Abstract
The Neotropical savanna is characterized by a set of different phytophysiognomies occurring in a wide expanse of Brazilian lands. Based on the known higher diversity of orchid bees in forests rather than in savanna formations, we hypothesized that the occurrence of forest formations inside the Brazilian savanna increases the diversity of euglossine bees in that domain and that there are species more associated with these environments. To test this hypothesis, we sampled the euglossine fauna in eight forest and woody savanna remnants and analyzed their community structure. We sampled 1,010 males of 13 species of orchid bees. Bee abundance and species richness ranged from 30 to 341 individuals and from 4 to 12 species, respectively. The forest remnants showed the highest diversity indices and species richness. Our data suggest that some species of Euglossa are mainly associated with forest remnants. We concluded that environmental heterogeneity in the Neotropical savanna contributes to higher diversity of euglossine and that some species are more frequently found in forested habitats. Additionally, considering that some sampled species are typical of the Atlantic and Amazon forests, our data reinforce the hypothesis that forest environments inside the Brazilian savanna can be considered bio-corridors for orchid bees.




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References
Aguiar, W.M., Gaglianone, M.C. (2008) Comunidade de abelhas Euglossina (Hymenoptera: Apidae) em remanescentes de Mata Estacional Semidecidual sobre Tabuleiro no Estado do Rio de Janeiro. Neotrop. Entomol. 37, 118–125
Aguiar, W.M., Gaglianone, M.C. (2011) Euglossine bees (Hymenoptera Apidae Euglossina) on an inselberg in the Atlantic Forest domain of southeastern Brazil. Trop. Zool. 24, 107–125
Aguiar, W.M., Gaglianone, M.C. (2012) Euglossine bee communities in small forest fragments of the Atlantic Forest, Rio de Janeiro state, southeastern Brazil (Hymenoptera, Apidae). Rev. Bras. Entomol. 56(2), 210–219
Aguiar, W.M., Melo, G.A.R., Gaglianone, M.C. (2014) Does forest physiognomy affect the structure of orchid bee (Hymenoptera, Apidae, Euglossini) communities? A study in the Atlantic Forest of Rio de Janeiro state, Brazil. Sociobiology 61(1), 68–77
Aizen, M.A., Feinsinger, P. (1994) Forest Fragmentation, Pollination, and Plant Reproduction in a Chaco Dry Forest, Argentina. Ecology. 75(2), 330–351
Alvarenga, P.E.F., Freitas, R.F., Augusto, S.C. (2007) Diversidade de Euglossini (Hymenoptera: Apidae) em áreas de cerrado do Triângulo Mineiro. MG. Biosci. J. 23, 30–37
Brosi, B.J. (2009) The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biol. Conserv. 142, 414–423
Brosi, B.J., Daily, G.C., Ehrlich, P.R. (2007) Bee community shifts with landscape context in a tropical countryside. Ecol. Appl. 17(2), 418–430
Brower, J.E., Zar, J.H., von Ende, C.N. (1998) Field & laboratory methods for general ecology, 4th edn. Wm. C. Brown Publishers, EUA
Calvillo, L.M., Ramírez, V.M., Parra-Tabla, V., Navarro, J. (2010) Bee diversity in a fragmented landscape of the Mexican neotropic. J. Insect Conserv. 14, 323–334
Cardoso, E., Moreno, M.I.C., Bruna, E.M., Vasconcelos, H.L. (2009) Mudanças fitofisionômicas no Cerrado: 18 anos de sucessão ecológica na Estação Ecológica do Panga. Caminhos da Geografia. 10(32), 254–268
Carvalho, A.M.C., Bego, L.R. (1996) Studies on Apoidea fauna of Cerrado vegetation at the Panga Ecological Reserve, Uberlândia, MG. Brazil. Rev. Bras. Entomol. 40, 147–156
Colwell R.K. (2013) EstimateS: Statistical estimation of species richness and shared species from samples, version 9. [online] http://purl.oclc.org/estimates (accessed on 15 February 2014)
Cordeiro, G.D., Boff, S., Caetano, T.A., Fernandes, P.C., Alves-dos-Santos, I. (2013) Euglossine bees (Apidae) in Atlantic forest areas of São Paulo State, southeastern Brazil. Apidologie. 44, 254–267
Dressler, R.L. (1982) Biology of the Orchid bees. Annu. Rev. Ecol. Syst. 13, 373–394
Faria, L.R.R., Silveira, F.A. (2011) The orchid bee fauna (Hymenoptera, Apidae) of a core area of the Cerrado. Brazil: the role of riparian forests as corridors for forest-associated bees. Biota Neotrop. 11, 87–94
Furley, P.A. (1999) The nature and diversity of neotropical savanna vegetation with particular reference to the Brazilian cerrados. Global Ecol. Biogeogr. 8, 223–241
Giangarelli, D.C., Sofia, S.H. (2011) First record of the orchid bee Euglossa viridis (Perty) (Hymenoptera, Apidae, Euglossini) from Paraná State, southern Brazil. Braz. J. Biol. 1, 223
Giangarelli, D.C., Freiria, G.A., Colatreli, O.P., Suzuki, K.M., Sofia, S.H. (2009) Eufriesea violacea (Blanchard): a euglossine species potentially sensitive to forest patch deterioration in Brazil. Neotrop. Entomol. 38, 610–615
Hatten, T.D., Looney, C., Strange, J.P., Bosque-Pérez, N.A. (2013) Bumble bee fauna of Palouse Prairie: Survey of native bee pollinators in a fragmented ecosystem. J. Insect Sci. 13(26), 1–19
Hutcheson, K. (1970) A test for comparing diversities based on the Shannon formula. J. Theoret. BioI. 29, 151–154
Justino, D.G., Augusto, S.C. (2010) Avaliação da eficiência de coleta utilizando armadilhas aromáticas e riqueza de Euglossini (Hymenoptera, Apidae) em áreas de Cerrado no Triângulo Mineiro. Rev. Bras. Zoociênc. 12, 227–239
Klink, C.A., Machado, R.B. (2005) A conservação do Cerrado brasileiro. Megadiversidade. 1, 147–155
Knoll, F.R.N., Penatti, N.C. (2012) Habitat Fragmentation Effects on the Orchid Bee Communities in Remnant Forests of Southeastern Brazil. Neotrop. Entomol. 41, 355–365
Lopes, S.F., Prado Júnior, J.A., Vale, V.S., Schiavini, I. (2013) Impactos ambientais antrópicos como modificadores da estrutura e funcionalidade de florestas estacionais semideciduais no Triângulo Mineiro, Brasil. Caminhos de geografia. 14(47), 233–242
Méio, B.B., Freitas, C.V., Jatoba, L., Silva, M.E.F., Ribeiro, J.F., Henriques, R.P.B. (2003) The influence of Amazonian and Atlantic flora in the vegetation of cerrado sensu stricto. Rev. Bras. Bot. 26(4), 437–444
Mesquita, T.M.S., Augusto, S.C. (2011) Diversity of trap-nesting bees and their natural enemies in the Brazilian savanna. Trop. Zool. 24, 127–144
Miles, L., Newton, A.C., Defries, R.S., Ravilious, C., May, I., Blyth, S., Kapos, V., Gordon, J.E. (2006) A global overview of the conservation status of tropical dry forests. J. Biogeogr. 33, 491–505
Morato, E.F. (1994) Abundância e riqueza de machos de Euglossini (Hymenoptera: Apidae) em mata de terra firme e áreas de derrubada, nas vizinhanças de Manaus (Brasil). Bol. Mus. Para. Emílio Goeldi sér. Zool. 10(1), 95–105
Moreno, M.I.C., Schiavini, I. (2001) Relação entre vegetação e solo em um gradiente florestal na Estação Ecológica do Panga, Uberlândia (MG). Rev. Bras. Botânica. 4, 537–544
Moura, D.C., Schlindwein, C. (2009) Mata Ciliar do Rio São Francisco como Biocorredor para Euglossini (Hymenoptera Apidae) de Florestas Tropicais Úmidas. Neotrop. Entomol. 38(2), 281–284
Moure, J.S., Urban, D., Melo, G.A.R. (2007) Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Sociedade Brasileira de Entomologia, Curitiba
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B.., Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature. 403, 853–858
Nemésio, A. (2012) The western limits of the “Hileia Baiana” for orchid bees, including seven new records for the state of Minas Gerais, eastern Brazil. Spixiana. 35(1), 109–116
Nemésio, A., Faria Jr., 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. 5, 113–117
Nemésio, A., Silveira, F.A. (2007a) Orchid bee fauna (Hymenoptera: Apidae: Euglossina) of Atlantic Forest fragments inside an urban area in southeastern Brazil. Neotrop. Entomol. 36, 186–191
Nemésio, A., Silveira, F.A. (2007b) Diversity and distribution of orchid bees (Hymenoptera: Apidae) with a revised checklist of species. Neotrop. Entomol. 36(6), 874–888
Neves, E.L., Viana, B.F. (1997) Inventário da fauna de Euglossinae (Hymenoptera, Apidae) do baixo sul da Bahia. Rev. Bras. Zool. 14(4), 831–837
Oliveira-Filho, A.T., Ratter, J.A. (1995) A study of the origin of central Brazilian forests by the analysis of plant species distribution patterns. Edinburgh J. Bot. 52, 141–194
Oliveira-Filho, A.T., Ratter, J.A. (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira, P.S., Marquis, R.J. (eds.) The Cerrados of Brazil: ecology and natural history of a Neotropical savanna, pp. 91–120. Columbia University Press, New York
Quinn, G.P., Keough, M.J. (2002) Experimental design and data analysis for biologists. CUP, UK
Ramalho, A.V., Gaglianone, M.C., Oliveira, M.L. (2009) Comunidades de abelhas Euglossina (Hymenoptera, Apidae) em fragmentos de Mata Atlântica no Sudeste do Brasil. Rev. Bras. Entomol. 53, 95–101
Rebêlo, J.M.M., Garófalo, C.A. (1997) Comunidades de machos de Euglossini (Hymenoptera, Apidae) em matas decíduas do Nordeste do estado de São Paulo. An. Soc. Entomol. Bras. 26, 243–255
Rebêlo, J.M.M., Silva, F.S. (1999) Distribuição das abelhas Euglossini (Hymenoptera: Apidae) no Estado do Maranhão. Brasil. An. Soc. Entomol. Bras. 28(3), 389–401
Rocha-Filho, L.C., Garófalo, C.A. (2013) Community ecology of Euglossine bees in the coastal Atlantic Forest of São Paulo State. Brazil. J. Insect Sci. 13(23), 1–19
Roubik, D.W., Ackerman, J.D. (1987) Long-term ecology of euglossine orchid-bees (Apidae: Euglossini) in Panama. Oecologia. 73, 321–333
Ruggiero, P.G.C., Batalha, M.A., Pivello, V.R., Meirelles, S.T. (2002) Soil-vegetation relationships in cerrado (Brazilian savanna) and semideciduous forest. Southeastern Brazil. Plant Ecol. 160, 1–16
Schiavini, I., Araujo, G.M. (1989) Considerações sobre a vegetação da Reserva Ecológica do Panga (Uberlândia). Revista Sociedade & Natureza. 1, 61–65
Silva, J.M.C., Bates, J.M. (2002) Biogeographic patterns and conservation in the South America Cerrado: A tropical savanna hotspot. BioScience. 52, 225–234
Silva, J.F., Fariñas, M.R., Felfili, J.M., Klink, C.A. (2006) Spatial heterogeneity, land use and conservation in the cerrado region of Brazil. J. Biogeogr. 33, 536–548
Silva, L.C.R., Sternberg, L., Haridasan, M., Hoffmann, W.A., Miralles-Wilhelm, F., Franco, A.C. (2008) Expansion of gallery forest into central Brazilian savannas. Glob. Change Biol. 14, 2108–2118
Silva, D.P., Aguiar, A.J.C., Melo, G.A.R., Anjos-Silva, E.J., Marco Jr., P. (2013) Amazon species within the Cerrado savanna new records and potential distribution for Aglae caerulea (Apidae: Euglossini). Apidologie 44, 673–683
Silveira, F.A., Melo, G.A.R., Almeida, E.A.B.. (2002) Abelhas Brasileiras: Sistemática e Identificação. Belo Horizonte
Silveira, G.C., Nascimento, A.M., Sofia, S.H., Augusto, S.C. (2011) Diversity of the Euglossine bee community (Hymenoptera, Apidae) of an Atlantic Forest remnant in southeastern Brazil. Rev. Bras. Entomol. 55(1), 109–115
Sofia, S.H., Suzuki, K.M. (2004) Comunidades de machos de abelhas Euglossina (Hymenoptera: Apidae) em fragmentos florestais no Sul do Brasil. Neotrop. Entomol. 33(6), 693–702
Sofia, S.H., Santos, A.M., Silva, C.R.M. (2004) Euglossine bees (Hymenoptera, Apidae) in a remnant of Atlantic Forest in Paraná State. Brazil. Iheringia Ser. Zool. 94(2), 217–222
Williams, N.M., Minckley, R.L., Silveira, F.A. (2001) Variation in native bee faunas and its implications for detecting community changes. Conservation Ecology 5(1), 7. [online] http://www.consecol.org/vol5/iss1/art7/ (accessed on 26 May 2014)
Zimmermann, Y., Schorkopf, D.L.P., Moritz, R.F.A., Pemberton, R.W., Quezada-Euan, J.J.G., Eltz, T. (2011) Population genetic structure of orchid bees (Euglossini) in anthropogenically altered landscapes. Conserv Genet. 12(5), 1183–1194
Acknowledgments
The authors are grateful to Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-PROCAD 158/07) and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the PQ scholarships to SC Augusto and MC Gaglianone. We would like to thank Dr. Ivan Schiavini for providing information about the study areas, the biologists Thiago T. Brescia and Guilherme C. Pires for the samplings made in Irara and Sucupira Cassu farm, Gabriel A. R. Melo for his help with the identification of euglossine species, and to anonymous reviewers that contributed to improve the manuscript.
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Silveira, G.C., Freitas, R.F., Tosta, T.H.A. et al. The orchid bee fauna in the Brazilian savanna: do forest formations contribute to higher species diversity?. Apidologie 46, 197–208 (2015). https://doi.org/10.1007/s13592-014-0314-1
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DOI: https://doi.org/10.1007/s13592-014-0314-1


