Honeybees can discriminate between Monet and Picasso paintings

Abstract

Honeybees (Apis mellifera) have remarkable visual learning and discrimination abilities that extend beyond learning simple colours, shapes or patterns. They can discriminate landscape scenes, types of flowers, and even human faces. This suggests that in spite of their small brain, honeybees have a highly developed capacity for processing complex visual information, comparable in many respects to vertebrates. Here, we investigated whether this capacity extends to complex images that humans distinguish on the basis of artistic style: Impressionist paintings by Monet and Cubist paintings by Picasso. We show that honeybees learned to simultaneously discriminate between five different Monet and Picasso paintings, and that they do not rely on luminance, colour, or spatial frequency information for discrimination. When presented with novel paintings of the same style, the bees even demonstrated some ability to generalize. This suggests that honeybees are able to discriminate Monet paintings from Picasso ones by extracting and learning the characteristic visual information inherent in each painting style. Our study further suggests that discrimination of artistic styles is not a higher cognitive function that is unique to humans, but simply due to the capacity of animals—from insects to humans—to extract and categorize the visual characteristics of complex images.

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References

  1. Abdi H, Valentin D, Edelman B, O’Toole AJ (1995) More about the difference between men and women: evidence from linear neural networks and the principal component approach. Percept 24:539–562

    Article  CAS  Google Scholar 

  2. Avarguès-Weber A, Portelli G, Benard J, Dyer AG, Giurfa M (2010) Configural processing enables discrimination and categorization of face-like stimuli in honeybees. J Exp Biol 213:593–601

    PubMed  Article  Google Scholar 

  3. Avarguès-Weber A, Deisig N, Giurfa M (2011) Visual cognition in social insects. Annu Rev Entomol 56:423–443

    PubMed  Article  Google Scholar 

  4. Avarguès-Weber A, Dyer AG, Combe M, Giurfa M (2012) Simultaneous mastering of two abstract concepts by the miniature brain of bees. PNAS 109:7481–7486

    PubMed  Article  Google Scholar 

  5. Benard J, Stach S, Giurfa M (2006) Categorization of visual stimuli in the honeybee Apis mellifera. Anim Cogn 9:257–270

    PubMed  Article  Google Scholar 

  6. Burton AM, Bruce V, Hancock PJB (1999) From pixels to people: a model of familiar face recognition. Cogn Sci 23:1–31

    Article  Google Scholar 

  7. Chittka L, Walker J (2006) Do bees like Van Gogh’s sunflowers? Optics Laser Technol 38:323–328

    Article  Google Scholar 

  8. Chittka L, Walker J (2007) Insects as art lovers: bees for Van Gogh. Antennae 2:37–42

    Google Scholar 

  9. Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Bees trade off foraging speed for accuracy. Nature 424:388

    PubMed  Article  CAS  Google Scholar 

  10. Collett TS (1996) Insect navigation en route to the goal—multiple strategies for the use of landmarks. J Exp Biol 199:227–235

    PubMed  Article  Google Scholar 

  11. Collett TS, Collett M (2002) Memory use in insect visual navigation. Nat Rev Neurosci 3:542–552

    PubMed  Article  CAS  Google Scholar 

  12. Collett TS, Graham P, Durier V (2003) Route learning by insects. Curr Opin Neurobiol 13:718–725

    PubMed  Article  CAS  Google Scholar 

  13. Dyer AG (2012) The mysterious cognitive abilities of bees: why models of visual processing need to consider experience and individual differences in animal performance. J Exp Biol 215:387–395

    PubMed  Article  Google Scholar 

  14. Dyer AG, Griffiths DW (2012) Seeing near and seeing far: behavioural evidence for dual mechanisms of pattern vision in the honeybee (Apis mellifera). J Exp Biol 215:397–404

    PubMed  Article  Google Scholar 

  15. Dyer AG, Vuong QC (2008) Insect brains use image interpolation mechanisms to recognise rotated objects. PLoS ONE 3:e4086

    PubMed  Article  Google Scholar 

  16. Dyer AG, Neumeyer C, Chittka L (2005) Honeybee (Apis mellifera) vision can discriminate between and recognise images of human faces. J Exp Biol 208:4709–4714

    PubMed  Article  Google Scholar 

  17. Dyer AG, Rosa MGP, Reser DH (2008) Honeybees can recognise images of complex natural scenes for use as potential landmarks. J Exp Biol 211:1180–1186

    PubMed  Article  Google Scholar 

  18. Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193:801–824

    Article  Google Scholar 

  19. Giurfa M, Lehrer M (2001) Honeybee vision and floral displays: from detection to close-up recognition. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 61–82

    Google Scholar 

  20. Giurfa M, Zhang SW, Jenett A, Menzel R, Srinivasan MV (2001) The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410:930–933

    PubMed  Article  CAS  Google Scholar 

  21. Giurfa M, Schubert M, Reisenman C, Gerber B, Lachnit H (2003) The effect of cumulative experience on the use of elemental and configural visual discrimination strategies in honeybees. Behav Brain Res 145:161–169

    PubMed  Article  Google Scholar 

  22. Gordon R, Forge A (1983) Monet. Abrams, New York

    Google Scholar 

  23. Gould JL (1985) How bees remember flower shapes. Science 227:1492–1494

    PubMed  Article  CAS  Google Scholar 

  24. Gould JL (1986) Pattern learning by honeybees. Anim Behav 34:990–997

    Article  Google Scholar 

  25. Gross HJ, Pahl M, Si A, Zhu H, Tautz J, Zhang SW (2009) Number-based visual generalisation in the honeybee. PLoS ONE 4:e4263

    PubMed  Article  Google Scholar 

  26. Horridge A (2000) Seven experiments on pattern vision of the honeybee, with a model. Vision Res 40:2589–2603

    PubMed  Article  CAS  Google Scholar 

  27. Horridge A (2005) What the honeybee sees: a review of the recognition system of Apis mellifera. Physiol Entomol 30:2–13

    Article  Google Scholar 

  28. Horridge A (2007) The preferences of the honeybee (Apis mellifera) for different visual cues during the learning process. J Insect Physiol 53:877–889

    PubMed  Article  CAS  Google Scholar 

  29. Horridge A (2009a) Generalization in visual recognition by the honeybee (Apis mellifera): a review and explanation. J Insect Physiol 55:499–511

    PubMed  Article  CAS  Google Scholar 

  30. Horridge A (2009b) What does an insect see? J Exp Biol 212:2721–2729

    PubMed  Article  Google Scholar 

  31. Lehrer M, Campan R (2005) Generalization of convex shapes by bees: what are shapes made of? J Exp Biol 208:3233–3247

    PubMed  Article  Google Scholar 

  32. O’Toole AJ, Abdi H, Deffenbacher K, Valentin D (1993) Low-dimensional representation of faces in higher dimensions of face space. J Opt Soc Am 10:405–411

    Article  Google Scholar 

  33. Poggi C (1992) In defiance of painting: cubism, futurism and the invention of collage. Yale University Press, New Haven Connecticut

    Google Scholar 

  34. Reinhard J, Srinivasan MV, Zhang SW (2006) Complex memories in honeybees: can there be more than two? J Comp Physiol A 192:409–416

    Article  Google Scholar 

  35. Rubin WS (1989) Picasso and Braque: pioneering cubism. Museum of Modern Art, New York

    Google Scholar 

  36. Srinivasan MV (2010) Honey bees as a model for vision, perception, and cognition. Annu Rev Entomol 55:184–267

    Article  Google Scholar 

  37. Srinivasan MV, Zhang SW, Zhu H (1998) Honeybees link sights to smells. Nature 396:637–638

    Article  CAS  Google Scholar 

  38. Stach S, Giurfa M (2005) The influence of training length on generalization of visual feature assemblies in honeybees. Behav Brain Res 161:8–17

    PubMed  Article  Google Scholar 

  39. Stach S, Benard J, Giurfa M (2004) Local-feature assembling in visual pattern recognition and generalization in honeybees. Nature 429:758–761

    PubMed  Article  CAS  Google Scholar 

  40. Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured landscapes. Proc R Soc Lond B 270:569–575

    Article  Google Scholar 

  41. Stuckey CF (1995) Claude Monet 1840–1926. Thames and Hudson, New York

    Google Scholar 

  42. Turk M, Pentland A (1991) Eigenfaces for recognition. J Cogn Neurosci 3:71–86

    Article  Google Scholar 

  43. von Frisch K (1914) Der Farbensinn und Formensinn der Biene. Zool Jb Physiol 37:1–238

    Google Scholar 

  44. von Frisch K (1967) The dance language and orientation of bees. Belknap Press, Cambridge

    Google Scholar 

  45. Watanabe S (2001) Van Gogh, Chagall and pigeons: picture discrimination in pigeons and humans. Anim Cogn 4:147–151

    Article  Google Scholar 

  46. Watanabe S, Sakamoto J, Wakita M (1995) Pigeon’s discrimination of paintings by Monet and Picasso. J Exp Anal Beh 63:165–174

    Article  CAS  Google Scholar 

  47. Wehner R (1971) The generalization of directional visual stimuli in the honey bee, Apis mellifera. J Insect Physiol 7:1579–1591

    Article  Google Scholar 

  48. Zentall T, Wasserman EA, Lazareva OF, Thompson R, Ratterman MJ (2008) Concept learning in animals. Comp Cogn Behav Rev 3:13–45

    Google Scholar 

  49. Zhang SW, Srinivasan MV (2004) Exploration of cognitive capacity in honeybees: higher functions emerge from a small brain. In: Prete FR (ed) Complex worlds from simpler nervous systems. MIT Press, Cambridge, pp 41–74

    Google Scholar 

  50. Zhang SW, Srinivasan MV, Collett TS (1995) Convergent processing in honeybee vision: multiple channels for the recognition of shape. PNAS 92:3029–3031

    PubMed  Article  CAS  Google Scholar 

  51. Zhang SW, Srinivasan MV, Zhu H, Wong J (2004) Grouping of visual objects by honeybees. J Exp Biol 207:3289–3298

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

We thank Chin Y. J. Yuen for help with the experiments, and Adrian Dyer and Allen Cheung for advice on the image analyses. W.W. was funded through an Australian Postgraduate Award by the Australian Government and an Australian Research Council Discovery grant to JT (DP0985830). A.M.M. was funded by a FAPESP doctorate scholarship (08/50576-8), Brazil.

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Correspondence to Judith Reinhard.

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Wu, W., Moreno, A.M., Tangen, J.M. et al. Honeybees can discriminate between Monet and Picasso paintings. J Comp Physiol A 199, 45–55 (2013). https://doi.org/10.1007/s00359-012-0767-5

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Keywords:

  • Honeybee
  • Learning
  • Vision
  • Discrimination
  • Generalization