Does Forest Phisiognomy affect the Structure of Orchid Bee (Hymenoptera, Apidae, Euglossini) Communities? A Study in the Atlantic Forest of Rio de Janeiro state, Brazil

Willian Moura de Aguiar, Gabriel Augusto Rodrigues de Melo, Maria Cristina Gaglianone

Abstract


We describe and discuss the composition, abundance and diversity of euglossine in three vegetation types of the Atlantic Forest (Lowland Seasonal Semideciduous, Submontane Seasonal and Dense Montane Ombrophilous Forest) in Rio de Janeiro state, Brazil, compare them to previous studies in the region and investigate the importance of the vegetation types, climatic and geomorphological factors on the species composition. Male euglossine bees attracted by fragrances were sampled monthly from August/2008 to July/2009 using entomological nets and traps. Euglossine bee communities exhibited differences in their species composition and abundance along the year and in the vegetation types. The precipitation, altitude and vegetation types demonstrated a significant influence on the ordination of the euglossine communities. Our study found differences in the composition of euglossine bee communities as well as in their patterns of abundance and dominance among different vegetation formations, stressing the importance of the conservation of landscape mosaics in the region.


Keywords


Biodiversity, conservation, neotropics, biogeographic, pollinators

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References


Abrahamczyk, S., Gottleuber, P., Matauschek, C. & Kessler, M. (2011). Diversity and community composition of euglossine bee assemblages (Hymenoptera: Apidae) in western Amazonia. Biodiversity and Conservation, 20: 2981-3001. doi: 10.1007/s10531-011-0105-1

Ackerman, J.D. (1983). Specificity and mutual dependency of the orchid-euglossine bee interaction. Biological Journal of the Linnean Society, 20: 301-314. doi: 10.1111/j.1095-8312.1983.tb01878.x

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. Neotropical Entomology, 37: 118-125. Doi 10.1590/S1519-566X2008000200002

Aguiar, W.M. & Gaglianone, M.C. (2011). Euglossine bees (Hymenoptera, Apidae, Euglossina) on an inselberg in the Atlantic Forest domain of southeastern Brazil. Tropical Zoology, 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). Revista Brasileira de Entomologia, 56: 210-219. doi 10.1590/S0085-56262012005000018

Alvarenga, P.E.F., Freitas, R.F. & Augusto, S.C. (2007). Diversidade de Euglossini (Hymenoptera: Apidae) em áreas de cerrado do Triângulo Mineiro, MG. Bioscience, 23 Supplement 1: 30-37.

Andrade-Silva, A.C.R., Nemésio, A., Oliveira, F.F., & Nascimento, F.S. (2012). Spatial-Temporal Variation in Orchid Bee Communities (Hymenoptera: Apidae) in Remnants of Arboreal Caatinga in the Chapada Diamantina Region, State of Bahia, Brazil. Neotropical Entomology, 41: 296-305. doi 10.1007/s13744-012-0053-9.

Armbuster, W.S. (1993). Within-habitat heterogeneity in baiting samples of male Euglossine bees: possible causes and implications. Biotropica, 25: 122-128.

Augusto, S.C. & Garófalo, C.A. (2004). Nesting biology and social structure of Euglossa (Euglossa) townsendi Cockerell (Hymenoptera, Apidae, Euglossini). Insectes Sociaux, 51: 400-409.

Becker, P., Moure, J.S. & Peralta, F.J.A. (1991). More about euglossine bees in Amazonian forest fragments. Biotropica, 23: 586-591. doi: 10.2307/2388396

Bonilla-Gómez M.A. (1999). Caracterização da estrutura espaço-temporal da comunidade de abelhas euglossinas (Hymenoptera, Apidae) na Hiléia Baiana. Tese de Doutorado. Universidade Estadual de Campinas, 153p.

Brosi, B.J. (2009). The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biological Conservation, 142: 414-423.

Chao, A. & Shen, T.J. (2005). Program SPADE (Species Prediction And Diversity Estimation). Programand user’s guide at http://chao.stat.nthu.edu.tw (accessed on 18 October 12).

Colwell, R.K. (2006). EstimateS: statistical estimation of species richness and shared species from samples. Version 8.0. User’s guide and application. University of Connecticut, USA. Available at: http://purl.oclc.org/estimates (accessed on 18 October 12)

Cortopassi-Laurino, M., Zillikens, A. & Steiner, J. (2009). Pollen sources of the orchid bee Euglossa annectans Dressler 1982 (Hymenoptera: Apidae, Euglossini) analyzed from larval provisions. Genetics and Molecular Research, 8: 546-556.

Dan, M.L., Braga, J.M.A. & Nascimento, M.T. (2010). Estrutura da comunidade arbórea de fragmentos de floresta estacional semidecidual na bacia hidrográfica do rio São Domingos, Rio de Janeiro, Brasil. Rodriguésia, 61: 1-18.

Darrault, R., Medeiros, P.C.R., Locatelli, E., Lopes, A. V., Machado, I. C. & Schlindwein, C. (2006). Abelhas Euglossini, in: Porto, K. Almeida Cortez, J. & Tabarelli (eds), Diversidade biológica e conservação da floresta Atlântica ao norte do rio São Francisco, Ministério do Meio Ambiente, Brasília, pp.352-354.

Dressler, R.L. (1982a). New species of Euglossa II. (Hymenoptera: Apidae). Revista de Biologia Tropical, 30: 121-129.

Dressler, R.L. (1982b). Biology of the orchid bee (Euglossini). Annual Review of Ecology and Systematics, 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 Neotropica, 11: 87-94 . doi 10.1590/S1676-06032011000400009

Farias, R.C.A.P., Madeira-da-Silva, M.C., Pereira-Peixoto, M.H. & Martins, C.F. (2008). Composição e Sazonalidade de Espécies de Euglossina (Hymenoptera: Apidae) em Mata e Duna na Área de Proteção Ambiental da Barra do Rio Mamanguape, Rio Tinto, PB. Neotropical Entomology, 37: 253-258. doi: 10.1590/S1519-566X2008000300003

Galindo-Leal, C. & Câmara, I.G. (2003). Atlantic forest hotspots status: an overview. In: C. Galindo-Leal & I.G. Câmara (Eds). The Atlantic Forest of South America: biodiversity status, threats, and outlook (pp. 3-11).Center for Applied Biodiversity Science e Island Press, Washington, D.C.

Garófalo, C.A. (1992). Comportamento de nidificação e estrutura de ninhos de Euglossa cordata (Hymenoptera: Apidae: Euglossini). Revista Brasileira de Biologia, 52: 187-198.

Giangarelli, D.C., Freiria, G.A., Colatreli, O.P., Suzuki, K.M. & Sofia, S.H. (2009). Eufriesea violacea (Blanchard) (Hymenoptera: Apidae): An orchid bee apparently sensitive to size reduction in forest patches. Neotropical Entomology, 38: 1-6.

Gotelli, N.J. & Entsminger, G.L. (2001). EcoSim: Null models programa for ecology. Version 7.0. Acquired Intelligence Inc. & Kesey-Bear (accessed on 23 September 12)

Hammer, O., Harper, D.A.T. & Ryan, P.D. (2001). Past. Paleontological Statistics Programa Package for Education and Data Analysis. Paleontologia Eletronica 4: 1-9.

Hegland, S.J. & Boeke, L. (2006). Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecological Entomology, 31: 532–538.

Janzen, D.H., de Vries, P.J., Higgins, M.L. & Kimsey, L.S. (1982). Seasonal and site variation in Costa Rican euglossine bees at chemical baits in lowland deciduous and evergreen forests. Ecology , 63: 6-74.

Köppen, W. & Geiger, R. (1928). Klimate der Erde. Gotha: Verlag Justus Perthes. Wall-map 150cmx200cm.

Lázaro, A. & Totland, O. (2010). Local floral composition and the behaviour of pollinators: attraction to and foraging within experimental patches. Ecological Entomology, 35: 652 - 661.

Linsley, E.G. (1958). The ecology of solitary bees. Hilgardia 27: 543-597.

Magurran, A.E. (2003). Measuring biological diversity. Blackwell Publishing, Oxford. 215p.

Mattozo, V.C., Faria, L.R.R. & Melo, G.A.R. (2011). Orchid bees (Hymenoptera: Apidae) in the coastal forests of southern Brazil: Diversity, efficiency of sampling methods and comparison with other Atlantic forest surveys. Papéis Avulsos de Zoologia, 51: 505-515. 10.1590/S0031-10492011003300001

Michener, C.D. (1979). Biogeography of the bees. Annals of the Missouri Botanical Garden, 66: 277–347.

Morato, E.F., Campos, L.A.O. & Moure, J.S. (1992). Abelhas Euglossini (Hymenoptera, Apidae) coletadas na Amazônia Central. Revista Brasileira de Entomologia, 36: 767-771.

Moure, J.S., Melo, G.A.R. & Faria Jr., L.R.R. (2007). Euglossini Latreille, 1802. In: J.S. Moure, D. Urban& G.A.R.Melo (Eds). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. (pp. 214–255). Sociedade Brasileira de Entomologia, Curitiba-PR.

Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B. & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853-858. doi: 10.1038/35002501

Nemésio, A. & Silveira, F.A. (2006a). Edge effects on the orchid-bee fauna (Hymenoptera: Apidae) at a large remnant of Atlantic Forest in southeastern Brazil. Neotropical Entomology, 35: 313–323. doi: 10.1590/S1519-566X2006000300004

Nemésio, A. & Silveira, F.A. (2006b). Deriving ecological relationships from geographical correlations between host and parasitic species: an example with orchid bees. Journal of Biogeography, 33: 91-97. doi: 10.1111/j.1365-2699.2005.01370.x

Nemésio, A. & Silveira, F.A. (2007). Diversity and distribution of orchid bees (Hymenoptera: Apidae: Euglossina) with a revised checklist of their species. Neotropical Entomology, 36: 874-888. doi: 10.1590/S1519-566X2007000600008

Nemésio, A. & Silveira, F.A. (2010). Forest Fragments with Larger Core Areas Better Sustain Diverse Orchid Bee Faunas (Hymenoptera: Apidae: Euglossina). Neotropical Entomology, 39: 555-561. Doi 10.1590/S1519-566X2010000400014

Nemésio, A. & Vasconcelos, H. L. (2013). Beta diversity of orchid bees in a tropical biodiversity hotspot. Biodiversity and Conservation, 22: 1647-1661. doi: 10.1007/s10531-013-0500-x

Nemésio, A. (2007). The community structure of male orchid bees along the Neotropical Region. Revista Brasileira de Zoologia, 9: 151-158.

Nemésio, A. (2008). Orchid bee community (Hymenoptera, Apidae) at an altitudinal gradient in a large forest fragment in southeastern Brazil. Revista Brasileira de Zoologia, 10: 249-256.

Nemésio, A. (2009). Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa, 2041: 1–242.

Oliveira, M.L. & 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, 12: 547-556. doi: 10.1590/S0101-81751995000300009

Oliveira-Filho, A.T. & Fontes, M.A.L. (2000). Patterns of floristic differentiation among Atlantic Forests in Southeastern Brazil and the influence of climate. Biotropica, 32: 793-810. doi: 10.1111/j.1744-7429.2000.tb00619.x

Oliveira-Filho, A.T., Tameirão-Neto, E., Carvalho, W.A.C.; Werneck, M., Brina, A.E., et al. (2005). Análise florística do compartimento arbóreo de áreas de Floresta Atlântica sensu lato na região das Bacias do Leste (Bahia, Minas Gerais, Espírito Santo e Rio de Janeiro). Rodriguésia: 56: 185-235.

Pereira, T.S, Costa, M.L.M.N., Moraes, L.F.D. & Luchiari, C. (2008). Fenologia de espécies arbóreas em Floresta Atlântica da Reserva Biológica de Poço das Antas, Rio de Janeiro, Brasil. Iheringia Sér. Bot., 63, 329-339.

Peruquetti, R.C., Campos, L.A.O., Coelho, C.D.P., Abrantes, C.V.M. & Lisboa, L.C.O. (1999). Abelhas Euglossini (Apidae) de áreas de Mata Atlântica: abundância, riqueza e aspectos biológicos. Revista Brasileira de Zoologia, 16: 101-118. doi: 10.1590/S0101-81751999000600012

Powell, A.H. & Powell, V.N. (1987). Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica, 19: 176-179.

RadamBrasil (1983) Levantamento de recursos naturais, v. 32. folha S / F 23 / 24. Rio de Janeiro/ Vitória. Ministério das Minas e Energia, Rio de Janeiro.

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. Revista Brasileira de Entomologia, 53: 95-101. doi: 10.1590/S0085-56262009000100022

Rebêlo, J.M.M. & Garófalo, C.A. (1991). Diversidade e sazonalidade de machos de Euglossini (Hymenoptera, Apidae) e preferências por iscas-odores em um fragmento de floresta no sudoeste do Brasil. Revista Brasileira de Biologia, 51: 787-799.

Rebêlo, J.M.M. & Garófalo, C.A. (1997). Comunidades de machos de Euglossini (Hymenoptera: Apidae) em matas semidecíduas do nordeste do estado de São Paulo. Anais da Sociedade Entomológica do Brasil, 26: 243-255.

Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J. & Hirota, M.M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142: 1141-1153. doi: 10.1016/j.biocon.2009.02.021

RIORURAL-GEF (2007) Marco Zero: Sub-Componente Monitoramento e Avaliação, Microbacia Santa Maria/Cambiocó, São José de Ubá. Relatório Técnico. Rio de Janeiro.

Rosenzweig, M.L. (1995) Species Diversity in Space and Time. Cambridge University Press, New York, NY.

Roubik, D.W. & Hanson, P.E. (2004). Orchids bees of Tropical America: Biology and Field Guide. INBio Press, Heredia, Costa Rica. 370p.

Roubik, D.W. (2001). Ups and downs in pollinator populations: When is there a decline? Conservation Ecology, 5: 2. [online] URL: http: //www. Consecol .org/vol5 /iss1 /art2/. (accessed on 14 March 2013).

Silva, G.C. & Nascimento, M.T. (2001). Fitossociologia de um remanescente de mata sobre tabuleiros no norte do estado do Rio de Janeiro (Mata do Carvão), RJ, Brasil. Revista Brasileira de Botânica, 24: 51-62. doi: 10.1590/S0100-84042001000100006

Silva, O., Rego, M.M.C., Albuquerque, P.M.C. & Ramos, M.C. (2009). Abelhas Euglossina (Hymenoptera: Apidae) em Área de Restinga do Nordeste do Maranhão. Neotropical Entomology, 38: 186-196. doi: 10.1590/S1519-566X2009000200004

Silveira, F.A., Melo, G.A.R. & Almeida, E.A.B. (2002). Abelhas Brasileiras, Sistemática e Identificação. Belo Horizonte, 253p.

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. Revista Brasileira de Entomologia, 55: 109-115.

Smith, A.R., López Quintero, I.J., Moreno Patiño, J.E., Roubik, D.W. & Wcislo, W.T. (2012). Pollen use by Megalopta sweat bees in relation to resource availability in a tropical forest. Ecological Entomology, 37: 309–317.

Sofia, S.H. & Suzuki, K.A. (2004). Comunidade de machos de abelhas Euglossina (Hymenoptera: Apidae) em fragmentos florestais no sul do Brasil. Neotropical Entomology, 33: 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 Série Zoologia, 94: 217-222. doi: 10.1590/S0073-47212004000200015

Souza, A.K.P., Hernández, M.I.M. & Martins, C.F. (2005). Riqueza, abundância e diversidade de Euglossina (Hymenoptera, Apidae) em três áreas da Reserva Biológica Guaribas, Paraíba, Brasil. Revista Brasileira de Zoologia, 22: 320-325. doi: 10.1590/S0101-81752005000200004

StatSoft, Inc. (2007). Statistica (data analysis software system), version 8.0. www.statsoft.com.

Storck-Tonon, D.; Morato, E.F. & Oliveira, M.L. (2009). Fauna de Euglossina (Hymenoptera: Apidae) da Amazônia Sul-Ocidental, Acre, Brasil. Acta Amazonica, 39: 693-706.

Sydney, N.V., Goncalves, R.B. & Faria, L.R.R. (2010). Padrões espaciais na distribuição de abelhas Euglossina (Hymenoptera, Apidae) da região Neotropical. Papéis Avulsos de Zoologia, 50: 667-679. doi: 10.1590/S0031-10492010004300001

Talora, D.C. & Morellato, L.P.C. (2000). Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brasil. Revista Brasileira de Botânica, 1: 13-26.

Ter Braak, C.J.F. (1995). Ordination. In: R.H.G. Jongman, C.J.F ter Braak, & O.F.R. van Tongeren (Eds.). Data analysis in community and landscape ecology (pp. 90-212). Cambridge, Cambridge University Press.

Tonhasca, Jr.A., Blackmer, J.L. & Albuquerque, G.S. (2002a). Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic Forest. Biotropica, 34: 416-422.

Tonhasca, Jr.A., Blackmer, J.L. & Albuquerque, G.S. (2002b). Within-hábitat heterogeneity of euglossine bee populations: a re-evaluation of the evidence. Journal of Tropical Ecology, 18: 929-933. doi: 10.1017/S0266467402002602.

Uehara-Prado, M. & Garófalo, C.A. (2006). Small-scale elevational variation in the abundance of Eufriesea violacea (Blanchard) (Hymenoptera: Apidae). Neotropical Entomology, 5: 446-451.

Veloso, H.P., Rangel-Filho, A.L.R. & Lima, J.C.A. (1991). Classificação de vegetação brasileira adaptada a um sistema universal. Rio de Janeiro, Instituto Brasileiro de Geografia e Estatística. 123p.

Wcislo, W.T. & Cane, J.H. (1996). Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Annual Review of Entomo-logy, 41: 257-86. doi: 10.1146/annurev.en.41.010196.001353

Whittaker, R.H. (1965). Dominance and diversity in land plant communities. Science, 147: 250-260.

Zahl, S. (1977). Jackknifing an Index of Diversity. Ecology, 58: 907-913. doi: 10.2307/1936227

Zucchi, R., Sakagami, S.F. & Camargo, J.M.F. (1969). Biological observations on a neotropical parasocial bee, Eulaema nigrita, with a review on the biology of Euglossinae. Journal of the Faculty of Sciences of Hokkaido Univerdity, 17: 271-380.




DOI: http://dx.doi.org/10.13102/sociobiology.v61i1.

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