Continuous Micro-Environments Associated Orchid Bees Benefit from an Atlantic Forest Remnant, Paraná State, Brazil

Ana Isabel Sobreiro, Lucas Lopes da Silveira Peres, Samuel Boff, Jessica Amaral Henrique, Valter Vieira Alves Junior

Abstract


The fragmentation and habitat loss are the main causes of pollinators decline worldwide, however very little is known about the composition and distribution of neotropical pollinators along continuous micro-environments. To fill this gap, we carried out samplings of Euglossini bees in a continuous area of forest with micro-environments of primary (remnant) and secondary (regeneration) forest of Atlantic Forest. We evaluated the differences in the composition and uniformity of orchid bees in different micro-environments, in order to characterize the responses of the local environmental changes in the attraction of bees to chemical traps. Our results indicated that the composition and uniformity were similar between the two forest fragments studied here, although there are greater abundance of some species by micro-environments. We conclude that the characteristics of the sites in a continuous environment with primary and secondary forest do not seem to have an effect on the composition of the Euglossini fauna, and that the chemical substances are complementary in the attractiveness of the orchid bee males. Thus, our findings suggest that micro-environments in a continuous matrix near forest remnants can help to promote the reintegration of the orchid bee communities and contribute to the conservation of areas in process of forest regeneration.


Keywords


Conservation, Diversity, Euglossini, Pollinators, Primary versus secondary forest

Full Text:

PDF

References


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

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. (2012). Euglossini 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

Aguiar, W.M., Melo, G.A.R. & Gaglianone, M.C. (2014). 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. Sociobiology, 61: 68-77. doi: 10.13102/sociobiology.v61i1.68-77

Boff S., Soro, A., Paxton, R.J., Alves-dos-Santos, I. (2014). Island isolation reduces genetic diversity and connectivity but does not significantly elevate diploid male production in a neotropical orchid bee. Conservation Genetics, 15: 1123-35. doi: 10.1007/s10592-014-0605-0

Boscolo, D., Tokumoto, P.M., Ferreria, P.A., Ribeiro, J.W. & Santos, J.S. (2017). Positive responses of flower visiting bees to landscape heterogeneity depend on functional connectivity levels. Perspectives in Ecology and Conservation, 15: 18-24. doi: 10.1016/j.pecon.2017.03.002.

Botsch, J.C., Walter, S.T., Karubian, J., González, N., González, E.K. & Brosi, B.J. (2017). Impacts of forest fragmentation on orchid bee (Hymenoptera: Apidae: Euglossini) communities in the Chocó biodiversity hotspot of northwest Ecuador. Journal of Insect Conservation, 21: 633-643. doi: 10.1007/s10841-017-0006-z

Brasil. (1994). Define formações vegetais primarias e estágios sucessionais de vegetação secundária. Ministério do Meio Ambiente, Conselho Nacional de Meio Ambiente, CONAMA. Resolução CONAMA n°2, de 18 de março de 1994. In: Resoluções, 1994. Retrived from: http://www.mma.gov.br/port/conama/res/res94/res0294.html (accessed date: 29 November, 2016).

Brasil. (2009). Caderno de Licenciamento Ambiental. Programa Nacional de Capacitação de gestores ambientais: licenciamento ambiental / Ministério do Meio Ambiente. – Brasília: MMA, 2009.

Brasil. (2010a). Mata Atlântica Manual de Adequação Ambiental. Ministério do Meio Ambiente. Secretaria de Biodiversidade e Florestas. Departamento de Conservação da Biodiversidade Núcleo Mata Atlântica e Pampa. Brasília: MMA/SBF, 2010.

Brasil. (2010b). Florestas do Brasil em resumo – 2010: dados de 2005-2010. Serviço de Florestal Brasileiro – Brasília: SFB, 2010.

Cameron, S.A. (2004). Phylogeny and biology of neotropical orchid bees (Euglossini). Annual Review of Entomology, 49: 377–404. doi: 10.1146/annurev.ento.49.072103.115855

Campos, L.A.C., Silveira, F.A., Oliveira, M.L., Abrantes, C.V.M., Morato, E.F. & Melo, G.A.R. (1989). Utilização de armadilhas para a captura de machos de Euglossini (Hymenoptera, Apoidea). Revista Brasileira de Zoologia, 6: 621-626. doi: 10.1590/S0101-81751989000400008

Clements, F.E. (1916). Plant succession: an analysis of the development of vegetation. Carnegie Institute of Washington, No. 242, USA. doi: 10.5962/bhl.title.56234

Cordeiro, G.D., Boff, S., Caetano, T.A., Fernandes, P.C. & Alves-dos-Santos, I. (2012). Euglossini bees (Apidae) in Atlantic forest areas of São Paulo state Southeastern Brazil. Apidologie, 44: 254-267. doi: 10.1007/s13592-012-0176-3

Dambros, C. (2014). poncho.R. figshare. Code. doi: 10.6084/m9.figshare.753347.v3

Dodson, C.H., Dreller, R.L., Hills, H.G., Adams, R.M. & Williams, N.H. (1969). Biologically active compounds in orchid fragrances. Science, 164: 1243-1249. doi: 10.1126/science.164.3885.1243

Dressler, R.L. (1982). Biology of the orchid bees (Euglossini). Annual Review of Ecology, Evolution and Systematics, 13: 373-394. doi: 10.1146/annurev.es.13.110182.002105

Eltz, T., Bause, C., Hund, K., Quezada-Euan, J.J.G. & Pokorny, T. (2015). Correlates of perfume load in male orchid bees. Chemoecology, 25: 193-199. doi: 10.1007/s00049-015-0190-9

Ferreira, R.P., Martins, C., Dutra, M.C., Mentone, C.B. & Antonini, Y. (2013). Old fragments of forest inside an urban area able to keep orchid bee (Hymenoptera: Apidae: Euglossini) assemblages? The Case of a Brazilian Historical City. Neotropical Entomology, 42: 466-473. doi: 10.1007/s13744-013-0145-1

Ferronato, M.C.F., Giangarelli, D.C., Mazzaro, D., Uemura, N. & Sofia, S.H. (2017). Orchid bee (Apidae: Euglossini) communities in Atlantic Forest remnants and restored areas in Paraná State, Brazil. Neotropical Entomology, 47: 352-361. doi: 10.1007/s13744-017-0530-2

Fischer, L.K., Eichfeld, J., Kowarik, J. & Buchholz, S. (2016). Disentangling urban habitat and matrix effects on wild bee species. Peer J, 4: e2729. doi: 10.7717/peerj.2729

Gathmann, A. & Tscharntke, T. (2002). Foraging ranges of solitary bees. Journal of Animal Ecology, 71: 757-764. doi: 10.1046/j.1365-2656.2002.00641.x

Giangarelli, D.C., Aguiar, W.M. & Sofia, S.H. (2015). Orchid bee (Hymenoptera: Apidae: Euglossini) assemblages from three different threatened phytophysiognomies of the subtropical Brazilian Atlantic Forest. Apidologie, 46: 71-83. doi: 10.1007/s13592-014-0303-4

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: 610-615. doi: 10.1590/S1519-566X2009000500008

Giannini, T.C., Garibaldi, L.A., Acosta, A.T., Silva, J.S., Maia, K.P., Saraiva, A.M., Guimarães Jr, P.R. & Kleinert, A.M.P. (2015). Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLOS ONE, 10: e0137198. doi: 10.1371/journal.pone.0137198

Gonçalves, R.B., Scherer, V.L. & Oliveira, O.S. (2014). The orchid bees (Hymenoptera, Apidae, Euglossina) in a forest fragment from western Paraná state, Brazil. Papéis Avulsos de Zoologia, 54: 63-68. doi: 10.1590/0031-1049.2014.54.06

Google Earth-mapas. Retrived from: http://mapas.google.com. (acessed date: 22 September, 2017).

Griswold T., Herndon J.D. & Gonzalez V.H. (2015). First record of the orchid bee genus Eufriesea Cockerell (Hymenoptera: Apidae: Euglossini) in the United States. Zootaxa, 3957: 342-346. doi: 10.11646/zootaxa.3957.3.7.

Hansen, M.C., Potapov, P.V., Moore, R., Hancher, M., Turubanova, S.A., Tyukavina, A., Thau, D., Stehman, S.V., Goetz, S.J., Loveland, T.R., Kommareddy, A., Egorov, A., Chini, L., Justice, C.O. & Townshend, J.R.C. (2013). High-resolution global maps of 21st-century forest cover change. Science, 342: 850-853. doi: 10.1126/science.1244693.

Hurlbert, S.H. (1971). The nonconcept of species diversity: a critique and alternative parameters. Ecology, 52: 577–586. doi: 10.2307/1934145

IBAMA. (1991). Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis. PORTARIA N.º 83-N, DE 26 DE SETEMBRO DE 1991 - In: Resoluções, 1991. Retrived from: http://www.mp.go.gov.br/nat_sucroalcooleiro/Documentos/legislacao/Geral/florestas/flo10 (accessed date: 05 September, 2016).

ITAIPU BINACIONAL. (1978). Inventário Florestal da região de influência da represa Itaipu. Curitiba: Itaipu Binacional. Retrieved from: http://www.scielo.br/scielo.php?script=sci_nlinks&ref=000176& pid=S1414753X201400010000500013&lng=en (accessed date: 05 September, 2016).

Janzen, D.H. (1971). Euglossine bees as long-distance pollinators of tropical plants. Science, 171: 203-205. doi: 10.1126/science.171.3967.203

Jha, S. & Dick, C.W. (2010). Native bees mediate long-distance pollen dispersal in a shade coffee landscape mosaic. PNAS, 107: 13760-13764. doi: 10.1073/pnas.1002490107

Knoll, F.R.N. & Penatti, N.C. (2012). Habitat fragmentation effects on the orchid bee communities in remnant forests of southeastern Brazil. Neotropical Entomology, 41: 355-365. doi: 10.1007/s13744-012-0057-5

Magurran, A.E. (2004). Measuring biological diversity. Blackwell Publishing company, Oxford, 256 p.

Mateus, S., Andrade-Silva, A.C.R. & Garófalo, C.A. (2015). Diversity and temporal variation in the orchid bee community (Hymenoptera: Apidae) of a remnant of a Neotropical Seasonal Semi-deciduous Forest. Sociobiology, 62: 571-577. doi: 10. 13102/sociobiology.v62i4.391

McCravy, K.W., Dyke, J.V., Creedy, T.J. & Roubik, D.W. (2016). Orchid bees (Hymenoptera: Apidae: Euglossini) of Cusuco National Park, State of Cortés, Honduras. Florida Entomologist, 99: 765-768. doi: 10.1653/024.099.0431

Medeiros, R.L.S., Aguiar, W.M., Aguiar, C.M.L. & Borges, I.G.M. (2017). The orchid bee communities in different phytophysiognomies in the Atlantic Forest: from lowland to montane rainforests. Sociobiology, 64: 182-190. doi: 10.13102/sociobiology.v64i2.1348

Melo, A.S. (2008). O que ganhamos ‘confundindo’ riqueza de espécies e equabilidade em um índice de diversidade? Biota Neotropica, 8: 021-027.

Milet-Pinheiro, P. & Schlinweln, C. (2005). Do euglossini males (Apidae, Euglossini) leave tropical rainforest to collect fragrances in sugarcane monocultures? Revista Brasileira de Zoologia, 22: 853-858. doi: 10.1590/S0101-81752005000400008

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). Boletim do Museu Paraense Emílio Goeldi, série Zoologia, 10: 95-105.

Moreira, E.F., Boscolo, D. & Viana, B.F. (2015). Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales. PLOS ONE, 10: e0123628. doi: 10.1371/journal.pone.0123628

Murlis, J., Elkinton, J.S. & Cardé, R.T. (1992). Odor plumes and how insect use them. Annual Review of Entomology, 37: 505-532. doi: 10.1146/annurev.en.37.010192.002445

Neame, L.A., Griswold, T. & Elle, E.B. (2012). Pollinator nesting guilds respond differently to urban habitat fragmentation in an oak-savannah ecosystem. Insect Conservation and Diversity, 6: 56-66. doi: 10.1111/j.1752-4598.2012.00187.x

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

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

Nemésio, A. (2012). Methodological concerns and challenges in ecological studies with orchid bees (Hymenoptera: Apidae: Euglossina). Bioscience Journal, 28: 118-135.

Nemésio, A. (2013). Are orchid bees at risk? First comparative survey suggests declining populations of forest-dependent species. Brazilian Journal of Biology, 73: 367-374. doi: 10. 1590/S1519-69842013000200017

Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Henry M., Stevens, H., Szoecs E. & Wagner, H. (2018). vegan: Community Ecology Package. R package version 2.4-6. . Retrived from: https://CRAN.R project.org/package=vegan (accessed date: 01 August, 2017).

Oliveira, R., Pinto, C.E. & Schlindwein, C. (2015). Two common species dominate the species-rich Euglossini bee fauna of an Atlantic Rainforest remnant in Pernambuco, Brazil. Brazilian Journal of Biology, 75: 1-8. doi: 10.1590/1519-6984.18513.

Oliveira-Junior, J.M.B., Almeida, S.M., Rodrigues, L., Silvério-Júnior, A.J. & Anjos-Silva, E.J. (2015). Orchid bees (Apidae: Euglossini) in a forest fragment in the ecotone cerrado-amazonian forest, Brazil. Acta Biologica Colombiana, 20: 67-78. doi: 10.15446/abc.v20n3.41122

Pemberton, R.W. & Wheeler, G.S. (2006). Orchid bees don’t need orchids evidence from the naturalization of an orchid bee in Florida. Ecology, 87: 1995-2001. doi: 90/0012-9658(2006)87[1995:OBDNOE]2.0.CO;2

Penha, R.E., Gaglianone, M.C., Almeida, F.S., Boff, S.V., Sofia, S.H. (2015). Mitochondrial DNA of Euglossa iopoecila (Apidae, Euglossini) reveals two distinct lineages for this orchid bee species endemic to the Atlantic Forest. Apidologie, 46:346-58. doi: 10.1007/s13592-014-0329-7

Peruquetti, R.C., Campo, 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

Pokorny, T., Loose, D., Dyker, G., Javier, J., Quezada-Euán, J.J.G. & Eltz, T. (2014). Dispersal ability of male orchid bees and direct evidence for long-range flights. Apidologie, 46: 224-237. doi: 10.1007/s13592-014-0317-y

R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

R Development Core Team (2013). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria.

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

Ramírez, S., Dressler, R.L. & Ospina, M. (2002). Abejas euglossinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies con notas sobre su biología. Biota Colombiana, 3: 7-118.

Raw, A. (1989). The dispersal of Euglossini bees between isolated patches of eastern brazilian wet forest (Hymenoptera, Apidae). Revista Brasileira de Entomologia, 33: 103-107.

Rebêlo, J.M.M. & Cabral, A.J. (1997). Espécies de Euglossinae (Hymenoptera, Apidae) de Barreirinhas, Zona do Litoral da Baixada Oriental Maranhense. Acta Amazônica, 27: 145-152.

Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F. & 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

Rosa, J.F., Ramalho, M., Monteiro, D. & Silva, M.D. (2015). Permeability of matrices of agricultural crops to Euglossina bees (Hymenoptera, Apidae) in the Atlantic Rain Forest. Apidologie, 46: 691-702. doi: 10.1007/s13592-015-0359-9

Roubik, D.W. & Hanson, P.E. (2004). Orchids bees of tropical America: biology and field guide. Instituto Nacional de Biodiversidade [INBio], Santo Domingo de Heredia, Costa Rica, 352pp.

Roubik, D.W. (1989). Ecology and natural history of tropical bees. Cambridge University Press, New York, 514pp. doi: 10.1126/science.248.4958.1026

Santos, A.M. & Sofia, S.H. (2002). Horário de atividade de machos de Euglossinae (Hymenoptera, Apidae) em um fragmento de floresta semidecídua no Norte do Estado do Paraná. Acta Scientiarum, 24: 375-381. doi: 10.4025/actascibiolsci.v24i0.2297

Santos, C.F. & Absy, M.L. (2012). Interactions between carpenter bees and orchid bees (Hymenoptera: Apidae) in flowers of Bertholletia excels Bonpl. (Lecythidaceae). Acta Amazonica, 42: 89-94. doi: 10.1590/S0044-59672012000100011

Silva, F.S. & 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. Brazilian Journal of Biology, 62: 15-23. doi: 10.1590/S1519-69842002000100003

Silveira, G.C., Nascimento, A.M., Sofia, S.H. & Augusto, S.C. (2011). Diversity of the Euglossini bee community (Hymenoptera, Apidae) of an Atlantic Forest remnant in southeastern Brazil. Revista Brasileira de Entomologia, 55: 109-115. doi: 10.1590/S0085-56262011000100017

Sofia, S.H. & Suzuki, K.M. (2004). Comunidades de machos de abelhas Euglossina (Hymenoptera: Apidae) em fragmentos florestais do sul do Brasil. Neotropical Entomology, 33: 693-702. doi: 10.1590/S1519-566X2004000600006

Sofia, S.H., Santos, A.M. & Silva, C.R.M. (2004). Euglossini bees (Hymenoptera, Apidae) in a remnant of Atlantic Forest in Paraná State, Brazil. Iheringia Série Zoologia, 94: 217-222. doi: 10.1590/S0073-47212004000200015

Stern, D.L. (1991). Male territoriality and alternative male behaviors in the Euglossini bee, Eulaema meriana (Hymenoptera: Apidae). Journal of the Kansas Entomological Society, 64: 421-437.

Storck-Tonon, D., Morato, E.F., Melo, A.W.F. & Oliveira, M.L. (2013). Orchid bees of forest fragments in southwestern Amazônia. Biota Neotropica, 13: 133-141. doi: 10.1590/S1676-06032013000100015

Wikelski M., Moxley J., Eaton-Mordas A., López-Uribe M.M., Holland R., Moskowitz D., Roubik D.W. & Kays R. (2010). Large-range movements of neotropical orchid bees observed via radio telemetry. PLOS ONE, 5: 5–10. doi: 10.1371/journal.pone.0010738

Ziober, B.R. & Zanirato, S.H. (2014). Ações para a salvaguarda da biodiversidade na construção da usina hidrelétrica Itaipu Binacional. Ambiente & Sociedade, 17: 59-75. Retrieved from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1414-753X2014000100005. (accessed date: 10 January, 2017).




DOI: http://dx.doi.org/10.13102/sociobiology.v66i2.3443

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2018: 0.604