Skip to main content

Functional Organization of Appetitive Learning and Memory in a Generalist Pollinator, the Honey Bee

  • Chapter
Insect Learning

Abstract

Individual experience with environmental stimuli leaves multiple traces of neuronal plasticities in the nervous system. Receptors adapt to prolonged stimulation; neural circuits habituate to repeated stimuli and dishabituate or sensitize to arousing stimuli; and new functional connections are formed or existing ones abolished by associative and latent learning. What are the rules of neural plasticity and how do they relate to the biological constraints under which they have evolved? The neuroethological approach taken in the study of honey bee learning and memory tries to understand the neuronal mechanisms of the multiple memory traces as adaptations to the particular demands of foraging by a generalist pollinating insect. The study of the functional dynamics of memory thus serves two goals: to unravel the informational sources which guide the sequences and time dependencies of the animal’s choice behavior, and to better understand the neural correlates of the various forms of memory.

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

Access this chapter

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Bitterman, M.E. 1988. Vertebrate-invertebrate comparisons. NATO ASI Ser.Intell. Evol. Biol. 17:251–275.

    Google Scholar 

  • Carew, T.J., Abrams, T.W., Hawkins, R.D. and Kandel, E.R. 1984. The use of simple invertebrate systems to explore psychological issues related to associative learning. In D.L. Alkon and J. Farley (eds.), Primary Neural Substrates of Learning and Behavioral Change. Cambridge University Press, New York, pp. 169–183.

    Google Scholar 

  • Colwill, R.M., and Rescorla, R.A., 1988. The role of response-reinforcer associations increases throughout extended instrumental training. Anim. Learn. Be-hay. 16:105–111.

    Google Scholar 

  • Ebbinghaus, M. 1885. Über das Gedächtnis. K. Buehler, Leipzig. Erber, J. 1972. The time-dependent storing of optical information in the honeybee. In R. Wehner (ed.), Information Processing in the Visual Systems of Arthropods. Springer, Berlin-Heidelberg-New York, pp. 309–314.

    Google Scholar 

  • Erber, J. 1975a. The dynamics of learning in the honeybee (Apis mellifera carnica). I. The time dependence of the choice reaction. J. Comp. Physiol. 99:231–242.

    Google Scholar 

  • Erber, J. 1975b. The dynamics of learning in the honeybee (Apis mellifica carnica). II. Principles of information processing. J. Comp. Physiol. 99:243–255.

    Article  Google Scholar 

  • Erber, J., Masuhr, T. and Menzel, R., 1980. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 5:343–358.

    Article  Google Scholar 

  • Fabre 1879. Souvenirs entomologiques. Paris.

    Google Scholar 

  • Forel, A. 1910. Das Sinnesleben der Insekten. Reinhardt, München.

    Google Scholar 

  • Frisch, K. v. 1967. The Dance Language and Orientation of Bees. Harvard University Press, Cambridge.

    Google Scholar 

  • Garcia, J., and Koelling, R.A., 1966. Relation of cue to consequence in avoidance learning. Psychol. Sci 4:124–124.

    Google Scholar 

  • Gormezano, I. 1984. The study of associative learning with CS-CR paradigms. In D.L. Alkon and J. Farley (eds.), Primary Neural Substrates of Learning and Behavioral Change. Cambridge University Press, New York, pp. 5–24.

    Google Scholar 

  • Gould, J.L., and Marier, P. 1984. Ethology and the natural history of learning. In P. Marler and H.S. Terrace (eds.), The Biology of Learning. Springer-Verlag, Berlin-Heidelberg-New York, pp. 47–74.

    Chapter  Google Scholar 

  • Greggers, U. 1989. Optimizing strategies in choice behavior in the honey bee. In J. Erber, R. Menzel, H.J. Pflüger, and D. Todt (eds.), Neural Mechanisms of Behavior—Proceedings of the 2nd International Congress of Neuroethology. Georg Thieme Verlag, Stuttgart-New York, p. 219.

    Google Scholar 

  • Greggers, U., and Menzel, R. Memory dynamics and the foraging strategy of honey bees. Behay. Ecol. Sociobiol, in press.

    Google Scholar 

  • Griffin, D.R. 1984. Animal Thinking. Harvard University Press, Harvard.

    Google Scholar 

  • Grossman, K.E. 1971. Belohnungsverzögerung beim Erlernen einer Farbe an einer künstlichen Futterstelle durch Honigbienen. Z. Tierpsychol. 29:28–41.

    Article  Google Scholar 

  • Hawkins, R.D. and Kandel, E.R. 1984. Is there a cell-biological alphabet for simple forms of learning? Psychol. Rev. 91:375–391.

    Article  PubMed  CAS  Google Scholar 

  • Heinrich, B. 1979. Resource heterogeneity and patterns of movement in foraging bumble bees. Oecologia 40:235–245.

    Article  Google Scholar 

  • Heinrich, B. 1983. Do bumble bees forage optimally, and does it matter? Am. Zool. 23:273–281.

    Google Scholar 

  • Heinrich, B. 1984. Learning in Invertebrates. In P. Marler and H.S. Terrace (eds), The Biology of Learning. Dahlem Konferenzen. Springer-Verlag, New York, pp. 135–147.

    Google Scholar 

  • Houston, A., Kacelnik, A., and McNamara, J. 1982. Some learning rules for acquiring information. In J. McFarland (ed.), Functional Ontogeny. Plenum Press, London, pp. 140–191.

    Google Scholar 

  • Hull, C.L. 1934. Learning II: The factor of the conditioned reflex. In C. Murchison (ed.), Handbook of General Experimental Psychology. Clark University Press, Worcester.

    Google Scholar 

  • Hull, C.L. 1943. Principles of Behaviour. Appleton-Century-Crofts, New York.

    Google Scholar 

  • Kamin, L.J. 1969. Selective association and conditioning. In W.K. Honig (ed.), Fundamental Issues in Associative Learning. Dalhousie University Press, Halifax.

    Google Scholar 

  • Kiltermann, R. 1969. Lern-und Vergessensprozesse bei der Honigbiene—aufgezeigt anhand von Duftdressuren. Z. Vergl. Physiol 63:310–334.

    Google Scholar 

  • Krebs, J.R. Kacelnik, A., and Taylor, P. 1978. Test of optimal sampling by foraging great tits. Nature 275:27–31.

    Article  Google Scholar 

  • Kuwabara, M. 1957. Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifera. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool 13:458–464.

    Google Scholar 

  • Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Z. Vergl. Physiol. 37:263–324.

    Google Scholar 

  • Lindauer, M. 1959. Angeborene und erlernte Komponenten in der Sonnenorientierung der Bienen. Z. Vergl. Physiol. 42:43–62.

    Google Scholar 

  • MacArthur, R.H., and Pianka, E.R. 1966. On optimal use of patchy environment. Am. Nat. 100:603–609.

    Article  Google Scholar 

  • Maynard Smith, J. 1978. Optimization theory in evolution. Annu. Rev. Ecol. Syst. 9:31–56.

    Article  Google Scholar 

  • Meineke, H. 1978. Umlernen einer Honigbiene zwischen gelb-und blau-Belohnung im Dauerversuch. J. Insect Physiol. 24:155–163.

    Article  Google Scholar 

  • Menzel, R. 1967. Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). Z. Vergl. Physiol. 56:22–62.

    Google Scholar 

  • Menzel, R. 1968. Das Gedächtnis der Honigbiene für Spektralfarben. I Kurzzeitiges und langzeitiges Behalten, Z. Vergl. Physiol. 60:82–102.

    Google Scholar 

  • Menzel, R. 1969. Das Gedächtnis der Honigbiene für Spektralfarben. II. Umlernen und Mehrfachlernen. Z. Vergl. Physiol. 63:290–309.

    Google Scholar 

  • Menzel, R. 1979. Behavioral access to short-term memory in bees. Nature 281:368–369.

    Article  PubMed  CAS  Google Scholar 

  • Menzel, R. 1984. Short-term memory in bees. In D.L. Alkon and I. Farley (eds.), Primary Neural Substrates of Learning and Behavioral Change. Cambridge University Press, Cambridge, pp. 259–274.

    Google Scholar 

  • Menzel, R. 1985. Learning in honey bees in an ecological and behavioral context. In B. Hölldobler and M Lindauer (eds.), Experimental Behavioral Ecology. Gustav Fischer Verlag, Stuttgart, pp. 55–74.

    Google Scholar 

  • Menzel, R. 1987. Memory traces in honeybees. In R. Menzel and A. Mercer (eds.), Neurobiology and Behavior of Honeybees. Springer, Berlin, pp. 310–325.

    Chapter  Google Scholar 

  • Menzel, R. 1990. Learning, memory and “cognition” in honey bees. In R.P. Kesner and D.S. Olten (eds.), Neurobiology of Comparative Cognition. Erlbaum, Hillsdale, NJ, pp. 237–292.

    Google Scholar 

  • Menzel, R. and Erber, J. 1972. The influence of the quantity of reward on the learning performance in honeybees. Behavior 41:27–42.

    Article  Google Scholar 

  • Menzel, R., Erber, J. and Masuhr, T. 1974. Learning and memory in the honey bee. In L. Barton-Browne (ed.), Experimental Analysis of Insect Behavior. Springer, Berlin, pp. 195–217.

    Chapter  Google Scholar 

  • Menzel, R. and Greggers, U. 1992. Temporal dynamics and foraging behavior in honeybees. In J. Billen (ed.), Biology and Evolution of Social Insects. Leuven University Press, Leuven.

    Google Scholar 

  • Menzel, R. and Sugawa, M. 1986. Time course of short-term memory depends on associative events. Naturwissenschaften 73:564–565.

    Article  PubMed  CAS  Google Scholar 

  • Müller, G.E., and Pilzecker, A., 1900. Experimentelle Beiträge zur Lehre vom Gedächtnis. Z. Psychol. 1:1–288.

    Google Scholar 

  • Pavlov, I.P. 1967. Lectures on conditioned reflexes. International Publishers, New York.

    Google Scholar 

  • Pleasants, J.M. 1981. Bumblebee response to variation in nectar availability. Ecology 62:1648–1661.

    Article  Google Scholar 

  • Pyke, G.H. 1978a. Optimal foraging: movement patterns of bumble bees between inflorescences. Theor. Popul. Biol. 13:72–98.

    CAS  Google Scholar 

  • Pyke, G.H. 1978b. Optimal foraging in bumblebees and coevolution with their plants. Oecologia 36:281–293.

    Article  Google Scholar 

  • Pyke, G.H. 1984. Optimal foraging theory: A critical review. Annu. Rev. Ecol. Syst. 15:523–575.

    Article  Google Scholar 

  • Rescorla, R.A. 1967. Pavlovian conditioning and its proper control procedures. Psychol Rev. 74:71–80.

    CAS  Google Scholar 

  • Rescorla, R.A. 1988. Behavioral studies of pavlovian conditioning. Annu. Rev. Neurosci. 11:329–352.

    Article  CAS  Google Scholar 

  • Rescorla, R.A. and Holland, P.C. 1982. Behavioral studies of associative learning in animals. Annu. Rev. Psychol 33:265–308.

    Article  Google Scholar 

  • Rescorla, R.A. and Wagner, A.R. 1972. A theory of classical conditioning: Variations in the effectivness of reinforcement and non-reinforcement. In A.H. Black and W.F. Prokasy (eds.), Classical Conditioning. II: Current Research and Theory. Appleton-Century Crofts, New York, pp. 64–99.

    Google Scholar 

  • Schmid-Hempel, P. 1984. The importance of handling time for the flight directionality in bees. Behay. Ecol. Sociobiol. 15:303–309.

    Article  Google Scholar 

  • Schmid-Hempel, P. 1985a. How do bees choose flight direction while foraging? Physiol. Entomol. 10:439–442.

    Google Scholar 

  • Schmid-Hempel, P. and Schmid-Hempel, R. 1985b. Nectar-collecting bees use distant-sensitive movement rules. Anim. Behay. 34(2):605–607.

    Article  Google Scholar 

  • Schreurs, B.G. 1989. Classical conditioning of model systems: A behavioral review. Psychobiology 17:145–155.

    Google Scholar 

  • Seeley, T.D. 1985. Honeybee ecology. A study of adaptation in social life. Princeton University Press, Princeton.

    Google Scholar 

  • Smith, B., and Menzel, R. 1989. An analysis of variability in the feeding motor program of the honey bee: The role of learning in releasing a modal action pattern. Ethology 82:68–81.

    Article  Google Scholar 

  • Squire, L., and Cohen, N. 1982. Remote memory, retrograde amnesia and the neuropsychology of memory. In L.S. Cermak (ed.), Human Memory and Amnesia. Erlbaum, Hillsdale, NJ, pp. 275–303.

    Google Scholar 

  • Vareschi, E. 1971. Duftunterscheidung bei der Honigbiene-Einzelzell-Ableitungen and Verhaltensreaktionen. Z. Vergl Physiol. 75:143–173.

    Google Scholar 

  • Waddington, K.D. 1985. Cost-intake information used in foraging. J. Insect Physiol: 31:891–889.

    Article  Google Scholar 

  • Waddington, K.D. Allen, T. and Heinrich, B. 1981. Floral preferences of bumble bees (Bombus edwardsii) in relation to intermittent versus continuous rewards. Anim Behay. 29:779–784.

    Article  Google Scholar 

  • Waddington, K.D., and Holden, L.R. 1979. Optimal foraging: On flower selection by bees. Am. Nat. 114:179–196.

    Article  Google Scholar 

  • Weiskrantz, L. 1970. A long-term view of short-term memory in psychology. In G. Horn and R.A. Hinde (eds.), Short-Term Changes in Neural Activity and Behavior. Cambridge Univ. Press, London, pp. 63–74.

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Menzel, R., Greggers, U., Hammer, M. (1993). Functional Organization of Appetitive Learning and Memory in a Generalist Pollinator, the Honey Bee. In: Papaj, D.R., Lewis, A.C. (eds) Insect Learning. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-2814-2_4

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-2814-2_4

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6216-6

  • Online ISBN: 978-1-4615-2814-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics