Associative learning in honey bees R Menzel To cite this version: R Menzel. Associative learning in honey bees. Apidologie, Springer Verlag, 1993, 24 (3), pp.157-168. hal-00891068 HAL Id: hal-00891068 https://hal.archives-ouvertes.fr/hal-00891068 Submitted on 1 Jan 1993 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Review article Associative learning in honey bees R Menzel Freie Universität Berlin, Fachbereich Biologie, Institut für Neurobiologie, Königin-Luise-Straße 28-30, 1000 Berlin 33, Germany (Received 20 October 1992; accepted 9 February 1993) Summary — The learning behavior of honey bees has been reviewed. In the context of foraging be havior, bees perform 2 forms of learning, latent (or observatory) and associative learning. Latent learning plays an important role in spatial orientation and learning during dance communication, but the mechanisms of this kind of learning are little understood. In associative learning, stimuli experi- enced immediately before the reward (usually sucrose solution) are memorized for the guidance of future behavior. Well-established paradigms have been used to characterize operant and classical conditioning. The classical conditioning of olfactory stimuli is a very effective form of learning in bees and has helped to describe the behavioral and physiological basis of memory formation. It is con- cluded that memory needs time to be established and is processed in sequential phases. The neuro- nal compartments of the brain involved in the chemosensory pathway appear to participate different- ly in the sequential memory phases. A model is developed which assigns the strong non-associative components in olfactory conditioning to the antennal lobes, and the associative components to the mushroom bodies and the lateral output region of the protocerebrum. It is speculated that the amne- sia-sensitive memory resides in the mushroom bodies and the amnesia-resistant memory in certain structures (eg the lateral protocerebrum) perhaps together with the mushroom bodies. learning / olfactory conditioning / memory / protocerebrum / mushroom bodies / Apis melli- fera INTRODUCTION Bees foraging for food (nectar and pol- len for the colony storehouse), water and The social life of the honey bee (Apis mel- resin (for colony care purposes) com- lifera L) colony forms the evolutionary mence their foraging trips at the colony framework for the behavior of the individu- and return to it within minutes or hours. As al insect and is crucial for the survival of young bees, they learn the landmarks sur- each bee, as it cannot exist independent- rounding the nest location on self-training ly. The lifespan of the individual bee is rel- flights. They also learn to orientate them- atively short (4-6 wk in summer, several selves to the sun compass in relation to months in autumn, winter and spring), but the landmarks surrounding the nest. When the colony itself is potentially everlasting. the colony reproduces, a large number of the well-experienced bees leave the colo- The study of learning in bees has fo- ny, together with the old queen, in search cused on appetitive learning in the context of a new nesting place. During this pro- of food collection, because experimenta- cess, each bee has to replace the old tion is most convenient under these condi- memory of its terrestrial and celestial or- tions: stimuli are easily selected and stimu- ientation cues with a new memory (Lin- lus-response conditions can be accurately dauer, 1955, 1959, 1967; von Frisch, controlled. Since an average colony con- 1967). Food is collected from flowers tains > 40 000 foraging bees, a virtually un- when and wherever available and is stored limited number of test animals are availa- for periods of starvation. Consequently, ble and can be motivated to search for the innate search image for food sources food by means of the recruitment behavior has to be very general, and individual as- of experienced bees. Motivation for both sociative learning processes are most im- recruitment and seach behavior can be portant for the effective accomplishment of manipulated by the concentration of the foraging activities. Celestial and terrestial sucrose reward. Because bees learn very cues, position in relation to landmarks and fast (often by a single trial), experimenta- features (color, shape, odor, etc) of the tion is facilitated. The experimental insect new feeding place are learned afresh for returns to the artificial feeding station relia- each new location. An individual bee may bly and shuttles back and forth between collect food from only one location and the colony and the feeding station at inter- one kind of flower during its lifetime, but in vals of minutes. Choice behavior can be most cases, each bee will visit many differ- easily tested because extinction proce- ent place and learn many different flower dures have little effect and search motiva- cues throughout its lifespan. tion is high. The training procedure of indi- marked bees is also used Within the colony, the foragers commu- vidually nicate using ritualized body movements effectively to study other forms of learning (waggle dance), which encode the dis- (eg latent learning during orientation to ce- tance, direction and relative profitability of lestial and terrestrial cues) and cooperative behavior in the communica- the food source. The odor of the food colony (dance allocation of social source can be smelled by the attending tion, duties) (von bees from the hairy body of the dancing Frisch, 1967; Lindauer, 1967; Menzel, bee and, in the case of nectar collection, 1985; Seeley, 1985b; Gould, 1986b). the collected food may be sampled, as the Genetic predispositions to learning may dancer offers minute amounts for tasting. be of particular importance in insects. It is The relative profitability of the food source often assumed, though with limited experi- is estimated by the foraging bee on the ba- mental verification, that the small brain of sis of how quickly its sample is taken up an insect (in the bee: 1 mm3, 900 000 neu- by the young receiving bees at the colony rons) might be more effective if it had a entrance. Since the young receiving bees particularly large proportion of stereotyped register the needs of the colony (brood behaviors, genetically controlled connec- condition, storage space, size and density tions and a preprogrammed switchboard of of the colony) and the quality of the incom- potential neural contacts. In other words, ing food, the feedback to the individual for- sensory cues may be preordained, motor ager provides the necessary information for programs adjusted only within strict limits, quick adjustments to the colony’s needs reinforcing conditions preprogrammed so and a relative rating of its foraging behavior that associations can be formed quickly (von Frisch, 1967; Seeley, 1985a, b). but selectively, and internal memory pro- cesses may run under the tight control of However, it is not known whether this be- automatic storage routines (Gould and havior indicates a backward conditioning, Marler, 1984; Menzel, 1984). In view of because the unconditioned stimulus has this, it is astounding how adaptable the be- not yet been identified for this kind of learn- havior of bees actually is, how important ing. how learning phenomena are, persistent During departure from a newly-discover- the memories and how are, many signals ed natural food source, the bees perform and motor are learned. The programs ge- circular flights at an increasing distance netic frame for learning has, therefore, to from the feeding place. Most learning dur- in be quite broad order to allow the estab- ing this phase is directed towards more lishment of new neural connections under distant signals such as landmarks, celes- the conditions of learning rules (Menzel, tial cues and the direction of and distance Menzel 1990; et al, 1993). between the food source and the colony. It is not known what kind of learning guides the bee during the circular observatory APPETITIVE LEARNING flights. Associative learning is unlikely, be- IN THE NATURAL CONTEXT cause bees transported to an unknown place perform the same circling flights and When a searching bee discovers a source learn to fly back to the hive along the short- of sweet solution, eg an artificial feeder est possible route without being fed at the with sucrose solution, it quickly learns to release site (Menzel, 1989). What bees re- associate the surrounding visual and olfac- port through their dance behavior within tory signals with the reward. Acquisition the colony also relates to their experience functions indicate that olfactory stimuli (eg during the return flight to the colony. It ap- floral odorants) are learned within 1-2 pears from these results that both forward learning trials, colors within 1-5 learning and observatory learning are effective in trials, and black and white patterns from learning of freely-flying bees. the 5th learning trial onward. Most of this Long-distance orientation (usually up to learning is forward