Apidologie

, Volume 44, Issue 5, pp 501–510 | Cite as

The potential of cleptoparasitic bees as indicator taxa for assessing bee communities

  • Cory S. Sheffield
  • Alana Pindar
  • Laurence Packer
  • Peter G. Kevan
Original article

Abstract

Many factors affect bee diversity and abundance, and knowledge of these is crucial for maintaining healthy bee communities. However, there are few means to fully evaluate the status of bee communities; most are based on monitoring species richness and abundance and do not consider the diverse life histories of bees. We propose that functional diversity of bee communities offers a more consistent means of evaluation and suggest that cleptoparasitic bees in particular show much promise as indicator taxa. Cleptoparasitic bees play a stabilising role within bee communities. They represent the apex of bee communities and are the first guild to respond to disturbances, are easily distinguished as such and are diverse enough to be representative of entire bee communities. The diversity and abundance of cleptoparasites in relation to all bees is indicative of the status of the total bee community, and monitoring them should form an integral part of assessing bee communities.

Keywords

pollinator communities guild structure cleptoparasites indicator taxa ecosystem health 

References

  1. Balvanera, P., Pfisterer, A.B., Buchmann, N., He, J., Nakashizuka, T., Raffaelli, D., Schmid, B. (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol. Lett. 9, 1146–1156PubMedCrossRefGoogle Scholar
  2. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and The Netherlands. Science 313, 351–354PubMedCrossRefGoogle Scholar
  3. Blondel, J. (2003) Guilds or functional groups: does it matter? Oikos 100, 223–231CrossRefGoogle Scholar
  4. Bogusch, P., Kratochvíl, L., Straka, J. (2006) Generalist cuckoo bees (Hymenoptera: Apoidea: Sphecodes) are species-specialist at the individual level. Behav. Ecol. Sociobiol. 60, 422–429CrossRefGoogle Scholar
  5. Cane, J.H., Minckley, R., Roulston, T., Kervin, L.J., Williams, N.M. (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol. Appl. 16, 632–644PubMedCrossRefGoogle Scholar
  6. Cardinale, B.J., Srivastava, D.S., Duffy, J.E., Wright, J.P., Downing, A.L., Sankaran, M., Jouseau, C. (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443, 989–992PubMedCrossRefGoogle Scholar
  7. Chiarucci, A., Giovanni, B., Scheiner, S.M. (2011) Old and new challenges in using species diversity for assessing biodiversity. Philos. Trans. R. Soc. London, Ser. B 366, 2426–2437PubMedCrossRefGoogle Scholar
  8. Combes, C. (1996) Parasites, biodiversity and ecosystem stability. Biodivers. Conserv. 5, 953–962CrossRefGoogle Scholar
  9. Duffy, J.E. (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol. Lett. 6, 680–687CrossRefGoogle Scholar
  10. Duffy, J.E., Cardinale, B.J., France, K.E., McIntyre, P.B., Thébault, E., Loreau, M. (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett. 10, 522–538PubMedCrossRefGoogle Scholar
  11. Elmqvist, T., Folke, C., Nyström, M., Peterson, G., Bengtsson, J., Walker, B., Norberg, J. (2003) Response diversity, ecosystem change, and resilience. Front. Ecol. Environ. 1, 488–494CrossRefGoogle Scholar
  12. Finke, D.L., Denno, R.F. (2004) Predator diversity dampens trophic cascades. Nature 429, 407–410PubMedCrossRefGoogle Scholar
  13. Grundel, R., Frohnapple, K.J., Jean, R.P., Pavlovic, N.B. (2011) Effectiveness of bowl trapping and netting for inventory of a bee community. Environ. Entomol. 40, 374–380CrossRefGoogle Scholar
  14. Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35CrossRefGoogle Scholar
  15. Horwitz, P., Wilcox, B.A. (2005) Parasites, ecosystems and sustainability: an ecological and complex systems perspective. Int. J. Parasitol. 35, 725–732PubMedCrossRefGoogle Scholar
  16. Hubbell, S.P. (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, PrincetonGoogle Scholar
  17. Hudson, P.J., Dobson, A.P., Lafferty, K.D. (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol. 21, 381–385PubMedCrossRefGoogle Scholar
  18. Iyengar, E.V. (2008) Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism. Biol. J. Linn. Soc. 93, 745–762CrossRefGoogle Scholar
  19. Kevan, P.G., Greco, C.F., Belaoussoff, S. (1997) Log-normality of biodiversity and abundance in diagnosis and measuring of ecosystem health: pesticide stress on pollinators on blueberry heaths. J. Appl. Ecol. 34, 1122–1136CrossRefGoogle Scholar
  20. Klein, A.M., Vassiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313PubMedCrossRefGoogle Scholar
  21. Kremen, C., Williams, N.M., Thorp, R.W. (2002) Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. USA 99, 16812–16816PubMedCrossRefGoogle Scholar
  22. Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P., Thorp, R.W. (2004) The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecol. Lett. 7, 1109–1119CrossRefGoogle Scholar
  23. Magurran, A.E. (2004) Measuring Biological Diversity. Blackwell, MaldenGoogle Scholar
  24. Marcogliese, D.J. (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1, 151–164CrossRefGoogle Scholar
  25. Marcogliese, D.J., Cone, D.K. (1997) Food webs: a plea for parasites. Trends Ecol. Evol. 12, 320–325PubMedCrossRefGoogle Scholar
  26. Michener, C.D. (1974) The Social Behavior of the Bees. Harvard University Press, BostonGoogle Scholar
  27. Michener, C.D. (1979) Biogeography of the bees. Ann. Mo. Bot. Gard. 66, 277–347CrossRefGoogle Scholar
  28. Michener, C.D. (2007) The Bees of the World, 2nd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  29. Morand, S., Gonzalez, E.A. (1997) Is parasitism a missing ingredient in model ecosystems? Ecol. Model. 95, 61–74CrossRefGoogle Scholar
  30. Moretti, M., de Bello, F., Roberts, S.P.M., Potts, S.G. (2009) Taxonomical vs. functional responses of bee communities to fire in two contrasting climatic regions. J. Anim. Ecol. 78, 98–108PubMedCrossRefGoogle Scholar
  31. National Research Council (2007) Status of Pollinators in North America. National Academies Press, WashingtonGoogle Scholar
  32. Neame, L.A., Griswold, T., Elle, E. (2012) Pollinator nesting guilds respond differently to urban habitat fragmentation in an oak-savannah ecosystem. Insect Conserv. Diver. 6, 57–66. doi:10.1111/j.1752-4598.2012.00187.x CrossRefGoogle Scholar
  33. Nielsen, A., Steffan-Dewenter, I., Westphal, C., Messinger, O., Potts, S.G., et al. (2011) Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques. Ecol. Res. 26, 969–983CrossRefGoogle Scholar
  34. O’Neill, R.V., Krummel, J.R., Gardner, R.H., Sugihara, G., Jackson, B., et al. (1988) Indices of landscape pattern. Landscape Ecol. 1, 153–162CrossRefGoogle Scholar
  35. Oertli, S., Muller, A., Dorn, S. (2005) Ecological and seasonal patterns in the diversity of a species-rich bee assemblage (Hymenoptera: Apoidea: Apiformes). Eur. J. Entomol. 102, 53–63Google Scholar
  36. O'Gorman, E.J., Yearsley, J.M., Crowe, T.P., Emmerson, M.C., Jacob, U., Petchey, O.L. (2011) Loss of functionally unique species may gradually undermine ecosystems. Proc. R. Soc. Lond. B 278, 1886–1893CrossRefGoogle Scholar
  37. Petchey, O.L., Hector, A., Gaston, K.J. (2004) How do different measures of functional diversity perform? Ecology 85, 847–857CrossRefGoogle Scholar
  38. Peterson, G., Allen, C.R., Holling, C.S. (1998) Ecological resilience, biodiversity, and scale. Ecosystems 1, 6–18CrossRefGoogle Scholar
  39. Polidori, C., Borruso, L., Boesi, R., Andrietti, F. (2009) Segregation of temporal and spatial distribution between kleptoparasites and parasitoids of the eusocial sweat bee, Lasioglossum malachurum (Hymenoptera: Halictidae, Mutillidae). Entomol. Sci. 12, 116–129CrossRefGoogle Scholar
  40. Rosenheim, J.A. (1990) Density-dependent parasitism and the evolution of nesting aggregations in the solitary Hymenoptera. Ann. Entomol. Soc. Amer. 83, 277–286Google Scholar
  41. Roulston, T.H., Smith, S.A., Brewster, A.L. (2007) A comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. J. Kansas Entomol. Soc. 80, 179–181CrossRefGoogle Scholar
  42. Rozen Jr., J.G. (2001) A taxonomic key to mature larvae of cleptoparasitic bees (Hymenoptera: Apoidea). Amer. Mus. Nov. 3309, 1–28CrossRefGoogle Scholar
  43. Scrosati, R.A., van Genne, B., Heaven, C.S., Watt, C.A. (2011) Species richness and diversity in different functional groups across environmental stress gradients: a model for marine rocky shores. Ecography 34, 151–161CrossRefGoogle Scholar
  44. Sheffield, C.S., Kevan, P.G., Westby, S.M., Smith, R.F. (2008) Diversity of cavity-nesting bees (Hymenoptera: Apoidea) within apple orchards and wild habitats in the Annapolis Valley, Nova Scotia. Canada. Can. Ent. 140, 235–249CrossRefGoogle Scholar
  45. Sheffield, C.S., Kevan, P.G., Pindar, A., Packer, L. (2013) Bee (Hymenoptera: Apoidea) diversity within apple orchards and old fields habitats in the Annapolis Valley, Nova Scotia, Canada. Can. Ent. 145, 94–114Google Scholar
  46. Tilman, D., Lehman, C. (2001) Biodiversity, composition, and ecosystem processes: theory and concepts. In: Kinzig, A.P., Pacala, S.W., Tilman, D. (eds.) The Functional Consequences Of Biodiversity: Empirical Progress and Theoretical Extensions, pp. 9–41. Princeton University Press, PrincetonGoogle Scholar
  47. Toler, T.R., Evans, E.W., Tepedino, V.J. (2005) Pan-trapping for bees (Hymenoptera: Apiformes) in Utah’s West Desert: the importance of color diversity. Pan-Pac. Entomol. 81, 103–113Google Scholar
  48. Walker, B.H. (1992) Biological diversity and ecological redundancy. Conserv. Biol. 6, 18–23CrossRefGoogle Scholar
  49. Wcislo, W.T. (1981) The roles of seasonality, host synchrony, and behaviour in the evolutions and distributions of nest parasites in the Hymenoptera (Insecta), with special reference to bees (Apoidea). Biol. Rev. 62, 515–543CrossRefGoogle Scholar
  50. Westphal, C., Bommarco, R., Carré, G., Lamborn, E., Morison, N., et al. (2008) Measuring bee diversity in different European habitats and biogeographical regions. Ecol. Mono. 78, 654–671CrossRefGoogle Scholar
  51. Williams, N.M., Crone, E.E., Roulston, T.H., Minckley, R.L., Packer, L., Potts, S.G. (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 143, 2280–2291CrossRefGoogle Scholar
  52. Wood, C.L., Byers, J.E., Cottingham, K.L., Altman, I., Donahue, M.J., Blakeslee, A.M.H. (2007) Parasites alter community structure. Proc. Natl. Acad. Sci. USA 104, 9335–9339PubMedCrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France 2013

Authors and Affiliations

  • Cory S. Sheffield
    • 1
  • Alana Pindar
    • 2
  • Laurence Packer
    • 2
  • Peter G. Kevan
    • 3
  1. 1.Royal Saskatchewan MuseumReginaCanada
  2. 2.Department of BiologyYork UniversityTorontoCanada
  3. 3.School of Environmental BiologyGuelphCanada

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