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First published online February 4, 2005
Journal of Experimental Biology 208, 671-680 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01474

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Olfactory learning by means of trophallaxis in Apis mellifera

Mariana Gil¹ and Rodrigo J. De Marco^2,*

¹ Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón II, C1428EHA, Buenos Aires, Argentina
² Freie Universität Berlin, Fachbereich Biologie, Chemie, Pharmazie, Institut für Biologie-Neurobiologie, Berlin D-14195, Germany

^* Author for correspondence (e-mail: rjdm02{at}yahoo.com.ar)

Accepted 27 October 2004

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.

Key words: honeybee, Apis mellifera, trophallaxis, olfactory conditioning, associative learning

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