Colony-level non-associative plasticity of alarm responses in the stingless honey bee, Tetragonisca angustula

Abstract: In ants, bees, and other social Hymenoptera, alarm pheromones are widely employed to coordinate colony nest defense. In that context, alarm pheromones elicit innate species-specific defensive behaviors. Therefore, in terms of classical conditioning, an alarm pheromone could act as an unconditioned stimulus (US). Here, we test this hypothesis by establishing whether repeated exposure to alarm pheromone in different testing contexts modifies the alarm response. We evaluate colony-level alarm responses in the stingless bee, Tetragonisca angustula, which has a morphologically distinct guard caste. First, we describe the overall topology of defense behaviors in the presence of an alarm pheromone. Second, we show that repeated, regular exposure to synthetic alarm pheromone reduces different components of the alarm response, and memory of that exposure decays over time. This observed decrease followed by recovery occurs over different time frames and is consistent with behavioral habituation. We further tested whether the alarm pheromone can act as a US to classically condition guards to modify their defense behaviors in the presence of a novel (conditioned) stimulus (CS). We found no consistent changes in the response to the CS. Our study demonstrates the possibility that colony-level alarm responses can be adaptively modified by experience in response to changing environmental threats. Further studies are now needed to reveal the extent of these habituation-like responses in regard to other pheromones, the potential mechanisms that underlie this phenomenon, and the range of adaptive contexts in which they function at the colony level. Significance statement: Pheromones are classically thought to elicit stereotyped action patterns. Here, we test the idea that responses to pheromones are plastic and show characteristics of an unconditioned stimulus. This study demonstrates clear non-associative plasticity in the colony-level response to alarm pheromone, in the stingless honey bee, Tetragonisca angustula. Colonies of T. angustula show habituation-like responses across multiple measures to repeated stimulation of their alarm pheromone. We therefore demonstrate that colony-level responses to pheromones are adaptively plastic. Finally, we failed to demonstrate colony-level conditioning using alarm pheromone as the unconditioned stimulus; however, these findings and others warrant further investigation.