Behavioral Ecology and Sociobiology

, Volume 67, Issue 7, pp 1141–1150 | Cite as

Social learning drives handedness in nectar-robbing bumblebees

  • D. GoulsonEmail author
  • K. J. Park
  • M. C. Tinsley
  • L. F. Bussière
  • M. Vallejo-Marin
Original Paper


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.


Bombus Foraging behaviour Floral larceny Learning Apidae Hymenoptera 



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.


  1. 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:e18903PubMedCrossRefGoogle Scholar
  2. Baayen RH (2011) languageR: data sets and functions with “Analyzing linguistic data: a practical introduction to statistics”. R package version 1.4. Available at
  3. Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. Available at
  4. Cavalli-Sforza L, Feldman MW (1981) Cultural transmission and evolution: a quantitative approach. Princeton University Press, PrincetonGoogle Scholar
  5. Chittka L (1998) Sensorimotor learning in bumblebees: long-term retention and reversal training. J Exp Biol 201:515–524Google Scholar
  6. Crawley MJ (2007) The R book. Wiley, Chichester, p 942CrossRefGoogle Scholar
  7. Darwin C (1872) The effects of cross and self fertilisation in the vegetable kingdom. Murray, LondonGoogle Scholar
  8. Dawson EH, Chittka L (2012) Conspecific and heterospecific information use in bumblebees. PLoS One 7:e31444PubMedCrossRefGoogle Scholar
  9. Giraldeau LA, Caraco T (2000) Social foraging theory. Princeton University Press, PrincetonGoogle Scholar
  10. Goulson D (2010) Bumblebees; their behaviour, ecology and conservation. Oxford University Press, Oxford, p 317Google Scholar
  11. Goulson D, Lye GC, Darvill B (2008) Diet breadth, coexistence and rarity in bumblebees. Biodivers Conserv 17:3269–3288CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. Inouye DW (1983) The terminology of floral larceny. Ecology 61:1251–1252CrossRefGoogle Scholar
  14. 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 274:2661–2667CrossRefGoogle Scholar
  15. Kawai M (1965) Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 6:1–30CrossRefGoogle Scholar
  16. Kells AR, Goulson D (2001) Evidence for handedness in bumblebees. J Insect Behav 14:47–55CrossRefGoogle Scholar
  17. 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 14:1811–1820PubMedCrossRefGoogle Scholar
  18. Kwak MM (1979) Effects of bumblebee visits on the seed set of Pedicularis, Rhinanthus and Melampyrum (Scrophulariaceae) in the Netherlands. Acta Botanica Neerlandica 28:177–195Google Scholar
  19. Kwak MM, Holthuijzen YA, Prins HHT (1985) A comparison of nectar characteristics of the bumblebee-pollinated Rhinanthus minor and R. serotinus. Oikos 44:123–126CrossRefGoogle Scholar
  20. Leadbeater E, Chittka L (2005) A new mode of information transfer in foraging bumblebees? Curr Biol 15:R447–R448PubMedCrossRefGoogle Scholar
  21. Leadbeater E, Chittka L (2009) Bumble-bees learn the value of social cues through experience. Biol Lett. doi: 10.1098/rsbl.2008.0692 PubMedGoogle Scholar
  22. Leadbeater E, Chittka L (2008) Social transmission of nectar-robbing behaviour in bumble-bees. Proc Roy Soc B 275:1669–1674CrossRefGoogle Scholar
  23. Maloof JE (2001) The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am J Bot 88:1960–1965PubMedCrossRefGoogle Scholar
  24. Menzel R, Erber I (1978) Learning and memory in bees. Sci Am 239:102–110CrossRefGoogle Scholar
  25. 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 77:401–415CrossRefGoogle Scholar
  26. 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
  27. Seppӓnen JT, Forsman JT, Mӧnkӓnen M, Thomson RL (2007) Social information use is a process across time, space and ecology, reaching heterospecifics. Ecology 88:1622–1633CrossRefGoogle Scholar
  28. Sherry DF (2008) Social Learning: Nectar Robbing Spreads Socially in Bumble Beessource: Current Biol 18:R608–R610Google Scholar
  29. 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 21:277–283CrossRefGoogle Scholar
  30. 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 17–47CrossRefGoogle Scholar
  31. Westbury DB (2004) Rhinanthus minor L. J Ecol 92:906–927CrossRefGoogle Scholar
  32. Worden BD, Papaj DR (2005) Flower choice copying in bumblebees. Biol Lett 1:504–507PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • D. Goulson
    • 1
    Email author
  • K. J. Park
    • 1
  • M. C. Tinsley
    • 1
  • L. F. Bussière
    • 1
  • M. Vallejo-Marin
    • 1
  1. 1.Biological and Environmental SciencesUniversity of StirlingStirlingUK

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