Biodiversity and Conservation

, Volume 20, Issue 13, pp 2981–3001 | Cite as

Diversity and community composition of euglossine bee assemblages (Hymenoptera: Apidae) in western Amazonia

  • Stefan Abrahamczyk
  • Peter Gottleuber
  • Christian Matauschek
  • Michael Kessler
Original Paper
First Online:
Received:
Accepted:

Abstract

Tropical forests are known for their diverse insect fauna. We aimed to determine the effect and relative importance of latitude, elevation and climatic factors affecting species richness and turnover in euglossine bee assemblages along a gradient of 18° latitude from tropical rainforests to subtropical, deciduous dry forests in Peru and Bolivia. Sixteen forest sites were sampled during the dry season. Variance partitioning techniques were applied to assess the relative effects of the spatial and environmental variables on species richness and composition. Furthermore, we conducted a Species Indicator Analysis to find characteristic species for the biogeographic zones. There was a significant decrease in species richness towards the subtropical area. The best predictors of species richness were precipitation and its consequences on soil properties as well as temperature seasonality. The abundance of euglossines was most closely related to precipitation and soil-pH, but the causal links of abundance to these factors is unclear since soil-pH itself is correlated to a drastic turnover of vegetation structure. Based on the analysis of assemblage composition we propose three different assemblages with a transitional zone at the southern tropical area. The biogeographical distribution of euglossine bees along our study transect appears to be primarily related to climatic conditions and does not reflect the common subdividion of Amazonia into drainage systems.

Keywords

Beta diversity Bolivia Euglossini Indicator species Latitudinal gradient Orchid bees Peru Species turnover 
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Notes

Acknowledgements

We thank Y. Gareca, C. Hamel, S. K. Herzog, S. Reichle, V. Sandoval and J. Q. Vidoz for their support and advice during field work. We are grateful to the Botanical Garden in Santa Cruz, the University of Cochabamba, Prometa, the municipal governments of Villa Tunari and Río Seco, and R. Clarke Gemuseus for the permission to work on their land, and to G. Lamas, the National Herbarium at La Paz, the Museum for Natural History, Lima, Peru, as well as the Ministry of the Environment and the INRENA for supporting our study. Furthermore, we thank B. Bembé and G. Gerlach for technical advice, C. Rasmussen and B. Bembé for the support and advice in identifying the specimens, J. Diller for the kind support and advice in the preparation phase, S. Sylvester for reviewing the manuscript, and M. Schwerdtfeger for the baiting agents. Funding was provided by the Konrad-Adenauer-Stiftung and the DFG (Deutsche Forschungsgemeinschaft).

References

  1. Abrahamczyk S, Kessler M (2010) Hummingbird diversity, food niche characters, and assemblage composition along a latitudinal precipitation gradient in the Bolivian lowlands. J Ornithol 151:615–625CrossRefGoogle Scholar
  2. Ackerman D (1983a) Specificity and mutual dependency of the orchid-euglossine bee interaction. Biol J Linn Soc 20:301–314CrossRefGoogle Scholar
  3. Ackerman D (1983b) Euglossine bee pollination of the orchid Cochleanthes lipscombiae: a food source mimic. Am J Bot 70:830–834CrossRefGoogle Scholar
  4. Ackerman D (1983c) Diversity and seasonality of the male euglossine bees (Hymenoptera: Apidae) in central Panamá. Ecol 64:274–283CrossRefGoogle Scholar
  5. Ackerman D (1985) Euglossine bees and their nectar hosts. In: D’Arcy WG, Correa MD (eds) The botany and natural history of Panama: La botánica e historia natural de Panamá. Mis Bot Garden, St. LouisGoogle Scholar
  6. Anjos-Silva EJ, Rebêlo JMM (2006) A new species of Exaerete Hoffmannsegg (Hymenoptera: Apidae: Euglossini) from Brazil. Zootaxa 1105:27–35Google Scholar
  7. Bates JM, Hackett SJ, Cracraft J (1998) Area-relationships in the Neotropical lowlands: an hypothesis based on raw distributions of Passerine birds. J Biogeogr 25:783–793CrossRefGoogle Scholar
  8. Bawa KS (1990) Plant pollinator interactions in tropical forests. Ann Rev Ecol Evol Syst 21:399–422CrossRefGoogle Scholar
  9. Bembé B (2004) Revision der Euglossa cordata-Gruppe und Untersuchung zur Funktionsmorphologie und Faunistik der Euglossini. Ph.D Thesis, Ludwig- Maximilian-Universität München, GermanyGoogle Scholar
  10. Bonilla-Gómez MA, Nates-Parra G (1992) Abejas euglosinas de Colombia (Hymenoptera: Apidae) I. Claves ilustradas. Caldasia 17:149–172Google Scholar
  11. Braga PIS (1976) Atração de abelhas polinizadoras de Orchidaceae com auxílio de iscas-odores na campina, campinarana e floresta tropical úmida da região de Manaus. Ciência e Cultura 28:767–773Google Scholar
  12. Braga AK (2000) A comunidade de Euglossini de Estação Ecológica de Paulo Faria, Paulo Faria, SP, e comportamento de colecta de fragrãncias pelo machos de Euglossa townsendi Cockerell (Hymenoptera: Apidae: Euglossini). Master thesis, FFCLRP-USP, Ribeirão Preto, BrasilGoogle Scholar
  13. Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279CrossRefGoogle Scholar
  14. Burnham KP, Anderson DR (2004) Multimodel inference—understanding AIC and BIC in model selection. Sociol Meth Res 33:261–304CrossRefGoogle Scholar
  15. Búrquez A (1997) Distributional limits of euglossine and meliponine bees (Hymenoptera, Apidae) in northwestern México. Pan-Pac Entomol 73:137Google Scholar
  16. Cameron SA (2004) Phylogeny and biology of the neotropical orchid bees (Euglossini). Ann Rev Entomol 49:377–404CrossRefGoogle Scholar
  17. Carranza A, Defeo O, Arim M (2011) Taxonomic relatedness and spatial structure of a shelf benthic gastropod assemblage. Divers Distrib 17:25–34CrossRefGoogle Scholar
  18. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727CrossRefGoogle Scholar
  19. Condit R, Pitman NCA, Leigh EG et al (2002) Beta-diversity in tropical forest trees. Science 295:666–669PubMedCrossRefGoogle Scholar
  20. Dick CW, Roubik DW, Gruber KF et al (2004) Long-distance gene flow and cross-Andean dispersal of lowland rain forest bees (Apidae: Euglossini) revealed by comparative mitochondrial DNA phylogeny. Mol Ecol 13:3775–3785PubMedCrossRefGoogle Scholar
  21. Dressler RL (1982a) New species of Euglossa II. (Hymenoptera: Apidae). Rev Biol Trop 30:121–129Google Scholar
  22. Dressler RL (1982b) New species of Euglossa III. The Bursigera species group (Hymenoptera: Apidae). Rev Biol Trop 30:131–140Google Scholar
  23. Dressler RL (1982c) New species of Euglossa IV. The cordata and purpurea species groups (Hymenoptera: Apidae). Rev Biol Trop 30:141–150Google Scholar
  24. Dressler RL (1982d) Biology of the orchid bees (Euglossini). Ann Rev Ecol Syst 13:373–394CrossRefGoogle Scholar
  25. Dressler RL (1985) Euglossine bees (Hymenoptera: Apidae) of the Tambopata reserved zone, Madre de Dios, Perú. Rev Per Entomol 27:75–79Google Scholar
  26. Ducke A (1902) As espécies Paraenses do gênero Euglossa. Boletim do Museu Paraense 3:561–577Google Scholar
  27. Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  28. Duque A, Sánchez M, Cavalier J et al (2002) Different floristic patterns of woody understorey and canopy plants in Colombian Amazonia. J Trop Ecol 18:499–525CrossRefGoogle Scholar
  29. Duque A, Phillips JF, von Hildebrand P et al (2009) Distance decay of tree species similarity in protected areas on Terra Firme forests in Colombian Amazonia. Biotropica 41:599–607CrossRefGoogle Scholar
  30. Eberhard JR, Bermingham E (2005) Phylogeny and comparative biogeography of Pionopsitta parrots and Pteroglossus toucans. Mol Phylogenet Evol 36:288–304PubMedCrossRefGoogle Scholar
  31. Fleming TH, Muchala N (2008) Nectar-feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems. J Biogeogr 35:764–780CrossRefGoogle Scholar
  32. Gentry AH (1988) Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann Mo Bot Gard 75:1–34CrossRefGoogle Scholar
  33. Gilbert LE (1980) Food web organization and the conservation of Neotropical diversity. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary—ecological perspective 1. Sinauer, SunderlandGoogle Scholar
  34. Hawkins BA, De Vries PJ (2009) Tropical niche conservationism and the species richness gradient of North American butterflies. J Biogeogr 36:1698–1711CrossRefGoogle Scholar
  35. Hawkins BA, Field R, Cornell HV et al (2003) Energy, water, and broad-scale geographic pattern of species richness. Ecology 84:3105–3117CrossRefGoogle Scholar
  36. Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Inter J Climatol 25:1965–1978CrossRefGoogle Scholar
  37. Hoorn C, Wesselingh FP, ter Steege H et al (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931PubMedCrossRefGoogle Scholar
  38. Hu L, Li MG, Li Z (2010) Geographical and environmental gradients of lianas and vines in China. Glob Ecol Biogeogr 19:554–561Google Scholar
  39. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  40. Hubbell SP, Foster RB (1986) Biology, chance, and history and the structure of tropical rain forest tree communities. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York, pp 314–329Google Scholar
  41. Hurtt GC, Pacala SW (1995) The consequences of recruitment limitation: reconciling chance, history and competitive differences between plants. J Theor Biol 176:1–12CrossRefGoogle Scholar
  42. Janzen DH (1971) Euglossine bees as long distance pollinators of tropical plants. Science 171:203–205PubMedCrossRefGoogle Scholar
  43. Justiniano MJ, Fredericksen TS (2000) Phenology of tree species in Bolivian dry forests. Biotropica 32:276–281Google Scholar
  44. Kimsey LS (1982) Systematics of bees of the genus Eufriesea (Hymenoptera, Apidae). Univ Cal Publ Entomol 95Google Scholar
  45. Kimsey LS, Dressler RL (1986) Synonymic species list of Euglossini. Pan-Pacific Entomol 62:229–236Google Scholar
  46. Leyer I, Wesche K (2008) Multivariate Statistik in der Ökologie. Springer, BerlinGoogle Scholar
  47. McCune B, Mefford MJ (1999) PC-ORD (data analysis software system), version 5. MjM Software Design, Gleneden BeachGoogle Scholar
  48. Michener CD (1979) Biogeography of the bees. Ann Mo Bot Gard 66:277–342CrossRefGoogle Scholar
  49. Michener CD (2007) The bees of the world, 2nd edn. John Hopkins University Press, BaltimoreGoogle Scholar
  50. Minckley RL, Reyes SG (1996) Capture of the orchid bee, Eulaema polychroma (Friese) (Apidae: Euglossini) in Arizona, with notes on the northern distributions of other Mesoamerican bees. J Kans Entomol Soc 69:102–104Google Scholar
  51. Moure JS (1967) A check-list of the known euglossine bees (Hymenoptera, Apidae). Atlas do Simpósio sôbre a Biota Amazônica (Zoologia) 5:395–415Google Scholar
  52. Myers N (1986) Tropical deforestation and a megaextiction spasm. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 394–409Google Scholar
  53. Nemésio A, Silveira FA (2006a) Deriving ecological relationships between host and parasitic species—an example with orchid bees. J Biogeogr 33:91–97CrossRefGoogle Scholar
  54. Nemésio A, Silveira FA (2006b) Edge effects on the orchid-bee fauna (Hymenoptera: Apidae) at a large remnant of Atlantic forest in southeastern Brazil. Neotropical Entomol 35:313–323CrossRefGoogle Scholar
  55. Nemésio A, Silveira FA (2007a) Orchid bee fauna (Hymenoptera: Apidae: Euglossinae) of Atlantic Forest fragments inside an urban area in southeastern Brazil. Neotropical Entomol 36:186–191CrossRefGoogle Scholar
  56. Nemésio A, Silveira FA (2007b) Diversity and distribution of orchid bees (Hymenoptera: Apidae: Euglossini) with a revised checklist of species. Neotropical Entomol 36:874–888CrossRefGoogle Scholar
  57. Nemésio A, Silveira FA (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic forest. Zootaxa 2041:1–242Google Scholar
  58. Oliveira ML (2006) Três novas espécies de abelhas da Amazônia pertencentes ao gênero Eulaema (Hymenoptera: Apidae: Euglossini). Acta Amaz 36:121–128CrossRefGoogle Scholar
  59. Oliveira ML, Campos LAO (1995) Abundância, riqueza e diversidade de abelhas Euglossinae (Hymenoptera: Apidae) em florestas contínuas de terra firme na Amazônia central, Brasil. Rev Brasil Zool 12:547–556CrossRefGoogle Scholar
  60. Pitman NCA, Terborgh J, Silman M et al (2001) Dominance and distribution of tree species in upper Amazonian Terra Firme forests. Ecol 82:2101–2117CrossRefGoogle Scholar
  61. R Development Core Team (2007) R (data anlysis software system), version 2.11.0. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  62. Radchenko VG, Pesenko YA (1994) Biology of bees (Hymenoptera, Apoidea). Russian Academy of Sciences, Zoological Institute, St. PetersburgGoogle Scholar
  63. Ramirez SG, Roubik DW, Skov C, Pierce NE (2010) Phylogeny, diversification patterns and historical biogeography of euglossine orchid bees (Hymenoptera: Apidae). Biol J Lin Soc 100:552–572CrossRefGoogle Scholar
  64. Ramírez S, Dressler RL, Ospina AM (2002) Euglossine bees (Hymenoptera: Apidae) from the Neotropical region: a species checklist with notes on their biology. Biota Colombiana 3:7–118Google Scholar
  65. Rangel TFL, Diniz-Filho JAF, Bini LM (2006) Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Glob Ecol Biogeogr 15:321–327CrossRefGoogle Scholar
  66. Ren-Cang B, Yu C, Yuan-Man H, Xiu-Zhen L, Hong-Shi H (2008) Sensitivity of coniferous trees to environmental factors at different scales in the Small Xing’ an Mountains, China. Zhiwu Shengtai Xuebao 32:80–87Google Scholar
  67. Roig-Alsina A, Michener CD (1993) Studies of the phylogeny and classification of long-tongued bees (Hymenoptera: Apoidea). Univ Kans Sci Bul 55:123–173Google Scholar
  68. Rosenzweig M (1995) Species diversity in space and time. Cambridge University Press, New YorkCrossRefGoogle Scholar
  69. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  70. Roubik DW (2004a) Long-term studies of solitary bees: what the orchid bees are telling us. In: Freitas BM, Pereira JO (eds) Solitary bees? Conservation, rearing, management for pollination. Imprensa Universitaria, Fortaleza, Brazil, pp 97–103Google Scholar
  71. Roubik DW (2004b) Sibling species of Glossuropoda in the Amazon region (Hymenoptera: Apidae: Euglossini). J Kans Entomol Soc 77:235–253CrossRefGoogle Scholar
  72. Roubik DW, Ackerman JD (1987) Long-term ecology of euglossine orchid-bees (Apidae: Euglossini) in Panama. Oecologia 73:321–333CrossRefGoogle Scholar
  73. Roubik DW, Hanson PE (2004) Orchid bees of tropical America, 1st edn. INBio, Santo Domingo de Heredia, Costa RicaGoogle Scholar
  74. Sazima M, Vogel S, Cocucci A, Hausner G (1993) The perfume flowers of Cyphomandra (Solanaceae): pollination by euglossine bees, bellows mechanism, osmophores, and volatiles. Plant Syst Evol 187:55–88CrossRefGoogle Scholar
  75. Schwerdtfeger M, Gerlach G, Kaiser R (2002) Anthecology in the neotropical genus Anthurium (Araceae): a preliminary report. Selbyana 23:258–267Google Scholar
  76. Silva JMC, Oren DC (1996) Application of parsimony analysis of endemicity in amazonian biogeography: an example with primates. Biol J Linn Soc 59:427–437CrossRefGoogle Scholar
  77. Steyskal GC (1977) History and use of the Mc Phail trap. Fla Entomol 60:11–16CrossRefGoogle Scholar
  78. ter Steege H, Pitman N, Sabatier D et al (2003) A spatial model of tree α-diversity and tree density for the Amazon. Biodivers Conerv 12:2255–2277CrossRefGoogle Scholar
  79. Toledo M, Poorter L, Peña-Claros M et al (2010) Patterns and determinants of floristic variation across lowland forests of Bolivia. Biotropica 1–9. doi: 10.1111/j.1744-7429.2010.00711.x
  80. Tuomisto H, Ruokolainen K, Kalliola R et al (1995) Dissecting Amazonian biodiversity. Science 269:63–66PubMedCrossRefGoogle Scholar
  81. Tuomisto H, Ruokolainen K, Yli-Halla M (2003a) Dispersal, environment, and floristic variation of western Amazonian forests. Science 299:241–244PubMedCrossRefGoogle Scholar
  82. Tuomisto H, Ruokulainen K, Aguilar M, Sarmiento A (2003b) Floristic patterns along a 43-km long transect in an Amazonian rain forest. J Ecol 91:743–756CrossRefGoogle Scholar
  83. Vasconcelos HL, Vilhena JM, Facure KG et al (2010) Pattern of ant species diversity and turnover across 2000 km of Amazonian floodplain forest. J Biogeogr 37:432–440CrossRefGoogle Scholar
  84. Vormisto J, Svenning JC, Hall P et al (2004) Diversity and dominance in palm (Arecaceae) communities in terra firme forests in the western Amazon basin. J Ecol 92:577–588CrossRefGoogle Scholar
  85. Wcislo WT, Cane JH (1996) Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Ann Rev Entomol 41:257–286CrossRefGoogle Scholar
  86. Werneck FP, Costa GC, Colli GR et al (2010) Revisiting the historical distribution of seasonally dry tropical forests: new insights based on palaeodistribution modelling and palynological evidence. Glob Ecol Biogeogr 20:272–288CrossRefGoogle Scholar
  87. Whitfield J (2002) Ecology: neutrality versus the niche. Nature 417:480–481PubMedCrossRefGoogle Scholar
  88. Whittaker RH, Levin SA (1977) The role of mosaic phenomena in natural communities. Theor Pop Biol 12:117CrossRefGoogle Scholar
  89. Wiens JJ, Donoghue MJ (2004) Historical biogeography, ecology and species richness. Trends Ecol Evol 19:639–644PubMedCrossRefGoogle Scholar
  90. Wiens JJ, Graham CH, Moen DS et al (2006) Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: treefrog trees unearth the roots of high tropical diversity. Am Nat 168:579–596PubMedCrossRefGoogle Scholar
  91. Williams NH, Dressler RL (1982) Euglossine pollination of Spathyphyllum (Araceae). Selbyana 1:349–356Google Scholar
  92. Williams JW, Jackson ST, Kutzbach JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. Proc Nat Acad Sci 104:5738–5742PubMedCrossRefGoogle Scholar
  93. Wittmann F, Schöngart J, Montero JC et al (2006) Tree species composition and diversity gradients in white-water forests across the Amazon basin. J Biogeogr 33:1334–1347CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Stefan Abrahamczyk
    • 1
  • Peter Gottleuber
    • 2
  • Christian Matauschek
    • 3
  • Michael Kessler
    • 1
  1. 1.Institute for Systematic BotanyUniversity of ZurichZurichSwitzerland
  2. 2.Department of Systematic BotanyUniversity of GoettingenGoettingenGermany
  3. 3.Department of Behavioral Ecology and SociobiologyGerman Primate Center (DPZ)GoettingenGermany

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