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

Apidologie volume 45, pages 504–513 (2014)Cite this article

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.

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References

  • 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 

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Article  Google Scholar 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

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

    Article  Google Scholar 

  • 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 

  • 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 

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

    Article  Google Scholar 

  • 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 

  • 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 

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

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

    Article  Google Scholar 

  • 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 

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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.

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Authors and Affiliations

  1. School of Biology, University of Leeds, Leeds, LS2 9JT, UK

    Twfeik Elbgami & William E. Kunin

  2. School of Life Sciences, University of Sussex, Brighton, BN1 9QG, UK

    William O. H. Hughes

  3. Naturalis Biodiversity Center, Postbus 9517, 2300 RA, Leiden, Netherlands

    Jacobus C. Biesmeijer

Authors
  1. Twfeik Elbgami
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  2. William E. Kunin
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  3. William O. H. Hughes
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  4. Jacobus C. Biesmeijer
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Corresponding author

Correspondence to William O. H. Hughes.

Additional information

Manuscript editor: James Nieh

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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

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  • DOI: https://doi.org/10.1007/s13592-013-0265-y

Keywords

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