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First record of Aglae caerulea (Hymenoptera, Apidae, Euglossini) in Brazilian Cerrado east of the Amazon Region, Maranhão State, Brazil

1 Introduction

Aglae caerulea Lepeletier & Serville, a monospecific genus of Euglossini is characterized by its small body size (20 to 28 mm) and blue color (Dressler, 1982Dressler, R.L., 1982. Biology of the orchid bees (Euglossini). Annual Review of Ecology Evolution and Systematics, vol. 13, no. 1, pp. 373-394. http://dx.doi.org/10.1146/annurev.es.13.110182.002105.
http://dx.doi.org/10.1146/annurev.es.13....
). Females of this species are cleptoparasites of Eufriesea and Eulaema nests (Moure, 1964Moure, J.S., 1964. A key to the parasitic Euglossinae bees and a new species of Exaerete from Mexico (Hymenoptera, Apoidea). Revista de Biologia Tropical, vol. 12, no. 1, pp. 15-18.). The males are rarely found in flowers or in other natural sources of aromatic substances, or even in baited traps. For this reason, they are underrepresented in entomological collections (Morato, 2001Morato, E.F., 2001. Ocorrência de Lepeletier & Serville (Hymenoptera, Apidae, Apini, Euglossina) no estado do Acre, Brasil. Aglae caeruleaRevista Brasileira de Zoologia, vol. 18, no. 3, pp. 1031-1034. http://dx.doi.org/10.1590/S0101-81752001000300034.
http://dx.doi.org/10.1590/S0101-81752001...
). A. caerulae males attracted to aromatic substances under natural conditions (as is characteristic of Euglossini bees) were first observed recently in inflorescences of Anthurium rubrinervium (Link) G. Don (Araceae) in an area of tropical forest in French Guiana (Hentrich et al., 2007Hentrich, H., Kaiser, R. and Gottsberger, G., 2007. Floral scent collection at the perfume flowers of Anthurium rubrinervium (Araceae) by the kleptoparasitic orchid bee (Euglossini). Aglae CaeruleaEcotropica, vol. 13, pp. 149-155.). Moreover, three specimens of this species had been attracted and collected using methyl cinnamate baits in Dawa, British Guiana (Williams and Dodson, 1972Williams, N.H. and Dodson, C.H., 1972. Selective attraction of male euglossine bee to orchid floral fragrances and its importance in long distance pollen flow. Evolution; International Journal of Organic Evolution, vol. 26, no. 1, pp. 84-95. http://dx.doi.org/10.2307/2406985.
http://dx.doi.org/10.2307/2406985...
).

Until recently, A. caerulea was considered endemic to the Amazon region (Cameron, 2004Cameron, S.A., 2004. Phylogeny and biology of neotropical orchid bees (Euglossini). Annual Review of Entomology, vol. 49, no. 1, pp. 377-404. http://dx.doi.org/10.1146/annurev.ento.49.072103.115855. PMid:14651469.
http://dx.doi.org/10.1146/annurev.ento.4...
), and was found in the Amazon rainforest of Brazil, Colombia, French Guiana, and Guyana (Ramirez et al., 2002Ramírez, S., Dressler, R.L. and Ospina, M., 2002. Abejas euglosinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notas sobre su biologia. Biota Colombiana, vol. 3, no. 1, pp. 7-118.). In Brazil, records indicate the presence of A. caerulea in the states of Acre, Amazonas, Amapá, and Pará (Silveira et al., 2002Silveira, F.A., MELO, G.A.R. and ALMEIDA, E.A.B., 2002. Abelhas brasileiras: sistemática e identificação. Belo Horizonte: Edição do autor. 253 p.). Recently, its presence was recorded in phytophysiognomic studies of gallery forests within areas of Cerrado in Mato Grosso State, Brazil, where males were attracted and captured in methyl cinnamate baited traps (Anjos-Silva et al., 2006Anjos-Silva, E.J., Camillo, E. and Garófalo, C.A., 2006. Occurrence of (Hymenoptera: Apidae: Euglossini) in the Parque Nacional da Chapada dos Guimarães, Mato Grosso state, Brazil. Aglae caeruleaNeotropical Entomology, vol. 35, no. 6, pp. 868-870. http://dx.doi.org/10.1590/S1519-566X2006000600024. PMid:17273723.
http://dx.doi.org/10.1590/S1519-566X2006...
; Silva et al., 2013Silva, D.P., Aguiar, A.J.C., Melo, G.A.R., Anjos-Silva, E.J. and Marco JUNIOR, P., 2013. Amazonian species within the Cerrado savanna: new records and potential distribution for (Apidae: Euglossini). Aglae caeruleaApidologie, vol. 44, no. 6, pp. 673-683. http://dx.doi.org/10.1007/s13592-013-0216-7.
http://dx.doi.org/10.1007/s13592-013-021...
). Although several entomological surveys have used a variety of chemical baits (Rebêlo and Silva, 1999Rebêlo, J.M.M. and SILVA, F.S., 1999. Distribuição das abelhas Euglossini (Hymenoptera, Apidae) no Estado do Maranhão, Brasil. Anais da Sociedade Entomológica do Brasil, vol. 28, no. 3, pp. 389-401. http://dx.doi.org/10.1590/S0301-80591999000300003.
http://dx.doi.org/10.1590/S0301-80591999...
; Albuquerque et al., 2001Albuquerque, P.M.C., Ferreira, R.G., Rêgo, M.M.C., Santos, C.S. and Brito, C.M.S., 2001. Levantamento da fauna de abelhas silvestres (Hymenoptera, Apoidea) na região da Baixada Maranhense: Vitória do Mearim, MA, Brasil. Acta Amazonica, vol. 31, no. 3, pp. 419-430. http://dx.doi.org/10.1590/1809-43922001313430.
http://dx.doi.org/10.1590/1809-439220013...
; Brito and Rêgo, 2001Brito, 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/S1519-69842001...
; Silva and Rêbelo, 2002Silva, 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/S1519-69842002...
, Carvalho et al., 2006CARVALHO, C.C., RÊGO, M.M.C. and MENDES, F.N., 2006. Dinâmica de populações de Euglossina (Hymenoptera, Apidae) em mata ciliar, Urbano Santos, Maranhão, Brasil. Iheringia: Série Zoologia, vol. 96, no. 2, pp. 249-256. http://dx.doi.org/10.1590/S0073-47212006000200016.
http://dx.doi.org/10.1590/S0073-47212006...
; Mendes et al., 2008Mendes, F.N., RÊGO, M.M.C. and CARVALHO, C.C., 2008. Abelhas Euglossina (Hymenoptera, Apidae) coletadas em uma monocultura de eucalipto circundada por cerrado em Urbano Santos, Maranhão, Brasil. Iheringia: Série Zoologia, vol. 98, no. 3, pp. 285-290. http://dx.doi.org/10.1590/S0073-47212008000300001.
http://dx.doi.org/10.1590/S0073-47212008...
; Silva et al., 2009Silva, O., Rêgo, M.M.C., ALBUQUERQUE, P.M.C. and RAMOS, M.C., 2009. Abelhas Euglossina (Hymenoptera: Apidae) em área de restinga do nordeste do Maranhão. Neotropical Entomology, vol. 38, no. 2, pp. 186-196. http://dx.doi.org/10.1590/S1519-566X2009000200004. PMid:19488506.
http://dx.doi.org/10.1590/S1519-566X2009...
; Silva, 2012Silva, F.S., 2012. Orchid bee (Hymenoptera: Apidae) community from a gallery forest in the Brazilian Cerrado. Revista de Biologia 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.v60i2.394...
), A. caerulea was not previously found in any of the areas studied in Maranhão State. The absence of this species, especially in rainforests, is most likely because methyl cinnamate baits, for which A. caerulea has an affinity, were not used. This was also observed by Morato (2001)Morato, E.F., 2001. Ocorrência de Lepeletier & Serville (Hymenoptera, Apidae, Apini, Euglossina) no estado do Acre, Brasil. Aglae caeruleaRevista Brasileira de Zoologia, vol. 18, no. 3, pp. 1031-1034. http://dx.doi.org/10.1590/S0101-81752001000300034.
http://dx.doi.org/10.1590/S0101-81752001...
in studies performed in the Parque Nacional da Serra do Divisor in Acre State, and by Anjos-Silva et al. (2006)Anjos-Silva, E.J., Camillo, E. and Garófalo, C.A., 2006. Occurrence of (Hymenoptera: Apidae: Euglossini) in the Parque Nacional da Chapada dos Guimarães, Mato Grosso state, Brazil. Aglae caeruleaNeotropical Entomology, vol. 35, no. 6, pp. 868-870. http://dx.doi.org/10.1590/S1519-566X2006000600024. PMid:17273723.
http://dx.doi.org/10.1590/S1519-566X2006...
in a gallery forest in the Chapada dos Guimarães Brazilian National Park in Mato Grosso State. The main goal of the present study was to check if Aglae caerulea occurs in the Cerrado domain east of the Amazon Region.

2 Material and Methods

The study was conducted in a gallery forest in the savannah of the Parque Estadual do Mirador within the limits of the municipality of Formosa da Serra Negra (6º 37’ 56.29” S; 45º 53’ 4.25” W), Maranhão State, Brazil. It is Maranhão State’s largest conservation unit and is located between the sources of the Alpercatas and Itapecuru rivers (6° 37’ 30.15” S; 45° 52’ 30.70” W, respectively), occupying approximately 450 ha within the south central region of the state. The park extends through portions of Mirador, Grajaú, São Raimundo das Mangabeiras, and Formosa da Serra Negra (Conceição and Rodrigues, 2010Conceição, G.M. and Rodrigues, M. S., 2010. Pteridófitas do Parque Estadual do Mirador, Maranhão, Brasil. Caderno de Geociência, vol. 7, pp. 47-53.). The climate is sub-humid, with an annual rainfall of 1,200 mm. The mean maximum temperature ranges from 31.4 °C to 33 °C and the mean minimum temperature ranges from 19.5 °C to 21 °C (Conceição et al., 2011Conceição, G.M., Ruggieri, A.C. and Rodrigues, M.S., 2011. Malpighiaceae do cerrado do Parque Estadual do Mirador, Maranhão, Brasil. Scientia Plena, vol. 7, no. 2, pp. 1-6.).

The sampling was done between January 2012 and December 2013. Five aromatic compounds were used to attract the male euglossine bees: methyl cinnamate, eucalyptol, eugenol, methyl salicylate, and vanillin (modified from Campos et al., 1989Campos, L.A.O., Silveira, F.A., Oliveira, M.L., Abrantes, C.V.M., Morato, E.F. and Melo, G.A.R., 1989. Utilização de armadilhas para a captura de machos de Euglossini (Hymenoptera, Apoidea). Revista Brasileira de Zoologia, vol. 6, no. 4, pp. 621-626. http://dx.doi.org/10.1590/S0101-81751989000400008.
http://dx.doi.org/10.1590/S0101-81751989...
). For each aromatic compound, we used three baits that were exposed for 10 consecutive hours (from 7 to 17 h). In total, 15 baits were installed 8 meters apart from each other along the riverbank. The captured specimens were deposited in the bee collection of the Laboratory of Bee Studies of the Biology Department of the Federal University of Maranhão, Brazil.

3 Results and Discussion

In this study, two A. caerulea males (Figure 1) were obtained in August 2013 and November 2013 during a survey performed in a gallery forest. The area where the male A. caerulea specimens were found is part of a polygon of possible occurrence, which extends throughout the gallery forests in Pará, Amazonas, Mato Grosso (northern region), and Tocantins states, according to Silva et al. (2013)Silva, D.P., Aguiar, A.J.C., Melo, G.A.R., Anjos-Silva, E.J. and Marco JUNIOR, P., 2013. Amazonian species within the Cerrado savanna: new records and potential distribution for (Apidae: Euglossini). Aglae caeruleaApidologie, vol. 44, no. 6, pp. 673-683. http://dx.doi.org/10.1007/s13592-013-0216-7.
http://dx.doi.org/10.1007/s13592-013-021...
(Figure 2).

Figure 1
Aglae caerulea male collected using methyl cinnamate baited traps: (A) anterior view, slightly greenish clypeus; (B) dorsal view, showing the flat scutellum; (C) lateral view, mesosome; (D) very elongated and straight hind tibia, with tibial groove in terminal position.
Figure 2
Map showing the Brazilian Cerrado (grey area) and known geographic distribution of Aglae caerulea (black circles) according to Silva et al. (2013)Silva, D.P., Aguiar, A.J.C., Melo, G.A.R., Anjos-Silva, E.J. and Marco JUNIOR, P., 2013. Amazonian species within the Cerrado savanna: new records and potential distribution for (Apidae: Euglossini). Aglae caeruleaApidologie, vol. 44, no. 6, pp. 673-683. http://dx.doi.org/10.1007/s13592-013-0216-7.
http://dx.doi.org/10.1007/s13592-013-021...
, with highlight for the new record found in the Maranhão state (star).

The occurrence of species from the Amazon region in other nearby ecosystems is most likely due to the presence of closed areas such as gallery forests, coconut forests, and sandbanks, which comprise denser vegetation and thus favor the dispersal of Euglossini species, which are considered common in forest environments (Dressler, 1982Dressler, R.L., 1982. Biology of the orchid bees (Euglossini). Annual Review of Ecology Evolution and Systematics, vol. 13, no. 1, pp. 373-394. http://dx.doi.org/10.1146/annurev.es.13.110182.002105.
http://dx.doi.org/10.1146/annurev.es.13....
). The results obtained by Moura and Schlindwein (2009)Moura, D.C. and Schlindwein, C., 2009. Mata Ciliar do Rio São Francisco como biocorredor para Euglossini (Hymenoptera, Apidae) de florestas tropicais úmidas. Neotropical Entomology, vol. 38, no. 2, pp. 281-284. http://dx.doi.org/10.1590/S1519-566X2009000200018. PMid:19488520.
http://dx.doi.org/10.1590/S1519-566X2009...
in studies on riparian forests of the São Francisco River corroborate this hypothesis, highlighting that these environments are used as wildlife corridors, harboring and maintaining Euglossini species that are only common in tropical rainforests.

  • (With 2 figures)

References

  • Albuquerque, P.M.C., Ferreira, R.G., Rêgo, M.M.C., Santos, C.S. and Brito, C.M.S., 2001. Levantamento da fauna de abelhas silvestres (Hymenoptera, Apoidea) na região da Baixada Maranhense: Vitória do Mearim, MA, Brasil. Acta Amazonica, vol. 31, no. 3, pp. 419-430. http://dx.doi.org/10.1590/1809-43922001313430
    » http://dx.doi.org/10.1590/1809-43922001313430
  • Anjos-Silva, E.J., Camillo, E. and Garófalo, C.A., 2006. Occurrence of (Hymenoptera: Apidae: Euglossini) in the Parque Nacional da Chapada dos Guimarães, Mato Grosso state, Brazil. Aglae caeruleaNeotropical Entomology, vol. 35, no. 6, pp. 868-870. http://dx.doi.org/10.1590/S1519-566X2006000600024 PMid:17273723.
    » http://dx.doi.org/10.1590/S1519-566X2006000600024
  • 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/S1519-69842001000400012
  • Cameron, S.A., 2004. Phylogeny and biology of neotropical orchid bees (Euglossini). Annual Review of Entomology, vol. 49, no. 1, pp. 377-404. http://dx.doi.org/10.1146/annurev.ento.49.072103.115855 PMid:14651469.
    » http://dx.doi.org/10.1146/annurev.ento.49.072103.115855
  • Campos, L.A.O., Silveira, F.A., Oliveira, M.L., Abrantes, C.V.M., Morato, E.F. and Melo, G.A.R., 1989. Utilização de armadilhas para a captura de machos de Euglossini (Hymenoptera, Apoidea). Revista Brasileira de Zoologia, vol. 6, no. 4, pp. 621-626. http://dx.doi.org/10.1590/S0101-81751989000400008
    » http://dx.doi.org/10.1590/S0101-81751989000400008
  • CARVALHO, C.C., RÊGO, M.M.C. and MENDES, F.N., 2006. Dinâmica de populações de Euglossina (Hymenoptera, Apidae) em mata ciliar, Urbano Santos, Maranhão, Brasil. Iheringia: Série Zoologia, vol. 96, no. 2, pp. 249-256. http://dx.doi.org/10.1590/S0073-47212006000200016
    » http://dx.doi.org/10.1590/S0073-47212006000200016
  • Conceição, G.M. and Rodrigues, M. S., 2010. Pteridófitas do Parque Estadual do Mirador, Maranhão, Brasil. Caderno de Geociência, vol. 7, pp. 47-53.
  • Conceição, G.M., Ruggieri, A.C. and Rodrigues, M.S., 2011. Malpighiaceae do cerrado do Parque Estadual do Mirador, Maranhão, Brasil. Scientia Plena, vol. 7, no. 2, pp. 1-6.
  • Dressler, R.L., 1982. Biology of the orchid bees (Euglossini). Annual Review of Ecology Evolution and Systematics, vol. 13, no. 1, pp. 373-394. http://dx.doi.org/10.1146/annurev.es.13.110182.002105
    » http://dx.doi.org/10.1146/annurev.es.13.110182.002105
  • Hentrich, H., Kaiser, R. and Gottsberger, G., 2007. Floral scent collection at the perfume flowers of Anthurium rubrinervium (Araceae) by the kleptoparasitic orchid bee (Euglossini). Aglae CaeruleaEcotropica, vol. 13, pp. 149-155.
  • Mendes, F.N., RÊGO, M.M.C. and CARVALHO, C.C., 2008. Abelhas Euglossina (Hymenoptera, Apidae) coletadas em uma monocultura de eucalipto circundada por cerrado em Urbano Santos, Maranhão, Brasil. Iheringia: Série Zoologia, vol. 98, no. 3, pp. 285-290. http://dx.doi.org/10.1590/S0073-47212008000300001
    » http://dx.doi.org/10.1590/S0073-47212008000300001
  • Morato, E.F., 2001. Ocorrência de Lepeletier & Serville (Hymenoptera, Apidae, Apini, Euglossina) no estado do Acre, Brasil. Aglae caeruleaRevista Brasileira de Zoologia, vol. 18, no. 3, pp. 1031-1034. http://dx.doi.org/10.1590/S0101-81752001000300034
    » http://dx.doi.org/10.1590/S0101-81752001000300034
  • Moura, D.C. and Schlindwein, C., 2009. Mata Ciliar do Rio São Francisco como biocorredor para Euglossini (Hymenoptera, Apidae) de florestas tropicais úmidas. Neotropical Entomology, vol. 38, no. 2, pp. 281-284. http://dx.doi.org/10.1590/S1519-566X2009000200018 PMid:19488520.
    » http://dx.doi.org/10.1590/S1519-566X2009000200018
  • Moure, J.S., 1964. A key to the parasitic Euglossinae bees and a new species of Exaerete from Mexico (Hymenoptera, Apoidea). Revista de Biologia Tropical, vol. 12, no. 1, pp. 15-18.
  • Ramírez, S., Dressler, R.L. and Ospina, M., 2002. Abejas euglosinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notas sobre su biologia. Biota Colombiana, vol. 3, no. 1, pp. 7-118.
  • Rebêlo, J.M.M. and SILVA, F.S., 1999. Distribuição das abelhas Euglossini (Hymenoptera, Apidae) no Estado do Maranhão, Brasil. Anais da Sociedade Entomológica do Brasil, vol. 28, no. 3, pp. 389-401. http://dx.doi.org/10.1590/S0301-80591999000300003
    » http://dx.doi.org/10.1590/S0301-80591999000300003
  • Silva, D.P., Aguiar, A.J.C., Melo, G.A.R., Anjos-Silva, E.J. and Marco JUNIOR, P., 2013. Amazonian species within the Cerrado savanna: new records and potential distribution for (Apidae: Euglossini). Aglae caeruleaApidologie, vol. 44, no. 6, pp. 673-683. http://dx.doi.org/10.1007/s13592-013-0216-7
    » http://dx.doi.org/10.1007/s13592-013-0216-7
  • 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/S1519-69842002000100003
  • Silva, F.S., 2012. Orchid bee (Hymenoptera: Apidae) community from a gallery forest in the Brazilian Cerrado. Revista de Biologia 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.v60i2.3949
  • Silva, O., Rêgo, M.M.C., ALBUQUERQUE, P.M.C. and RAMOS, M.C., 2009. Abelhas Euglossina (Hymenoptera: Apidae) em área de restinga do nordeste do Maranhão. Neotropical Entomology, vol. 38, no. 2, pp. 186-196. http://dx.doi.org/10.1590/S1519-566X2009000200004 PMid:19488506.
    » http://dx.doi.org/10.1590/S1519-566X2009000200004
  • Silveira, F.A., MELO, G.A.R. and ALMEIDA, E.A.B., 2002. Abelhas brasileiras: sistemática e identificação. Belo Horizonte: Edição do autor. 253 p.
  • Williams, N.H. and Dodson, C.H., 1972. Selective attraction of male euglossine bee to orchid floral fragrances and its importance in long distance pollen flow. Evolution; International Journal of Organic Evolution, vol. 26, no. 1, pp. 84-95. http://dx.doi.org/10.2307/2406985
    » http://dx.doi.org/10.2307/2406985

Publication Dates

  • Publication in this collection
    08 Mar 2016
  • Date of issue
    Apr-Jun 2016

History

  • Received
    24 Apr 2015
  • Accepted
    03 Sept 2015
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br