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Apidologie

, Volume 43, Issue 4, pp 449–464 | Cite as

The same, but different: pollen foraging in honeybee and bumblebee colonies

  • Sara Diana LeonhardtEmail author
  • Nico Blüthgen
Original article

Abstract

Like many other bees worldwide, honeybees and bumblebees are threatened by human-induced disturbances. Yet some species decline and others thrive, likely due to different foraging strategies. As little is known about how resource intake translates into nutrients available to colonies, our study aimed to better understand how differences in foraging strategies may affect colony health by relating differences in pollen spectra collected to differences in nutrient composition. The Apis and Bombus colonies studied were all located at the same site, but nevertheless differed in the spectra of plant species visited for pollen collection and the quality of pollen collected. Bumblebees generally collected pollen with significantly higher pollen protein content and more essential amino acids. Unlike honeybees that tend to exploit large resource patches, bumblebees thus seem to select the “better” pollen and to focus on quality instead of quantity.

Keywords

generalist pollinators amino acids floral resources 

Notes

Acknowledgements

Marcus Ulbrich as well as Susan Oppermann assisted with the data collection. Linda-Maria Jung and Andrea Hilpert greatly helped with the processing of samples and chemical analyses. Dirk Ahrens-Lagast and Jürgen Tautz kindly provided the honeybee colonies and pollen traps for this study. The comments of two anonymous reviewers greatly improved a previous version of our manuscript. Sara Leonhardt is funded by the Deutsche Forschungs-Gemeinschaft (DFG project: LE 2750/1-1).

References

  1. Aizen, M.A., Feinsinger, P. (2003) Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. In: Bradshaw, G., Marquet, P., Mooney, H.A. (eds.) How Landscapes Change: Human Disturbance and Ecosystem Disruption in the Americas, pp. 111–129. Springer, New YorkGoogle Scholar
  2. Banaszak, J. (1995) Changes in Fauna of Wild Bees in Europe. Pedagogical University, BydgoszczGoogle Scholar
  3. Benton, T. (2006) Bumble Bees: The Natural History and Identification of the Species Found in Britain. Collins, LondonGoogle Scholar
  4. Beug H.-J. (2004) Leitfaden der Pollenbestimmung: für Mitteleuropa und angrenzende Gebiete, Dr. Friedrich Pfeil, München, GermanyGoogle Scholar
  5. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354PubMedCrossRefGoogle Scholar
  6. Blüthgen, N., Menzel, F., Blüthgen, N. (2006) Measuring specialization in species interaction networks. BMC Ecol. 6, 9PubMedCrossRefGoogle Scholar
  7. Bommarco, R., Biesmeijer, J.C., Meyer, B., Potts, S.G., Pöyry, J., Roberts, S.P.M., Steffan-Dewenter, I., Öckinger, E. (2010) Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc. R. Soc. Lond. B 277, 2075–2082CrossRefGoogle Scholar
  8. Bommarco, R., Lundin, O., Smith, H.G., Rundlöf, M. (2011) Drastic historic shifts in bumble-bee community composition in Sweden. Proc. R. Soc. Lond. B. doi:10.1098/rspb.2011.0647
  9. Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F., Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. U. S. A 108, 662–667PubMedCrossRefGoogle Scholar
  10. Connop, S., Hill, T., Steer, J., Shaw, P. (2010) The role of dietary breadth in national bumblebee (Bombus) declines: simple correlation? Biol. Conserv. 143, 2739–2746CrossRefGoogle Scholar
  11. Crawley, M.J. (2008) The R Book. Wiley, ChichesterGoogle Scholar
  12. Darvill, B., Knight, M.E., Goulson, D. (2004) Use of genetic markers to quantify bumblebee foraging range and nest density. Oikos 107, 471–478CrossRefGoogle Scholar
  13. de Groot, A.P. (1953) Protein and amino acid requirements of the honey bee (Apis mellifera L.). Physiol. Comp. Oecol. 3, 197–285Google Scholar
  14. Devictor, V., Julliard, R., Jiguet, F. (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117, 507–514CrossRefGoogle Scholar
  15. Dietz, A. (1992) Nutrition of the adult honeybee. In: Graham, J.M. (ed.) The Hive and the Honeybee, pp. 125–156. Dadant and Sons, HamiltonGoogle Scholar
  16. Dormann, C.F. (2008) Angewandte Statistik für die biologischen Wissenschaften. Helmholtz Zentrum für Umweltforschung-UFZ, LeipzigGoogle Scholar
  17. Fitzpatrick, U., Murray, T.E., Paxton, R.J., Breen, J., Cotton, D., Santorum, V., Brown, M.J.F. (2007) Rarity and decline in bumblebees—a test of causes and correlates in the Irish fauna. Biol. Conserv. 136, 185–194CrossRefGoogle Scholar
  18. Génissel, A., Aupinel, P., Bressac, C., Tasei, J.N., Chevrier, C. (2002) Influence of pollen origin on performance of Bombus terrestris micro-colonies. Entomol. Exp. Appl. 104, 329–336CrossRefGoogle Scholar
  19. Goulson, D., Darvill, B. (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35, 55–63CrossRefGoogle Scholar
  20. Goulson, D., Hanley, M.E., Darvill, B., Ellis, J.S., Knight, M.E. (2005) Causes of rarity in bumblebees. Biol. Conserv. 122, 1–8CrossRefGoogle Scholar
  21. Goulson, D., Lye, G.C., Darvill, B. (2008) Decline and conservation of bumblebees. Annu. Rev. Entomol. 53, 191–208PubMedCrossRefGoogle Scholar
  22. Hanley, M.E., Franco, M., Pichon, S., Darvill, B., Goulson, D. (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct. Ecol. 22, 592–598CrossRefGoogle Scholar
  23. Haydak, M.H. (1970) Honey bee nutrition. Annu. Rev. Entomol. 15, 146–156CrossRefGoogle Scholar
  24. Heinrich, B. (1976) The foraging specializations of individual bumblebees. Ecol. Monogr. 46, 105–128CrossRefGoogle Scholar
  25. Heinrich, B. (1979) Majoring and minoring by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology 60, 245–255CrossRefGoogle Scholar
  26. Heinrich, B., Mudge, P.R., Deringis, P.G. (1977) Laboratory analysis of flower constancy in foraging bumblebees: Bombus ternarius and B. terricola. Behav. Ecol. Sociobiol. 2, 247–265CrossRefGoogle Scholar
  27. Herbert, E.W. (1992) Honey bee nutrition. In: Graham, J.E. (ed.) The Hive and the Honey Bee. Dadant and Sons, HamiltonGoogle Scholar
  28. Herbert, E.W.J., Miller-Ihli, N.J. (1987) Seasonal variation of seven minerals in honey bee collected pollen. Am. Bee J. 127, 367–369Google Scholar
  29. Hines, H.M., Hendrix, S.D. (2005) Bumble bee (Hymenoptera: Apidae) diversity and abundance in tallgrass prairie patches: effects of local and landscape floral resources. Environ. Entomol. 34, 1477–1484CrossRefGoogle Scholar
  30. Johnson, S.D., Steiner, K.E. (2000) Generalization versus specialization in plant pollination systems. Trends Ecol. Evol. 15, 140–143PubMedCrossRefGoogle Scholar
  31. Keller, I., Fluri, P., Imdorf, A. (2005) Pollen nutrition and colony development in honey bees: part I. Bee World 86, 3–10Google Scholar
  32. Kitaoka, T.K., Nieh, J.C. (2009) Bumble bee pollen foraging regulation: role of pollen quality, storage levels, and odor. Behav. Ecol. Sociobiol. 63, 501–510CrossRefGoogle Scholar
  33. Kleijn, D., Raemakers, I. (2008) A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89, 1811–1823PubMedCrossRefGoogle Scholar
  34. Klein, A.M. (2011) Plant–pollinator interactions in changing environments. Basic Appl. Ecol. 12, 279–281CrossRefGoogle Scholar
  35. Klein, A.M., Vaissiere, B.E., Cane, J.H., Cunningham, S., Kremen, C., Tscharntke, T. (2007a) The role of pollinators for global crop production. Ecol. Soc. Am. Annu. Meet. AbstractsGoogle Scholar
  36. Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T. (2007b) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. Lond. B 274, 303–313CrossRefGoogle Scholar
  37. Kosior, A., Celary, W., Olejniczak, P., Fijal, J., Król, W., Solarz, W., Plonka, P. (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of western and central Europe. Oryx 41, 79–88CrossRefGoogle Scholar
  38. Kratochwil, A., Kohl, A. (1988) Pollensammel-Präferenzen bei Hummeln - ein Vergleich mit der Honigbiene, Mittelbadischer Landesverb. Nat.kd. Nat.schutz 3, 697–715Google Scholar
  39. Leonhardt, S.D., Dworschak, K., Eltz, T., Blüthgen, N. (2007) Foraging loads of stingless bees and utilisation of stored nectar for pollen harvesting. Apidologie 38, 125–135CrossRefGoogle Scholar
  40. Leonhardt, S.D., Schmitt, T., Blüthgen, N. (2011) Tree resin composition, collection behavior and selective filters shape chemical profiles of tropical bees (Apidae: Meliponini). PLoS One 6, e23445PubMedCrossRefGoogle Scholar
  41. Michener, C.D. (2007) The Bees of the World. Johns Hopkins University Press, BaltimoreGoogle Scholar
  42. Munidasa, D.T., Toquenaga, Y. (2010) Do pollen diets vary among adjacent bumble bee colonies? Ecol. Res. 25, 639–646CrossRefGoogle Scholar
  43. National Research Council (2007) Status of Pollinators in North America. The National Academics Press, WashingtonGoogle Scholar
  44. Parker, R.L. (1926) The collection and utilization of pollen by the honeybee. University Agricultural Experiment Station, Memoir CornellGoogle Scholar
  45. Peat, J., Goulson, D. (2005) Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee, Bombus terrestris. Behav. Ecol. Sociobiol. 58, 152–156CrossRefGoogle Scholar
  46. Peat, J., Tucker, J., Goulson, D. (2005) Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers? Ecol. Entomol. 30, 176–181CrossRefGoogle Scholar
  47. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353PubMedCrossRefGoogle Scholar
  48. Robertson, A.W., Mountjoy, C., Faulkner, B.E., Roberts, M.V., Macnair, M.R. (1999) Bumble bee selection of Mimulus guttatus flowers: the effects of pollen quality and reward depletion. Ecology 80, 2594–2606Google Scholar
  49. Roulston, T.H., Cane, J.H. (2000) Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222, 187–209CrossRefGoogle Scholar
  50. Roulston, T.H., Cane, J.H., Buchmann, S.L. (2000) What governs protein content of pollen: pollinator preferences, pollen–pistil interactions, or phylogeny? Ecol. Monogr. 70, 617–643Google Scholar
  51. Rundlöf, M., Nilsson, H., Smith, H.G. (2008) Interacting effects of farming practice and landscape context on bumblebees. Biol. Conserv. 141, 417–426CrossRefGoogle Scholar
  52. Sowig, P. (1989) Effects of flowering plant’s patch size on species composition of pollinator communities, foraging strategies, and resource partitioning in bumblebees (Hymenoptera: Apidae). Oecologia 78, 550–558CrossRefGoogle Scholar
  53. Steffan-Dewenter, I., Tscharntke, T. (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121, 432–440CrossRefGoogle Scholar
  54. Steffan-Dewenter, I., Klein, A.M., Gaebele, V., Alfert, T., Tscharntke, T. (2006) Bee diversity and plant–pollinator interactions in fragmented landscapes. In: Waser, N.M., Ollerton, J. (eds.) Plant–Pollinator Interactions: From Specialization to Generalization, pp. 387–407. University of Chicago Press, ChicagoGoogle Scholar
  55. Teräs, I. (1985) Food plants and flower visits of bumblebees (Bombus: Hymenoptera, Apidae) in southern Finland. Acta Zool. Fenn. 179, 1–120Google Scholar
  56. Walther-Hellwig, K., Frankl, R. (2000) Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., apidae), in an agricultural landscape. J. Appl. Entomol.-Z. Angew. Entomol. 124, 299–306Google Scholar
  57. Weiner, C.N., Hilpert, A., Werner, M., Linsenmair, K.E., Blüthgen, N. (2010) Pollen amino acids and flower specialisation in solitary bees. Apidologie 41, 476–487CrossRefGoogle Scholar
  58. Westphal, C., Steffan-Dewenter, I., Tscharntke, T. (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149, 289–300PubMedCrossRefGoogle Scholar
  59. Wille, H., Wille, M. (1984) Die Pollenversorgung des Bienenvolkes: Die wichtigsten Pollenarten bewertet nach ihrem Eiweissgehalt und ihrer Häufigkeit im Pollensammelgut. Schweiz. Bienen-Ztg 2, 64–80Google Scholar
  60. Williams, P.H. (1982) The distribution and decline of British bumble bees (Bombus Latr). J. Apic. Res. 21, 236–245Google Scholar
  61. Williams, P.H. (1986) Environmental change and the distributions of British bumble bees (Bombus Latr). Bee World 67, 50–61Google Scholar
  62. Williams, P.H. (1989) Why are there so many species of bumble bees at Dungeness? Bot. J. Linn. Soc. 101, 31–44CrossRefGoogle Scholar
  63. Williams, P.H. (2005) Does specialization explain rarity and decline among British bumblebees? A response to Goulson et al. Biol. Conserv. 122, 33–43CrossRefGoogle Scholar
  64. Williams, P.H., Araujo, M.B., Rasmont, P. (2007) Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth? Biol. Conserv. 138, 493–505CrossRefGoogle Scholar
  65. Williams, P., Colla, S., Xie, Z.H. (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conserv. Biol. 23, 931–940PubMedCrossRefGoogle Scholar
  66. Williams, G.R., Tarpy, D.R., vanEngelsdorp, D., Chauzat, M.-P., Cox-Foster, D.L., Delaplane, K.S., Neumann, P., Pettis, J.S., Rogers, R.E.L., Shutler, D. (2010) Colony collapse disorder in context. Bioessays 32, 845–846PubMedCrossRefGoogle Scholar
  67. Winfree, R. (2010) The conservation and restoration of wild bees. Ann. N. Y. Acad. Sci. 1195, 169–197PubMedCrossRefGoogle Scholar
  68. Winfree, R., Aguilar, R., Vazquez, D.P., LeBuhn, G., Aizen, M.A. (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076PubMedCrossRefGoogle Scholar
  69. Xie, Z., Williams, P.H., Tang, Y. (2008) The effect of grazing on bumblebees in the high rangelands of the eastern Tibetan Plateau of Sichuan. J. Insect Conserv. 12, 695–703CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag, France 2011

Authors and Affiliations

  1. 1.Department of EcologyLeuphana UniversityLüneburgGermany
  2. 2.Department of BiologyUniversity of DarmstadtDarmstadtGermany

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