Skip to main content
SpringerLink
Log in

Categorization of visual stimuli in the honeybee Apis mellifera

  • Review
  • Published:
Animal Cognition Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Benard J, Giurfa M (2004) A test of transitive inferences in free-flying honeybees: unsuccessful performance due to memory constraints. Learn Mem 11:328–336

    Article  PubMed  Google Scholar 

  • Bitterman ME (1996) Comparative analysis of learning in honeybees. Anim Learn Behav 24:123–141

    Google Scholar 

  • Campan R, Lehrer M (2002) Discrimination of closed shapes by two species of bee, Apis mellifera and Megachile rotundata. J Exp Biol 205:559–572

    PubMed  Google Scholar 

  • Cartwright BA, Collett TS (1983) Landmark learning in bees. Experiments and models. J Comp Physiol A 151:521–543

    Article  Google Scholar 

  • Chen L (1982) Topological structure in visual perception. Science 218:699–700

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Zhang S, Srinivasan MV (2003) Global perception in small brains: topological pattern recognition in honeybees. Proc Natl Acad Sci USA 100:6884–6889

    Article  PubMed  CAS  Google Scholar 

  • Chittka L, Thomson J, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377

    Article  CAS  Google Scholar 

  • 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 103–122

    Google Scholar 

  • Dill M, Wolf R, Heisenberg M (1993) Visual pattern recognition in Drosophila involves retinotopic matching. Nature 365:751–753

    Article  PubMed  CAS  Google Scholar 

  • Efler D, Ronacher B (2000) Evidence against retinotopic-template matching in honeybees’ pattern recognition. Vis Res 40:3391–3403

    Article  PubMed  CAS  Google Scholar 

  • Ernst R, Heisenberg M (1999) The memory template in Drosophila pattern vision at the flight simulator. Vis Res 39:3920–3933

    Article  PubMed  CAS  Google Scholar 

  • Estes WK (1994) Classification and cognition. Oxford University Press, Oxford

    Google Scholar 

  • Frisch Kv (1915) Der Farbensinn und Formensinn der Bienen. Zool Jb Abt Allg Zool Physiol 35:1–182

    Google Scholar 

  • Frisch Kv (1962) Dialects in the language of bees. Sci Am 207:78–87

    Article  Google Scholar 

  • Frisch Kv (1967) The dance language and orientation of bees. Belknap Press, Cambridge, MA

    Google Scholar 

  • Ghirlanda S, Enquist M (2003) A century of generalization. Anim Behav 66:15–36

    Article  Google Scholar 

  • Giurfa M, Núñez JA (1992) Honeybees mark with scent and reject recently visited flowers. Oecologia 89:113–117

    Article  Google Scholar 

  • Giurfa M (1993) The repellent scent-mark of the honeybee Apis mellifera ligustica and its role as communication cue during foraging. Insect Soc 40:59–67

    Article  Google Scholar 

  • Giurfa M, Eichmann B, Menzel R (1996) Symmetry perception in an insect. Nature 382:458–461

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M, Menzel R (1997) Insect visual perception: complex ability of a simple nervous system. Curr Opin Neurobiol 7:505–513

    Article  PubMed  CAS  Google Scholar 

  • 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 57:315–324

    Article  PubMed  Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726–735

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Grossmann K (1970) Erlernen von Farbreizen an der Futterquelle durch Honigbienen während des Anfluges und während des Saugens. Z Tierpsychol 27:553–562

    Google Scholar 

  • Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005) Perceptual and neural olfactory similarity in the honeybee. PLoS Biol 3(4):e60

    Article  PubMed  CAS  Google Scholar 

  • Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63

    Article  Google Scholar 

  • Harlow HF (1949) The formation of learning sets. Psychol Rev 56:51–65

    Article  CAS  PubMed  Google Scholar 

  • Harnard S (1987) Categorical perception. The groundwork of cognition. Cambridge University Press, Cambridge

    Google Scholar 

  • Hateren JH, Srinivasan MV, Wait PB (1990) Pattern recognition in bees: orientation discrimination. J Comp Physiol A 197:649–654

    Google Scholar 

  • Hempel de Ibarra N, Giurfa M (2003) Discrimination of closed coloured shapes requires only contrast to the long wavelength receptor. Anim Behav 66:903–910

    Article  Google Scholar 

  • Herrnstein RJ (1990) Levels of stimulus control: a functional approach. Cognition 37:133–166

    Article  PubMed  CAS  Google Scholar 

  • Hertz M (1933) Über figurale Intensität und Qualität in der optische Wahrnehmung der Biene. Biol Zentralbl 53:10–40

    Google Scholar 

  • Hertz M (1935) Die Untersuchungen über den Formensinn der Honigbiene. Naturwissenschaften 23:618–624

    Article  Google Scholar 

  • Horridge GA, Zhang SW (1995) Pattern vision in honeybees (Apis mellifera): flower-like patterns with no predominant orientation. J Insect Physiol 41:681–688

    Article  CAS  Google Scholar 

  • Horridge GA (1996) Vision of the honeybee Apis mellifera for patterns with two pairs of equal orthogonal bars. J Insect Physiol 42:131–138

    Article  CAS  Google Scholar 

  • Horridge GA (1997a) Pattern discrimination by the honeybee: disruption as a cue. J Comp Physiol A 181:267–277

    Article  Google Scholar 

  • Horridge GA (1997b) Vision of the honeybee Apis mellifera for patterns with one pair of equal orthogonal bars. J Insect Physiol 43:741–748

    Article  PubMed  CAS  Google Scholar 

  • Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:106–154

    PubMed  CAS  Google Scholar 

  • Huber L (2001) Visual categorization in pigeons. In: Cook RG (ed) Avian visual cognition [on-line]. Available: www.pigeon.psy.tufts.edu/avc/huber/

  • Keller FS, Schoenfeld WN (1950) Principles of psychology. Appleton-Century-Crofts, New York

    Google Scholar 

  • Maurer D, Le Grand R, Mondloch CJ (2002) The many faces of configural processing. TICS 6:255–260

    Google Scholar 

  • 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 262–288

    Google Scholar 

  • Menzel R (1999) Memory dynamics in the honeybee. J Comp Physiol A 185:323–340

    Article  Google Scholar 

  • Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62

    Article  PubMed  CAS  Google Scholar 

  • Menzel R, Giurfa M (2001) Cognitive architecture of a minibrain: the honeybee. TICS 5:62–71

    Google Scholar 

  • Møller AP, Eriksson M (1994) Patterns of fluctuating asymmetry in flowers: implications for sexual selection in plants. J Evol Biol 7:97–113

    Article  Google Scholar 

  • Møller AP, Eriksson M (1995) Pollinator preference for symmetrical flowers and sexual selection in plants. Oikos 73:15–22

    Google Scholar 

  • Pastore RE (1987) Categorical perception: some psychophysical models. In: Harnard S (ed) Categorical perception. The groundwork of cognition. Cambridge University Press, Cambridge, pp 29–52

    Google Scholar 

  • Robertson SI (2001) Problem solving. Psychology Press, East Sussex

    Google Scholar 

  • 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 91:374–377

    PubMed  CAS  Google Scholar 

  • Shepard RN (1958) Stimulus and response generalization: deduction of the generalization gradient from a trace model. Psychol Rev 65:242–256

    Article  PubMed  CAS  Google Scholar 

  • Spence K (1937) The differential response in animals to stimuli varying within a single dimension. Psychol Rev 44:430–444

    Article  Google Scholar 

  • Srinivasan MV, Zhang SW, Rolfe B (1993) Pattern vision in insects: “cortical” processing? Nature 362:539–540

    Article  Google Scholar 

  • 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) 343:199–210

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Thorndike EL (1913) Educational physiology, vol II. Columbia University Press, New York

    Google Scholar 

  • 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 39:353–366

    Article  PubMed  CAS  Google Scholar 

  • Watanabe S, Huber L (2006) Animal logics: decisions in the absence of human language. Anim Cogn DOI 10.1007/s10071-006-0043-6

  • Wehner R, Lindauer M (1966) Zur Physiologie des Formensehens bei der Honigbiene. I. Winkelunterscheidung an vertikal orientierten Streifenmustern. Z vergl Physiol 52:290–324

    Article  Google Scholar 

  • Wehner R (1972a) Dorsoventral asymmetry in the visual field of the bee, Apis mellifica. J Comp Physiol 77:256–277

    Article  Google Scholar 

  • 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 183–194

    Google Scholar 

  • Wehner R (1974) Pattern recognition. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon Press, Oxford, pp 75–113

    Google Scholar 

  • Wehner R (1981) Spatial vision in arthropods. In: Autrum HJ (ed) Handbook of sensory physiology, vol VII/6C. Springer, Berlin Heidelberg New York, pp 287–616

    Google Scholar 

  • 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 11–53

    Google Scholar 

  • Yang EC, Maddess T (1997) Orientation-sensitive neurons in the brain of the honey bee (Apis mellifera). J Insect Physiol 43:329–336

    Article  PubMed  CAS  Google Scholar 

  • Zentall TR, Galizio M, Critchfield TS (2002) Categorization, concept learning and behavior analysis: an introduction. J Exp Anal Behav 78:237–248

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank four anonymous referees and G. Beugnon and M. Gauthier for their constructive and helpful comments on our manuscript. J. Benard thanks the University Paul-Sabatier (ATUPS fellowships 2005 & 2006), the Foundation Naturalia & Biologia and the French Research Ministry for financial support. M. Giurfa was supported by the French Research Council (CNRS), the University Paul-Sabatier and the Institut Universitaire de France. Thanks are also due to W. Farina and his team at the University of Buenos Aires for supporting our experimental work.

Author information

Author notes

  1. Silke Stach

    Present address: Länderinstitut für Bienenkunde Hohen Neuendorf e.V., Friedrich-Engels-Str. 32, 16540, Hohen Neuendorf, Germany

Authors and Affiliations

  1. Centre de Recherches sur la Cognition Animale (UMR 5169), CNRS – Université Paul Sabatier, 118 route de Narbonne, 31062, Toulouse cedex 4, France

    Julie Benard, Silke Stach & Martin Giurfa

Authors
  1. Julie Benard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Silke Stach
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Giurfa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Giurfa.

Additional information

This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Benard, J., Stach, S. & Giurfa, M. Categorization of visual stimuli in the honeybee Apis mellifera . Anim Cogn 9, 257–270 (2006). https://doi.org/10.1007/s10071-006-0032-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-006-0032-9

Keywords

Search

Navigation