Animal Cognition

, Volume 9, Issue 4, pp 257–270 | Cite as

Categorization of visual stimuli in the honeybee Apis mellifera

Review

Abstract

Categorization refers to the classification of perceptual input into defined functional groups. We present and discuss evidence suggesting that stimulus categorization can also be found in an invertebrate, the honeybee Apis mellifera, thus underlining the generality across species of this cognitive process. Honeybees show positive transfer of appropriate responding from a trained to a novel set of visual stimuli. Such a transfer was demonstrated for specific isolated features such as symmetry or orientation, but also for assemblies (layouts) of features. Although transfer from training to novel stimuli can be achieved by stimulus generalization of the training stimuli, most of these transfer tests involved clearly distinguishable stimuli for which generalization would be reduced. Though in most cases specific experimental controls such as stimulus balance and discriminability are still required, it seems appropriate to characterize the performance of honeybees as reflecting categorization. Further experiments should address the issue of which categorization theory accounts better for the visual performances of honeybees.

Keywords

Honeybee Insect Vision Categorization Cognition 

References

  1. Benard J, Giurfa M (2004) A test of transitive inferences in free-flying honeybees: unsuccessful performance due to memory constraints. Learn Mem 11:328–336PubMedCrossRefGoogle Scholar
  2. Bitterman ME (1996) Comparative analysis of learning in honeybees. Anim Learn Behav 24:123–141Google Scholar
  3. Campan R, Lehrer M (2002) Discrimination of closed shapes by two species of bee, Apis mellifera and Megachile rotundata. J Exp Biol 205:559–572PubMedGoogle Scholar
  4. Cartwright BA, Collett TS (1983) Landmark learning in bees. Experiments and models. J Comp Physiol A 151:521–543CrossRefGoogle Scholar
  5. Chen L (1982) Topological structure in visual perception. Science 218:699–700PubMedCrossRefGoogle Scholar
  6. Chen L, Zhang S, Srinivasan MV (2003) Global perception in small brains: topological pattern recognition in honeybees. Proc Natl Acad Sci USA 100:6884–6889PubMedCrossRefGoogle Scholar
  7. Chittka L, Thomson J, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377CrossRefGoogle Scholar
  8. Delius JD, Jitsumori M, Siemann M (2000) Stimulus equivalences through discrimination reversals. In: Heyes C, Huber L (eds) The evolution of cognition. MIT Press, Cambridge, MA, pp 103–122Google Scholar
  9. Dill M, Wolf R, Heisenberg M (1993) Visual pattern recognition in Drosophila involves retinotopic matching. Nature 365:751–753PubMedCrossRefGoogle Scholar
  10. Efler D, Ronacher B (2000) Evidence against retinotopic-template matching in honeybees’ pattern recognition. Vis Res 40:3391–3403PubMedCrossRefGoogle Scholar
  11. Ernst R, Heisenberg M (1999) The memory template in Drosophila pattern vision at the flight simulator. Vis Res 39:3920–3933PubMedCrossRefGoogle Scholar
  12. Estes WK (1994) Classification and cognition. Oxford University Press, OxfordGoogle Scholar
  13. Frisch Kv (1915) Der Farbensinn und Formensinn der Bienen. Zool Jb Abt Allg Zool Physiol 35:1–182Google Scholar
  14. Frisch Kv (1962) Dialects in the language of bees. Sci Am 207:78–87CrossRefGoogle Scholar
  15. Frisch Kv (1967) The dance language and orientation of bees. Belknap Press, Cambridge, MAGoogle Scholar
  16. Ghirlanda S, Enquist M (2003) A century of generalization. Anim Behav 66:15–36CrossRefGoogle Scholar
  17. Giurfa M, Núñez JA (1992) Honeybees mark with scent and reject recently visited flowers. Oecologia 89:113–117CrossRefGoogle Scholar
  18. Giurfa M (1993) The repellent scent-mark of the honeybee Apis mellifera ligustica and its role as communication cue during foraging. Insect Soc 40:59–67CrossRefGoogle Scholar
  19. Giurfa M, Eichmann B, Menzel R (1996) Symmetry perception in an insect. Nature 382:458–461CrossRefPubMedGoogle Scholar
  20. Giurfa M, Menzel R (1997) Insect visual perception: complex ability of a simple nervous system. Curr Opin Neurobiol 7:505–513PubMedCrossRefGoogle Scholar
  21. Giurfa M, Hammer M, Stach S, Stollhoff N, Müller-Deisig N, Mizyrycki C (1999) Pattern learning by honeybees: conditioning procedures and recognition strategy. Anim Behav 57:315–324PubMedCrossRefGoogle Scholar
  22. 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 61–82Google Scholar
  23. Giurfa M, Zhang S, Jenett A, Menzel R, Srinivasan MV (2001) The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410:930–933PubMedCrossRefGoogle Scholar
  24. Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726–735PubMedCrossRefGoogle Scholar
  25. 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(1–2):161–169.PubMedCrossRefGoogle Scholar
  26. Gould JL (1985) How bees remember flower shapes. Science 227:1492–1494CrossRefPubMedGoogle Scholar
  27. Grossmann K (1970) Erlernen von Farbreizen an der Futterquelle durch Honigbienen während des Anfluges und während des Saugens. Z Tierpsychol 27:553–562Google Scholar
  28. Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005) Perceptual and neural olfactory similarity in the honeybee. PLoS Biol 3(4):e60PubMedCrossRefGoogle Scholar
  29. Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63CrossRefGoogle Scholar
  30. Harlow HF (1949) The formation of learning sets. Psychol Rev 56:51–65CrossRefPubMedGoogle Scholar
  31. Harnard S (1987) Categorical perception. The groundwork of cognition. Cambridge University Press, CambridgeGoogle Scholar
  32. Hateren JH, Srinivasan MV, Wait PB (1990) Pattern recognition in bees: orientation discrimination. J Comp Physiol A 197:649–654Google Scholar
  33. Hempel de Ibarra N, Giurfa M (2003) Discrimination of closed coloured shapes requires only contrast to the long wavelength receptor. Anim Behav 66:903–910CrossRefGoogle Scholar
  34. Herrnstein RJ (1990) Levels of stimulus control: a functional approach. Cognition 37:133–166PubMedCrossRefGoogle Scholar
  35. Hertz M (1933) Über figurale Intensität und Qualität in der optische Wahrnehmung der Biene. Biol Zentralbl 53:10–40Google Scholar
  36. Hertz M (1935) Die Untersuchungen über den Formensinn der Honigbiene. Naturwissenschaften 23:618–624CrossRefGoogle Scholar
  37. Horridge GA, Zhang SW (1995) Pattern vision in honeybees (Apis mellifera): flower-like patterns with no predominant orientation. J Insect Physiol 41:681–688CrossRefGoogle Scholar
  38. Horridge GA (1996) Vision of the honeybee Apis mellifera for patterns with two pairs of equal orthogonal bars. J Insect Physiol 42:131–138CrossRefGoogle Scholar
  39. Horridge GA (1997a) Pattern discrimination by the honeybee: disruption as a cue. J Comp Physiol A 181:267–277CrossRefGoogle Scholar
  40. Horridge GA (1997b) Vision of the honeybee Apis mellifera for patterns with one pair of equal orthogonal bars. J Insect Physiol 43:741–748PubMedCrossRefGoogle Scholar
  41. Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:106–154PubMedGoogle Scholar
  42. Huber L (2001) Visual categorization in pigeons. In: Cook RG (ed) Avian visual cognition [on-line]. Available: www.pigeon.psy.tufts.edu/avc/huber/Google Scholar
  43. Keller FS, Schoenfeld WN (1950) Principles of psychology. Appleton-Century-Crofts, New YorkGoogle Scholar
  44. Maurer D, Le Grand R, Mondloch CJ (2002) The many faces of configural processing. TICS 6:255–260Google Scholar
  45. Menzel R, Backhaus W (1991) Color vision in insects. In: Gouras P (ed) Vision and visual dysfunction. The perception of color. MacMillan Press, London, pp 262–288Google Scholar
  46. Menzel R (1999) Memory dynamics in the honeybee. J Comp Physiol A 185:323–340CrossRefGoogle Scholar
  47. Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62PubMedCrossRefGoogle Scholar
  48. Menzel R, Giurfa M (2001) Cognitive architecture of a minibrain: the honeybee. TICS 5:62–71Google Scholar
  49. Møller AP, Eriksson M (1994) Patterns of fluctuating asymmetry in flowers: implications for sexual selection in plants. J Evol Biol 7:97–113CrossRefGoogle Scholar
  50. Møller AP, Eriksson M (1995) Pollinator preference for symmetrical flowers and sexual selection in plants. Oikos 73:15–22Google Scholar
  51. Pastore RE (1987) Categorical perception: some psychophysical models. In: Harnard S (ed) Categorical perception. The groundwork of cognition. Cambridge University Press, Cambridge, pp 29–52Google Scholar
  52. Robertson SI (2001) Problem solving. Psychology Press, East SussexGoogle Scholar
  53. Rodriguez I, Gumbert A, Hempel de Ibarra N, Kunze J, Giurfa M (2004) Symmetry is in the eye of the beeholder: innate preference for bilateral symmetry in flower-naive bumblebees. Naturwissenschaften 91:374–377PubMedGoogle Scholar
  54. Shepard RN (1958) Stimulus and response generalization: deduction of the generalization gradient from a trace model. Psychol Rev 65:242–256PubMedCrossRefGoogle Scholar
  55. Spence K (1937) The differential response in animals to stimuli varying within a single dimension. Psychol Rev 44:430–444CrossRefGoogle Scholar
  56. Srinivasan MV, Zhang SW, Rolfe B (1993) Pattern vision in insects: “cortical” processing? Nature 362:539–540CrossRefGoogle Scholar
  57. Srinivasan MV, Zhang SW, Witney K (1994) Visual discrimination of pattern orientation by honeybees: performance and implications for “cortical” processing. Phil Trans Royal Soc Lond (B) 343:199–210Google Scholar
  58. Stach S, Benard J, Giurfa M (2004) Local-feature assembling in visual pattern recognition and generalization in honeybees. Nature 429:758–761PubMedCrossRefGoogle Scholar
  59. Stach S, Giurfa M (2005) The influence of training length on generalization of visual feature assemblies in honeybees. Behav Brain Res 161:8–17PubMedCrossRefGoogle Scholar
  60. Thorndike EL (1913) Educational physiology, vol II. Columbia University Press, New YorkGoogle Scholar
  61. Troje F, Huber L, Loidolt M, Aust U, Fieder M (1999) Categorical learning in pigeons: the role of texture and shape in complex static stimuli. Vis Res 39:353–366PubMedCrossRefGoogle Scholar
  62. Watanabe S, Huber L (2006) Animal logics: decisions in the absence of human language. Anim Cogn DOI 10.1007/s10071-006-0043-6Google Scholar
  63. Wehner R, Lindauer M (1966) Zur Physiologie des Formensehens bei der Honigbiene. I. Winkelunterscheidung an vertikal orientierten Streifenmustern. Z vergl Physiol 52:290–324CrossRefGoogle Scholar
  64. Wehner R (1972a) Dorsoventral asymmetry in the visual field of the bee, Apis mellifica. J Comp Physiol 77:256–277CrossRefGoogle Scholar
  65. Wehner R (1972b) Pattern modulation and pattern detection in the visual system of Hymenoptera. In: Wehner R (ed) Information processing in the visual system of Arthropods. Springer, Berlin Heidelberg New York, pp 183–194Google Scholar
  66. Wehner R (1974) Pattern recognition. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 75–113Google Scholar
  67. Wehner R (1981) Spatial vision in arthropods. In: Autrum HJ (ed) Handbook of sensory physiology, vol VII/6C. Springer, Berlin Heidelberg New York, pp 287–616Google Scholar
  68. Wehner R, Rossel S (1985) The bee's celestial compass. A case study in behavioural neurobiology. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Fischer, Stuttgart, pp 11–53Google Scholar
  69. Yang EC, Maddess T (1997) Orientation-sensitive neurons in the brain of the honey bee (Apis mellifera). J Insect Physiol 43:329–336PubMedCrossRefGoogle Scholar
  70. Zentall TR, Galizio M, Critchfield TS (2002) Categorization, concept learning and behavior analysis: an introduction. J Exp Anal Behav 78:237–248PubMedCrossRefGoogle Scholar
  71. Zhang SW, Srinivasan MV, Zhu H, Wong J (2004) Grouping of visual objects by honeybees. J Exp Biol 207:3289–3298PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Centre de Recherches sur la Cognition Animale (UMR 5169)CNRS – Université Paul SabatierToulouse cedex 4France
  2. 2.Länderinstitut für Bienenkunde Hohen Neuendorf e.V.Hohen NeuendorfGermany

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