Skip to main content

The effect of proximity to a honeybee apiary on bumblebee colony fitness, development, and performance

Abstract

Competition between managed honeybees and wild pollinators is thought to be a key factor in structuring foraging communities on flowers. The majority of studies have focused on impacts such as floral visitation rates and resource overlap. However, direct measurement of fitness is required to fully assess the impacts of competition. We compared in 2 years the weight and reproductive success of bumblebee colonies located at two sites that were either close to or far from a large honeybee apiary, and which were located in the same landscape and with access to similar floral resources. We found that bumblebee colonies located at the site near the honeybee apiary gained less weight, and produced fewer and smaller queens, in both years than colonies at the site far from the apiary. The ratio of queen weight/size was lower in the colonies near honeybees in 1 year, while males were smaller and offspring sex ratio more male biased in colonies close to honeybees than in those far from honeybees. Proximity to managed honeybee hives was therefore associated with significantly reduced fitness of bumblebee colonies, but studies from many more sites are needed to confirm the effect.

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

Figure 1.
Figure 2.

References

  1. Beekman, M., Van Stratum, P. (1998) Bumblebee sex ratios: why do bumblebees produce so many males? Proc. R. Soc. Lond. B 265, 1535–1543

    Article  Google Scholar 

  2. Beekman, M., Van Stratum, P., Lingeman, R. (1998) Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entomol. Exp. Appl. 89, 207–214

    Article  Google Scholar 

  3. Blanckenhorn, W.U. (2000) The evolution of body size: what keeps organisms small? Q. Rev. Biol. 75, 385–407

    CAS  Article  PubMed  Google Scholar 

  4. Butz Huryn, V.M. (1997) Ecological impacts of introduced honey bees. Q. Rev. Biol. 72, 275–297

    Article  Google Scholar 

  5. 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 bumblebees. Proc. Natl. Acad. Sci. USA 108, 662–667

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  6. Colla, S.R., Packer, L. (2008) Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson. Biodivers. Conserv. 17, 1379–1391

    Article  Google Scholar 

  7. Corbet, S.A., Saville, N.M., Fussell, M., Prys-Jones, O.E., Unwin, D.M. (1995) The competition box: a graphical aid to forecasting pollinator performance. J. Appl. Ecol. 32, 707–719

    Article  Google Scholar 

  8. Couvillon, M.J., Dornhaus, A. (2009) Location, location, location: larvae position inside the nest is correlated with adult body size in worker bumble-bees (Bombus impatiens). Proc. Biol. Sci. B 276, 2411–2418

    Article  Google Scholar 

  9. Denno, R.F., Mcclure, M.S., Ott, J.R. (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu. Rev. Entomol. 40, 297–331

    CAS  Article  Google Scholar 

  10. Durrer, S., Schmid-Hempel, P. (1994) Shared use of flowers leads to horizontal pathogen transmission. Proc. R. Soc. Lond. B 258, 299–302

    Article  Google Scholar 

  11. Fontaine, C., Dajoz, I., Meriguet, J., Loreau, M. (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol. 4, 129–135

    CAS  Article  Google Scholar 

  12. Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., Morales, J.M., Bommarco, R., et al. (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett. 14, 1062–1072

    Article  PubMed  Google Scholar 

  13. Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., et al. (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611

    CAS  Article  PubMed  Google Scholar 

  14. Genersch, E., Yue, C., Fries, I., De Miranda, J.R. (2006) Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J. Invertebr. Pathol. 91, 61–63

    Article  PubMed  Google Scholar 

  15. Ginsberg, H.S. (1983) Foraging ecology of bees in an old field. Ecology 64, 165–175

    Article  Google Scholar 

  16. Goulson, D. (2004) Keeping bees in their place: impacts of bees outside their native range. Bee World 85, 45–46

    Google Scholar 

  17. Goulson, D., Sparrow, K. (2009) Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size. J. Insect Conserv. 13, 177–181

    Article  Google Scholar 

  18. Goulson, D., Hughes, W.O.H., Derwent, L.C., Stout, J.C. (2002a) Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130, 267–273

    Google Scholar 

  19. Goulson, D., Peat, J., Stout, J.C., Tucker, J., Darvill, B., Derwent, L.C., Hughes, W.O.H. (2002b) Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? Anim. Behav. 64, 123–130

    Article  Google Scholar 

  20. Graystock, P., Yates, K., Evison, S.E.F., Darvill, B., Goulson, D., Hughes, W.O.H. (2013a) The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J. Appl. Ecol. 50, 1207–1215

    Google Scholar 

  21. Graystock, P., Yates, K., Darvill, B., Goulson, D., Hughes, W.O.H. (2013b) Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. J. Invert. Pathol. 114, 114–119

    Article  Google Scholar 

  22. Gross, C.L. (1993) The breeding system and pollinators of Melastoma affine (Melastomataceae); a pioneer shrub in tropical Australia. Biotropica 25, 468–474

    Article  Google Scholar 

  23. Holland, J., Guidat, F.S., Bourke, A.F.G. (2013) Queen control of a key life-history event in a eusocial insect. Biol. Lett. 9, 20130056

    Article  PubMed  Google Scholar 

  24. Holm, S.N. (1972) Weight and life length of hibernating bumble bee queens (Hymenoptera: Bombidae) under controlled conditions. Insect Syst. Evol. 3, 313–320

    Article  Google Scholar 

  25. Inoue, M.N. (2011) Size-dependent selection against small queens of the invasive bumblebee Bombus terrestris in Japan. Entomol. Exp. Appl. 138, 65–70

    Article  Google Scholar 

  26. 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, 79–88

    Article  Google Scholar 

  27. Oldroyd, B.P., Lawler, S.H., Crozier, R.H. (1994) Do feral honey bees (Apis mellifera) and regent parrots (Polytelis anthopeplus) compete for nest sites? Aust. J. Ecol. 19, 444–450

    Article  Google Scholar 

  28. Owen, R.E. (1988) Body size variation and optimal body size of bumble bee queens (Hymenoptera: Apidae). Can. Entomol. 120, 19–27

    Article  Google Scholar 

  29. Paini, D.R. (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: a review. Austral Ecol. 29, 399–407

    Article  Google Scholar 

  30. Peat, J., Darvill, B., Ellis, J., Goulson, D. (2005a) Effects of climate on intra- and interspecific size variation in bumble-bees. Funct. Ecol. 19, 145–151

    Article  Google Scholar 

  31. Peat, J., Tucker, J., Goulson, D. (2005b) Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers? Ecol. Entomol. 30, 176–181

    Article  Google Scholar 

  32. Roubik, D.W. (1983) Experimental community studies: time-series tests of competition between African and neotropical bees. Ecology 64, 971–978

    Article  Google Scholar 

  33. Roubik, D.W., Wolda, H. (2001) Do competing honey bees matter? Dynamics and abundance of native bees before and after honey bee invasion. Popul. Ecol. 43, 53–62

    Article  Google Scholar 

  34. Schaffer, W.M., Zeh, D.W., Buchmann, S.L., Kleinhans, S., Schaffer, M.V., Antrim, J. (1983) Competition for nectar between introduced honey bees and native North American bees and ants. Ecology 64, 564–577

    Article  Google Scholar 

  35. Spaethe, J., Weidenmüller, A. (2002) Size variation and foraging rate in bumblebees (Bombus terrestris). Insectes Soc. 49, 142–146

    Article  Google Scholar 

  36. Sugden, E.A., Pyke, G.H. (1991) Effects of honey bees on colonies of Exoneura asimillima, an Australian native bee. Aust. J. Ecol. 16, 171–181

    Article  Google Scholar 

  37. Sugden, E.A., Thorp, R.W., Buchmann, S.L. (1996) Honey bee-native bee competition: focal point for environmental change and apicultural response in Australia. Bee World 77, 26–44

    Google Scholar 

  38. Szabo, N.D., Colla, S.R., Wagner, D.L., Gall, L.F., Keer, J.T. (2012) Do pathogen spillover, pesticide use, or habitat loss explain recent North American bumblebee declines? Cons. Lett. 5, 232–239

    Article  Google Scholar 

  39. Thomson, D. (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85, 458–470

    Article  Google Scholar 

  40. Thomson, D.M. (2006) Detecting the effects of introduced species: a case study of competition between Apis and Bombus. Oikos 114, 407–418

    Article  Google Scholar 

  41. Thornhill, R., Alcock, J. (2000) The evolution of insect mating systems. Harvard Univ. Press, Cambridge

    Google Scholar 

  42. Walther-Hellwig, K., Fokul, G., Frankl, R., Büchler, R., Ekschmitt, K., Wolters, V. (2006) Increased density of honeybee colonies affects foraging bumblebees. Apidologie 37, 517–532

    Article  Google Scholar 

  43. Wenner, A.M. (1992) Removal of feral honey bee (Apis mellifera) colonies from Santa Cruz Island. In: Halverson, W.L., Maender, G.J. (eds.) Fourth California Islands Symposium: Update on the Status of Resources, pp. 351–365. Santa Barbara Mus. Nat. Hist, Santa Barbara

    Google Scholar 

  44. Westphal, C., Steffan-Dewenter, I., Tscharntke, T. (2006) Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecol. Entomol. 31, 389–394

    Article  Google Scholar 

  45. Williams, P.H., Osborne, J.L. (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40, 367–387

    Article  Google Scholar 

  46. Wilms, W., Wiechers, B. (1997) Floral resource partitioning between native Melipona bees and the introduced Africanized honey bee in the Brazilian Atlantic rain forest. Apidologie 28, 339–355

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Holly Mottershead, Chris Wright and Martin Lappage for assistance with field work, and the two anonymous reviewers for their constructive comments. This research was funded by the Higher Education Ministry of Libya.

Author information

Affiliations

Authors

Corresponding author

Correspondence to William O. H. Hughes.

Additional information

Effet de la présence proche dun rucher dabeilles sur une colonie de bourdons en terme de santé, développement et performance

Écologie / pollinisateur / compétition interspécifique / Bombus terrestris / Apis mellifera

Der Effekt der Nähe zu einem Bienenstand auf die Fitness, die Entwicklung und die Leistungsfähigkeit von Hummelkolonien

Bestäuberökologie / Wettbewerb / Bienen / Bombus terrestris / Apis mellifera

Manuscript editor: James Nieh

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 155 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Elbgami, T., Kunin, W.E., Hughes, W.O.H. et al. The effect of proximity to a honeybee apiary on bumblebee colony fitness, development, and performance. Apidologie 45, 504–513 (2014). https://doi.org/10.1007/s13592-013-0265-y

Download citation

Keywords

  • pollinator ecology
  • competition
  • bees
  • Bombus terrestris
  • Apis mellifera