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Genetica

, Volume 141, Issue 1–3, pp 65–74 | Cite as

Genetic differentiation of the Euglossini (Hymenoptera, Apidae) populations on a mainland coastal plain and an island in southeastern Brazil

  • Léo Correia da Rocha FilhoEmail author
  • Natália de Campos Muradas Cerântola
  • Carlos Alberto Garófalo
  • Vera Lúcia Imperatriz-Fonseca
  • Marco Antonio Del Lama
Article

Abstract

Euglossini bees are among the main pollinators of plant species in tropical and subtropical forests in Central and South America. These bees are known as long-distance pollinators due to their exceptional flight performance. Here we assessed through microsatellite loci the gene variation and genetic differentiation between populations of four abundant Euglossini species populations sampled in two areas, Picinguaba (mainland) and Anchieta Island, Ubatuba, São Paulo State, southeastern Brazil. There was no significant genetic differentiation between the island and mainland samples of Euglossa cordata (Fst = 0.008, P = 0.60), Eulaema cingulata (Fst = 0.029, P = 0.29) and Eulaema nigrita (Fst = 0.062, P = 0.38), but a significant gene differentiation between mainland and island samples of Euglossa stellfeldi (Fst = 0.028, P = 0.016) was detected. As expected, our results showed that the water body that separates the island from the mainland does not constitute a geographic barrier for these Euglossini bees. The absence of populational structuring of three out the four species studied corroborates previous reports on those bees, characterized by large populations, with high gene diversity and gene flow and very low levels of diploid males. But the Eg. stellfeldi results clearly point that dispersal ability is not similar to all euglossine bees, what requires the development of different conservationist strategies to the Euglossini species.

Keywords

Population Genetics Euglossini Gene flow Dispersion Microsatellites 

Notes

Acknowledgments

The authors would like to thank “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq; Grant No. 141022/2007-8) for the scholarship granted to LC Rocha-Filho, “Fundação de Amparo à Pesquisa do Estado de São Paulo” (FAPESP 2004/15801-0) and the staff at the study sites (Picinguaba and Anchieta Island) for their support.

References

  1. Ackerman JD, Montalvo AM (1985) Longevity of euglossine bees. Biotropica 17:79–81CrossRefGoogle Scholar
  2. Aguiar WM, Gaglianone MC (2008) Comunidade de Abelhas Euglossina (Hymenoptera: Apidae) em Remanescentes de Mata Estacional Semidecidual sobre Tabuleiro no Estado do Rio de Janeiro. Neotrop Entomol 37:118–125PubMedCrossRefGoogle Scholar
  3. Archie JW (1985) Statistical analysis of heterozygosity data: independent sample comparisons. Evolution 39:623–637CrossRefGoogle Scholar
  4. Augusto SC, Garófalo CA (2011) Task allocation and interactions among females in Euglossa carolina nests (Hymenoptera, Apidae, Euglossi). Apidologie 42:162–173CrossRefGoogle Scholar
  5. Becker P, Moure JS, Peralta FJA (1991) More about euglossine bees in Amazonian forest fragments. Biotropica 23:340–591CrossRefGoogle Scholar
  6. Bembé B (2004) Functional morphology in male euglossine bees and their ability to spray fragrances (Hymenoptera, Apidae, Euglossini). Apidologie 35:283–291CrossRefGoogle Scholar
  7. Bonilla-Gómez MA (1999) Caracterização da estrutura espaço-temporal da comunidade de abelhas euglossinas (Hymenoptera, Apidae) na Hiléia Baiana. PhD Thesis. Universidade Estadual de CampinasGoogle Scholar
  8. Brosi BJ (2009) The effects of forest fragmentation on euglossine bee communities (Hymenoptera: Apidae: Euglossini). Biol Conserv 142:414–423CrossRefGoogle Scholar
  9. Cameron SA, Ramírez S (2001) Nest architecture and nesting ecology of orchid bee Eulaema meriana (Hymenoptera: Apidae: Euglossini). J Kansas Entomol Soc 74:142–165Google Scholar
  10. Cerântola NCM, Oi CA, Cervini M, Del Lama MA (2011) Genetic differentiation of urban populations of Euglossa cordata from the state of São Paulo, Brazil. Apidologie 42:214–222CrossRefGoogle Scholar
  11. Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557PubMedCrossRefGoogle Scholar
  12. Darvill B, Ellis JS, Lye GC, Goulson D (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol Ecol 15:601–611PubMedCrossRefGoogle Scholar
  13. Dick CW, Roubik DW, Gruber KF, Bermingham E (2004) Long-distance gene flow and across-Andean dispersal of lowland rainforest bee (Apidae: Euglossini) revealed by comparative mitochondrial DNA phylogeography. Mol Ecol 13:3775–3785PubMedCrossRefGoogle Scholar
  14. Dodson CH, Hills HG (1966) Gas chromatography of orchid fragrances. Amer Orchid Soc Bull 35:720–725Google Scholar
  15. Dodson CH, Dressler HG, Hills RM, Adams RM, Williams NH (1969) Biologically active compounds in orchid fragrances. Science 164:1243–1249PubMedCrossRefGoogle Scholar
  16. Dressler RL (1968) Pollination by euglossine bees. Evolution 22:202–210CrossRefGoogle Scholar
  17. Dressler RL (1982) Biology of the orchid bees (Euglossini). Annu Rev Ecol Syst 13:373–394CrossRefGoogle Scholar
  18. Ellis JS, Knight ME, Darvill B, Goulson D (2006) Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Mol Ecol 15:4375–4386PubMedCrossRefGoogle Scholar
  19. Eltz T, Sager A, Lunau K (2005) Juggling with volatiles: exposure of perfumes by displaying male orchid bees. J Comp Physiol A 191:575–581CrossRefGoogle Scholar
  20. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.1: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  21. Faria LRR Jr, Melo GAR (2007) Species of Euglossa (Glossura) in the Brazilian Atlantic forest, with taxonomic notes on Euglossa stellfeldi Moure (Hymenoptera, Apidae, Euglossina). Rev Bras Entomol 51:275–284Google Scholar
  22. Freiria GA, Ruim JB, Souza RF, Sofia SH (2011) Population structure and genetic diversity of the orchid bee Eufriesea violacea (Hymenoptera, Apidae, Euglossini) from Atlantic Forest remnants in southern and southeastern Brazil. Apidologie 43:392–402CrossRefGoogle Scholar
  23. Garófalo CA (1985) Social structure of Euglossa cordata nests (Hymenoptera: Apidae: Euglossini). Entomol Gen 11:77–83Google Scholar
  24. Gárofalo CA, Camillo E, Serrano JC, Rebêlo JMM (1993) Utilization of trap nests by Euglossini species (Hymenoptera, Apidae). Rev Bras Biol 52:177–187Google Scholar
  25. Gerlach G, Schill R (1991) Composition of orchid scents attracting euglossine bees. Bot Acta 104:379–391Google Scholar
  26. Giangarelli DC, Freiria GA, Colatreli OP, Suzuki KM, Sofia SH (2009) Eufriesea violacea (Blanchard) (Hymenoptera: Apidae): an orchid bee apparently sensitive to size reduction in forest patches. Neotrop Entomol 38:610–615PubMedCrossRefGoogle Scholar
  27. Goudet J (2001) FSTAT: a program to estimate and test gene diversity and fixation indices (version 2.9.3.2) [updated from Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  28. Guillaumon JR, Marcondes MAP, Negreiros OC, Mota IS, Emmerich W, Barbosa AF, Branco IHDC, Camara JJC, Ostini S, Pereira RTL, Scorvo Filho JD, Shimomichi PY, Silva SA, Melo Neto JE (1989) Plano de Manejo do Parque Estadual da Ilha Anchieta. I.F.—Série Registros. Instituto Florestal, São PauloGoogle Scholar
  29. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638PubMedGoogle Scholar
  30. Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205PubMedCrossRefGoogle Scholar
  31. Janzen DH (1981) Reduction in euglossine bees species richness on Isla del cano, a costa rican offshore island. Biotropica 13:238–240CrossRefGoogle Scholar
  32. Janzen DH, Devries PJ, Higgins ML, Kimsey LS (1982) Seasonal and site variation in costa rica euglossine bees at chemical baits in lowland deciduous and evergreen forest. Ecology 63:66–74CrossRefGoogle Scholar
  33. Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
  34. Kalinowski ST (2005) Hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  35. Kimsey LS (1980) The behaviour of male orchid bees (Apidae, Hymenoptera, Insecta) and the question of leks. Anim Behav 28:996–1004CrossRefGoogle Scholar
  36. Knoll FRN, Bego LR, Imperatriz-Fonseca VL (2004) Abelhas da Juréia. In: Marques OAV, Duleba W (orgs) Estação Ecológica Juréia-Itatins. Ambiente físico, flora e fauna. Editora Holos, Ribeirão Preto, p 222–229Google Scholar
  37. Kroodsma DE (1975) Flight distances of male euglossine bees in orchid pollination. Biotropica 7:71–72CrossRefGoogle Scholar
  38. López-Uribe MM (2006) Dinâmica e estrutura genética populacional de abelhas Euglossini (Hymenoptera: Apidae) visitantes florais de Thevetia peruviana em áreas urbanas. Universidade Federal de São Carlos, DissertationGoogle Scholar
  39. López-Uribe MM, Oi CA, Del Lama MA (2008) Nectar-foraging behavior of Euglossine bees (Hymenoptera: Apidae) in urban areas. Apidologie 39:410–418CrossRefGoogle Scholar
  40. Mattozo VC, Faria LRR Jr, Melo GAR (2011) Orchid bees (Hymenoptera: Apidae) in the coastal forests of southern Brazil: diversity, efficiency of sampling methods and comparison with other Atlantic forest surveys. Pap Avulsos Zool 51:505–515Google Scholar
  41. Milet-Pinheiro P, Schlindwein C (2005) Do euglossine males (Apidae, Euglossini) leave tropical rainforest to collect fragrances in sugarcane monocultures? Rev Bras Zool 22:853–858CrossRefGoogle Scholar
  42. Morato EF (1994) Abundância e riqueza de machos de Euglossinae (Hymenoptera, Apidae) em mata de terra firme e áreas de derrubada nas vizinhanças de Manaus (Brasil). Bol Mus Para Emilio Goeldi. Ser Zool 10:95–105Google Scholar
  43. Moure JS, Melo GAR, Faria Jr LRR (2008) Euglossini Latreille, 1802. In: Moure JS, Urban D, Melo GAR (orgs) Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region—online version. http://www.moure.cria.org.br/catalogue. Accessed 15 March 2012
  44. Murren CJ (2002) Effects of habitat fragmentation on pollination: Pollinators, pollinia viability and reproductive success. J Ecol 90:100–107CrossRefGoogle Scholar
  45. Nemésio A (2010) The orchid-bee fauna (Hymenoptera: Apidae) of a forest remnant in northeastern Brazil, with new geographic records and an identification key to the known species of the Atlantic Forest of northeastern Brazil. Zootaxa 2656:55–66Google Scholar
  46. Nemésio A (2011) The orchid-bee fauna (Hymenoptera: Apidae) of a forest remnant in southern Bahia, Brazil, with new geographic records and an identification key to the known species of the area. Zootaxa 2821:47–54Google Scholar
  47. Nemésio A, Silveira FA (2006) Edge effects on the orchid-bee fauna (Hymenoptera: Apidae) at a large remnant of Atlantic Rain Forest in southeastern Brazil. Neotrop Entomol 35:313–323PubMedCrossRefGoogle Scholar
  48. Neves EL, Viana BF (1997) Inventário da fauna de Euglossinae (Hymenoptera, Apidae) do baixo sul da Bahia, Brasil. Rev Bras Zool 14:831–837CrossRefGoogle Scholar
  49. Paxton RJ, Zobel UM, Steiner J, Zillikens A (2009) Microsatellite loci for Euglossa annectans (Hymenoptera: Apidae) and their variability in other orchid bees. Mol Ecol Resour 9:1221–1223PubMedCrossRefGoogle Scholar
  50. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. population genetic software for teaching and research. Mol Ecol 6:288–295CrossRefGoogle Scholar
  51. Peruquetti RC, Campos LAO, Coelho CDP, Abrantes CVM, Lisboa LCO (1999) Abelhas Euglossini (Apidae) de áreas de Mata Atlântica: abundância, riqueza e aspectos biológicos. Rev Bras Zool 16:101–118CrossRefGoogle Scholar
  52. Powell AH, Powell GVN (1987) Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica 19:176–179CrossRefGoogle Scholar
  53. Ramalho AV, Gaglianone MC, Oliveira ML (2009) Comunidades de abelhas Euglossina (Hymenoptera; Apidae) em fragmentos de Mata Atlântica no Sudeste do Brasil. Rev Bras Entomol 53:95–101CrossRefGoogle Scholar
  54. Raw A (1989) The dispersal of euglossine bees between isolated patches of eastern Brazilian wet forest (Hymenoptera, Apidae). Rev Bras Entomol 33:103–107Google Scholar
  55. Rocha-Filho LC, Garófalo CA Community ecology of euglossine bees (Hymenoptera, Apidae) in the coastal Atlantic Forest of Sao Paulo State, Brazil. J Insect Sci (in press)Google Scholar
  56. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New YorkCrossRefGoogle Scholar
  57. Roubik DW, Hanson PE (2004) Orchid bees of tropical America: biology and field guide. Instituto Nacional de Biodiversidad, Santo Domingo de HerediaGoogle Scholar
  58. Santos ML, Garófalo CA (1994) Nesting biology and nest re-use of Eulaema nigrita (Hymenoptera, Apidae, Euglossini). Insectes Soc 41:99–110CrossRefGoogle Scholar
  59. Sofia SH, Paula FM, Santos AM, Almeida FS, Sodré LMK (2005) Genetic structure analysis of Eufriesea violacea (Hymenoptera, Apidae) populations from southern Brazilian Atlantic rainforest remnants. Genet Mol Biol 28:479–484CrossRefGoogle Scholar
  60. Souza RO, Cervini M, Del Lama MA, Paxton RJ (2007) Microsatellite loci for euglossine bees (Hymenoptera: Apidae). Mol Ecol Notes 7:1352–1356CrossRefGoogle Scholar
  61. Souza RO, Del Lama MA, Cervini M, Mortari N, Eltz T, Zimmermann Y, Bach C, Brosi BJ, Suni S, Quezada-Euán JJG, Paxton RJ (2010) Conservation genetics of neotropical pollinators revisited: microsatellite analysis suggests that diploid males are rare in orchid bees. Evolution 64:3318–3326PubMedCrossRefGoogle Scholar
  62. Steiner J, Zillikens A, Kamke R, Feja EP, Falkenberg DB (2010) Bees and melittophilous plants of secondary Atlantic forest habitats at Santa Catarina Island, southern Brazil. Oecol Aust 14:16–39CrossRefGoogle Scholar
  63. Suni SS, Brosi BJ (2012) Population genetics of orchid bees in a fragmented tropical landscape. Conserv Genet 13:323–332CrossRefGoogle Scholar
  64. Takahashi J, Ayabe T, Mitsuhata M, Shimizu I, Ono M (2008) Diploid male production in a rare and locally distributed bumblebee, Bombus florilegus (Hymenoptera, Apidae). Insectes Soc 55:43–50CrossRefGoogle Scholar
  65. Tonhasca A, Blackmer JL, Albuquerque GS (2002) Abundance and diversity of euglossine bees in the fragmented landscape of the Brazilian Atlantic forest. Biotropica 34:416–422Google Scholar
  66. Tonhasca A, Albuquerque GS, Blackmer JL (2003) Dispersal of euglossine bees between fragments of the Brazilian Atlantic Forest. J Trop Ecol 19:99–102CrossRefGoogle Scholar
  67. Walsh PS, Metzger DA, Higuchi R (1991) Chelex® 100 as a medium of simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513PubMedGoogle Scholar
  68. Whitten WN, Young AM, Williams NH (1989) Function of glandular secretions in fragrance collection by male euglossine bees. J Chem Ecol 19:3017–3027CrossRefGoogle Scholar
  69. Wikelski M, Moxley J, Eaton-Mordas A, López-Uribe MM, Holland R, Moskowitz D, Roubik DW, Kays R (2010) Large-range movements of neotropical orchid bees observed via radio telemetry. PLoS ONE 5:1–6CrossRefGoogle Scholar
  70. Wilson A, Arecase P, Keller LF, Pruett CL, Winker K, Patten MA, Chan Y (2009) The contribution of island populations to in situ genetic conservation. Conserv Genet 10:419–430CrossRefGoogle Scholar
  71. Zimmermann Y, Roubik DW, Eltz T (2006) Species-specific attraction to pheromonal analogues in orchid bees. Behav Ecol Sociobiol 60:833–843CrossRefGoogle Scholar
  72. Zimmermann Y, Schorkopf DLP, Mortiz RFA, Pemberton RW, Quezada-Euán JJG, Eltz T (2011) Population genetic structure of orchid bees (Euglossini) in anthropogenically altered landscapes. Conserv Genet 12:1183–1194CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Léo Correia da Rocha Filho
    • 1
    Email author
  • Natália de Campos Muradas Cerântola
    • 2
  • Carlos Alberto Garófalo
    • 1
  • Vera Lúcia Imperatriz-Fonseca
    • 3
  • Marco Antonio Del Lama
    • 2
  1. 1.Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto-FFCLRPUniversidade de São Paulo-USPRibeirão PretoBrazil
  2. 2.Departamento de Genética e EvoluçãoUniversidade Federal de São Carlos-UFSCarSão CarlosBrazil
  3. 3.Departamento de Ciências AnimaisUniversidade Federal Rural do SemiáridoMossoróBrazil

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