Skip to main content

No Evidence of Habitat Loss Affecting the Orchid Bees Eulaema nigrita Lepeletier and Eufriesea auriceps Friese (Apidae: Euglossini) in the Brazilian Cerrado Savanna

Abstract

Habitat loss, landscape fragmentation, and agriculture intensification constitute the main threats to bees. As the organisms responsible for almost one third of the food produced worldwide, there are growing concerns on bees’ response to human-related disturbances. Among all bee groups, orchid bees (Apidae: Euglossini) compose an interesting group to test landscape-related hypotheses. In here, we tested the effect of landscape features (amount of anthropic areas and isolation) on the probability of occurrence and the abundances of both Eulaema nigrita Lepeletier and Eufriesea auriceps Friese in the Cerrado savanna. In general, we did not observe any effect of landscape features on the probability of occurrence and abundances of both species in our sampling sites. Given their potential high dispersal abilities, these bee species may be less sensitive to fragmented landscapes or even positively affected by the increase of anthropic habitats. Since we sampled many E. nigrita specimens in highly preserved Cerrado savanna areas, we believe that at least for this biome, this species may not be a good indicator of landscape disturbance.

This is a preview of subscription content, access via your institution.

Fig 1
Fig 2

References

  1. Ackerman JD (1983) Diversity and seasonality of male Euglossine bees (Hymenoptera: Apidae) in Central Panamá. Ecology 64:274–283

    Article  Google Scholar 

  2. Aguiar WM, Gaglianone MC (2012) Euglossine bee communities in small forest fragments of the Atlantic Forest, Rio de Janeiro state, southeastern Brazil (Hymenoptera, Apidae). Rev Bras Entomol 56:210–219

    Article  Google Scholar 

  3. Alvarenga PEF, Freitas RF, Augusto SC (2007) Diversidade de Euglossini (Hymenoptera: Apidae) em áreas de cerrado no triangulo mineiro, MG. Biosci J 23:30–37

    Google Scholar 

  4. Andrade-Silva ACR, Nemésio A, de Oliveira FF, Nascimento FS (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 41:296–305

    CAS  PubMed  Article  Google Scholar 

  5. Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci U S A 110:4656–4660

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  6. Batalha MA, Mantovani W (2000) Reproductive phenological patterns of cerrado plant species at the Pé-de-Gigante Reserve (Santa Rita do Passa Quatro, SP, Brazil): a comparison between the herbaceous and woody floras. Rev Bras Biol 60:129–145

    CAS  PubMed  Article  Google Scholar 

  7. Batalha MA, Martins FR (2004) Reproductive phenology of the cerrado plant community in Emas National Park (Central Brazil). Aust J Bot 52:149

    Article  Google Scholar 

  8. Baum KA, Haynes KJ, Dillemuth FP, Cronin JT (2004) The matrix enhances the effectiveness of corridors and stepping stones. Ecology 85:2671–2676

    Article  Google Scholar 

  9. Becker P, Moure JS, Peralta FJA (1991) More about euglossine bees in Amazonian forest fragments. Biotropica 23:586–591

    Article  Google Scholar 

  10. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354

    CAS  PubMed  Article  Google Scholar 

  11. Brittain CA, Vighi M, Bommarco R, Settele J, Potts SG (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl Ecol 11:106–115

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  13. Brosi BJ, Daily GC, Shih TM, Oviedo F, Durán G (2008) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45:773–783

    Article  Google Scholar 

  14. Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615

    CAS  PubMed  Article  Google Scholar 

  15. Campos LAO, Silveira FA, Oliveira ML, Abrantes CVM, Morato EF, Melo GAR (1989) Utilização de armadilhas para a captura de machos de Euglossini (Hymenoptera, Apoidea). Rev Bras Zool 6:621–626

    Article  Google Scholar 

  16. Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kansas Entomol Soc 60:145–147

    Google Scholar 

  17. Cardoso P, Erwin TL, Borges PAV, New TR (2011) The seven impediments in invertebrate conservation and how to overcome them. Biol Conserv 144:2647–2655

    Article  Google Scholar 

  18. Carrijo TF, Brandão D, Oliveira DE, Costa DA, Santos T (2008) Effects of pasture implantation on the termite (Isoptera) fauna in the Central Brazilian Savanna (Cerrado). J Insect Conserv 13:575–581

    Article  Google Scholar 

  19. Carvalho FMV, De Marco PJ, Ferreira LG (2009) The Cerrado into-pieces: habitat fragmentation as a function of landscape use in the savannas of central Brazil. Biol Conserv 142:1392–1403

    Article  Google Scholar 

  20. Casey TM, May ML, Morgan KR (1985) Flight energetics of Euglossini bees in relation to morphology and wing stroke frequency. J Exp Biol 289:271–289

    Google Scholar 

  21. Cirera X, Masset E (2010) Income distribution trends and future food demand. Philos Trans R Soc B Biol Sci 365:2821–2834

    Article  Google Scholar 

  22. Davies KF, Margules CR, Lawrence JF (2004) A synergistic effect puts rare, specialized species at greater risk of extinction. Ecology 85:265–271

    Article  Google Scholar 

  23. Diniz-Filho JAF, De Marco JP, Hawkins BA (2010) Defying the curse of ignorance: perspectives in insect macroecology and conservation biogeography. Insect Conserv Divers 3:172–179

    Google Scholar 

  24. Dobrovolski R, Diniz-Filho JAF, Loyola RD, De Marco JP (2011) Agricultural expansion and the fate of global conservation priorities. Biodivers Conserv 20:2445–2459

    Article  Google Scholar 

  25. Dobrovolski R, Loyola RD, Guilhaumon F, Gouveia SF, Diniz-Filho JAF (2013) Global agricultural expansion and carnivore conservation biogeography. Biol Conserv 165:162–170

    Article  Google Scholar 

  26. Dodson CH, Dressler RL, Hills GH, Adams RM, Williams NH (1969) Biologically active compounds in orchid fragrances. Science 167:1243–1249

    Article  Google Scholar 

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

    Article  Google Scholar 

  28. Eltz T, Ayasse M, Lunau K (2006) Species-specific antennal response to tibial fragrances in the male orchid bees. J Chem Ecol 32:71–79

    CAS  PubMed  Article  Google Scholar 

  29. Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

    Article  Google Scholar 

  30. Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller RJ, Sirami C, Siriwardena GM, Martin JL (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112

    PubMed  Article  Google Scholar 

  31. Faria LRR, Silveira FA (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 Neotrop 11:87–94

    Article  Google Scholar 

  32. Foley JA, Defries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs K, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574

    CAS  PubMed  Article  Google Scholar 

  33. Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S et al (2011) Solutions for a cultivated planet. Nature 478:337–342

    CAS  PubMed  Article  Google Scholar 

  34. 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 43:392–402

    Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  36. Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853

    CAS  PubMed  Article  Google Scholar 

  37. Hanski I (1994) A practical model of metapopulation dynamics. J Anim Ecol 63:151–162

    Article  Google Scholar 

  38. Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251

    Article  Google Scholar 

  39. IBGE (2004) Mapa de biomas do Brasil. Escala 1:5.000.000. In: http://mapas.ibge.gov.br/biomas2/viewer.htm. Accessed 11/09/2013

  40. Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landsc Ecol 27:929–941

    Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  42. Janzen DH, DeVries PJ, Higgins ML, Kimsey LS (1982) Seasonal and site variation in Costa Rican euglossine bees at chemical baits in lowland deciduous and evergreen forests. Ecology 63:66–74

    CAS  Article  Google Scholar 

  43. Kearney J (2010) Food consumption trends and drivers. Philos Trans R Soc B Biol Sci 365:2793–2807

    Article  Google Scholar 

  44. Kimsey LS (1982) Systematics of bees of the genus Eufriesea. Univ Calif Publ Entomol 95:1–125

    Google Scholar 

  45. Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter IF, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274:303–313

    Article  Google Scholar 

  46. Klink CA, Machado RB (2005) Conservation of the Brazilian Cerrado. Conserv Biol 19:707–713

    Article  Google Scholar 

  47. Klink CA, Moreira AG (2002) Past and current human occupation, and land use. In: Oliveira PS, Marquis RJ (eds) Cerrados Brazil Ecol Nat Hist a Neotrop Savanna. Columbia University Press, New York, pp 69–88

    Google Scholar 

  48. Knoll FRN, Penatti NC (2012) Habitat fragmentation effects on the orchid bee communities in remnant forests of southeastern Brazil. Neotrop Entomol 41:355–365

    Article  Google Scholar 

  49. Kupfer JA, Malanson GP, Franklin SB (2006) Not seeing the ocean for the islands: the mediating influence of matrix-based processes on forest fragmentation effects. Glob Ecol Biogeogr 15:8–20

    Article  Google Scholar 

  50. MacArthur RH, Levins R (1964) Competition, habitat selection, and character displacement in a patchy environment. Proc Natl Acad Sci U S A 51:1207–1210

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  51. Martins CF, Souza AKP (2005) Estratificação vertical de abelhas Euglossina (Hymenoptera, Apidae) em uma área de Mata Atlântica, Paraíba, Brasil. Rev Bras Zool 22:913–918

    Article  Google Scholar 

  52. Mattozo VC, Faria LRR, 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 Mus Zool Univ São Paulo 51:505–515

    Google Scholar 

  53. May ML, Casey TM (1983) Thermoregulation and heat exchange in Euglossine bees. Physiol Zool 56:541–551

    Google Scholar 

  54. McGarigal K, Marks BJ (1995) FRAGSTATS: spatial pattern analysis program for quantifying landscape structure

  55. Metzger J, Décamps H (1997) The structural connectivity threshold: an hypothesis in conservation biology at the landscape scale. Acta Oecol 18:1–12

    Article  Google Scholar 

  56. Michener CD (2007) The bees of the world, 2nd ed. 2nd:992 pp

  57. Milet-Pinheiro P, Schlindwein C (2005) Do euglossine males (Apidae, Euglossini) leave tropical rainforest to collect fragrances in sugar cane monocultures? Rev Bras Zool 22:853–858

    Article  Google Scholar 

  58. Moilanen A, Hanski I (1998) Metapopulation dynamics: effects of habitat quality and landscape structure. Ecology 79:2503–2515

    Article  Google Scholar 

  59. Morato EF (1994) Abundância e riqueza de machos de Euglossini (Hymenoptera: Apidae) em mata de terra firme e áreas de derrubada, nas vizinhanças de Manaus (Brasil). Bol Mus Para Emílio Goeldi 10:95–105

    Google Scholar 

  60. Morato EF (1998) Estudos sobre comunidades de abelhas Euglossini. An do III Encontro sobre Abelhas Ribeirão Preto, São Paulo. Ribeirão Preto, SP-Brasil, pp 135–143

  61. Moura DC, Schlindwein C (2009) Mata ciliar do Rio São Francisco como biocorredor para Euglossini (Hymenoptera: Apidae) de florestas tropicais úmidas. Neotrop Entomol 38:281–284

    PubMed  Article  Google Scholar 

  62. Moure JS (1967) Descrição de algumas espécies de Euglossine (Hym. Apoidea). Atlas Simp Biota Amaz 55:373–394

    Google Scholar 

  63. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  PubMed  Article  Google Scholar 

  64. Nemésio A (2008) Orchid bee community (Hymenoptera, Apidae) at an altitudinal gradient in a large forest fragment in southeastern Brazil. Rev Bras Zoociências 10:251–258

    Google Scholar 

  65. Nemésio A (2012) Methodological concerns and challenges in ecological studies with orchid bees (Hymenoptera: Apidae: Euglossina). Biosci J 28:118–135

    Google Scholar 

  66. Nemésio A (2013) Are orchid bees at risk? First comparative survey suggests declining populations of forest-dependent species. Braz J Biol 73:367–374

    PubMed  Article  Google Scholar 

  67. Nemésio A, Faria LRR (2004) First assessment of the orchid-bee fauna (Hymenoptera: Apidae) at Parque Estadual do Rio Preto, a cerrado area in southeastern. Lundiana 5:113–117

    Google Scholar 

  68. Nemésio A, Morato EF (2004) Euglossina (Hymenoptera: Apidae: Apini) of the Humaitá Reserve, Acre state, Brazilian Amazon, with comments on bait trap efficiency. Rev Tecnol Ambient 10:71–80

    Google Scholar 

  69. Nemésio A, Morato EF (2006) The orchid-bee fauna (Hymenoptera: Apidae) of Acre state (northwestern Brazil) and a re-evaluation of euglossine bait-trapping. Lundiana 7:59–64

    Google Scholar 

  70. Nemésio A, Rasmussen C (2011) Nomenclatural issues in the orchid bees (Hymenoptera: Apidae: Euglossina) and an updated catalogue. Zootaxa 42:1–42

    Google Scholar 

  71. 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 35:313–323

    PubMed  Article  Google Scholar 

  72. Nemésio A, Silveira FA (2007a) Orchid bee fauna (Hymenoptera: Apidae: Euglossina) of Atlantic Forest fragments inside an urban area in southeastern Brazil. Neotrop Entomol 36:186–191

    PubMed  Article  Google Scholar 

  73. Nemésio A, Silveira FA (2007b) Diversity and distribution of orchid bees (Hymenoptera: Apidae) with a revised checklist of species. Neotrop Entomol 36:874–888

    PubMed  Article  Google Scholar 

  74. 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

    PubMed  Article  Google Scholar 

  75. Nemésio A, Vasconcelos HL (2013) Beta diversity of orchid bees in a tropical biodiversity hotspot. Biodivers Conserv 22:1647–1661

    Article  Google Scholar 

  76. Nemésio A, Vasconcelos HL (2014) Effectiveness of two sampling protocols to survey orchid bees (Hymenoptera: Apidae) in the Neotropics. J Insect Conserv. doi:10.1007/s10841-014-9629-5

    Google Scholar 

  77. Nemésio A, Santos Júnior JE, Santos FR (2013) Eufriesea zhangi sp. n. (Hymenoptera: Apidae: Euglossina), a new orchid bee from Brazil revealed by molecular and morphological characters. Zootaxa 3609:568–582

    PubMed  Article  Google Scholar 

  78. 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 16:101–118

    Article  Google Scholar 

  79. Pinheiro F, Diniz IR, Coelho D, Bandeira MPS (2002) Seasonal pattern of insect abundance in the Brazilian cerrado. Aust Ecol 27:132–136

    Article  Google Scholar 

  80. Pires EP, Morgado LN, Souza B, Carvalho CF, Nemésio A (2013) Community of orchid bees (Hymenoptera: Apidae) in transitional vegetation between Cerrado and Atlantic Forest in southeastern Brazil. Rev Bras Biol 73:507–513

    CAS  Google Scholar 

  81. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  83. Raw A (1989) The dispersal of Euglossine bees between isolated patches of eastern Brazilian wet forest (Hymenoptera, Apidae). Rev Bras Entomol 33:103–107

    Google Scholar 

  84. Rebêlo JMM, Cabral AJM (1997) Abelhas Euglossinae de Barreirinhas, zona do litoral da baixada oriental maranhense. Acta Amazon 27:145–152

    Google Scholar 

  85. Rebêlo JMM, Silva FS (1999) Distribuição das abelhas Euglossini (Hymenoptera: Apidae) no estado do Maranhão, Brasil. Soc Entomol Bras 28:389–401

    Article  Google Scholar 

  86. Ribeiro JF, Walter BMT (1998) Fitofisionomias do Bioma Cerrado. In: Sano SM, Almeida SP (eds) Cerrado Ambient e Flora. Embrapa, Planaltina, pp 89–168

    Google Scholar 

  87. Robinson RA, Sutherland WJ (2002) Post-war changes in arable farming and biodiversity in Great Britain. J Appl Ecol 39:157–176

    Article  Google Scholar 

  88. Rockström J, Steffen W, Noone K, Persson A, Chapin FS III, Lambin EF, Lenton TM, Scheffer M, Folke C, Schellnhuber HJ, Nykvist B, de Wit CA, Hughes T, Van Der Leeuw S, Rohde H, Sörlin S, Snyder PK, Costanza R, Svedin U et al (2009) A safe operating space for humanity. Nature 461:472–475

    PubMed  Article  Google Scholar 

  89. Roubik DW (2001) Ups and downs in pollinator abundance peaks populations: when is there a decline? Conserv Ecol 5:article 2

  90. Roubik DW, Hanson PE (2004) Orchid bees of tropical America: biology and field guide, 1st ed. 370

  91. Sano EE, Rosa R, Brito JLS, Ferreira LG (2008) Mapeamento semidetalhado do uso da terra do Bioma Cerrado. Pesq Agrop Brasileira 43:153–156

    Article  Google Scholar 

  92. Sheffield CS, Pindar A, Packer L, Kevan PG (2013) The potential of cleptoparasitic bees as indicator taxa for assessing bee communities. Apidologie

  93. Silva DP, Aguiar AJC, Melo GAR, Anjos-Silva EJ, De Marco JP (2013) Amazonian species within the Cerrado savanna: new records and potential distribution for Aglae caerulea (Apidae: Euglossini). Apidologie 44:673–683

    Article  Google Scholar 

  94. Sofia SH, Suzuki KM (2004) Comunidades de machos de abelhas Euglossina (Hymenoptera: Apidae) em fragmentos florestais no sul do Brasil. Neotrop Entomol 33:693–702

    Article  Google Scholar 

  95. 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 28:479–484

    CAS  Article  Google Scholar 

  96. StatiSoft I (2004) Statistica 7.0

  97. Storck-Tonon D, Morato EF, Oliveira ML (2009) Fauna de Euglossina (Hymenoptera: Apidae) da Amazônia Sul-Ocidental, Acre, Brasil. Acta Amazon 39:693–706

    Article  Google Scholar 

  98. Storck-Tonon D, Morato EF, Melo AWF, Oliveira ML (2013) Orchid bees of forest fragments in Southwestern Amazonia. Biota Neotrop 13:133–141

    Article  Google Scholar 

  99. Taki H, Kevan PG, Ascher JS (2007) Landscape effects of forest loss in a pollination system. Landsc Ecol 22:1575–1587

    Article  Google Scholar 

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

    Article  Google Scholar 

  101. Tonhasca A Jr, Albuquerque GS, Blackmer JL (2003) Dispersal of euglossine bees between fragments of the Brazilian Atlantic forest. J Trop Ecol 19:99–102

    Article  Google Scholar 

  102. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    PubMed  Article  Google Scholar 

  103. Viotti MA, Moura FR, Lourenço AP (2013) Species diversity and temporal variation of the orchid-bee fauna (Hymenoptera, Apidae) in a conservation gradient of a rocky field area in the Espinhaço Range, state of Minas Gerais, southeastern Brazil. Neotrop Entomol 42:565–575

    Article  Google Scholar 

  104. 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:e10738

    PubMed Central  PubMed  Article  Google Scholar 

  105. Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291

    Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  107. Zar JH (2010) Biostatistical analysis, 5th ed. 944

  108. Zucchi R, Sakagami SF, Camargo JMF (1969) Biological observations on a neotropical parasocial bee, Eulaema nigrita, with a review on the biology of Euglossinae (Hymenoptera, Apidae). J Fac Sci Hokkaido Univ Ser VI Zool 17:271–380

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank Prof. Dr. André Nemésio for the confirmation of the species identities. The authors are also grateful to Dário P. Silva Júnior, Mírian Cristina de Almeida, and Fábio Martins Vilar de Carvalho who helped in the field campaigns. DPS received a doctorate scholarship from CNPq—Conselho Nacional de Desenvolvimento Científico e Tecnológico (147204/2010-0). PDMJ has been continuously supported by several productivity grants from CNPQ. DPS and PDMJ thank the financial support obtained from CNPq (477639/2010-0), Fundação “O Boticário” de Proteção à Natureza (0880/2010-2), and Whitley Wildlife Conservation Trust.

Author information

Affiliations

Authors

Corresponding author

Correspondence to D P Silva.

Additional information

Edited by Fernando B Noll – UNESP

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 16 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Silva, D.P., De Marco, P. 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 (2014). https://doi.org/10.1007/s13744-014-0244-7

Download citation

Keywords

  • Disturbed areas
  • euglossine bees
  • fragmentation
  • generalist bee species
  • indicator species
  • landscape change