossa)ﬁmbriataMoure,1968 1

Euglossa(Euglossa)gaianiiDressler,1982 1 17

Euglossa(Euglossa)liopodaDressler,1982 1 Euglossa(Euglossa)melanotrichaMoure,1967 1 Euglossa(Euglossa)modestiorDressler,1982 19 Euglossa(Glossura)chalybeataFriese,1925 3

Euglossasp. 1

Eulaema(Apeulaema)cingulata(Fabricius,1804) 105 Eulaema(Apeulaema)nigritaLepeletier,1841 1 49 Eulaema(Eulaema)meriana(Olivier,1789) 1 Apinae–Meliponini

Melipona(Melipona)subnitidaDucke,1910 8 Melipona(Michmelia)aff.ruﬁventrisLepeletier,1836 8 PartamonaseridoensisPedroandCamargo,2003 21

Plebeiaminima(Gribodo,1893) 8

PlebeiaalvarengaiMoure,1994 61 1 2

Tetragonasp. 1

Trigonasp.gr.fulviventrisGuérin,1835 333 1 21

TrigoniscaextremaAlbuquerqueandCamargo,2007 22 1 2 4 2 11

Trigoniscapediculana(Fabricius,1804) 4

Apinae–Anthophorini

Anthophorasp. 4

Apinae–Centridini

Centris(Centris)aeneaLepeletier,1841 78

Centris(Centris)caxiensisDucke,1907 96 366

Centris(Centris)byrsonimaeMahlmannandOliveira,2012 20

Centris(Centris)ﬂavifrons(Fabricius,1775) 3 22

Centris(Centris)decolorataLepeletier,1841 16

Centris(Centris)spilopodaMoure,1969 3

Centris(Hemisiella)trigonoidesLepeletier,1841 8

Centris(Hemisiella)tarsataSmith,1874 39 368

Centris(Melacentris)obsoletaLepeletier,1841 4 110

Centris(Ptilotopus)sponsaSmith,1854 1 4

Centris(Trachina)longimanaFabricius,1804 7

Centris(Xanthemisia)luteaFriese,1899 1

Centris(Xanthemisia)bicolorLepeletier,1841 1

Centrissp.1 6

Centrissp.2 133

Epicharis(Epicharis)bicolorSmith,1874 9

Epicharis(Epicharis)aff.umbraculata(Fabricius,1804) 3 131 Apinae–Eucerini

Florilegus(Florilegus)cf.condignus(Cresson,1878) 1 Exomalopsini

Exomalopsissp. 1

Apinae–Nomadini

Odyneropsissp. 4

Apinae–Tapinotaspidini

Paratetrapediaﬂavipennis(Smith,1879) 2

Xanthopediaglobulosa(Friese,1899) 67

Tropidopediapunctifrons(Smith,1879) 72

Apinae–Xylocopini

Ceratina(Ceratinula)sp. 3 9 1

Ceratina(Ceratinula)sp.1 2

Ceratina(Ceratinula)sp.2 6 1 1

Ceratina(Crewella)maculifronsSmith,1854 13

Ceratina(Crewella)sp. 1 9 21

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Table1

(Continued)

Species Net Bowltraps Chemicalbaits

Silvaetal. (2009) Trapnest Ramosetal. (2006) Muricivisitors Rêgoetal. (2006) Ye Wh Bl Gr Xylocopa(Neoxylocopa)cearensisDucke,1910 64 1 Xylocopa(Neoxylocopa)frontalis(Olivier,1789) 1

Xylocopa(Neoxylocopa)suspectaMoureandCamargo,1988 5 Xylocopa(Schonnherria)muscaria(Fabricius,1775) 1 Halictinae–Augochlorini

Augochlorasp. 1

Augochlorellasp. 1

Augochloropsissp. 1

Augochloropsissp.1 1

Pseudaugochlorapandora(Smith,1853) 1 Halictinae–Halictini Dialictussp.1 3 1 1 6 1 Dialictussp.2 1 Dialictussp.3 1 Megachilinae–Anthidiini Dicranthidiumsp. 25 3

Epanthidiumtigrinum(Schrottky,1905) 3

Saranthidiumsp. 1

Megachilinae–Megachilini

Megachile(Pseudocentron)sp. 5 Megachile(Pseudocentron)inscitaMitchell,1930 3 Megachile(Pseudocentron)cf.terrestrisSchrottky,1902 3

Megachilesp.1 1 30 Megachilesp.2 1 Megachilesp.3 1 Megachilesp.4 1 Megachilesp.5 2 Megachilesp.6 1 1 Megachilesp.7 2 Megachilesp.8 4 1 Megachilesp.9 1 2 Totalspecimens 991 32 58 125 5 429 129 1360 Totalspecies 48 6 9 19 4 14 5 23 180 30 nº individuals nº species

nº ind occasional (OC) nº ind dominant (D) Species

160 140 120 100 80 60 40 20 0 25 20 15 10 5 0 06-07h 07-08h 08-09h 09-10h 10-11h 11-12h 12-13h 13-14h 14-15h 15-16h 16-17h 17-18h

Fig.1.NumberofspeciesnettedandindividualsrecordedfromAugust2009to2010oftherestingaofthePNLM,Barreirinhas,MA,Brazil.

Activitypattern

Thehighestnumberofindividualswascollectedinthe morn-ing,between6:00and10:00h.Thisnumbergraduallydecreased throughoutthedayreachinganewpeakofcaptureat17:00h,when thehighestrelativehumidityandthelowesttemperatureswere recorded(Fig.1).Therewasapositivecorrelation(p>0.05)between temperature,relativehumidityandabundanceofindividualsper houroftheday.

Beeswerecapturedinallmonthsoftheyear,withadeclinein abundancebetweenAugust2009andMarch2010(Table2),which istheperiodthatcorrespondstothelowestprecipitationamount (the entire dry season and the beginning of the rainyseason). BetweenAprilandJuly,therewasapeakinabundancecoinciding withtherainyseason.ThemonthsofAugustandSeptemberhadthe greatestspeciesrichness,coincidingwiththebeginningofthedry season(Table2).Accordingtotheannualdistribution,the follow-ingspecieswereconsideredconstant(W):Trigonasp.gr.fulviventris

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Table2

ThemostfrequentspeciesofApidaecapturedwithnetandbowltrapsintherestingaofthePNLMinMaranhão,Brazil,fromAugust2009toJuly2010.

Species A S O N D J F M A M J J Total Class

Constancya _Dominanceb

Trigonasp.gr.fulviventrisGuérin, 1835

32 6 3 11 18 35 29 16 39 42 31 72 334 100.0W 36.53D

ApismelliferaLinnaeus,1758 2 8 37 6 2 7 8 9 22 16 55 172 91.66W 17.11D Callonychium(Callonychium)

brasiliense(Ducke,1907)

15 1 1 1 28 11 2 52 111 66.4W 9.16D

Centris(Centris)caxiensisDucke, 1907

5 4 1 2 4 4 22 9 6 10 14 15 96 100.00 W 9.69D

Centris(Centris)aeneaLepeletier, 1841

30 20 10 15 2 1 78 50.00 W 7.87D

Xylocopa(Neoxylocopa)cearensis Ducke,1910

3 2 1 4 3 15 5 11 6 6 9 65 91.66W 6.44D

PlebeiaalvarengaiMoure,1994 1 2 2 12 3 4 1 17 14 4 4 64 91.66W 6.14D TrigoniscaextremaAlbuquerque

andCamargo,2007

2 2 15 1 4 7 31 41.66Y 2.21OC

Ceratina(Crewella)sp. 1 4 3 5 5 3 1 8 30 66.4W 2.47OC

Callonychium(Callonychium)sp. 4 1 15 7 27 33.32Y 2.22OC PartamonaseridoensisPedroand

Camargo,2003

3 14 1 1 2 21 41.66Y 2.11OC

Centris(Centris)byrsonimae MahlmannandOliveira,2012

3 14 1 1 1 20 41.66Y 2.0OC

Xylocopa(Neoxylocopa)carbonaria Smith,1854

2 2 10 14 25.00Z 1.4OC

Ceratina(Ceratinula)sp. 1 1 2 2 1 1 1 2 3 14 74.97W 1.15OC Ceratina(Crewella)maculifrons

Smith,1854 1 2 2 3 1 3 1 13 50.00Y 1.3OC Dialictussp.1 3 3 6 12 24.9Z 0.9OC Othersspecies 17 13 13 1 8 4 1 5 11 6 12 18 109 Totalofspecimens 115 81 76 78 58 75 83 52 158 111 136 188 1211 Totalofspecies 20 20 16 12 14 12 10 15 15 16 16 18 59

a_Constancy_(C):_W₌_constant:_C_>_50%;_Y₌_accessory:_C_>_25%_and_<50%;_Z₌_accidental:_C_<_25%. b_Dominance_(D):_D₌_dominant:_D_>_5%;_A₌_accessory:_D_>_2.5%_and_<5%;_OC₌_occasional:_(D)_<_2.4%.

andC.caxiensis(capturedinallsamplingmonths),Apismellifera,X. cearensis,andPlebeiaalvarengai(capturedin11months), Callony-chiumbrasiliense(8months)andC.aenea(6months)(Table2).Of theotherspecies65.3%wereclassiﬁedasaccidentaland20.4%as accessory.

OnlyﬁvespecieswereclassiﬁedasDominant,andthey repre-sented74.7%oftheindividualscollectedbynetting,allofwhich belongedtotheApinae(A.mellifera,P.alvarengai,T.sp.gr. fulviven-tris,C.caxiensis,C.aenea,C.brasiliense,andX.cearensis)(Table3).

Thespeciesrarefactioncurveshowedatendencytoasymptote; however,itcontinuedtoincreasethroughoutthemonthsof collec-tion(Fig.2).Becauseofthenon-stabilizationoftheaccumulation curve,weusednon-parametrictotal richnessestimators,which rangedfrom89(Jackknife1)to163species (Chao1)forthe12 collectionmonthsforbothmethods(entomologicalnetsandbowl traps).Theseindices suggestthatbetween67.41% and 36.8%of thebeefaunaatthesiteweresampledusingthesetwocollection methods.

BeesinrestingaareasinnortheasternBrazil

Basedonotherstudiesconductedinthesameareausingother collectionmethods,thetotalrestingabeefaunaofthePNLM com-prises86speciesin30genera.Fromthattotal,43%ofthespecies wouldnothavebeencollectedifonlynetshadbeenused.Overall, 32specieswerecollectedonlywithnets,11specieswere exclu-sivetothebowltraps,11Euglossinispecieswerecapturedonly witharomaticbaits,12specieswerecollectedonlyonmuriciﬂower

(Table3).

Accordingtootherbeesofresearchconductedinrestingaareas of northeastern Brazil,network collectionobtained representa-tivesof50generaforseveralrestingas(Table3).Ofthesegenera morethan50%wererecordedinSalvadorand PNLM,40%were

120 110 100 90 80 70 60 50 40 30 20 nº of species Chao 1 Jack 1 Species accumulation curve 10 0 August September October NovemberDecemberJa nuar y Febr uar y March Apr il Ma y June July

Fig.2.Speciesaccumulationcurve(collectorcurve)andcurvesofspeciesrichness estimatorsChao1andJackknife1forthebeescollectedbynettingandbowltraps intherestingaofPNLM,Barreirinhas,MA,Brazil,fromAugust2009toJuly2010.

presentinAbaeté,SãoMarcosandCabedelo,andonly27%were recorded in Panaquatira. The total bee diversity is very similar amongtheseareas,withonlyPanaquatirahavingslightlylower diversity(Table3).However,differencesexistamongthe subfami-lies.ForApinae,thenumberofspeciesisthesamebetweenSalvador

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Table3

NumberofspeciespergenusofbeescollectedintherestingainnortheasternBrazil:Abaete(VianaandKleinert,2005),Salvador(Silvaetal.,2015),Cabedelo(Madeira-da-Silva andMartins,2003),S.Marcosbeach(Albuquerque,1998),Panaquatirabeach(Oliveiraetal.,2010)andPNLM(presentstudy).Sub-totalsintheﬁrstcolumnindicatethe numberofgenera;sub-totalsforeachsiteindicatethenumberofspeciesand,inbrackets,ofgenera.

Taxon Abaete/BA Salvador/BA Cabedelo/PB S.Marcos/MA Panaquatira/MA PNLM/MAnets PNLM/MA Totala ANDRENINAE Acamptopoeum 1 Oxaea 2 1 1 Protomeliturga 1 1 Callonychium 2 Sub-total(4)(3b₎ ₀₍₀₎ ₂₍₁₎ ₁₍₁₎ ₃₍₃₎ ₁₍₁₎ ₀₍₀₎ ₂₍₁₎ COLLETINAE Chilicola 1 Colletes 1 Hylaeus 2 1 Sub-total(3) 2(2) 2(1) 1(1) 0(0) 0(0) 0(0) 0(0) HALICTINAE Augochlora 2 2 2 1 1 Augochlorella 1 1 Augochloropsis 2 1 1 2 Dialictus 1 2 1 3 3 Pseudaugochlora 1 1 1 1 1 1 Sub-total(5) 6(4) 6(4) 4(3) 2(2) 1(1) 5(3) 8(5) MEGACHILINAE Dicranthidium 2 1 1 1 Epanthidium 1 1 1 Hypanthidium 1 Larocanthidium 1 Megachile 3 5 2 5 2 6 12 Saranthidium 1 1 Sub-total(6) 5(2) 6(2) 5(4) 6(2) 2(1) 8(3) 15(4) APINAE Acanthopus 1 1 Ancyloscelis 1 2 Anthophora 1 1 Apis 1 1 1 1 1 1 1 Bombus 1 1 Centris 12 13 10 7 14 10 15 Ceratina 2 1 4 4 4 5 Diadasina 1 Epicharis 2 4 1 1 1 2 Eufriesea 1 1 1 2 6 Euglossa 1 6 1 1 1 2 8 Eulaema 3 4 1 1 1 1 3 Exomalopsis 4 1 1 Florilegus 1 1 2 1 1 Frieseomellita 2 1 Melipona 2 2 Melitoma 1 Mesocheira 1 Mesonychium 1 1 1 1 1 Mesoplia 2 2 1 2 1 Nanotrigona 1 1 Odyneropsis 1 1 1 Oxytrigona 1 Partamona 1 1 1 Paratrigona 1 Paratetrapedia 1 1 1 Plebeia 1 1 2 Ptilothrix 1 Scaptotrigona 3 Tetragona 1 Tetragonisca 1 Thygater 1 Trigona 1 3 1 1 1 Trigonisca 1 1 1 2 Tropidopedia 1 Xanthopedia 1 Xylocopa 6 7 5 4 2 5 5 Sub-total(37)(35b₎ ₃₆₍₁₄₎ ₆₄₍₂₇₎ ₂₉₍₁₂₎ ₂₇₍₁₄₎ ₂₇₍₁₂₎ ₃₅₍₁₅₎ ₆₁₍₂₀₎ Total(55)(50b₎ ₄₉₍₂₂₎ ₈₀₍₃₅₎ ₄₀₍₂₁₎ ₃₈₍₂₁₎ ₃₁₍₁₅₎ ₄₈₍₂₁₎ ₈₆₍₃₀₎ a_Include_other_methods_of_sampling:_pan_traps,_chemical_baits₍_Silva_et_al.,₂₀₀₉_),_trap_nest₍_Ramos_et_al.,₂₀₀₆₎_and_murici_visitors₍_Rêgo_et_al.,₂₀₀₆_).

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1.0 SLuis_MA SJRibamar_MA Abaeté_BA Cabedelo_PB Salv ador_BA PNLM Similar ity 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2

Fig.3. DendrogramofMorisitasimilarityofthebeespeciescollectedbetweenPNLM (Barreirinhas,MA)andotherrestingaandduneareasofnortheasternBrazil:Paraíba (Madeira-da-SilvaandMartins,2003),Bahia(VianaandKleinert,2005),Salvador (Silvaetal.,2015),Panaquatira(Oliveiraetal.,2010),andSãoLuís(Albuquerque etal.,2007).

andPNLMandisslightlylessbutverysimilaramongAbaeté,São Marcos,Panaquatira,andCabedelo(Table3).TheApinaegeneric diversityofSalvador andPNLMare greaterthaninotherareas. PNLMalsohad moreMegachilinaeandHalictinaespeciesand a highergeneraldiversitythantheothersrestingaareas.SãoMarcos hadthehighestspeciﬁcandgenericspeciesrichnessof Andreni-nae,however,twospeciesofthissubfamilywerecollectedinPNLM bybowltraps.Colletinaewasalsoverypoorlyrepresentedinthe restingahabitatsofnortheasternBrazil.

Thesimilarityinthecompositionofthespeciessampledinthe restingaofPNLMandotherareasofdunesandrestingasof north-easternBrazil(Panaquatira,SãoMarcos,Cabedelo,Salvador and Abaeté)wasrelativelylow, asitwas≤44%(Fig.3).Thespecies diversity(H)forthebeecommunityofPNLMwas2.41,andthe equitabilityindex(J)was0.97.

Discussion

BeespeciesrichnessatPNLM

Similartopreviousstudies(KrugandAlves-dos-Santos,2008;

Kamkeetal.,2011;Topicetal.,2013;Moreiraetal.,2016),the

presentstudyindicatesthatusingcomplementarymethodsof col-lection,suchasbowltraps,shouldbeconsideredwhenthegoalis todeterminethespeciﬁcdiversitywithinanarea.Ifonly entomo-logicalnetshadbeenused,themostcommonlyusedmethodinbee surveysinBrazil(Pinheiro-Machadoetal.,2002,2006),then43% ofthebeespeciespresentinPNLMwouldremainunidentiﬁed.

ThenumberofbeespeciesknowntooccuratPNLMwasmore thandoubled.Thisiscertainlyduetothecombinationofdifferent methodsofcollectingbeesaswellastheincreasingofsampling hours.Whilenettingyieldedmorespeciesthantheothermethods together,itfailedforsomebeetaxalikeorchidbees.Callonychium speciesarecapturedinbowltraps,duethattheﬂowersvisitedby

thosebeeswerenotknownornotsampledbyus.Williamsetal.

(2001)calledattentiontothefactthat“rarespeciesarerarebecause

theyarenotreadilydetected”,forexampleduetothedependence ofMelissodessexcincta(Lepeletier)bypollenofTriumfetta,this com-monandwidespreadbeespeciesinBrazil,hadneverbeencollected until1993(SilveiraandGodínez,1996).

SomeMeliponini,asTrigoniscaforexample,whichareattracted bysweat,aresosmallthattheyarehardlycollectedwith entomo-logicalnets,alwaysbeingverypoorlyrepresentedinthevarious inventories.Inadditiontotheselimitationsinthemethodologies ofdatacollection,therearealsospeciesthatareoligolecticwitha lowspectrumofﬂowersvisited.Florilegus(Florilegus)cf.condignus (Cresson,1878) isoligolectic,restricting thenectarcollectionof Pontederia(Pontederiaceae)ﬂowers(Schlindwein,1998,2004).

Thespeciesrarefactioncurvedidnotcompletelystabilizeusing only thenetand bowltrapsmethods, suggestingtheexistence ofnon-sampledspecies,whichwasdemonstratedwhenwe com-paredthe speciescollectedin thesame studyareausing other samplingtechniques(Ramosetal.,2006;Rêgoetal.,2006;Silva etal.,2009).AlthoughthePNLMbeeinventorywasmuchimproved, diversityindicessuggestthatoursamplingisnotcomplete,somany morespeciesaretobeexpected.Itisofcoursedifﬁculttopredict whichspeciesarepresentbutnotyetrecorded,butitisplausibleto assumethatspeciesingeneralikeMesoplia,Mesonychium, Acamp-topoeum, Oxaea,Protomeliturga, and others,already collectedin otherrestingainnortheasternBrazil(Albuquerque,1998;

Madeira-da-SilvaandMartins,2003;VianaandKleinert,2005;Oliveiraetal.,

2010;Silvaetal.,2015)mightbepresentaswell.

Diurnalandannualactivitypattern

Thediurnalactivitytotalpatternofbeesisbimodalwithpeaks intheearlymorningandlateafternoon.Inenvironmentssuchas therestinga,hightemperaturesandlowhumidityarelimiting fac-torsforbeeactivity.Thebeesmostlikelyuseprimarilytheﬁrst andlasthoursofthedaywithlowertemperaturestoavoid heat-inducedstress(Hilárioetal., 2001;Ferreira-Júnioretal.,2010). Whenweexcludethedominantbeespecies(D),thediurnalactivity patternisaltered,beingsimilartothatobservedincoastal envi-ronmentswherethereisadecreaseinactivitythroughouttheday

(Albuquerque,1998;VianaandKleinert,2005;Oliveiraetal.,2010).

Nevertheless,beeactivityatinPNLMiscontinuous,indicatingthat ﬂowersofseveralplantspeciesremainopenthroughouttheday. Forexample,ﬂowersofB.crassifoliaremainopenforapproximately

twodays(RêgoandAlbuquerque,2006).Itiswelldocumentedthat

manybeesspeciessynchronizedtheiractivitytoperiodswhen ﬂo-ralresourcesareavailable(VianaandKleinert,2005;Oliveiraetal., 2010)andprobablythereisgreateravailabilityinthehoursthat showedgreateractivity.

Therewas a higher abundanceof bees throughout the year in PNLM during therainy period (April–August)and a greater number of species per month from June to October. A similar pattern occurredin theothers two restinga areas atMaranhão (PanaquatiraandSãoMarcos),withagreaterabundanceduring therainyseason(Oliveiraetal.,2010; Albuquerque,1998).The oppositepatternoccurredinAbaetéandCabedelo,whereahigher abundanceduringthedryseasonwasobserved(VianaandKleinert,

2005;Madeira-da-SilvaandMartins,2003).Floweringphenology

stronglyinfluencesthetemporalpatternoftheabundanceofflower visitors (Newstrom et al., 1994), and this explains the pattern observedinMaranhão(Panaquatira,SãoMarcosandPNLM),where floweringwasdependentontherainyseason.

Thehighnumberofbeescollectedduringtherainyseasonwas alsocausedbytheincreasedactivityoftheeusocialspeciesApis mellifera,Trigonafulviventris,and Plebeiaalvarengaiduringpeak ﬂowering,whichcausedthesespeciestobecomedominantinthe

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community.ThespeciesCenttriscaxiensisandXylocopacearensis werealsodominantandconstantprobablyduetotheavailability ofﬂoralresourcesinthearea.Centriscaxiensiswasamongthemost frequentvisitorsofB.crassifolia,asseenbyRêgoetal.(2006).The constancyofspeciessuchasC.caxiensis,C.aeneaandalsoX. cearen-siswerealsoobservedinotherrestingaareasinnortheasternBrazil

(Albuquerque,1998;VianaandKleinert,2005;Oliveiraetal.,2010).

AsjudgedbynettingEuglossiniwereclassiﬁedasoccasionaland accidental,butthisisamethodologicalﬂawasthehostplants vis-itedbythesebeesaremostlyunknownandthereforenotsampled. Theuseofscentbaiting,however,revealedlargepopulationsof severalspeciesoforchidbees(Silvaetal.,2009).Infact,Euglossa cordataandspeciesofEulaemaareknowntoreproducein commu-nalorprimitivelysocialmultifemalenestssothatlargenumbers ofoffspringareproduced.Megachilinaewerealsooccasionaland accidental,butagainthisisamethodologicalbias,asadifferent method(trapnesting)mayyieldmanyindividuals.

Speciesrichnessinnortheasternrestingaareas

ThePNLMbeediversity(H=2.41)wassimilartothatfoundin Cabedelo(2.45)andgreaterthanthoseatPanaquatirabeach(2.28), SãoMarcosbeach(2.05),andtheAbaetédunes(2.04).ThePielou equitabilityindexindicatedthattheindividualswereevenly dis-tributedamongthesampledspecies(LudwigandReynolds,1988), asobservedintherestingaenvironments.

IncoastalenvironmenttheApinaetypicallyexhibitthe high-estspeciesrichness(VianaandKleinert,2005;Albuquerqueetal.,

2007;Oliveiraetal.,2010;Silvaetal.,2015).However,thesmall

numberofcorbiculateApinaeinthisenvironmentappearstorelate rather tothehabitatcondition thanto latitudinal gradients,as reportedbyGonc¸alvesandMelo(2005)andBiesmeijerandSlaa

(2006).Incontrast,thenon-corbiculateApinaeexhibitedthe

high-estrichnessincoastalareas,rangingfrom49%to74%ofthesampled species(Madeira-da-SilvaandMartins,2003;VianaandKleinert,

2005;Oliveiraet al.,2010)andcorroboratingtheresultsfound

inthepresentstudy.Themoststrikingfeatureofthisinventory wasthegenusAnthophora,which wasonlycollectedwithbowl trapsandhadneverbeenpreviouslycollectedonthe15 Maran-hãobeesurveys(Rebêloetal.,2003).Thisisthefirstrecordofthis speciesinarestingaarea.Onlytwospeciesfromthisgenusoccurin Brazil,foundinthehighlandsofSãoPaulo,MinasGerais,Paranáand Brasília(UrbanandMelo,2005;Moureetal.,2012a,b).Thegenera MeliponaandPlebeiaalvarengaiandP.minimawerealsoreported forthefirsttimeinarestingaecosystem.Theabundanceofthese speciesatPNLMshowsthattheareahassometreeswithlarge cav-itiesfornestbuildingandsufficientfloralresourcesavailable.The absenceofstinglessbeeswasalsoobservedbyKamkeetal.(2011)

inarestingaatSantaCatarina,mostlikelyduetothelackorscarcity offoodplantsinaregionofyoungforestthatwasdistantfromareas withgreateravailabilityofnestingsubstrate.

FewspeciesofMegachilinae,Halictinae,andAndreninaewere recordedwiththeproceduredescribedbySakagamietal.(1967)

atPNLM,whichissimilartotheestimatesforthesesubfamilies reportedforotherrestingaandduneareasinnortheasternBrazil

(Madeira-da-Silva and Martins,2003; Vianaand Kleinert,2005;

Albuquerque et al.,2007)using the samemethodology.

Proba-blythetruerichnessofthesesubfamiliescouldbemuchhigher thanestimatediftherewascontinuityoftemporalsamplingand diversiﬁcationofmethods.Andreninaearepracticallyabsentinthe restingasofnortheasternBrazil.Althoughtherichnessof Halicti-naeandMegachilinaeissomewhatgreaterthanthatofAndreninae, itismuchlowerthaninrestingasfromsouthern Brazil(Laroca,

1974;Zanella,1991;Schwartz-FilhoandLaroca,1999;

Alves-dos-Santos,1999;Steineretal.,2010;Kamkeetal.,2011).Agradient

ofincreasingspeciesrichnessalongthenorth-southaxisbecomes

evident,whichwaspostulatedbyMichener(2000)anddiscussed

byGonc¸alvesandMelo(2005)inastudyofdiversityinParaná.

Allthesemethodsofcollectingareassociatedwithseveraltypes ofbias;forexample,somespeciesareoftennotcapturedwithnets becausetheyarefast,smallandinconspicuous,beinglessflashy thanotherslow-moving,largeandcolourfulinsects(Nielsenetal., 2011)orduetoalowspectrumofflowersvisited(oligolects)and thoseflowersare notat collectionareas.Bowltraps havebeen showntobeanefficientandunbiasedmethod,buttheycapture manyinsects,notjustbees.Therefore,ifweareinterestedinbee diversity,chemicalbaits,trapnestsandevenbowltrapsshouldall beusedasacomplementtonetcollections.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest.

Acknowledgements

We thanktheowner ofSítioBuriti, ManuelNascimento, for allowingaccessforfieldwork,andDr.GabrielMelo(Universidade FederaldoParaná–UFPR),Dr.SilviaPedro(FaculdadedeFilosofia, CiênciaseLetrasdeRibeirãoPretodaUniversidadedeSãoPaulo –FFCLRP-USP)andDr.FernandoSilveira(UniversidadeFederalde MinasGerais–UFMG)fortheidentificationofcertainbeespecies. ThisworkwasfinancedbyCNPq,project#579897/2008-7(M.Sc. grant)andFAPEMA(APP–UNIVERSAL999/09).

References

Aguiar, C.M.L., Zanella, F.C.V., 2005. Estrutura da comunidade de abelhas (Hymenoptera:Apoidea:Apiformes) deumaáreana margemdodomínio caatinga(Itatin,BA).Neotrop.Entomol.34,15–24.

Albuquerque,P.M.C.,(Ph.D.thesis)1998.Abelhassilvestres(Hymenoptera,Apoidea) esuasfontesdealimentoemumecossistemadedunas,nailhadoMaranhão, MA,Brasil:composição,fenologiaeinterações.FaculdadedeFilosofia,Ciências eLetrasdeRibeirãoPreto,RibeirãoPreto.

Albuquerque,P.M.C.,Camargo,J.M.F.,Mendonc¸a,A.C.,2007.Bee communityof abeachecosystemonMaranhãoisland,Brazil.Braz.Arch.Biol.Technol.50, 1005–1018.

Alves-dos-Santos,I.,1999.Abelhaseplantasmelíferasdamataatlântica,restingae dunasdolitoralnortedoestadodoRioGrandedoSul,Brasil.Rev.Bras.Entomol. 43,191–223.

Biesmeijer,J.C.,Slaa,E.J.,2006.ThestructureofeusocialbeeassemblagesinBrazil. Apidologie37,1–19.

Bodenheimer,F.S.,1955.Précisdécologieanimale.Payot,Paris.

CPTEC: Centro de Previsão de Tempo e Estudos Climáticos, 2010. Pro-clima, Available at: http://www6.cptec.inpe.br/proclima2/balancohidrico/ balancohidrico.shtml(accessed05.08.10).

Ferreira-Júnior,N.T.,Blochtein,B.,Moraes,J.F.,2010.Seasonalﬂightandresource collectionpatternsofcoloniesofthestinglessbeeMeliponabicolorschencki Gribodo(Apidae,Meliponini)inanAraucariaforestareainsouthernBrazil.Rev. Bras.Entomol.54,630–636.

Gazola,A.L.,Garófalo,C.A.,2009.Trap-nestingbees(Hymenoptera:Apoidea)in for-estfragmentsofthestateofSãoPaulo,Brazil.Genet.Mol.Res.8,607–622.

Gonc¸alves,R.B.,Melo,G.A.R.,2005.Acomunidadedeabelhas(Hymenoptera,Apidae s.l.)emumaárearestritadecamponaturalnoParqueEstadualdeVilaVelha, Paraná:diversidade,fenologiaefontesﬂoraisdealimento.Rev.Bras.Entomol. 49,557–571.

Gonc¸alves,R.B.,Oliveira, P.S.,2013.Preliminaryresultsofbowltrapping bees (Hymenoptera,Apoidea)inasouthernBrazilforestfragment.J.InsectBiodivers. 1,1–9.

Gottsberger,G.,Camargo,J.M.F.,Silberbauer-Gottsberger,I.,1988.Abee-pollinated tropicalcommunity:thebeachdunevegetationofIlhadeSãoLuis,Maranhão, Brazil.Bot.Jahr.Syst.109,469–500.

Grundel,R.,Frohnapple,K.J.,Jean,R.P.,Pavlovic,N.B.,2011.Effectivenessofbowl trappingandnettingforinventoryofabeecommunity.Environ.Entomol.40, 374–380,http://dx.doi.org/10.1603/EN09278.

Hammer,Ø.,Harper,D.A.T.,Ryan,P.D.,2001.PAST:paleontologicalstatistics soft-warepackageforeducationanddataanalysis.Palaeontol.Electron.4,1–9.

Hilário,S.D.,Imperatriz-Fonseca,V.L.,Kleinert-Giovannini,A.,2001.Responsesto cli-maticfactorsbyforagersofPlebeiapugnaxMoure(inlitt)(Apidae,Meliponinae). Rev.Bras.Biol.61,191–196.

Ibama–InstitutoBrasileirodoMeioAmbienteedosRecursosNaturaisRenováveis, 2003.PlanodemanejodoParqueNacionaldosLencoisMaranhenses.Ministério doMeioAmbiente,InstitutoBrasileirodoMeioAmbienteeRecursosNaturais Renováveis,SãoLuís,MA.

(9)

Kamke,R.,Zillikens,A.,Steiner,J.,2011.Speciesrichnessandseasonalityofbees (Hymenoptera,Apoidea)inarestingaareainSantaCatarina,southernBrazil. Stud.Neotrop.FaunaEnviron.46,35–48.

Köppen,W.,1948.Climatologia:conunestudiodelosclimasdelatierra.Fondode CulturaEconômica,México.

Krug,C.,Alves-dos-Santos,I.,2008.OUsodeDiferentesMétodosparaAmostragem daFaunadeAbelhas(Hymenoptera:Apoidea),umEstudoemFlorestaOmbróﬁla MistaemSantaCatarina.Neotrop.Entomol.37,265–278.

Laroca,S.J.R.,(Ph.D.thesis)1974.Estudofeno-ecológicoemApoideadoLitorale PrimeiroPlanaltoparanaense.UniversidadeFederaldoParaná,Curitiba.

Ludwig,J.A.,Reynolds,J.F.,1988.StatisticalEcology:APrimeronMethodsand Com-puting.JohnWileyandSons,Inc.

Madeira-da-Silva,M.C.,Martins,C.F.,2003.Abelhas(Hymenoptera,Apoidea Api-formes)deuma áreade restinga,Paraíba,nordestedoBrasil:abundância, diversidadeesazonalidade.Rev.Nord.Biol.17,75–90.

Maranhão,2002.AtlasdoMaranhão,2thed.Geplan/Labgeo-Uema,SãoLuís,MA.

Mcaleece,N.,Lambshead,P.J.D.,Paterson,G.L.J.,Gage,J.G.,1997.BioDiversity Pro-fessional.TheNaturalHistoryMuseumandtheScottishAssociationforMarine Sciences,London.

Michener,C.D.,2000.TheBeesoftheWorld.JohnsHopkinsUniversityPress, Balti-more.

Milet-Pinheiro,P.,Schlindwein,C.,2008.Comunidadedeabelhas(Hymenoptera, Apoidea)eplantasemumaáreadoAgrestepernambucanos,Brasil.Rev.Bras. Entomol.52,625–636.

Moreira,E.F.,Santos,R.L.S.,Penna,U.L.,Angel-Coca,A.,Oliveira,F.F.,Viana,B.F., 2016.Arepantrapscolorscomplementarytosamplecommunityofpotential pollinatorinsects?J.InsectConserv.,1–14.

Mouga,D.M.D.S.,(Ph.D.thesis)2004.Ascomunidadesdeabelhas(Hymenoptera, Apoidea)emMataAtlânticanaRegiãoNordestedoestadodeSantaCatarina, Brasil.UniversidadedeSãoPaulo,SãoPaulo.

Moure,J.S.,Urban,D.,Melo,G.A.R.(Eds.),2012a.CatalogueofBees(Hymenoptera, Apoidea) in the Neotropical Region – Online Version. , Available at:

http://www.moure.cria.org.br/catalogue(accessed26.07.16).

Moure,J.S., Urban, D., Melo, G.A.R., 2012b. AnthophoriniDahlbom, 1835. In: Moure,J.S.,Urban,D.,Melo,G.A.R.(Eds.),CatalogueofBees(Hymenoptera, Apoidea) in the Neotropical Region – Online Version. , Available at:

http://www.moure.cria.org.br/catalogue(accessed20.09.14).

Nemésio, A., Silveira, F.A., 2007. Diversity and distribution of orchid bees (Hymenoptera:Apidae)witharevisedchecklistofspecies.Neotrop.Entomol. 36,874–888.

Newstrom,L.E.,Frankie,G.W.,Baker,H.G.,1994.Anewclassiﬁcationforplant phen-ologybasedonﬂoweringpatternsinlowlandtropicalrainforesttreesatLa Selva,CostaRica.Biotropica26,141–159.

Nielsen,A.,Steffan-Dewenter,I.,Westphal,C.,Messinger,O.,Potts,S.G.,Roberts, S.P.M.,Settele,J.,Szentgyorgyi,H.,Vaissiere,B.E.,Vaitis,M.,etal.,2011.Assessing beespeciesrichnessintwoMediterraneancommunities:importanceofhabitat typeandsamplingtechniques.Ecol.Res.26,969–983.

Oliveira,F.S.,Mendonc¸a,M.W.A.,Vidigal,M.C.S.,Rêgo,M.M.C.,Albuquerque,P.M.C., 2010.Comunidadedeabelhas(Hymenoptera,Apoidea)emecossistemade dunasnaPraiadePanaquatira,SãoJosédeRibamar,Maranhão,Brasil.Rev.Bras. Entomol.54,82–90.

Pinheiro-Machado,C.,Alves-dos-Santos,I.,Imperatriz-Fonseca,V.L.,Kleinert,A.M.P., Silveira,F.A.,2002.BrazilianBeeSurveys:stateofknowledge,conservationand sustainableuse.In:Kevan,P.G.,Imperatiz-Fonseca,V.L.(Eds.),PollinatingBees: TheConservationLinkBetweenAgricultureandNature.BrazilianMinistryof Environment,Brasilia,pp.135–153.

Pinheiro-Machado,C.,Silveira,F.A.,Albuquerque,P.M.C.,Biesmeijer,J.,Campos, M.J.O.,Eardley,C.,Gemmill,B.,Griswold,T.,Kwapong,P.,DeMarco,P.,etal., 2006.Surveyingandmonitoringofpollinatorsinnaturallandscapesandin cul-tivatedﬁelds.In:Imperatriz-Fonseca,V.L.,Saraiva,A.M.,Jong,D.D.(Eds.),BeesAs

PollinatorsinBrazil:AssessingtheStatusandSuggestingBestPractices.Holos, RibeirãoPreto,pp.25–37.

Ramos, M.C.,Rêgo, M.M.C.,Albuquerque,P.C.M., 2006. Ninhos-armadilha:um método de amostragem para o conhecimento da biologiae aumento da populac¸ãodospolinizadoresdomurici.In:Rêgo,M.M.C.,Albuquerque,P.C.M. (Eds.),Polinizadoresdomurici.EDUFMA,SãoLuís,p.78.

Rebêlo,J.M.M.,Rêgo,M.M.C.,Albuquerque,P.M.C.,2003.Abelhas(Hymenoptera, Apoidea)daregiãosententrionaldoEstadodoMaranhão,Brasil.In:Melo,G.A.R., Alves-dos-Santos,I.(Eds.),ApoideaNeotropica:Homenagemaos80anosde JesusSantiagoMoure.EditoraUNESC,Criciúma,p.320.

Rêgo,M.M.C.,Albuquerque,P.M.C.,2006.RedescobertadeMeliponasubnitidaDucke (Hymenoptera:Apidae)nasRestingasdoParqueNacionaldosLenc¸ois Maran-henses,Barreirinhas,MA.Neotrop.Entomol.35(3),416–417.

Rêgo,M.,Albuquerque,P.M.C.,Ramos,M.C.,Silva,O.,Mendes,F.N.,2006. Polin-izadoresdoMurici(Byrsonimacrassifolia,Malpighiaceae)emÁreaNativa: DiversidadedeEspécies,Nidiﬁcac¸ãoeseuusosustentávelnaAgricultura.In: AnaisdoVIIEncontrosobreAbelhas,RibeirãoPreto,pp.455–462.

Sakagami,S.F.,Laroca,S.,Moure,J.S.,1967.WildbeesbiocenoticsinSãoJosédos Pinhais(PR),SouthBrazil–preliminaryreport.J.Fac.Sci.6,253–291.

Schlindwein,C.,1998.Frequentoligolectycharacterizingadiversebee-plant com-munityinaxerophyticbushlandofsubtropicalBrazil.Stud.Neotrop.Fauna Environ.33,46–59.

Schlindwein,C.,2004.Areoligolecticbeesalwaysthemosteffectivepollinators? In:Freitas,B.M.,Pereira,J.O.P.(Eds.),SolitaryBees.Conservation,Rearingand ManagementforPollination.ImprensaUniversitária,Fortaleza,pp.231–240.

Schwartz-Filho, D.L., Laroca, S., 1999. A comunidade de abelhas silvestres (Hymenoptera,Apoidea)daIlhadasCobras(Paraná,Brasil):aspectosecológicos ebiogeográﬁcos.ActaBiol.Parana.28,19–108.

Silva,D.L.B.,SilvaFilho,J.C.B.,2008.Aproblemáticadapresenc¸adepopulac¸ões res-identesemparquesnacionais.PeriódicoEletrônicoFórumAmbientaldaAlta Paulista4,1747–1752.

Silva,M.,Ramalho,M.,Aguiar,C.M.L.,Silva,M.D.,2015.Apifauna(Hymenoptera, Apoidea)emumaáreaderestingaarbórea-mataatlânticanacostaatlânticado NordestedoBrasil.Magistra27,110–121.

Silva,O.,Rêgo,M.M.C.,Albuquerque,P.M.C.,Ramos,M.C.,2009.AbelhasEuglossina (Hymenoptera:Apidae)emáreaderestingadonordestedoMaranhão.Neotrop. Entomol.38,186–196.

Silveira,F.A.,Godínez,L.M.,1996.Systematicsurveysoflocalbeefaunas.Melissa– TheMellitologist’sNewsletter9,1–4.

Silveira,F.A.,Melo,G.A.R.,Almeida,E.A.D.,2002.Abelhasbrasileiras:sistemáticae identiﬁcac¸ão.BeloHorizonte.

Silveira-Neto,S.,Nakano,O.,VilaNova,N.A.,1976.Manualdeecologiadosinsetos. Ceres,Piracicaba.

Steiner,J.,Zillikens,A.,Kamke,R.,Feja,E.P.,Falkenberg,D.B.,2010.Beesand melit-tophilousplantsofsecondaryAtlanticForesthabitatsatSantaCatarinaIsland, SouthernBrazil.Oecol.Aust.14,16–39.

Topic,J.P.,Davila,Y.C.,Wardle,G.M.,2013.Evaluationofcommonmethodsfor samp-linginvertebratepollinatorassemblages:netsamplingout-performpantraps. PLoSONE8,e66665.

Urban, D., Melo, G.A.R., 2005. Duas espécies novas de Anthophora Latreille (Hymenoptera,Apidae).Rev.Bras.Zool.22,81–83.

Viana, B.F., Kleinert, A.M.P., 2005. A community of ﬂower-visiting bees (Hymenoptera:Apoidea)inthecoastalsanddunesofnortheasternBrazil.Biota Neotrop.5,1–13.

Williams,N.M.,Minckley,R.L.,Silveira,F.A.,2001.Variationinnativebeefaunasand itsimplicationsfordetectingcommunitychanges.Conserv.Ecol.5,7.

Zanella,F.C.V.,(M.Sc.dissertation)1991.Estruturadacomunidadedeabelhas sil-vestres(Hymenoptera,Apoidea)daIlhadoMel,planícielitorâneaparanaense, SuldoBrasil.UniversidadeFederaldoParaná,Curitiba.