Colony-level non-associative plasticity of alarm responses in the stingless honey bee, Tetragonisca angustula
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.
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.
KeywordsStingless honey bee Tetragonisca angustula Colony-level plasticity Colony defense Alarm pheromone
We would like to thank Sonia Villa and Erik Rohner for their support helping to analyze video recordings. We would also like to thank Richard C. Gerkin for input on the analyses, and the anonymous reviewers for their comments on the manuscript.
C. M. Jernigan was supported by joint grants from Arizona State University and the Smithsonian Tropical Research Institute during data collection, and teaching assistantships from Arizona State University, School of Life Sciences. J. Birgiolas was supported by an Arizona State University Interdisciplinary Graduate Program in Neuroscience fellowship and NIH grants F31DC016811 to JB and R01MH1006674 to Sharon M. Crook. This work was also supported by an award from NIH-NIGMS (GM113967) to BHS.
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