Behavioral development in the honey bee: toward the study of learning under natural conditions.

I n t r o d u c t i o n The adult worker honey bee is a sophisticated learner in a small package. To a certain extent, the same may be said of many insects. But the striking tendency of the social insects-the ants, bees, wasps, and te rmi testo organize social life on the basis of age polyethism (division of labor by worker age) results in a relatively prolonged period of adult behavioral development (Wilson 1971; H611dobler and Wilson 1990). In colonies of the European honey bee, Apis mellifera, young adult workers rear the next generation and store food; middle-aged workers maintain the physical structure of the hive; and the oldest workers forage (Winston 1987; Robinson 1992; Moritz and Southwick 1993). T h e s e different tasks require different skills and provide different opportunit ies for skill improvement (learning). How best can one study the neural correlates of learning in the honey bee? The honey bee can be (and has been, with fruitful results) tested in well-defined learning paradigms in the laboratory and then probed by electrophysiological, anatomical, biochemical, and molecular means (for review, see Menzel 1990; see also Hammer and Menzel 1995). This approach takes advantage of the many economies and conveniences of using arthropod nervous systems for the experimental study of neural function but denies the bee's rich social life. The honey bee can also be studied within its own social and ecological context. With this approach, one focuses on the cellular mechanisms supporting the naturally occurring changes in behavior that accompany behavioral maturation and the accumulation of experience in a free-living animal. A long tradition of honey bee ethology, in particular, studies of foraging behavior (Lindauer 1961; von Frisch 1967; Seeley 1985), has provided insights into the relationship of the sensory and learning capacities of bees as they relate to floral stimuli (for review, see Menzel 1985). To date, however, even the most "natural" studies of neural mechanisms in honey bees have by and large lacked a developmental context. Behavioral development is widespread in the animal kingdom. As individuals age, their responses to the environment change predictably. Often, an individual's behavioral responses increase in complexity and involve learning and memory. A child refines its ability to reach for objects in its visual field (Thelen and Corbetta 1994): a worker bee shifts from hive activities to foraging and becomes efficient at searching for