Abstract
In honeybees, associative learning is embedded in a social context as bees possess a highly complex social organization in which communication among individuals is mediated by dance behavior informing about food sources, and by a high variety of pheromones that maintain the social links between individuals of a hive. Proboscis extension response conditioning is a case of appetitive learning, in which harnessed bees learn to associate odor stimuli with sucrose reward in the laboratory. Despite its recurrent use as a tool for uncovering the behavioral, cellular, and molecular bases underlying associative learning, the question of whether social signals (pheromones) affect appetitive learning has not been addressed in this experimental framework. This situation contrasts with reports underlining that foraging activity of bees is modulated by alarm pheromones released in the presence of a potential danger. Here, we show that appetitive learning is impaired by the sting alarm pheromone (SAP) which, when released by guards, recruits foragers to defend the hive. This effect is mimicked by the main component of SAP, isopentyl acetate, is dose-dependent and lasts up to 24 h. Learning impairment is specific to alarm signal exposure and is independent of the odorant used for conditioning. Our results suggest that learning impairment may be a response to the biological significance of SAP as an alarm signal, which would detract bees from responding to any appetitive stimuli in a situation in which such responses would be of secondary importance.
Highlights
Social insects have evolved sophisticated communication systems, which include behavioral displays such as the honeybee dances (Frisch, 1967) and chemical signals that play a crucial role in the coordination of individual behaviors inside a colony
Among the pheromones released by worker bees, the sting alarm pheromone (SAP), a releaser pheromone contained in the sting chamber, prompts stinging and fast recruiting of nest-mates to defend the resources of the colony when released by guards facing a potential danger (Free, 1987)
Exposure to alarm pheromones impairs learning performance We studied the effect of exposure to SAP on olfactory proboscis extension response (PER) conditioning, by comparing the learning performances of bees from the SAP-exposed group to those of control bees
Summary
Social insects have evolved sophisticated communication systems, which include behavioral displays such as the honeybee dances (Frisch, 1967) and chemical signals that play a crucial role in the coordination of individual behaviors inside a colony. Ants, and wasps release a high variety of chemical compounds that act as pheromones, ensuring intraspecific chemical communication and adaptive responses to a variety of stimuli across different timescales (Wilson, 1971; Vander Meer et al, 1997; Wilson and Hölldobler, 2009). While primer pheromones induce long-lasting changes in physiology and behavior, releaser pheromones trigger rapid and short-term behavioral responses (Wilson and Hölldobler, 2009). Honeybee pheromones have been the subject of intensive studies (Free, 1987) which have focused on their multiple behavioral and physiological consequences. Several studies have shown that SAP acts as a modulator of the sensitivity to environmental stimuli, as assessed by the quantification of reflex responses. Exposure to some of its main components changes the responsiveness (as usually measured by the threshold value of a given stimulus eliciting a response) to appetitive or nociceptive stimuli: it decreases responsiveness to sucrose (Balderrama et al, 2002) and, depending on the nature and dose of the SAP compound, increases or decreases responsiveness to electric shocks (Núñez et al, 1998; Balderrama et al, 2002)
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