Abstract
The spatial distribution of orchid bees was analyzed in a mosaic of tropical rainforest and rubber tree groves in the Atlantic coast of Brazil (ARRF), comparing abundances and species compositions between replicas of the following landscape elements: small and large forest fragments, and rubber tree groves. Species compositions responded to all of the factors examined (time, mosaic elements, and distances; P < 0.009). In contrast, total orchid bee abundance varied significantly only over time (P = 0.0001), but not among the different mosaic elements (P = 0.05). Fragment size and distances between the fragments have affected species composition and abundance of some few common species. Most local species were present in the rubber plantation, and several species were using this matrix as a source of odor. The seasonal quality shifting of this matrix (leaf fall) has had less influence on the spatial distribution of orchid bees than the distances between forest fragments and fragment sizes. Previous studies of forest fragmentation have shown very weak effects of matrix isolation in mosaics with 5 to 90 % of forest cover, which supports the generalized expectation that organisms with well-developed dispersal capacities can respond to much higher thresholds of forest fragmentation.
Similar content being viewed by others
References
Ackerman, J. D. (1983) Specificity and mutual dependency of the orchid Euglossine bee interaction. Biol. J. Linn. Soc. 20, 301–314
Ackerman, J. D. (1989) Geographic and seasonal variation in fragrance choices and preferences of male euglossine bees. Biotropica 21, 340–347
Ackerman, J. D. and Montalvo, A. M. (1985) Longevity of euglossine bees. Biotropica 17, 79–81
Ackerman, J. D., Mesler, M. R., Lu, K. L. and Montalvo, A. M. (1982). Food-foraging behavior of male Euglossini (Hymenoptera: Apidae): Vagabonds or Trapliners? Biotropica 14 (4), 241–248
Aguiar, W. M. and Gaglianone, M. C. (2012) Euglossine bees communities in small forest fragments of the Atlantic Forest in southeastern Brazil. Rev. Bras. Entomol. 56, 1–10
Anderson, M. J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46
Anderson, M. J. (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand
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. Neotrop. Entomol. 41 (4), 296–305.
Andrén, H. (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71, 355–366
Armbruster, W. S. (1993) Within-habitat heterogeneity in baiting samples of male euglossine bees: possible causes and implications. Biotropica 25, 122–128
Bascompte, J. and Solé, R. V. (1996) Habitat Fragmentation and Extinction Thresholds in spatialy explicit models. J. Anim. Ecol. 65, 465
Becker, P., Moure J. S. And Peralta, F. J. A. (1991) More about euglossine bees in Amazonian forest fragments. Biotropica 23, 586–591
Bezerra, C. P. And Martins, C. F. (2001) Diversidade de Euglossinae (Hymenoptera, Apidae) em dois fragmentos de Mata Atlântica localizados na região urbana de João Pessoa, Paraíba, Brasil. ver. Bras. Zool. 18, 823–835
Borrell, B. J. and Medeiros, M. J. (2004) Thermal stability and muscle efficiency in hovering orchid bees (Apidae: Euglossini). J. exp. Biol. 207, 2925–2933
Brosi, B. J. (2009) The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: euglossine). Biol. Conserv. 142, 414–423
Brown, J.H. (1995) Macroecology. University of Chicago Press, Chicago, USA
Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31 (20), 343–366
Cody, M. L. (1989) Discussion: Structure and Assembly of Communities. In : Roughgarden J., May, R.M. and Levin, S.A. (Eds), Perspectives in ecological theory. Princeton Univ. Press. New Jersey, USA, pp. 227–241
Dall, S. R. X. (2010) Managing risk: the perils of uncertainty. In: Weastneat, D. E. and Fox, C. W. (Eds), Evolutionary behavioral ecology. New York, Oxford Univ. Press. pp. 194–206
Darrault, R. O., Medeiros, P. C. R., Locatelli, E., Lopes, A. V., Machado, I. C., Schlindwein, C. (2006) Abelhas euglossine. In: Diversidade biológica e conservação da floresta Atlântica ao norte do Rio São Francisco (Pôrto, K.C.; Almeida-Cortêz, J.S. and Tabarelli, M. org.). MMA, Brasília. pp. 238–253
Dodson, C. H., Dressler, R. L., Hills, H. G., Adams, R. M., Williams, N. H. (1969) Biologically active compounds in orchid fragrances. Science 164, 1243–1249
Dressler, R. L. (1982) Biology of the orchid bees (Euglossine). Annu. Rev. Ecol. Syst.. 13, 373–394
Dudley, R. (1995) Extraordinary flight performance of orchid bees (Apidae: Euglossini) hovering in heliox (80 % He/20 % O2). J. exp. Biol. 198, 1065–1070
Eltz, T., Roubik, D.W., Lunau, K. (2005) Experience-dependent choices ensure species-specific fragrance accumulation in male orchid bees. Behav Ecol Sociobiol. 59, 149–156
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. Neotrop. Entomol. 37, 253–258
Faria, L.R. R. and Melo, G.A.R. (2007) Species of Euglossa (Glossura) in the Brazilian Atlantic forest, with taxonomic notes on Euglossa stellfeldi Moure (Hymenoptera, Apidae, Euglossina). Rev. Bras. Entomol. 51, 275–284
Fahrig, L. (2001) How much habitat is enough? Biol. Conserv. 100, 65–74
Flesher, K. M. (2006) The biogeography of the medium and large mammals in a human dominated landscape in the Atlantic Forest of Bahia, Brazil: evidence for the role of agroforestry systems as wildlife habitat. Program in Ecology and Evolution. School-New Brunswick Rutgers, The State University of New Jersey.
Gascon, C., Lovejoy, T. E. Jr., Malcom, R. O. B., Stouffer, J. R., Vasconcelos, P. C., Laurence, H. L., Zimmerman, B. W. F., Tocher, M., Borges, S. (1999) Matrix habitat and species richness in tropical forest remnants. Biol. Conserv. 91, 223–230
Hanski, I., Kouki, J., Halkka, A. (1993) Three explanations of the positive relationship between distribution and abundance of species. In : R. E. Ricklefs and D. Schluter (Eds), Species diversity in ecological communities. University of Chicago Press, Chicago, IL, pp. 108–16
Hanski, I. (1999) Metapopulation ecology. Oxford University Press, Oxford, United Kingdom
Holt, R. D. (1993) Ecology at the mesoscale: the influence of regional processes on local communities. In: Ricklefs, R. and Schluter, D. (Eds), Species Diversity in Ecological Communities. University of Chicago Press, Chicago, IL, pp. 77–88.
Janzen D. H. (1971) Euglossine bees as long distance pollinators of tropical plants. Science 171, 203–205
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 do Triângulo Mineiro. Rev. Bras. Zoo. 12, 227–239
Kroodsma, D. E. (1975) Flight distances of male euglossine bees in orchid pollination. Biotropica 7 (1), 71–72
Kuussaari, M., Saccheri, I., Camara, M., Hanski, I. (1998) Allee effect and population dynamics in the Glanville fritillary butterfly. Oikos 82, 384–392.
MacArthur, R. H., Diamond, J. M. and Karr, J. R. (1972) Density compensation in island faunas. Ecology 53, 330–342
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
Mccune, B., Grace, J. B. (2002) Analysis of Ecological communities. Oregon: MjM Software Design
Melo, P. M., Gimenes, M., Oliveira-Neto, A. (2009) Daily activity patterns of visits by males of four species of Eulaema (Apidea: Euglossini) to odor baits in a tropical forest fragment in Bahia. Bras. Zool. 26, 204–212
Michelin (2011) Histórico. Acesso em 22/04/2011. http://www.michelin-hevea.com/hevea/front/affich.jsp?codeRubrique=28102004110947026andlang=PT.
Milet-Pinheiro, P. ,Schlindwein, C. (2005) Do euglossine males (Apidae, euglossine) leave tropical rainforest to collect fragrances in sugarcane monocultures! Rev. Bras. Zoo. 22 (4), 853–858
Moorhead, L. C., Philpott, S. M. and Bichier, P. (2010) Epiphyte biodiversity in the coffee agricultural matrix: canopy stratification and distance from forest fragments. Conserv. Biol. 24, 737–746
Nemésio, A., Silveira, F. A. (2006) Edge effects on the orchid bee fauna (Hymenoptera: Apidae: Apini: Euglossina) at a large remnant of Atlantic Rain Forest in southeastern Brazil. Neotrop. Entomol. 35, 313–323
Nemésio, A., Silveira, F. A. (2010) Forest fragments with larger core areas better sustain diverse orchid bee faunas (Hymenoptera: Apidae: Euglossina). Neotrop. Entomol. 39, 555–561.
Neves, E. L., B. F. Viana. (2003) A fauna de abelhas da subtribo Euglossina (Hymenoptera, Apidae) do Estado da Bahia, Brasil, In: G.A.R. Melo and I.A. Santos (Eds). Apoidea Neotropica: Homenagem aos 90 anos de Jesus Santiago Moure. Criciúma, UNESC. pp. 223–229
Pereira J. P., Doretto, M., Leal, A. C., Castro, A. M. G. ,Rucker, N. A. (1996) Cadeia produtiva da borracha natural: análise diagnóstica e demandas atuais no Paraná. Ed. Iapar, Londrina-PR
Peruquetti, R. C., Campos, L. A. O., Coelho, C. D. P., Abrantes, C. V. M., Lisboa, L. C. O. (1999) Abelhas euglossine (Apidae) de áreas de Mata Atlântica: abundância, riqueza e aspectos biológicos. Rev. Bras. Zool. 16 ( 2), 101–118
Por, F. D. (1992) Sooretama. The Atlantic Rain Forest of Brazil. SPB Academic Publish. The Hague, The Netherlands
Powell, A. H. and Powell, G. V. N. (1987) Population dynamics of male euglossine bees in Amazonian Forest fragments. Biotropica 19, 176–179
Pulliam R. H. (1989) Individual behavior and the procurement of essential resources. In Roughgarden, J. May, R.M., Levin, S.A. (eds). 1989. Perspectives in ecological theory. Princeton University Press, New Jersey. pp.25-38
Pulliam, H. R. ,Danielson, B. J. (1991) Sources, sinks, and habitat selection: a landscape perspective on population dynamics. Am. Nat. 137 (Suppl.), S50-S66
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
Ramirez, S., R. L. Dressler ,M. Ospina. (2002) Abejas euglossinas (Hymenoptera: Apidae) de la Región Neotropical: Listado de especies com notas sobre su biología. Biol. Colomb. 3, 7–118
Raw, A. (1989) The dispersal of euglossine bees between isolated patches of eastern Brazilian wet forest (Hymenoptera, Apidae). Rev. Bras. Entomol. 33, 103–107
Reis, E. L. and Mello, F. A. F. (1987) Efeito da adubação no desenvolvimento da seringueira em formação (Hevea brasiliensis Muell, Arg.) no sul do estado da Bahia.: Anais da E.S.A. “Luiz de Queiroz” 44, 1165–1187
Roubik, D. W. (1993) Tropical pollinators in the canopy and understory: field data and theory for stratum “preferences.” J. Ins. Behav. 6, 659–673
Roubik, D. W. (2001) Ups and downs in pollinator populations: when is there a decline? Conserv. Ecol. 5, article 2. See http://www.consecol.org/vol5/iss1/art2.
Roubik, D. W. ,Hanson, P. E. (2004) Orchids bees: biology and field guide. San Jose, Costa Rica, INBIO
Rosa, J. F., Oliveira, J. P. L., Gurgel, Z. E. R., Duarte, C. S. A.; Ramalho, M. (2008) Estratificação da atividade de coleta de essência por abelhas Euglossina, em um remanescente de Mata Atlântica na Reserva da Michelin, Bahia, Brasil. Sitientibus. 8, 307–310
Roulston T. H., Goodell K. (2011) The role of resources and risks in regulating wild bee populations. Annu. Rev. Entomol. 56, 293–312
Silva, O., Rêgo, M. M. C., Albuquerque, P. M. C., Ramos, M. C. (2009) Abelhas euglossina (Hymenoptera, Apidae) em área de restinga do Nordeste do Maranhão, Brasil. Neotro. Entomol. 38, 186–196
Silveira, F. A., Melo, G. A. R. and Almeida, E. A. B. (2002) Abelhas Brasileiras: Sistemática e Identificação. Belo Horizonte, Edição do autor.
Schowalter, T. D. (2006) Insect Ecology: An Ecosystem Approach, 2nd edn. Elsevier, Burlington, USA
Summerville, K. S., and Crist, T. O. (2001) Effects of experimental habitat fragmentation on patch use by butterflies and skippers (Lepidoptera). Ecology 82, 1360–1370
Sutherland, W. J. (ed.) (2006) Ecological Census Techniques. 2a. ed. Cambridge Univ. Press
Taylor, P., Fahrig, L. And With, K. A. (2006) Landscape connectivity: a return to the basics. In: Krooks and Sanjayan, (Eds.). Connectivity Conservation (Cambridge University Press, Cambridge, UK. pp. 44–71
Tonhasca, A., Blackmer, J. L., Albuquerque, G. S. (2002) Within habitat heterogeneity of Euglossine bee populations: a reevaluation of the evidence. J. Trop. Ecol. 18, 929–933
Tonhasca, J. R., Albuquerque, A. G. S., Blackmer, J. L. (2003) Dispersal of euglossine bees between fragments of the brazilian Atlantic Forest. J. Trop. Ecol. 19, 990–102
Turner, M. G., Gardner, R. H. , O’Neill, R. V. (2003) Landscape ecology in theory and practice. Springer Verlag, New York.
Veloso, H. P.; Rangel Filho, A. L. and Lima, J. C. A. (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. IBGE, Rio de Janeiro.
Viana, B.F., A. M. P. Kleinert and E. L. das Neves. (2002) Comunidade de Euglossini (Hymenoptera, Apidae) das dunas litorâneas do Abaeté, Salvador, Bahia, Brasil. Rev. Bras. Entomol. 46, 539–545
Wiens, J. A. (1976) Population responses to patchy environments. Annu. Rev. Ecol. Syst. 7, 81–120
Williams, N. H. And Whitten, W. M. (1983) Orchid floral fragances and male euglossine bees: methods and advances in last sesquidecade. Biol. Bull. 164, 355–395
Williams, N. H., Dodson, C. H. (1972) Selective attraction of male euglossine bees to orchid floral fragrances and its importance in long distance pollen flow. Evolution 26, 84–95
Williams N. M., Thomson J. D. (1998) Trapline foraging by bumble bees. III. Temporal patterns of visitation and foraging success at single plants. Behav. Ecol. 9, 612–621
With, K. A. And Crist, T. O. (1995) Critical thresholds in species responses to landscape structure. Ecology 76, 2446–2459
Acknowledgments
We are grateful to Michelin for logistic support and CNPq (Process numbers 481113/2004-5, 478271/2008, and 474313/2011-5) and FAPESB (APR0114/2006) for financial support. We thank the ECOPOL team at UFBA for the help with fieldwork. We also thank the generous and careful criticism of two anonymous referees.
Author information
Authors and Affiliations
Corresponding author
Additional information
Distribution spatiale des abeilles à orchidée dans une mosaïque agro-forestière (forêt tropicale humide / plantations d’hévéas): utilisation de l’habitat ou connectivité.
Qualité de l’habitat / niveau de morcellement / paysage / Euglossini
Die räumliche Verbreitung von Prachtbienen in einem Regenwald / Gummigewinnungs-Nutzwaldmosaik: Habitatnutzung oder Vernetzung
Habitatsqualität / Landschaftskontext / Matrixnutzung
Manuscript editor: David Tarpy
Rights and permissions
About this article
Cite this article
Ramalho, M., Rosa, J.F., Dantas E Silva, M. et al. Spatial distribution of orchid bees in a rainforest/rubber agro-forest mosaic: habitat use or connectivity. Apidologie 44, 385–403 (2013). https://doi.org/10.1007/s13592-012-0189-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13592-012-0189-y