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Social learning drives handedness in nectar-robbing bumblebees

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Abstract

Bumblebees have been found to observe and copy the behaviour of others with regard to floral choices, particularly when investigating novel flower types. They can also learn to make nectar-robbing holes in flowers as a result of encountering them. Here, we investigate handedness in nectar-robbing bumblebees feeding on Rhinanthus minor, a flower that can be robbed from either the right-hand side or the left-hand side. We studied numerous patches of R. minor spread across an alpine landscape; each patch tended to be robbed on either the right or the left. The intensity of side bias increased through the season and was strongest in the most heavily robbed patches. We suggest that bees within patches learn robbing strategies (including handedness) from one another, either by direct observation or from experience with the location of holes, leading to rapid frequency-dependent selection for a common strategy. Primary robbing was predominantly carried out not only by a specialist robbing species, Bombus wurflenii, but also by Bombus lucorum, a widespread generalist. Both species adopted the same handedness within particular flower patches, providing the first evidence for social learning crossing the species boundary in wild insects.

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References

  • Anfora G, Rigosi E, Frasnelli E, Ruga V, Trona F, Vallortigara G (2011) Lateralization in the invertebrate brain: left–right asymmetry of olfaction in bumble bee, Bombus terrestris. PLOS ONE 6:e18903

    Article  PubMed  CAS  Google Scholar 

  • Baayen RH (2011) languageR: data sets and functions with “Analyzing linguistic data: a practical introduction to statistics”. R package version 1.4. Available at http://CRAN.R-project.org/package=languageR

  • Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. Available at http://CRAN.R-project.org/package=lme4

  • Cavalli-Sforza L, Feldman MW (1981) Cultural transmission and evolution: a quantitative approach. Princeton University Press, Princeton

    Google Scholar 

  • Chittka L (1998) Sensorimotor learning in bumblebees: long-term retention and reversal training. J Exp Biol 201:515–524

    Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester, p 942

    Book  Google Scholar 

  • Darwin C (1872) The effects of cross and self fertilisation in the vegetable kingdom. Murray, London

    Google Scholar 

  • Dawson EH, Chittka L (2012) Conspecific and heterospecific information use in bumblebees. PLoS One 7:e31444

    Article  PubMed  CAS  Google Scholar 

  • Giraldeau LA, Caraco T (2000) Social foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • Goulson D (2010) Bumblebees; their behaviour, ecology and conservation. Oxford University Press, Oxford, p 317

    Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Diet breadth, coexistence and rarity in bumblebees. Biodivers Conserv 17:3269–3288

    Article  Google Scholar 

  • Grueter C, Leadbeater E, Ratnieks FLW (2010) Social learning: the importance of copying others. Current Biology 20:R683–R685. doi:10.1016/j.cub.2010.06.052

    Article  CAS  Google Scholar 

  • Inouye DW (1983) The terminology of floral larceny. Ecology 61:1251–1252

    Article  Google Scholar 

  • Kawaguchi LG, Ohashi K, Toquenaga Y (2007) Contrasting responses of bumble bees to feeding conspecifics on their familiar and unfamiliar flowers. Proc Roy Soc B 274:2661–2667

    Article  Google Scholar 

  • Kawai M (1965) Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 6:1–30

    Article  Google Scholar 

  • Kells AR, Goulson D (2001) Evidence for handedness in bumblebees. J Insect Behav 14:47–55

    Article  Google Scholar 

  • Knight ME, Martin AP, Bishop S, Osborne JL, Hale RJ, Sanderson RA, Goulson D (2005) An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species. Mol Ecol 14:1811–1820

    Article  PubMed  CAS  Google Scholar 

  • Kwak MM (1979) Effects of bumblebee visits on the seed set of Pedicularis, Rhinanthus and Melampyrum (Scrophulariaceae) in the Netherlands. Acta Botanica Neerlandica 28:177–195

    Google Scholar 

  • Kwak MM, Holthuijzen YA, Prins HHT (1985) A comparison of nectar characteristics of the bumblebee-pollinated Rhinanthus minor and R. serotinus. Oikos 44:123–126

    Article  Google Scholar 

  • Leadbeater E, Chittka L (2005) A new mode of information transfer in foraging bumblebees? Curr Biol 15:R447–R448

    Article  PubMed  CAS  Google Scholar 

  • Leadbeater E, Chittka L (2009) Bumble-bees learn the value of social cues through experience. Biol Lett. doi:10.1098/rsbl.2008.0692

    PubMed  Google Scholar 

  • Leadbeater E, Chittka L (2008) Social transmission of nectar-robbing behaviour in bumble-bees. Proc Roy Soc B 275:1669–1674

    Article  Google Scholar 

  • Maloof JE (2001) The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am J Bot 88:1960–1965

    Article  PubMed  CAS  Google Scholar 

  • Menzel R, Erber I (1978) Learning and memory in bees. Sci Am 239:102–110

    Article  Google Scholar 

  • Osborne JL, Martin AP, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77:401–415

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available at http://www.R-project.org/

  • Seppӓnen JT, Forsman JT, Mӧnkӓnen M, Thomson RL (2007) Social information use is a process across time, space and ecology, reaching heterospecifics. Ecology 88:1622–1633

    Article  Google Scholar 

  • Sherry DF (2008) Social Learning: Nectar Robbing Spreads Socially in Bumble Beessource: Current Biol 18:R608–R610

    CAS  Google Scholar 

  • Stout JC, Allen JA, Goulson D (2000) Nectar robbing, forager efficiency and seed set: bumblebees foraging on the self incompatible plant Linaria vulgaris Mill. (Scrophulariaceae). Acta Oecologia 21:277–283

    Article  Google Scholar 

  • Terkel J (1996) Cultural transmission of feeding behaviour in the black rat (Rattus rattus). In: Heyes CM, Galef BG (eds) Social learning in animals: the roots of culture. Academic, San Diego, pp 17–47

    Chapter  Google Scholar 

  • Westbury DB (2004) Rhinanthus minor L. J Ecol 92:906–927

    Article  Google Scholar 

  • Worden BD, Papaj DR (2005) Flower choice copying in bumblebees. Biol Lett 1:504–507

    Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank E. Marín, G.C. Lye, M. Hall, C. Coates and L. Woodall for their assistance during data collection and discussion and Lars Chittka and two anonymous reviewers for their comments on the manuscript.

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Authors and Affiliations

  1. Biological and Environmental Sciences, University of Stirling, Stirling, FK9 4LA, UK

    D. Goulson, K. J. Park, M. C. Tinsley, L. F. Bussière & M. Vallejo-Marin

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  1. D. Goulson
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  2. K. J. Park
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  3. M. C. Tinsley
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  4. L. F. Bussière
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  5. M. Vallejo-Marin
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Correspondence to D. Goulson.

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Communicated by M. Giurfa

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Goulson, D., Park, K.J., Tinsley, M.C. et al. Social learning drives handedness in nectar-robbing bumblebees. Behav Ecol Sociobiol 67, 1141–1150 (2013). https://doi.org/10.1007/s00265-013-1539-0

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  • DOI: https://doi.org/10.1007/s00265-013-1539-0

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