Skip to main content

Advertisement

SpringerLink
Log in

Dispersal of the orchid bee Euglossa imperialis over degraded habitat and intact forest

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Fragmentation of habitat can decrease resource availability and restrict movement among geographic areas. Persistence in fragmented landscapes depends on the maintenance of connectivity among populations, without which genetic diversity may decrease and lead to population declines. Bees are particularly vulnerable to the negative effects of low genetic diversity so it is important to understand patterns of dispersal for native bees living in fragmented areas. I used population genetic techniques to characterize patterns of genetic diversity and dispersal for the orchid bee Euglossa imperialis within and among forest fragments in southern Costa Rica, in which the furthest two fragments were 226 km from one another. In addition, I compared results of population genetic analyses conducted with all bees sampled, and results from analyses conducted with a reduced dataset containing only one individual per full sibling family from each site. For both datasets genetic diversity was low within forest fragments, with expected heterozygosity averaging 0.28 for the full dataset and 0.29 for the dataset containing only one full sibling per site. I found no evidence that deforested areas restricted dispersal; pairwise estimates of genetic differentiation \(F_{\text{ST}}^{\prime }\) among forest fragments averaged 0.01 for the full dataset, and 0 for the dataset containing only one full sibling per site. Genetic distance among sites within forest fragments was significantly correlated to geographic distance for the full dataset, but there was no significant correlation for the dataset that contained only one individual from each full sibling family. This suggests that family structure can drive results of analyses of genetic structure, although reductions in sample sizes following removal of full siblings may have reduced power to detect genetic structure. Despite no evidence for restricted dispersal, the low genetic diversity found suggests that E. imperialis may be an important candidate for future conservation monitoring.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ackerman JD, Montaivo AM (1985) Longevity of Euglossine bees. Biotropica 17:79–81

    Article  Google Scholar 

  • Ackerman JD, Mesler MR, Lu KL, Montaivo AM (1982) Food-foraging behavior of male Euglossini (Hymenoptera: Apidae): vagabonds or trapliners? Biotropica 14:281–289

    Article  Google Scholar 

  • Aguiar W, Sofia SH, Melo GAR, Gaglianone MC (2015) Changes in orchid bee communities across forest-agroecosystem boundaries in Brazilian Atlantic forest landscapes. Environ Entomol 44:1465–1471

    Article  PubMed  Google Scholar 

  • Augusto SC, Garofalo CA (2010) Task allocation and interactions among females in Euglossa carolina nests (Hymenoptera, Apidae, Euglossini). Apidologie 42:162–173

    Article  Google Scholar 

  • Becker P, Moure JS, Peralta JA (1991) More about Euglossine bees in Amazonian forest fragments. Biotropica 23:586–591

    Article  Google Scholar 

  • Beye M, Hasselman M, Fondrk MK, Page RP Jr, Om-Holt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419–429

    Article  CAS  PubMed  Google Scholar 

  • Boff S, Soro A, Paxton RJ, Alves-dos-Santos I (2013) Island isolation reduces genetic diversity and connectivity but does not significantly elevate diploid male production in a neotropical orchid bee. Con Gen 15:1123–1135

    Article  Google Scholar 

  • Briggs HM, Perfecto I, Brosi BJ (2013) The role of the agricultural matrix: coffee management and Euglossine bee (Hymenoptera: Apidae: Euglossini) communities in southern Mexico. Environ Entomol 42:1210–1217

    Article  CAS  PubMed  Google Scholar 

  • Brosi BJ (2009) The effects of forest fragmentation on euglossine bee communities: (Hymenoptera: Apidea: Euglossini). Biol Conserv 142:414–423

    Article  Google Scholar 

  • Brosi B, Daily GC, Shih TM, Ovideo F, Dura G (2007) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45:773–783

    Article  Google Scholar 

  • Cerântola N, Oi CA, Cervini M, Del Lama MA (2010) Genetic differentiation of urban populations of Euglossa cordata from the state of São Paulo Brazil. Apidologie. doi:10.1051/apido/2010055

    Google Scholar 

  • Clement R, Horn S (2001) Pre-Columbian land-use history in Costa Rica: a 3000-year record of forest clearance, agriculture and fires from Laguna Zoncho. Holocene 11:419–426

    Article  Google Scholar 

  • Crozier RH (1976) Counter-intuitive property of effective population size. Nature 262:384

    Article  CAS  PubMed  Google Scholar 

  • Davis ES, Murray TE, Fitzpatrick U, Brown MJF, Paxton RJ (2010) Landscape effects on extremely fragmented populations of a rare solitary bee, Colletes floralis. Mol Ecol 19:4922–4935

    Article  PubMed  Google Scholar 

  • Dressler RL (1982) Biology of the orchid bees (Euglossini). Annu Rev Ecol Syst 13:373–394

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:259–361

    Article  Google Scholar 

  • Eltz T, Roubik DW, Lunau K (2005a) Experience-dependent choices ensure species-specific fragrance accumulation in male orchid bees. Behav Ecol Sociobiol 59:149–156

    Article  Google Scholar 

  • Eltz T, Sager A, Lunau K (2005b) Juggling with volatiles: exposure of perfumes by displaying male orchid bees. J Comp Physiol A 191:575–581

    Article  Google Scholar 

  • Ewers RM, Didham RK (2005) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142

    Article  PubMed  Google Scholar 

  • Freiria GA, Ruim JB, Souza RF, Sofia SH (2012) Population structure and genetic diversity of the orchid bee Eufriesea violacea (Hymenoptera, Apidae, Euglossini) from Atlantic forest remnants in southern and southeastern Brazil. Apidologie 4:392–402

    Article  Google Scholar 

  • Gaggiotti OE, Hanski I (2004) Mechanisms of population extinction. In: Hanski I, Gaggiotti OE (eds) Ecology, genetics, and evolution of metapopulations. Elsevier Academic Press, San Diego, pp 337–366

    Chapter  Google Scholar 

  • Giangarelli DC, Freiria GA, Ferreira DG, Aguiar WM, Penha RES, Alves AN, Gaglionone MC, Sofia SH (2015) Orchid bees: a new assessment on the rarity of diploid males in populations of this group of neotropical pollinators. Apidologie 46:606–617

    Article  Google Scholar 

  • Goudet J, Jombart T (2015). Hierfstat: estimation and tests of hierarchical F-statistics. R package version 0.04-22

  • Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596

    Article  PubMed  Google Scholar 

  • Guillot G, Rousset F (2013) Dismanteling the Mantel tests. Methods Ecol Evol 4:336–344

    Article  Google Scholar 

  • Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population Is enough to accurately estimate allele frequencies. PLoS ONE 7:e45170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedrick PW, Parker JD (1997) Evolutionary genetics and genetic variation of haplodiploids and x-lined genes. Annu Rev Ecol Syst 28:55–83

    Article  Google Scholar 

  • Hooke RL, Martín-Duque JF (2012) Land transformations by humans: a review. GSA Today 22:4–10

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • Janzen DH (1971) Euglossine bees as long-distance pollinators of tropical plants. Science 171:203–205

    Article  CAS  PubMed  Google Scholar 

  • Janzen DH (1981) Reduction in euglossine bee species richness on Isla del Caño, a Costa Rican offshore island. Biotropica 13:238–239

    Article  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kremen C, Chaplin-Kramer R (2007) Insects as providers of crop pollination and pest control. In Stewart AJA, New TR, Lewis OT (eds.). Insect Conservation Biology, CABI, Cambridge, pp. 349–382

  • Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legendre P, Fortin M (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol Resour 10:831–844

    Article  PubMed  Google Scholar 

  • López‐Uribe MM, Zamudio KR, Cardoso CF, Danforth BN (2014) Climate, physiological tolerance and sex‐biased dispersal shape genetic structure of Neotropical orchid bees. Mol Ecol 23:1874–1890

  • Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 13:3223–3231

    Article  Google Scholar 

  • Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Mol Ecol Resour 11:5–18

    Article  PubMed  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Milet-Pinheiro Schlindwein C (2005) Do Euglossine males (Apidae, Euglossini) leave tropical rainforest to collect fragrances in sugarcane monocultures? Rev Bras Zool 22:853–858

    Article  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for landscape genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nemésio A, Silveira FA (2010) Forest fragments with larger core areas better sustain diverse orchid bee faunas (Hymenoptera: Apidae: Euglossina). Neotrop Entomol 39:555–561

    Article  PubMed  Google Scholar 

  • Oi CA, López-Uribe M, Cervini M, Del Lama MA (2013) Non-lethal method of DNA sampling in euglossine bees supported by mark-recapture experiments and microsatellite genotyping. J Insect Conserv 17:1071–1079

    Article  Google Scholar 

  • Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Article  Google Scholar 

  • Paetkau D, Strobeck C (1995) The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 4:519–520

    Article  CAS  PubMed  Google Scholar 

  • Paxton RJ, Zobel MU, Steiner J, Zillikens A (2009) Microsatellite loci for Euglossa annectans (Hymenoptera: Apidae) and their variability in other orchid bees. Mol Ecol Resour 9:1221–1223

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Penha RES, Gaglianone MC, Almeida FS, Boff SV, Sofia SH (2015) Mitochondrial DNA of Euglossa Iopoecila (Apidae, Euglossini) reveals two distinct lineages for this orchid bee species endemic to the Atlantic Forest. Apidologie 46:346–358

  • Pokorny T, Hannibal M, Quezada-Euan JJG, Hedenström E, Sjöberg N, Bång J, Eltz T (2013) Acquisition of species-specific perfume blends: influence of habitat-dependent compound availability on odour choices of male orchid bees (Euglossa spp.). Oecologia 172:417–425

    Article  CAS  PubMed  Google Scholar 

  • Pokorny T, Loose D, Dyker G, Quezada-Euán Eltz T (2015) Dispersal ability of male orchid bees and direct evidence for long-range flights. Apidologie 46:224–237

    Article  Google Scholar 

  • Powell AH, Powell GVN (1987) Population dynamics of male euglossine bees in Amazonian forest fragments. Biotropica 19:176–179

    Article  Google Scholar 

  • Pritchard JM, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2007) Documentation for structure software: version 2.2. University of Chicago, Chicago, pp 1–36

  • Prugh LR, Hodges KE, Sinclair ARE, Brashares JS (2008) Effects of habitat area and isolation on fragmented animal populations. Proc Natl Acad Sci 105:20770–20775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdansk A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Potts SG, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515

    Article  PubMed  Google Scholar 

  • Rocha Filho LC, Cerântola NCM, Garófalo CA, Imperatriz-Fonseca VL, Del Lama MA (2013) Genetic differentiation of the Euglossini (Hymenoptera, Apidae) populations on a mainland coastal plain and an island in southeastern Brazil. Genetica 141:65–74

    Article  PubMed  Google Scholar 

  • Rodriguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol Ecol Resour 12:873–874

    Article  PubMed  Google Scholar 

  • Rosa JF, Ramalho M, Arias MC (2016) Functional connectivity and genetic diversity of Eulaema atleticana (Apidae, Euglossina) in the Brazilian atlantic forest corridor: assessment of gene flow. Biotropica. doi:10.1111/btp.12321

    Google Scholar 

  • Roubik DW, Hanson PH (2004) Orchid bees of tropical America, 1st edn. INBio, Santo Domingo

    Google Scholar 

  • Roubik DW, Weight LA, Bonilla MA (1996) Population genetics, diploid males, and limits to social evolution of Euglossine bees. Evolution 50:931–935

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for windows and linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Ryman N, Palm S, Andre C, Carvalho GR, Dahlgren TG, Jorde PE, Laikre L, Larsson LC, Palmé A, Ruzzante DE (2006) Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 15:2031–2045

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Press, Cold Spring Harbor

    Google Scholar 

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Silva DP, Marco JR (2014) No evidence of habitat loss affecting the orchid bees Eulaema nigrita Lepeletier and Eufriesea auriceps Friese (Apidae: Euglossini) in the Brazilian Cerrado Savanna. Neotrop Entomol 43:509–518

    Article  CAS  PubMed  Google Scholar 

  • Silveira FA, Melo GAR, Almeida EAB (2002) Abelhas Brasileiras: sistemática e identificação, Belo Horizonte

  • Silviera GC, Freitas RF, Tosta THA, Rabelo LS, Gaglianone MC, Augusto SC (2015) The orchid bee fauna in the Brazilian savanna: do forest formations contribute to higher species diversity? Apidologie 46:197–208

    Article  Google Scholar 

  • Sofia SH, Paula FM, dos 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 28:479–484

    Article  CAS  Google Scholar 

  • Souza RO, Cervini M, Del Lama MA, Paxton RJ (2007) Microsatellite loci for euglossine bees (Hymenoptera: Apidae). Mol Ecol Notes 7:1352–1356

    Article  CAS  Google Scholar 

  • 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 64:3318–3326

    Article  PubMed  Google Scholar 

  • Stern DL (1991) Male territoriality and alternative male behaviors in the euglossine bee, Eulaema meriana (Hymenoptera: Apidae). J Kans Entomol Soc 64:421–437

    Google Scholar 

  • Suni SS, Brosi BJ (2012) Population genetics of orchid bees in a fragmented tropical landscape. Conserv Genet 13:323–332

    Article  Google Scholar 

  • Suni SS, Brosi BJ, Bronstein J (2014) Spatio-temporal genetic structure suggests high dispersal over a fragmented landscape. Biotropica 46:202–209

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor A (2003) Assessing the consequences of inbreeding for population fitness: past challenges and future prospects. Cambridge University Press, Cambridge

    Google Scholar 

  • Tonhasca A, Blackmer JL, Albuquerque GS (2002a) Abundance and diversity of Euglossine bees in the fragmented landscape of the Brazilian Atlantic forest. Biotropica 34:416–422

    Article  Google Scholar 

  • Tonhasca A, Blackmer JL, Albuquerque GS (2002b) Within-habitat heterogeneity of euglossine bee populations: a re-evaluation of the evidence. J Trop Ecol 18:929–933

    Article  Google Scholar 

  • van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front Zool 3:1–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang JL (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang JL (2013) Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution 67:3401–3411

    Article  Google Scholar 

  • Whiteley AR, Coombs JA, Hudy M, Robinson Z, Colton AR, Nislow KH, Letcher BH (2013) Fragmentation and patch size shape genetic structure of brook trout populations. Can J Fish Aquat Sci 70:678–688

  • Whiteley AR, McGarigal K, Schwartz MK (2014) Pronounced differences in genetic structure despite overall ecological similarity for two Ambystoma salamanders in the same landscape. Conserv Genet 15:573–591

    Article  Google Scholar 

  • 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 5:1–6

    Article  Google Scholar 

  • Winfree R, Aguilar R, Casquez DP, Lebuhn G, Aizen MA (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076

    Article  PubMed  Google Scholar 

  • Wright S (1951) The genetical structure of natural populations. Ann Eugen 15:323–354

    Article  CAS  PubMed  Google Scholar 

  • Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742–10746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 12:1183–1194

    Article  Google Scholar 

Download references

Acknowledgements

I thank the staff at the Las Cruces Biological Station near San Vito, Costa Rica, H. Woodard at Saladero Lodge in Costa Rica, M. Kaplan and the staff of University of Arizona’s genomics core facility for help with laboratory work, B. Brosi and T. Brookhart for fieldwork assistance, and R. Hopkins for comments on the manuscript. Fieldwork and genotyping were supported by the Center for Insect Science at the University of Arizona (NIH grant 5K12 GM000708).

Author information

Authors and Affiliations

  1. Department of Organismic and Evolutionary Biology & The Arnold Arboretum, Harvard University, Boston, MA, 02131, USA

    Sevan S. Suni

Authors
  1. Sevan S. Suni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sevan S. Suni.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resources 1–4 (DOCX 64 kb)

Online resources 5–11 (DOCX 427 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suni, S.S. Dispersal of the orchid bee Euglossa imperialis over degraded habitat and intact forest. Conserv Genet 18, 621–630 (2017). https://doi.org/10.1007/s10592-016-0902-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0902-x

Keywords

Search

Navigation