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Historical records of orchid bees (Apidae: Euglossini) in Belém Endemism Center: species list of 92 years sampling

Registros históricos de abelhas-das-orquídeas (Apidae: Euglossini) no Centro de Endemismo Belém: lista de espécies de 92 anos de amostragens

Abstract

The distribution of most species occurs in delimited regions with unique characteristics called “centers of endemism”. In Eastern Amazon is located the Belém Endemism Center (BEC), one of the most intensely deforested in Brazilian Amazon. Here, we show information about orchid bee assemblages based on historical records from entomological collections. For each species, we calculated occurrence frequency and dominance, and we classified them in 3 statuses: common, intermediate or rare species. Curves of observed and estimated richness were built, based on Jackknife estimator. We found 1,257 specimens from 56 species, constituting records from 1917 to 2009, and one species is a new record for BEC. Higher number of specimens and species was concentrated in a few locations and surveys increased from the 70’s. The results suggest a high richness of orchid bees in the BEC, although this scenario is far from what is expected for the entire area. The high occurrence of rare species may be related to their low representativeness in the collections, and the proximity between the areas had favored samplings. Even so, the species list and the conservation status presented here may be useful information in studies comparing past and current orchid bee fauna, and, allied to data on bees’ responses to land use changes occurred in BEC over the years, can fit as a basis for defining priority areas for conservation.

Keywords:
Amazon; scent baits; collections; Brazil; deforestation

Resumo

A distribuição da maioria das espécies ocorre em regiões delimitadas com características únicas conhecidas como “centros de endemismo”. Na Amazônia Oriental está localizado o Centro de Endemismo Belém (CEB), uma das áreas mais intensivamente desmatadas na Amazônia Brasileira. Aqui, apresentamos informações sobre assembleias de abelhas orquídeas baseadas em registros históricos de coleções entomológicas. Para cada espécie, foram calculadas a frequência de ocorrência e a dominância, classificando-as em 3 estados: espécies comuns, intermediárias ou raras. Foram geradas curvas de riqueza observada e estimada, com base no estimador Jackknife. Encontramos 1.257 espécimes de 56 espécies, constituindo registros de 1917 a 2009, e uma espécie é um novo registro no CEB. Maior número de espécimes e espécies foi concentrado em poucos locais, com intensificação nas coletas a partir dos anos70. Os resultados sugerem alta riqueza de abelhas orquídeas no CEB, embora esse cenário esteja longe do que é esperado para toda a área. A elevada ocorrência de espécies raras pode estar relacionada à baixa representatividade nas coleções e a proximidade entre as áreas favoreceu as amostragens. Mesmo assim, a lista de espécies e o estado de conservação aqui apresentados podem ser informações úteis em estudos interessados em comparar a fauna passada e atual de abelhas das orquídeas e, aliado a dados sobre as respostas das abelhas às mudanças de uso da terra ocorridas no CEB ao longo dos anos, podem servir de base para definição de áreas prioritárias para conservação.

Palavras-chave:
Amazônia; armadilhas odoríferas; coleções; Brasil; desmatamento

1. Introduction

Amazonia is the most diverse ecosystem forming a mosaic of animal and plant communities. Most species are not widely distributed across this ecosystem but occur in clearly delimited areas, separated by the major rivers, each with their own evolutionary relationships and biotic assemblages, called “centers of endemism” ( Cracraft and Prum, 1988 CRACRAFT, J. and PRUM, R.O., 1988. Patterns and processes of diversification: speciation and historical congruence in some Neotropical birds. Evolution; International Journal of Organic Evolution, vol. 42, no. 3, pp. 603-620. http://dx.doi.org/10.1111/j.1558-5646.1988.tb04164.x. PMid:28563998.
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; Haffer and Prance, 2002 HAFFER, J. and PRANCE, G.T., 2002. Impulsos climáticos da evolução na Amazônia durante o Cenozóico: sobre a teoria dos refúgios da diferenciação biótica. Estudos Avançados, vol. 16, no. 46, pp. 175-206. http://dx.doi.org/10.1590/S0103-40142002000300014.
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). At least eight major areas or endemism are recognized based on terrestrial vertebrates in Amazonia, but similar analysis using butterflies and vascular plants distributions support this pattern, indicating spatial congruence by taxa from different groups ( Hall and Harvey, 2002 HALL, J.P.W. and HARVEY, D., 2002. The phylogeography of Amazonia revisited: new evidence from riodinid butterflies. Evolution; International Journal of Organic Evolution , vol. 56, no. 7, pp. 1489-1497. http://dx.doi.org/10.1111/j.0014-3820.2002.tb01460.x. PMid:12206248.
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; Prance, 1982 PRANCE, G.T. 1982. Forest refuges: evidence from woody angiosperms. In: G.T. PRANCE, ed. Biological diversification in the tropics. New York: Columbia University Press, pp. 137-158. ). The major threats to these areas are: human population density, highways, cattle ranching, agriculture and drought, all of which increase burning, deforestation, habitat loss, and land degradation ( Gascon et al., 2001 GASCON, C., BIERREGAARD JUNIOR, R.O., LAURANCE, W.F. and RANKIN-DEMERONA, J. 2001. Deforestation and forest fragmentation in the Amazon. In: R.O. BIERREGAARD, C. GASCON, T.E. LOVEJOY and R. MESQUITA, eds. Lessons from Amazonia: the ecology and conservation of a fragmented forest. Connecticut: Yale University Press, pp. 22-30. ; Laurance et al., 2002 LAURANCE, W.F., ALBERNAZ, A.K.M., SCHROTH, G., FEARNSIDE, P.M., BERGEN, S., VENTICINQUE, E.M. and COSTA, C., 2002. Predictors of deforestation in the Brazilian Amazon. Journal of Biogeography, vol. 29, no. 5-6, pp. 737-748. http://dx.doi.org/10.1046/j.1365-2699.2002.00721.x.
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).

In the extreme eastern portion of the Amazon region is located one of the eight areas of endemism, the Belém Endemism Center (BEC) that incorporates the associated biomes east of the Tocantins River in the state of Pará and includes a greater portion in the state of Maranhão ( Silva et al., 2005 SILVA, J.M.C., RYLANDS, A.B. and FONSECA, G.A.B., 2005. The Fate of the Amazonian Areas of Endemism. Conservation Biology, vol. 19, no. 3, pp. 689-694. http://dx.doi.org/10.1111/j.1523-1739.2005.00705.x.
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). With approximately 199,000 km2 total area, this area has the longest and highest levels of forest loss in Brazilian Amazon, retaining < 20% of its original primary forest cover and under some kind of protection ( Almeida and Vieira, 2010 ALMEIDA, A.S. and VIEIRA, I.C.G., 2010. Centro de endemismo Belém: status da vegetação remanescente e desafios para a conservação da biodiversidade e restauração ecológica. Revista de Estudos Universitários, vol. 36, no. 3, pp. 95-111. ), about 10% are conservation units, and 6% are indigenous land ( Silva et al., 2005 SILVA, J.M.C., RYLANDS, A.B. and FONSECA, G.A.B., 2005. The Fate of the Amazonian Areas of Endemism. Conservation Biology, vol. 19, no. 3, pp. 689-694. http://dx.doi.org/10.1111/j.1523-1739.2005.00705.x.
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). Recent evaluations of threatened species have shown that 61% of endangered birds in the Brazilian Amazon, occur on the BEC, several taxa have the highest level of local vulnerability in this area ( Instituto Brasileiro do Meio Ambiente, 2014 INSTITUTO BRASILEIRO DO MEIO AMBIENTE – IBAMA. 2014 [viewed 17 May 2017]. Lista das espécies da fauna brasileira ameaçada de extinção [online]. Brasília: Ministério do Meio Ambiente. Available from: http://www.ibama.gov.br
http://www.ibama.gov.br ...
; Oren and Roma, 2011 OREN, D.C. and ROMA, J.C. 2011 [viewed 17 May 2017]. Composição e vulnerabilidade da avifauna da Amazônia Maranhense, Brasil. In: M.B. Martins and T.G. Oliveira, eds. Amazônia Maranhense-diversidade e conservação [online]. Belém: Museu Paraense Emílio Goeldi, pp. 221-248. Available from: https://issuu.com/museu-goeldi/docs/amazonia_maranhense/15
https://issuu.com/museu-goeldi/docs/ama...
), and there is evidence of local extinction of >40 species in part of this area ( Moura et al., 2014 MOURA, N.G., LEES, A.C., ALEIXO, A., BARLOW, J., DANTAS, S.M., FERREIRA, J., LIMA, M.F. and GARDNER, T.A., 2014. Two hundred years of local avian extinctions in Eastern Amazonia. Conservation Biology, vol. 28, no. 5, pp. 1271-1281. http://dx.doi.org/10.1111/cobi.12300. PMid:24779443.
http://dx.doi.org/10.1111/cobi.12300 ...
).

Among the insects, bees are the major group responsible for pollination of native and crop plants in the world ( Klein et al., 2007 KLEIN, A.M., VAISSIÈRE, B.E., CANE, J.H., STEFFAN-DEWENTER, I., CUNNINGHAM, S.A., KREMEN, C. and TSCHARNTKE, T., 2007. Importance of pollinators in changing landscapes for world crops. Proceedings. Biological Sciences, vol. 274, no. 1608, pp. 303-313. http://dx.doi.org/10.1098/rspb.2006.3721. PMid:17164193.
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; Michener, 2007 MICHENER, C.D. 2007. The bees of the world. 2nd ed. Baltimore: The Johns Hopkins University Press. 972 p. ). Orchid bees (Apidae, Euglossini) encompass around 250 endemic species of Neotropics ( Nemésio and Rasmussen, 2011 NEMÉSIO, A. and RASMUSSEN, C., 2011. Nomenclatural issues in the orchid bees (Hymenoptera: Apidae: Euglossina) and an updated catalogue. Zootaxa, vol. 42, no. 1, pp. 1-42. ) and are the main pollinators of orchids and closely related with certain angiosperm families ( Ackerman, 1989 ACKERMAN, J.D., 1989. Geographic and seasonal variation in fragrance choices and preferences of male euglossine bees. Biotropica, vol. 21, no. 4, pp. 340-347. http://dx.doi.org/10.2307/2388284.
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; Roubik, 1989 ROUBIK, D.W. 1989. Ecology and natural history of tropical bees. Cambridge: Cambridge University Press. 514 p. http://dx.doi.org/10.1017/CBO9780511574641.
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; Roubik and Hanson, 2004 ROUBIK, D.W. and HANSON, P.E. 2004. Orchid bees of tropical America: biology and field guide. 1st ed. San José: INBio. 352 p. ). Some orchid bee species show sensitivity to environmental changes, suggesting that climatic regimes may influence the species distribution patterns of the group ( Nemésio and Vasconcelos, 2013 NEMÉSIO, A. and VASCONCELOS, H.L., 2013. Beta diversity of orchid bees in a tropical biodiversity hotspot. Biodiversity and Conservation, vol. 22, no. 8, pp. 1647-1661. http://dx.doi.org/10.1007/s10531-013-0500-x.
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). Even the habitat loss and fragmentation ( Brosi, 2009 BROSI, B.J., 2009. The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biological Conservation, vol. 142, no. 2, pp. 414-423. http://dx.doi.org/10.1016/j.biocon.2008.11.003.
http://dx.doi.org/10.1016/j.biocon.2008...
; Nemésio, 2013 NEMÉSIO, A., 2013. Are orchid bees at risk? First comparative survey suggests declining populations of forest-dependent species. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 73, no. 2, pp. 367-374. http://dx.doi.org/10.1590/S1519-69842013000200017. PMid:23917564.
http://dx.doi.org/10.1590/S1519-6984201...
; Nemésio et al., 2016 NEMÉSIO, A., SILVA, D.P., NABOUT, J.C. and VARELA, S., 2016. Effects of climate change and habitat loss on a forest-dependent bee species in a tropical fragmented landscape. Insect Conservation and Diversity, vol. 9, no. 2, pp. 149-160. http://dx.doi.org/10.1111/icad.12154.
http://dx.doi.org/10.1111/icad.12154 ...
), and the multiple land use types have altered species composition and induced a decline on richness and abundance from disturbed to preserved habitats ( Solar et al., 2015 SOLAR, R.R., BARLOW, J., FERREIRA, J., BERENGUER, E., LEES, A.C., THOMSON, J.R., LOUZADA, J., MAUÉS, M., MOURA, N.G., OLIVEIRA, V.H., CHAUL, J.C., SCHOEREDER, J.H., VIEIRA, I.C., MAC NALLY, R. and GARDNER, T.A., 2015. How pervasive is biotic homogenization in human-modified tropical forest landscapes? Ecology Letters, vol. 18, no. 10, pp. 1108-1118. http://dx.doi.org/10.1111/ele.12494. PMid:26299405.
http://dx.doi.org/10.1111/ele.12494 ...
; Brito et al., 2017 BRITO, T.F., PHIFER, C.C., KNOWLTON, J.L., FISER, C.M., BECKER, N.M., BARROS, F.C., CONTRERA, F.A.L., MAUÉS, M.M., JUEN, L., MONTAG, L.F.A., WEBSTER, C.R., FLASPOHLER, D.J., SANTOS, M.P.D. and SILVA, D.P., 2017. Forest reserves and riparian corridors help maintain orchid bee (Hymenoptera: Euglossini) communities in oil palm plantations in Brazil. Apidologie, vol. 48, no. 5, pp. 575-587. http://dx.doi.org/10.1007/s13592-017-0500-z.
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). Because of these particular characteristics, these bees have been highlighted as a key group of ecological disturbance indicator group.

Given the fast and historical land use changes in the BEC, recover information about species diversity of this unique area is fundamental to understanding the functioning of the systems and generate basis for studies addressing the effects of landscape changes on animal communities, which may be used as tools for restoration of degraded areas, and for identification of priority areas for conservation. Thus, in this paper we used orchid bee as a main group to provide data of abundance, richness and species composition from Belém Endemism Center, based on historical records of samples deposited in entomological collections. In addition to a species list occurring in the region, we provide an indication of the conservation status of the species based on data of frequency and dominance from each orchid bee species.

2. Material and Methods

2.1. Data collection

We have compiled euglossine bee information from surveys carried out in 27 of the 149 municipalities (sites) that are part of the Belém Endemism Center (BEC) ( Figure 1 ). The specimens are deposited in the Museu Paraense Emílio Goeldi (MPEG), Embrapa Amazônia Oriental (Embrapa CPATU), Instituto Nacional de Pesquisas da Amazônia (INPA), Kansas University Bee Collection (KUBC), United States National Museum of Natural History-Smithsonian Institution (USNM), Coleção Entomológica do Instituto Oswaldo Cruz (CEIOC), Coleção de Abelhas da Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto-Coleção Camargo (FFCL), and Departamento de Zoologia da Universidade Federal do Paraná-Coleção Pe. Jesus S. Moure (DZUP). These databases constitute records dating from 1917 to 2009 totalizing 92 years record. As this period, BEC had some municipalities today separated into two unities (i.e. part of Benevides is now the municipality of Santa Bárbara), the data on which the labels contained the locality “Santa Bárbara” we consider that the samples are from the new municipality. The cases of inaccuracy on the sample location, especially old records with reference only to the country or state, and specimens collected in islands were not included in our results. We also excluded the specimens with identification only to gender, since here we aim to approach the species found in this region. Taxonomic decisions were based on Moure’s Bee Catalogue ( Moure et al. 2012 MOURE, J.S., MELO, G.A.R. and FARIA JUNIOR, L.R.R. 2012 [viewed 17 May 2017]. Euglossini Latreille, 1802. In: J.S. MOURE, D. URBAN and G.R.A. MELO, orgs. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region [online]. Available from: http://www.moure.cria.org.br/catalogue
http://www.moure.cria.org.br/catalogue ...
).

Figure 1
Sampling sites of orchid bees (Apidae: Euglossini) from surveys carried out from 1917 to 2009 in Belém Endemism Center, eastern Amazon, Brazil.

2.2. Data analysis

For each registered species was calculated occurrence frequency (FO) and dominance (D), following what has been proposed by Palma (1975) PALMA, S.G. 1975. Contribuición al studio de los Sifonoforos encontrados frente a la costa de Valparaiso: aspectos ecológicos. In: Memorias del Segundo Simposio Latinoamericano de Oceanografia Biológica, 24-28 Noviembre 1975, Cumaná, Venezuela. Venezuela: University de Oriente. pp. 119-133. and adapted by Aguiar and Gaglianone (2008) AGUIAR, W.M. and GAGLIANONE, M.C., 2008. Comunidade de Abelhas Euglossina (Hymenoptera: Apidae) em Remanescentes de Mata Estacional Semidecidual sobre Tabuleiro no Estado do Rio de Janeiro. Neotropical Entomology, vol. 37, no. 2, pp. 118-125. http://dx.doi.org/10.1590/S1519-566X2008000200002. PMid:18506288.
http://dx.doi.org/10.1590/S1519-566X200...
. For FO calculation, we adopted as samples the number of municipalities where the species was found (FO = (number of municipalities containing the species x / total number of municipalities) x 100). For FO values > 50%, the species was considered very frequent; if 50% > FO > 25% it was considered frequent species; and FO < 25%, it was considered less frequent. The dominance values (D = (species abundance x / Total abundance) x 100) above 5% the species was named as dominant; if 5% > D >2.5% it was considered incidental; and D < 2.5% it was said occasional. These indexes when grouped can be used to classify the species into three categories: common species, intermediate and rare species.

We calculated estimator of species richness based on first-order Jackknife on EstimateS Win9.10 software ( Colwell, 2013 COLWELL, R.K., 2013. EstimateS: statistical estimation of species richness and shared species from samples. Version 9. Connecticut: UConn. ), using the sites as samples, and built a curve of observed and estimated richness.

3. Results

During our research, we found 1,257 specimens of 56 species, belonging to the five genera of orchid bees ( Table 1 ). In 92 years of collecting data in the Belém Endemism Center, approximately 43.20% of specimens were from Eulaema genus, followed by Euglossa (41.37%), Eufriesea (7.80%), Exaerete (6.36%) and Aglae (1.27%).

Table 1
Composition, number of specimens recorded, frequency of occurrence (FO), dominance (D) and category (CAT) of orchid bees from entomological collections, with occurrence in the municipalities of Belém Endemism Center, eastern Amazon, Brazil. CAT codes: Rare = species classified as less frequent and occasional, Common = species very frequent or frequent and dominant, and Inter = Intermediate, species classified as frequent and incidental, frequent and occasional, or frequent and incidental.

The most representative species were Eulaema cingulata (Fabricius, 1804) (16.31% of total records), followed by E. meriana Olivier, 1789 (10.02%) and E. nigrita Lepeletier, 1841 (8.27%), all classified as common species. Moreover, Eufriesea convexa Friese, 1899; E. flaviventris Friese, 1899; E. laniventris Ducke, 1902; Euglossa aff. mixta Friese, 1899; E. bidentataDressler, 1982 DRESSLER, R.L., 1982c. New species of Euglossa. IV. The cordata and purpurea species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 141-150. ; E. cognata Moure, 1970; E. ioprosopaDressler, 1982 DRESSLER, R.L., 1982c. New species of Euglossa. IV. The cordata and purpurea species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 141-150. ; E. laevicinctaDressler, 1982 DRESSLER, R.L., 1982c. New species of Euglossa. IV. The cordata and purpurea species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 141-150. ; E. liopodaDressler, 1982 DRESSLER, R.L., 1982c. New species of Euglossa. IV. The cordata and purpurea species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 141-150. ; E. polita Ducke, 1902; E. viridifronsDressler, 1982 DRESSLER, R.L., 1982c. New species of Euglossa. IV. The cordata and purpurea species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 141-150. ; Eulaema tenuifasciata Friese, 1925 and Exaerete frontalis Guérin, 1844 showed low number of specimens, responding together of about 1%, and are here classified as rare species ( Table 1 ).

Regarding the sites that have been sampled since 1917, we found a high number of specimens and species concentrated in a few localities. Approximately 48% of all specimens deposited in the collections are samples from Belém city and its surroundings (47 species), followed by the municipalities of Benevides (38 species; 27.29% of total specimens) and Tomé-Açú (18 species; 15.19% of total specimens) ( Figure 2 ). During the first 40 years of orchid bee records in BEC, there were few samples deposited in all collections. However, there was a significant increase of specimens from surveys in the 70s, but especially at the beginning of the current century, corresponding to about 50.27% of total records ( Figure 3 A). Accumulation curve of species sampled in BEC is lower than estimated richness based on first-order Jackknife ( Figure 3 B).

Figure 2
(A) Number of specimens and (B) species of orchid bees recorded in 27 localities from Belém Endemism Center, eastern Amazon, Brazil. Localities codes: ACA=Acará, ANA=Ananindeua, BAR=Barcarena, BEL=Belém, BEM=Benevides, BRA=Bragança, BR-BEL=BR Belém-Brasília, BUJ=Bujaru, BUR=Buriticupu, CPN=Capanema, CPÇ=Capitão Poço, CAS=Castanhal, IMP=Imperatriz, IPX=Ipixuna, MOJ=Moju, PGM=Paragominas, PXB=Peixe Boi, STB=Santa Bárbara, STI=Santa Inês, SIP=Santa Isabel do Pará, STN=Santarém Novo, SCO=São Caetano de Odivelas, SJP=São João de Pirabas, SMG=São Miguel do Guamá, TOM=Tomé-Açu, VIG=Vigia, ZDC=Zé Doca.
Figure 3
(A) Total number of specimens and species of orchid bees recorded in 92 years of sampling data, and (B) cumulative curves of estimated and observed species in the Belém Endemism Center, eastern Amazon, Brazil.

We checked the species distribution recorded in our research with information available on the literature for Neotropical region ( Dressler, 1982a DRESSLER, R.L., 1982a. New species of Euglossa. II. (Hymenoptera: Apidae). Revista de Biología Tropical, vol. 30, no. 2, pp. 121-129. , b DRESSLER, R.L., 1982b. New species of Euglossa. III. The bursigera species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 131-140. , c DRESSLER, R.L., 1982c. New species of Euglossa. IV. The cordata and purpurea species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 141-150. ; Hinojosa-Díaz and Engel, 2014 HINOJOSA-DÍAZ, I.A. and ENGEL, M., 2014. Revision of the orchid bee subgenus Euglossella (Hymenoptera: Apidae), Part II: The viridis and mandibularis species groups. Journal of Melittology , vol. 26, no. 36, pp. 1-108. http://dx.doi.org/10.17161/jom.v0i36.4777.
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; Oliveira, 2006, OLIVEIRA, M.L., 2006. Três novas espécies de abelhas da Amazônia pertencentes ao gênero Eulaema (Hymenoptera: Apidae: Euglossini). Acta Amazonica, vol. 36, no. 1, pp. 121-128. http://dx.doi.org/10.1590/S0044-59672006000100015.
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2007 OLIVEIRA, M.L., 2007. Catálogo comentado das espécies de abelhas do gênero Eulaema Lepeletier, 1841 (Hymenoptera: Apidae). Lundiana, vol. 8, no. 2, pp. 113-136. ; Ramírez et al., 2002, RAMÍREZ, S., DRESSLER, R.L. and OSPINA, M., 2002. Abejas euglosinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notas sobre su biología. Biota Colombiana, vol. 3, no. 1, pp. 7-118. 2015 RAMÍREZ, S.R., HERNÁNDEZ, C., LINK, A. and LÓPEZ-URIBE, M.M., 2015. Seasonal cycles, phylogenetic assembly, and functional diversity of orchid bee communities. Ecology and Evolution, vol. 5, no. 9, pp. 1896-1907. http://dx.doi.org/10.1002/ece3.1466. PMid:26140205.
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), Brazilian Amazon ( Nemésio and Morato, 2004, NEMÉSIO, A. and MORATO, E.F., 2004. Euglossina (Hymenoptera: Apidae) of the Humaitá Reserve, Acre state, Brazilian Amazon, with comments on bait trap efficiency. Revista Tecnologia e Ambiente, vol. 10, pp. 71-80. 2006 NEMÉSIO, A. and MORATO, E.F., 2006. The orchid-bee fauna (Hymenoptera: Apidae) of Acre state (northwestern Brazil) and a re-evaluation of euglossine bait-trapping. Lundiana, vol. 7, no. 1, pp. 59-64. ; Nemésio, 2005 NEMÉSIO, A., 2005. Orchid bees (Hymenoptera: Apidae) of Ilha de Maracá, Roraima, northern Brazil. Lundiana, vol. 6, no. 2, pp. 117-119. ; Oliveira and Campos, 1995 OLIVEIRA, M.L. and CAMPOS, L.A.O., 1995. Abundância, riqueza e diversidade de abelhas Euglossinae (Hymenoptera, Apidae) em florestas contínuas de terra firme na Amazônia Central, Brasil. Revista Brasileira de Zoologia, vol. 12, no. 3, pp. 547-556. http://dx.doi.org/10.1590/S0101-81751995000300009.
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; Oliveira and Nemésio, 2003 OLIVEIRA, M.L. and NEMÉSIO, A., 2003. Exaerete lepeletieri (Hymenoptera: Apidae: Apini: Euglossina): A new cleptoparasitic bee from Amazonia. Lundiana , vol. 4, no. 2, pp. 117-120. ; Santos-Júnior et al., 2014 SANTOS-JÚNIOR, J.E., FERRARI, R.R. and NEMÉSIO, A., 2014. The orchid-bee fauna (Hymenoptera: Apidae) of a forest remnant in the southern portion of the Brazilian Amazon. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 74, no. 3, suppl. 1, pp. S184-S190. http://dx.doi.org/10.1590/1519-6984.25712. PMid:25627384.
http://dx.doi.org/10.1590/1519-6984.257...
; Storck-Tonon et al., 2009, STORCK-TONON, D., MORATO, E.F. and OLIVEIRA, M.L., 2009. Fauna de Euglossina (Hymenoptera: Apidae) da Amazônia Sul-Ocidental, Acre, Brasil. Acta Amazonica , vol. 39, no. 3, pp. 693-706. http://dx.doi.org/10.1590/S0044-59672009000300026.
http://dx.doi.org/10.1590/S0044-5967200...
2011 STORCK-TONON, D., SILVA, M.V. and MORATO, E.F., 2011. Checklist of orchid bees (Hymenoptera: Apidae) of “Lago do Silêncio” area, Boca do Acre, Amazonas, Brazil. Check List, vol. 7, no. 5, pp. 648-651. http://dx.doi.org/10.15560/7.5.648.
http://dx.doi.org/10.15560/7.5.648 ...
, 2013); Atlantic Forest and Cerrado ( Nemésio, 2009, NEMÉSIO, A., 2009. Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa, vol. 2041, pp. 1-242. 2010 NEMÉSIO, A., 2010. The orchid-bee fauna (Hymenoptera: Apidae) of a forest remnant in northeastern Brazil, with geographic records and an identification key to the known species of the Atlantic Forest of northeastern Brazil. Zootaxa, vol. 2656, pp. 55-66. , 2012b NEMÉSIO, A., 2012b. The western limits of the “Hileia Baiana” for orchid bees, including seven new records for the state of Minas Gerais, eastern Brazil (Hymenoptera, Apidae, Euglossina). Spixiana, vol. 35, no. 1, pp. 109-116. ; Nemésio and Silveira, 2007, NEMÉSIO, A. and SILVEIRA, F.A., 2007. Diversity and distribution of orchid bees (Hymenoptera: Apidae) with a revised checklist of species. Neotropical Entomology , vol. 36, no. 6, pp. 874-888. http://dx.doi.org/10.1590/S1519-566X2007000600008. PMid:18246261.
http://dx.doi.org/10.1590/S1519-566X200...
2010 NEMÉSIO, A. and SILVEIRA, F.A., 2010. Forest Fragments with larger core areas better sustain diverse orchid bee faunas (Hymenoptera: Apidae: Euglossina). Neotropical Entomology, vol. 39, no. 4, pp. 555-561. http://dx.doi.org/10.1590/S1519-566X2010000400014. PMid:20877991.
http://dx.doi.org/10.1590/S1519-566X201...
; Nemésio and Faria-Junior, 2004 NEMÉSIO, A. and FARIA-JUNIOR, L.R.R., 2004. First assessment of orchid bee fauna (Hymenoptera: Apidae: Apini: Euglossina) of Parque Estadual do Rio Preto, a cerrado area in southeastern Brazil. Lundiana, vol. 5, pp. 113-117. ; Oliveira-Junior et al., 2015 OLIVEIRA-JUNIOR, J.M.B., ALMEIDA, S.M., RODRIGUES, L., SILVÉRIO JÚNIOR, A.J. and ANJOS-SILVA, E.J., 2015. Orchid Bees (Apidae: Euglossini) in a forest fragment in the Ecotone Cerrado-Amazonian Forest, Brazil. Acta Biologica Colombiana , vol. 20, no. 3, pp. 67-78. http://dx.doi.org/10.15446/abc.v20n3.41122.
http://dx.doi.org/10.15446/abc.v20n3.41...
; Silva, 2012 SILVA, F.S., 2012. Orchid bee (Hymenoptera: Apidae) community from a gallery forest in the Brazilian Cerrado. Revista de Biología Tropical, vol. 60, no. 2, pp. 625-633. http://dx.doi.org/10.15517/rbt.v60i2.3949. PMid:23894934.
http://dx.doi.org/10.15517/rbt.v60i2.39...
); and current studies carried out on the states of Pará and Maranhão ( Antonini et al., 2017 ANTONINI, Y., MACHADO, C.B., GALETTI JUNIOR, P.M., OLIVEIRA, M., DIRZO, R. and FERNANDES, G.W., 2017. Patterns of orchid bee species diversity and turnover among forested plateaus of central Amazonia. PLoS One, vol. 12, no. 4, pp. e0175884. http://dx.doi.org/10.1371/journal.pone.0175884. PMid:28410432.
http://dx.doi.org/10.1371/journal.pone....
; Brito et al., 2017 BRITO, T.F., PHIFER, C.C., KNOWLTON, J.L., FISER, C.M., BECKER, N.M., BARROS, F.C., CONTRERA, F.A.L., MAUÉS, M.M., JUEN, L., MONTAG, L.F.A., WEBSTER, C.R., FLASPOHLER, D.J., SANTOS, M.P.D. and SILVA, D.P., 2017. Forest reserves and riparian corridors help maintain orchid bee (Hymenoptera: Euglossini) communities in oil palm plantations in Brazil. Apidologie, vol. 48, no. 5, pp. 575-587. http://dx.doi.org/10.1007/s13592-017-0500-z.
http://dx.doi.org/10.1007/s13592-017-05...
; Brito and Rêgo, 2001 BRITO, C.M.S. and RÊGO, M.M.C., 2001. Community of male Euglossini Bees (Hymenoptera: Apidae) in a secondary forest, Alcântara, MA, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 61, no. 4, pp. 631-638. http://dx.doi.org/10.1590/S1519-69842001000400012. PMid:12071319.
http://dx.doi.org/10.1590/S1519-6984200...
; Maués et al., 2008 MAUÉS, M.M., OLIVEIRA, P.E.A.M. and KANASHIRO, M., 2008. Pollination biology in Jacaranda copaia (Aubl.) D. Don. (Bignoniaceae) at the “Floresta Nacional do Tapajós”, Central Amazon, Brazil. Revista Brasileira de Botanica. Brazilian Journal of Botany, vol. 31, no. 3, pp. 517-527. http://dx.doi.org/10.1590/S0100-84042008000300015.
http://dx.doi.org/10.1590/S0100-8404200...
; Rebêlo and Cabral, 1997 REBÊLO, J.M.M. and CABRAL, A.J.M., 1997. Abelhas Euglossine de Barreirinhas, zona do litoral da baixada oriental maranhense. Acta Amazonica, vol. 27, no. 2, pp. 145-152. http://dx.doi.org/10.1590/1809-43921997272152.
http://dx.doi.org/10.1590/1809-43921997...
; Silva and Rebêlo, 1999, SILVA, F.S. and REBÊLO, J.M.M., 1999. Euglossine bees (Hymenoptera: Apidae) of Buriticupu, Amazonia of Maranhão, Brazil. Acta Amazonica, vol. 29, no. 4, pp. 587-599. http://dx.doi.org/10.1590/1809-43921999294599.
http://dx.doi.org/10.1590/1809-43921999...
2002 SILVA, F.S. and REBÊLO, J.M.M., 2002. Population dynamics of Euglossinae bees (Hymenoptera, Apidae) in an early second-growth forest of Cajual Island, in the State of Maranhão, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia , vol. 62, no. 1, pp. 15-23. http://dx.doi.org/10.1590/S1519-69842002000100003. PMid:12185914.
http://dx.doi.org/10.1590/S1519-6984200...
; Solar et al., 2016 SOLAR, R.R.C., CHAUL, J.C.M., MAUÉS, M. and SCHOEREDER, J.H., 2016. A quantitative baseline of ants and orchid bees in human-modified Amazonian landscapes in Paragominas, Pará, Brazil. Sociobiology, vol. 63, no. 3, pp. 925-940. http://dx.doi.org/10.13102/sociobiology.v63i3.1052.
http://dx.doi.org/10.13102/sociobiology...
).

We found one species with new record for BEC. In Brazil, Euglossa prasinaDressler, 1982 DRESSLER, R.L., 1982c. New species of Euglossa. IV. The cordata and purpurea species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 141-150. is recognized as occurring on Amazon basin and Southwestern Amazon ( Dressler, 1982b DRESSLER, R.L., 1982b. New species of Euglossa. III. The bursigera species group (Hymenoptera: Apidae). Revista de Biología Tropical , vol. 30, no. 2, pp. 131-140. ; Nemésio, 2009 NEMÉSIO, A., 2009. Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa, vol. 2041, pp. 1-242. ; Nemésio and Morato, 2004 NEMÉSIO, A. and MORATO, E.F., 2004. Euglossina (Hymenoptera: Apidae) of the Humaitá Reserve, Acre state, Brazilian Amazon, with comments on bait trap efficiency. Revista Tecnologia e Ambiente, vol. 10, pp. 71-80. ; Oliveira and Campos, 1995 OLIVEIRA, M.L. and CAMPOS, L.A.O., 1995. Abundância, riqueza e diversidade de abelhas Euglossinae (Hymenoptera, Apidae) em florestas contínuas de terra firme na Amazônia Central, Brasil. Revista Brasileira de Zoologia, vol. 12, no. 3, pp. 547-556. http://dx.doi.org/10.1590/S0101-81751995000300009.
http://dx.doi.org/10.1590/S0101-8175199...
; Storck-Tonon et al., 2013 STORCK-TONON, D., MORATO, E.F., MELO, A.W.F. and OLIVEIRA, M.L., 2013. Orchid bees of forest fragments in Southwestern Amazonia. Biota Neotropica, vol. 13, no. 1, pp. 133-141. http://dx.doi.org/10.1590/S1676-06032013000100015.
http://dx.doi.org/10.1590/S1676-0603201...
), and there is only one recent record in the municipality of Oriximiná, Pará, located on Central Amazonia ( Antonini et al., 2017 ANTONINI, Y., MACHADO, C.B., GALETTI JUNIOR, P.M., OLIVEIRA, M., DIRZO, R. and FERNANDES, G.W., 2017. Patterns of orchid bee species diversity and turnover among forested plateaus of central Amazonia. PLoS One, vol. 12, no. 4, pp. e0175884. http://dx.doi.org/10.1371/journal.pone.0175884. PMid:28410432.
http://dx.doi.org/10.1371/journal.pone....
).

4. Discussion

The results of this study suggest a high richness of orchid bees in the Belém Endemism Center and the occurrence of a high number of rare species, based on data from biological collections and whose specimens were collected in years prior to 2009. Nevertheless, the number of species sampled in BEC is far from what is expected to be recorded, since the species accumulation curves never plateaued, indicating that the communities are under-sampled in the entire area. Moreover, the concentration of most records in few locations may have occurred both due to the proximity of these areas, especially Belém and Benevides (which are less than 30 km away from each other), but also because of the proximity of the sampled sites to cities, which promoted easy access to research institutions and their partners, increasing sampling efforts carried out in these areas.

The number of published studies showing the species composition of orchid bee fauna in the states of Pará and Maranhão is still less significant ( Brito and Rêgo, 2001 BRITO, C.M.S. and RÊGO, M.M.C., 2001. Community of male Euglossini Bees (Hymenoptera: Apidae) in a secondary forest, Alcântara, MA, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 61, no. 4, pp. 631-638. http://dx.doi.org/10.1590/S1519-69842001000400012. PMid:12071319.
http://dx.doi.org/10.1590/S1519-6984200...
; Silva and Rebêlo, 1999 SILVA, F.S. and REBÊLO, J.M.M., 1999. Euglossine bees (Hymenoptera: Apidae) of Buriticupu, Amazonia of Maranhão, Brazil. Acta Amazonica, vol. 29, no. 4, pp. 587-599. http://dx.doi.org/10.1590/1809-43921999294599.
http://dx.doi.org/10.1590/1809-43921999...
) and most of them are small inventories carried out in very specific localities ( Maués et al., 2012 MAUÉS, M.M., MOURA, T.S.A., NASCIMENTO, I.M., MARTINS, M.B. and MOURÃO JUNIOR, M. 2012. Inventário estratificado da comunidade de machos de abelhas-das-orquídeas (Apidae, Euglossina) na Flona do Tapajós, Belterra, PA. In: Anais do 5° Seminário Científico do PPBio Amazônia Oriental [online]. 08-12 Julho 2012, Macapá, Amapá, Brasil. Campinas: AINFO/CNPTIA. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/103448/1/6764.pdf
http://ainfo.cnptia.embrapa.br/digital/...
; Moura et al., 2011 MOURA, T.S.A., MAUÉS, M.M., SOUSA, J.T.A. and SANTOS, A.C.S. 2011. Biomonitoramento de abelhas euglossina (Apidae, Hymenoptera) em um SAF com castanheira-do-brasil (Bertholletia excelsa Bonpl., Lecythidaceae) em Tomé-Açu, Pará. In: Anais do 15° Seminário de Iniciação Científica da Embrapa Amazônia Oriental. Embrapa Amazônia Oriental, 24-25 Agosto 2011, Belém, Pará, Brasil. Brasília: Embrapa. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/41283/1/Res-Exp-SeminrioPIBIC2011-FINAL-JUL2011-TALYANNE-MOURA.pdf
http://ainfo.cnptia.embrapa.br/digital/...
; Santos et al., 2011 SANTOS, T.F., MAUÉS, M.M., FIGUEIREDO, D.M. and MOURA, T.S.A. 2011. Biomonitoramento de abelhas da subtribo Euglossina (Hymenoptera: Apoidea) em um plantio de castanheira-do-brasil (Bertholletia excelsa Bonpl., Lecythidaceae) em Belém, Pará. In: Anais do 15° Seminário de Iniciação Científica da Embrapa Amazônia Oriental [online]. 24-25 Agosto 2011, Belém, Pará, Brasil. Brasília: Embrapa. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/41350/1/Resumo-Pibic-2011-CORRIGIDO.pdf
http://ainfo.cnptia.embrapa.br/digital/...
; Pereira et al., 2014 PEREIRA, S.V.S., COSTA, T.S.M. and MAUÉS, M.M. 2014 [viewed 17 May 2017]. Abelhas Euglossina (Apidae, Hymenoptera) coletadas em armadilhas aromáticas em plantio de castanheira-do-brasil (Bertholletia excelsa Bonpl.) em Tomé-Açu/PA. In: Anais do 20º Congresso Brasileiro de Apicultura e 6º Congresso Brasileiro de Meliponicultura, 5-8 Novembro 2014, Belém, Pará, Brasil. Brasília: Embrapa. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/118864/1/Conbrapi-p33.pdf
http://ainfo.cnptia.embrapa.br/digital/...
; Taniguchi et al., 2012 TANIGUCHI, T., MAUÉS, M.M. and MOURA, T.S.A. 2012 [viewed 17 May 2017]. Riqueza de espécies de abelhas euglossina (Hymenoptera, Apidae) em dois fragmentos florestais inseridos no arco do desmatamento amazônico, Estado do Pará. In: Anais do 16° Seminário de Iniciação Científica da Embrapa. Embrapa Amazônia Oriental [online]. 16-17 Agosto 2012, Belém, Pará, Brasil. Brasília: Embrapa. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/76571/1/Mariana-Taniguchi.pdf
http://ainfo.cnptia.embrapa.br/digital/...
). Although recent studies have been taken on the state of Pará, addressing the effects of land use, isolation and climate changes on orchid bee assemblages, they are concentrated in the southeast and western of the state of Pará, outside of the BEC domain ( Antonini et al., 2017 ANTONINI, Y., MACHADO, C.B., GALETTI JUNIOR, P.M., OLIVEIRA, M., DIRZO, R. and FERNANDES, G.W., 2017. Patterns of orchid bee species diversity and turnover among forested plateaus of central Amazonia. PLoS One, vol. 12, no. 4, pp. e0175884. http://dx.doi.org/10.1371/journal.pone.0175884. PMid:28410432.
http://dx.doi.org/10.1371/journal.pone....
; Brito et al., 2017 BRITO, T.F., PHIFER, C.C., KNOWLTON, J.L., FISER, C.M., BECKER, N.M., BARROS, F.C., CONTRERA, F.A.L., MAUÉS, M.M., JUEN, L., MONTAG, L.F.A., WEBSTER, C.R., FLASPOHLER, D.J., SANTOS, M.P.D. and SILVA, D.P., 2017. Forest reserves and riparian corridors help maintain orchid bee (Hymenoptera: Euglossini) communities in oil palm plantations in Brazil. Apidologie, vol. 48, no. 5, pp. 575-587. http://dx.doi.org/10.1007/s13592-017-0500-z.
http://dx.doi.org/10.1007/s13592-017-05...
; Solar et al., 2016 SOLAR, R.R.C., CHAUL, J.C.M., MAUÉS, M. and SCHOEREDER, J.H., 2016. A quantitative baseline of ants and orchid bees in human-modified Amazonian landscapes in Paragominas, Pará, Brazil. Sociobiology, vol. 63, no. 3, pp. 925-940. http://dx.doi.org/10.13102/sociobiology.v63i3.1052.
http://dx.doi.org/10.13102/sociobiology...
), and ours is the first to addresses the rescue of historical records of these bees in the area.

Eulaema cingulata, E. meriana and E. nigrita are the species that stand out in inventories and monitoring samplings of the orchid bee fauna carried out in the Amazon ( Nemésio, 2005 NEMÉSIO, A., 2005. Orchid bees (Hymenoptera: Apidae) of Ilha de Maracá, Roraima, northern Brazil. Lundiana, vol. 6, no. 2, pp. 117-119. ; Storck-Tonon et al., 2013 STORCK-TONON, D., MORATO, E.F., MELO, A.W.F. and OLIVEIRA, M.L., 2013. Orchid bees of forest fragments in Southwestern Amazonia. Biota Neotropica, vol. 13, no. 1, pp. 133-141. http://dx.doi.org/10.1590/S1676-06032013000100015.
http://dx.doi.org/10.1590/S1676-0603201...
), and the latter one also appears in high abundance in other Brazilian forest areas, such as Atlantic Forest and Cerrado ( Oliveira et al., 2015 OLIVEIRA, R., PINTO, C.E. and SCHLINDWEIN, C., 2015. Two common species dominate the species-rich Euglossine bee fauna of an Atlantic Rainforest remnant in Pernambuco, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 4, suppl. 1, pp. S1-S8. http://dx.doi.org/10.1590/1519-6984.18513. PMid:26602351.
http://dx.doi.org/10.1590/1519-6984.185...
; Pires et al., 2013 PIRES, E.P., MORGADO, L.N., SOUZA, B., CARVALHO, C.F. and NEMÉSIO, A., 2013. Community of orchid bees (Hymenoptera: Apidae) in transitional vegetation between Cerrado and Atlantic Forest in southeastern Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 73, no. 3, pp. 507-513. http://dx.doi.org/10.1590/S1519-69842013000300007. PMid:24212690.
http://dx.doi.org/10.1590/S1519-6984201...
). Orchid bees are an important group of Neotropical pollinators and are particularly vulnerable to the effects of deforestation than other bee groups, with some species occurring only in continuous forest ( Brosi, 2009 BROSI, B.J., 2009. The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biological Conservation, vol. 142, no. 2, pp. 414-423. http://dx.doi.org/10.1016/j.biocon.2008.11.003.
http://dx.doi.org/10.1016/j.biocon.2008...
; Becker et al., 1991 BECKER, P., MOURE, J.S. and PERALTA, F.J.A., 1991. More about euglossine bees in Amazonian forest fragments. Biotropica, vol. 23, no. 4, pp. 586-591. http://dx.doi.org/10.2307/2388396.
http://dx.doi.org/10.2307/2388396 ...
; Powell and Powell, 1987 POWELL, A.H. and POWELL, G.V.N., 1987. Population dynamics of male Euglossine bees in Amazonian forest fragments. Biotropica, vol. 19, no. 2, pp. 176-179. http://dx.doi.org/10.2307/2388742.
http://dx.doi.org/10.2307/2388742 ...
), but most species appear to respond to specific and ephemeral local conditions ( Tonhasca et al., 2002 TONHASCA, A., BLACKMER, J.L. and ALBUQUERQUE, G.S., 2002. Abundance and diversity of Euglossine Bees in the fragmented landscape of the Brazilian Atlantic Forest. Biotropica , vol. 34, no. 3, pp. 416-422. http://dx.doi.org/10.1111/j.1744-7429.2002.tb00555.x.
http://dx.doi.org/10.1111/j.1744-7429.2...
) and forest patch isolation ( Storck-Tonon and Peres, 2017 STORCK-TONON, D. and PERES, C.A., 2017. Forest patch isolation drives local extinctions of Amazonian orchid bees in a 26 years old archipelago. Biological Conservation , vol. 214, pp. 270-277. http://dx.doi.org/10.1016/j.biocon.2017.07.018.
http://dx.doi.org/10.1016/j.biocon.2017...
). Given the historical landscape change in BEC, some orchid bee species may have already suffered or being negatively affected. However, there is evidence that landscape features in Brazilian Cerrado did not affect, at least, E. nigrita occurrence, where even in pristine areas the vegetation is naturally opened when compared with pristine areas of Amazonian and Atlantic rainforests (Silva and Marco-Junior, 2014 SILVA, D.P. and MARCO JUNIOR, P., 2014. No Evidence of Habitat Loss Affecting the Orchid Bees Eulaema nigrita Lepeletier and Eufriesea auriceps Friese (Apidae: Euglossini) in the Brazilian Cerrado Savanna. Neotropical Entomology , vol. 43, no. 6, pp. 509-518. http://dx.doi.org/10.1007/s13744-014-0244-7. PMid:27194058.
http://dx.doi.org/10.1007/s13744-014-02...
).

First surveys with scent baits were performed in Central America, in order to evaluate the bees attracted to pure compounds and to mixtures of compounds in 1968 ( Dodson et al., 1969 DODSON, C.H., DRESSLER, R.L., HILLS, G.H., ADAMS, R.M. and WILLIAMS, N.H., 1969. Biologically active compounds in orchid fragrances. Science, vol. 164, no. 3885, pp. 1243-1249. http://dx.doi.org/10.1126/science.164.3885.1243. PMid:17772561.
http://dx.doi.org/10.1126/science.164.3...
). Therefore, the increase of specimens in collections after the first 50 years is probably related with the use of new techniques of orchid bee surveys using chemical scent attractants, since those fragrances could be artificially synthesized. In addition, the growing interest in the effects of environmental factors, such as habitat fragmentation, on orchid bee assemblages, may have encouraged increasing research and sampling in the region from the 2000’s ( Martins et al., 2016 MARTINS, D.C., ALBUQUERQUE, P.M.C., SILVA, F.S. and REBÊLO, J.M., 2016. First record of Aglae caerulea (Hymenoptera, Apidae, Euglossini) in Brazilian Cerrado east of the Amazon Region, Maranhão State, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 76, no. 2, pp. 554-556. http://dx.doi.org/10.1590/1519-6984.06415. PMid:26959953.
http://dx.doi.org/10.1590/1519-6984.064...
; Moura et al., 2011 MOURA, T.S.A., MAUÉS, M.M., SOUSA, J.T.A. and SANTOS, A.C.S. 2011. Biomonitoramento de abelhas euglossina (Apidae, Hymenoptera) em um SAF com castanheira-do-brasil (Bertholletia excelsa Bonpl., Lecythidaceae) em Tomé-Açu, Pará. In: Anais do 15° Seminário de Iniciação Científica da Embrapa Amazônia Oriental. Embrapa Amazônia Oriental, 24-25 Agosto 2011, Belém, Pará, Brasil. Brasília: Embrapa. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/41283/1/Res-Exp-SeminrioPIBIC2011-FINAL-JUL2011-TALYANNE-MOURA.pdf
http://ainfo.cnptia.embrapa.br/digital/...
; Taniguchi et al., 2012 TANIGUCHI, T., MAUÉS, M.M. and MOURA, T.S.A. 2012 [viewed 17 May 2017]. Riqueza de espécies de abelhas euglossina (Hymenoptera, Apidae) em dois fragmentos florestais inseridos no arco do desmatamento amazônico, Estado do Pará. In: Anais do 16° Seminário de Iniciação Científica da Embrapa. Embrapa Amazônia Oriental [online]. 16-17 Agosto 2012, Belém, Pará, Brasil. Brasília: Embrapa. Available from: http://ainfo.cnptia.embrapa.br/digital/bitstream/item/76571/1/Mariana-Taniguchi.pdf
http://ainfo.cnptia.embrapa.br/digital/...
).

Although we have recorded a large number of species considered rare, there are some aspects that can affect these results in orchid bee communities. Differences in sampling effort, considering that surveys were concentrated in a few sites and the sporadic frequency of samplings ( Silveira et al., 2011 SILVEIRA, G.C., NASCIMENTO, A.M., SOFIA, S.H. and AUGUSTO, S.C., 2011. Diversity of the euglossine bee community (Hymenoptera, Apidae) of an Atlantic Forest remnant in southeastern Brazil. Revista Brasileira de Entomologia, vol. 55, no. 1, pp. 109-115. http://dx.doi.org/10.1590/S0085-56262011000100017.
http://dx.doi.org/10.1590/S0085-5626201...
), the efficiency of sampling method, either by the use of few attractive substances and the collection method used ( Nemésio and Morato, 2004 NEMÉSIO, A. and MORATO, E.F., 2004. Euglossina (Hymenoptera: Apidae) of the Humaitá Reserve, Acre state, Brazilian Amazon, with comments on bait trap efficiency. Revista Tecnologia e Ambiente, vol. 10, pp. 71-80. ; Nemésio, 2012a NEMÉSIO, A., 2012a. Methodological concerns and challenges in ecological studies with orchid bees (Hymenoptera: Apidae: Euglossina). Bioscience Journal , vol. 28, pp. 118-134. ), or differences in the way these scents were handled and offered to the bees ( Nemésio and Rasmussen, 2014 NEMÉSIO, A. and RASMUSSEN, C., 2014. Sampling a biodiversity hotspot: the orchid-bee fauna (Hymenoptera: Apidae) of Tarapoto, northeastern Peru, the richest and most diverse site of the Neotropics. Brazilian Journal of Biology = Revista Brasileira de Biologia , vol. 74, no. 3, suppl. 1, pp. S33-S44. http://dx.doi.org/10.1590/1519-6984.20412. PMid:25627364.
http://dx.doi.org/10.1590/1519-6984.204...
), are all some of possible explanations to variations found on species richness and abundance in euglossine communities.

A recent study addressing digital and non-digital records of orchid bees in Brazilian Amazon, showed that in >50% of collection places it is known the presence of just one orchid bee species, indicating that the majority of the locations sampled represent casual collections ( Oliveira et al., 2017 OLIVEIRA, M.L., BROWN, J.C. and MOREIRA, M.P., 2017. Highway infrastructure, protected areas, and orchid bee distribution and conservation in the Brazilian Amazon. Journal of Environmental Protection, vol. 8, no. 8, pp. 923-939. http://dx.doi.org/10.4236/jep.2017.88058.
http://dx.doi.org/10.4236/jep.2017.8805...
). The species Euglossa imperialis and Exaerete frontalis categorized in this work as rare species, are actually very common, being collected in most inventories carried out in Amazonia (e.g. Silva and Rebêlo, 1999 SILVA, F.S. and REBÊLO, J.M.M., 1999. Euglossine bees (Hymenoptera: Apidae) of Buriticupu, Amazonia of Maranhão, Brazil. Acta Amazonica, vol. 29, no. 4, pp. 587-599. http://dx.doi.org/10.1590/1809-43921999294599.
http://dx.doi.org/10.1590/1809-43921999...
; Oliveira and Campos, 1995 OLIVEIRA, M.L. and CAMPOS, L.A.O., 1995. Abundância, riqueza e diversidade de abelhas Euglossinae (Hymenoptera, Apidae) em florestas contínuas de terra firme na Amazônia Central, Brasil. Revista Brasileira de Zoologia, vol. 12, no. 3, pp. 547-556. http://dx.doi.org/10.1590/S0101-81751995000300009.
http://dx.doi.org/10.1590/S0101-8175199...
). Thus, the status of “rare” attributed to them may be related to a low representativeness in the studied collections.

Our results show that, despite a long period of recordings of orchid bees at BEC, there is still a large gap of sites with no information about species composition, richness and occurrence of these bees in this area. The Amazon basin contains about 127 species of euglossine bees ( Nemésio and Silveira, 2007 NEMÉSIO, A. and SILVEIRA, F.A., 2007. Diversity and distribution of orchid bees (Hymenoptera: Apidae) with a revised checklist of species. Neotropical Entomology , vol. 36, no. 6, pp. 874-888. http://dx.doi.org/10.1590/S1519-566X2007000600008. PMid:18246261.
http://dx.doi.org/10.1590/S1519-566X200...
), and in this study, was possible to record more than 40% of this species analyzing historical data in the BEC. Nevertheless, we emphasize the importance of distributing more sampling sites, especially in the state of Maranhão, given the rapid disappearance of natural vegetation and few conservation units in the state ( Oliveira et al., 2017 OLIVEIRA, M.L., BROWN, J.C. and MOREIRA, M.P., 2017. Highway infrastructure, protected areas, and orchid bee distribution and conservation in the Brazilian Amazon. Journal of Environmental Protection, vol. 8, no. 8, pp. 923-939. http://dx.doi.org/10.4236/jep.2017.88058.
http://dx.doi.org/10.4236/jep.2017.8805...
), but also in southwestern portion of the state of Pará. Additionally, is necessary to adopt standardized studies with orchid bees in future sampling in the region.

Contrary to what have been shown for Atlantic Forest in Brazil ( Garraffoni et al., 2017 GARRAFFONI, A.R.S., MOURA, F.R. and LOURENÇO, A.P., 2017. Areas of endemism in the Atlantic Forest: quantitative biogeography insights from orchid bees (Apidae: Euglossini). Apidologie, vol. 48, no. 4, pp. 513-522. http://dx.doi.org/10.1007/s13592-017-0494-6.
http://dx.doi.org/10.1007/s13592-017-04...
; Nemésio and Santos-Junior, 2014 NEMÉSIO, A. and SANTOS-JUNIOR, J., 2014. Is the “Centro de Endemismo Pernambuco” a biodiversity hotspot for orchid bees? Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 74, no. 3, suppl. 1, pp. S78-S92. PMid:25627369. ), we did not find endemic species of BEC. Pearson and Dressler (1985) PEARSON, D.L. and DRESSLER, R.L., 1985. Two-year study of male orchid bee (Hymenoptera: Apidae: Euglossini) attraction to chemical baits in lowland south-eastern Perú. Journal of Tropical Ecology, vol. 1, no. 1, pp. 37-54. http://dx.doi.org/10.1017/S0266467400000067.
http://dx.doi.org/10.1017/S026646740000...
suggested that orchid bees apparently were not affected by historical isolation and speciation events occurred on forest refuges during the Pleistocene. Thus, the group may not respond to these biogeographic entities in the Amazon, what means that many euglossine species range across extensive geographic areas. Even so, the list and the conservation status of species we presented in this study may be useful information in later works interested to compare the past and current orchid bee fauna, and, allied to data on bees’ responses to land use changes occurred in BEC over the years, can fit as a basis for defining priority areas for conservation.

Acknowledgements

We thank CAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (grant FAPAC 007/2014). We received financial support from Instituto Nacional de Ciência e Tecnologia – Biodiversidade e Uso da Terra na Amazônia (CNPq 574008/2008-0). We also thank Luiz Henrique Borges (Programa de Pós-Graduação em Ecologia - UFPA) for his readiness to draw up the study area map. MLO is scholarship of CNPq (process # 306100/2016-9).

  • (With 3 figures)

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Publication Dates

  • Publication in this collection
    13 Aug 2018
  • Date of issue
    Apr-Jun 2019

History

  • Received
    17 May 2017
  • Accepted
    17 Oct 2017
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