Artículo

Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Early reports indicate that trophallaxis, i.e. the exchange of liquid food by mouth, may allow honeybees to assign nectar odours with predictive values to anticipate biological meaningful reward stimuli. Nevertheless, this type of learning has not been addressed directly. In the present study, pairs of animals were isolated to induce trophallaxis under controlled conditions and, afterwards, the honeybee proboscis extension reflex was used to investigate the possible role of trophallaxis in learning olfactory cues. The results demonstrate unambiguously that associative learning actually occurs by means of trophallaxis. Animals associate the odour (as the conditioned stimulus or CS) and the sucrose (as the unconditioned stimulus or US) present in the solution they receive through trophallaxis. Moreover, this particular kind of learning leads to long-term olfactory memories after a single learning trial, even when trophallaxis is brief. In addition, we found that the strength of association is clearly affected by CS and US intensity as well as the recent previous foraging experiences of the animals. Comparisons are presented among several features of the learning during trophallaxis and the classical conditioning of the proboscis extension reflex with restrained subjects. Finally, the relevance of learning through trophallaxis in the task of successful foraging is discussed.

Registro:

Documento: Artículo
Título:Olfactory learning by means of trophallaxis in Apis mellifera
Autor:Gil, M.; De Marco, R.J.
Filiación:Depto. Fisiol., Biol. Molec. Y Cel., Fac. de Ciencias Exactas Y Naturales, Pabellón II, C1428EHA, Buenos Aires, Argentina
Freie Universität Berlin, Fb. Biologie, Chemie, Pharmazie, Inst. F. Biologie-Neurobiologie, Berlin D-14195, Germany
Palabras clave:Apis mellifera; Associative learning; Honeybee; Olfactory conditioning; Trophallaxis; analysis of variance; animal; article; association; bee; comparative study; conditioned reflex; feeding behavior; learning; odor; physiology; Analysis of Variance; Animals; Association Learning; Bees; Conditioning, Classical; Cues; Feeding Behavior; Odors; Smell; Animalia; Apis mellifera
Año:2005
Volumen:208
Número:4
Página de inicio:671
Página de fin:680
DOI: http://dx.doi.org/10.1242/jeb.01474
Título revista:Journal of Experimental Biology
Título revista abreviado:J. Exp. Biol.
ISSN:00220949
CODEN:JEBIA
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00220949_v208_n4_p671_Gil.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00220949_v208_n4_p671_Gil

Referencias:

  • Bitterman, M.E., Menzel, R., Fietz, A., Schäfer, S., Classical conditioning of proboscis extension in honeybees (Apis mellifera) (1983) J. Comp. Psychol., 97, pp. 107-119
  • Buchanan, G.M., Bitterman, M.E., Learning in honeybees as a function of amount and frequency of reward (1988) Anim. Learn. Behav., 16, pp. 247-255
  • Butler, C.G., The importance of perfume on the discovery of food by the worker honeybee Apis mellifera L. (1951) Proc. R. Soc. Lond. B, 138, pp. 403-413
  • Colwill, R.M., Rescorla, R.A., Associative structures in instrumental learning (1986) The Psychology of Learning and Motivation, pp. 55-104. , ed. G. H. Bower, New York: Academic Press
  • Couvillon, P.A., Lee, Y., Bittermann, M.E., Learning in honeybees as a function of amount of reward: Rejection of the equalasymptote assumption (1991) Anim. Learn. Behav., 19, pp. 381-387
  • De Marco, R.J., Farina, W.M., Changes in food source profitability affect the trophallactic and dance behavior of forager honeybees (Apis mellifera L.) (2001) Behav. Ecol. Sociobiol., 50, pp. 441-449
  • De Marco, R.J., Farina, W.M., Trophallaxis in forager honeybees (Apis mellifera): Resource uncertainty enhances begging contacts? (2003) J. Comp. Physiol. A, 189, pp. 125-134
  • Dirscheld, H., (1960) Die Vermittlung des Blütenduftes Bei der Verständigung Im Bienenstock, , Dissert. Naturw. Fak. University of München, Germany
  • Doolittle, G.M., Where do the field-bees deposit their loads? (1907) Amer. Bee J., 42, pp. 653-654
  • Durlach, P.J., Learning and performance in Pavlovian conditioning: Are failures of contiguity failures of learning or performance? (1989) Contemporary Learning Theories: Pavlovian Conditioning and the Status of Traditional Learning Theory, pp. 19-60. , ed. S. B. Klein and R. R. Mowrer, Hillsdale, NJ: Erlbaum
  • Farina, W.M., Núñez, J.A., Trophallaxis in the honeybee Apis mellifera (L.) as related to the profitability of food sources (1991) Anim. Behav., 42, pp. 389-394
  • Free, J.B., A study of the stimuli which release the food begging and offering responses of worker honey-bees (1956) Br. J. Anim. Behav., 4, pp. 94-101
  • Free, J.B., The transmission of food between worker honeybees (1957) Br. J. Anim. Behav., 5, pp. 41-47
  • Free, J.B., The transfer of food between the adult members of a honeybee community (1959) Bee World, 40, pp. 193-201
  • Gould, J.L., Ethological and comparative aspects of honey bee learning (1993) Insect Learning: Ecological and Evolutionary Perspectives, pp. 19-50. , ed. A. C. Lewis and D. R. Papaj, New York: Chapman and Hall
  • Greggers, U., Menzel, R., Memory dynamics and foraging strategies of honeybees (1993) Behav. Ecol. Sociobiol., 32, pp. 17-29
  • Hammer, M., Menzel, R., Learning and memory in the honeybee (1995) J. Neurosc., 15, pp. 1617-1630
  • Hebb, D.O., The distinction between 'classical' and 'instrumental' (1956) Can. J. Psychol., 10, pp. 165-166
  • Hoban, J.S., Couvillon, P.A., Bitterman, M.E., Odor preference in honeybees as a function of amount of reward: Test of two explanations (1996) J. Insect Behav., 9, pp. 121-132
  • Kuwabara, M., Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica (1957) J. Fac. Hokkaido Univ. Ser. VI Zool., 13, pp. 458-464
  • Lindauer, M., (1961) Communication among Social Bees, , Cambridge, Mass: Harvard University Press
  • Menzel, R., Das Gedächtnis der Honigbiene für Spektralfarben. I. Kurtzzeitiges und langzeitiges Behalten (1968) Z. Vergl. Physiol., 60, pp. 82-102
  • Menzel, R., Das Gedächtnis der Honigbiene für Spektralfarben. II. Umlernen und Mehrfachlernen (1969) Z. Vergl. Physiol., 63, pp. 290-309
  • Menzel, R., Learning in honeybees in an ecological and behavioral context (1985) Experimental Behavioral Ecology, pp. 55-74. , ed. B. Holldobler and M. Lindauer, Stuttgart: Gustav Fischer
  • Menzel, R., Learning, memory, and 'cognition' in honey bees (1990) Neurobiology of Comparative Cognition, pp. 237-292. , ed. R. P. Kesner and D. S. Olten, Hillsdale NJ: Erlbaum
  • Menzel, R., Memory dynamics in the honeybee (1999) J. Comp. Physiol. A, 185, pp. 323-340
  • Menzel, R., Searching for the memory trace in a mini-brain, the honeybee (2001) Learn. Mem., 8, pp. 53-62
  • Menzel, R., Erber, J., The influence of the quantity of reward on the learning performance in honeybees (1972) Behaviour, 41, pp. 27-42
  • Menzel, R., Manz, G., Menzel, R., Greggers, U., Massed and spaced learning in honeybees: The role of CS, US, the intertrial interval, and the test interval (2001) Learn. Mem., 8, pp. 198-208
  • Nixon, H.L., Ribbands, C.R., Food transmission within the honeybee community (1952) Proc. R. Soc. Lond. B., 140, pp. 43-50
  • Opfinger, E., Über die Orientierng der Biene an der Futterquelle (1931) Z. Vergl. Physiol., 15, pp. 431-487
  • Opfinger, E., Zur Physiologie der Duftdressuren bei Bienen (1949) Z. Vergl. Physiol., 31, pp. 441-453
  • Pavlov, I.P., (1927) Conditioned Reflexes, , London: Oxford University Press
  • Pelz, C., Gerber, B., Menzel, R., Odorant intensity as determinant for olfactory conditioning in honeybees: Roles in discrimination, overshadowing and memory consolidation (1997) J. Exp. Biol., 200, pp. 837-847
  • Ray, S., Ferneyhough, B., Behavioral development and olfactory learning in the honeybee (Apis mellifera) (1999) Dev. Psychobiol., 34, pp. 21-27
  • Reinhard, J., Srinivasan, M.V., Guez, D., Zhang, S., Floral scents induce recall of navigational and visual memories in honeybees (2004) J. Exp. Biol., 207, pp. 4371-4381
  • Rescorla, R.A., Control of instrumental performance by Pavlovian and instrumental stimuli (1994) J. Exp. Psychol. Anim. Behav. Process, 20, pp. 44-50
  • Rescorla, R.A., Wagner, A.R., A theory of Pavlovian conditioning: Variations of the effectiveness of reinforcement and noreinforcement (1972) Classical Conditioning. II. Current Research and Theory, pp. 64-99. , ed. A. H. Black and W. T. Prokasy, New York: Appleton-Century-Crofts
  • Ribbands, C.R., Communication between honey bees. I. The response of crop-attached bees to the scent of their crop (1954) Proc. R. Entomol. Soc. Lond. A, 29, pp. 141-144
  • Ribbands, C.R., The scent perception of the honeybee (1955) Proc. R. Entomol. Soc. Lond. B, 143, pp. 367-379
  • Rösch, G.A., Untersuchungen über die arbeit-steilung im bienenstaat i teil: Die tätigkert im normalen bienenstaatte und ihre beziehung zum alter der arbeitsbienen (1925) Z. Vergl. Physiol., 2, pp. 571-631
  • Scheiner, R., Responsiveness to sucrose and habituation of the proboscis extension response in honey bees (2004) J. Comp. Physiol. A, 190, pp. 727-733
  • Scheiner, R., Erber, J., Page Jr., R.E., Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.) (1999) J. Comp Physiol. A, 185, pp. 1-10
  • Skinner, B.F., (1938) The Behavior of Organisms, , New York: Appleton
  • Spear, N.E., Miller, J.S., Jagiello, J.A., Animal memory and learning (1990) A. Rev. Psychol., 41, pp. 169-211
  • Sutton, R., Barto, A.G., Time-derivate models of Pavlovian reinforcement (1990) Learning and Computational Neuroscience: Foundations of Adaptive Networks, pp. 497-537. , ed. M. Gabriel and J. Moore, Cambridge, MA: MIT Press
  • Takeda, K., Classical conditioned response in the honey bee (1961) J. Insect. Physiol., 6, pp. 168-179
  • Wilson, E.O., (1971) The Insect Societies, , Cambridge, MA: Belknap Press of Harvard University Press
  • Frisch, K., Über den Sitz des Geruchsinnes bei Insecten (1919) Zool. Jb. Phisiol, 38, pp. 1-68
  • Von Frisch, K., Über die Spprache der Bienen (1923) Zool. Jb. Phisiol., 40, pp. 1-186
  • Von Frisch, K., Die Tänze der Bienen (1946) Österr. Zoolog. Zeitschr., 1, pp. 1-48
  • Von Frisch, K., (1965) Tanzsprache und Orientierung der Bienen, , Berlin. Heidelberg, New York: Springer. (English version: The Dance Language and Orientation of Bees, 1967. Harvard University Press, Cambridge, MA, USA The Belknap Press)
  • Zar, J.H., (1984) Biostatistical Analysts. Third Edition, , NJ: Prentice-Hall International

Citas:

---------- APA ----------
Gil, M. & De Marco, R.J. (2005) . Olfactory learning by means of trophallaxis in Apis mellifera. Journal of Experimental Biology, 208(4), 671-680.
http://dx.doi.org/10.1242/jeb.01474
---------- CHICAGO ----------
Gil, M., De Marco, R.J. "Olfactory learning by means of trophallaxis in Apis mellifera" . Journal of Experimental Biology 208, no. 4 (2005) : 671-680.
http://dx.doi.org/10.1242/jeb.01474
---------- MLA ----------
Gil, M., De Marco, R.J. "Olfactory learning by means of trophallaxis in Apis mellifera" . Journal of Experimental Biology, vol. 208, no. 4, 2005, pp. 671-680.
http://dx.doi.org/10.1242/jeb.01474
---------- VANCOUVER ----------
Gil, M., De Marco, R.J. Olfactory learning by means of trophallaxis in Apis mellifera. J. Exp. Biol. 2005;208(4):671-680.
http://dx.doi.org/10.1242/jeb.01474