Abstract
Foraging exposes organisms to rewarding and aversive events, providing a selective advantage for maximizing the former while minimizing the latter. Honey bees (Apis mellifera) associate environmental stimuli with appetitive or aversive experiences, forming preferences for scents, locations, and visual cues. Preference formation is influenced by inter-individual variation in sensitivity to rewarding and aversive stimuli, which can be modulated by pharmacological manipulation of biogenic amines. We propose that foraging experiences act on biogenic amine pathways to induce enduring changes to stimulus responsiveness. To simulate varied foraging conditions, freely-moving bees were housed in cages where feeders offered combinations of sucrose solution, floral scents, and aversive electric shock. Transient effects were excluded by providing bees with neutral conditions for three days prior to all subsequent assays. Sucrose responsiveness was reduced in bees that had foraged for scented rather than unscented sucrose under benign conditions. This was not the case under aversive foraging conditions, suggesting an adaptive tuning process which maximizes preference for high quality, non-aversive floral sites. Foraging conditions also influenced antennal lobe octopamine and serotonin, neuromodulators involved in stimulus responsiveness and foraging site evaluation. Our results suggest that individuals’ foraging experiences durably modify neurochemistry and shape future foraging behaviour.
Highlights
Aversive responsiveness has been studied in the honey bee using the Sting Extension Response (SER), a defensive response produced by individual bees when facing a noxious, aversive stimulus[25]
It has not been demonstrated that naturally occurring variation in individual responsiveness to sucrose or electric shock correlates with differences in biogenic amine pathways, but adult honey bees typically progress through a series of roles as they mature and age, and some behavioural changes correlate with, and can be induced by, alterations in biogenic amine signaling[34,35,36,37,38,39]
Bees that previously had access to feeders exhibited recall, as was evident from a higher PER in response to the scent paired with sucrose, which occurred at double the rate for scent that was not paired with food (Fig. 2A: Logistic Generalized Estimating Equations, β1 Wald χ2 = 7.14, p = 0.0075)
Summary
Aversive responsiveness has been studied in the honey bee using the Sting Extension Response (SER), a defensive response produced by individual bees when facing a noxious, aversive stimulus[25]. The role of 5-HT is less clear in honey bee associative learning as it does not seem to signal the presence of particular forms of reinforcement It modulates feeding[46] and the avoidance of odours associated with ingested toxins[43], olfactory PER conditioning and retention[30,47,48], aversive shock responsiveness[33], and defensive responses to alarm pheromones. The process of foraging provides individuals with a variety of potential experiences such as encounters with plant olfactory bouquets and nectars, aversive con-specific competition[53], predation from arthropods and birds[54,55], as well as noxious secondary compounds secreted by plants[56] We propose that such diverse foraging experiences induce sustained inter-individual differences in sucrose responsiveness through changes in biogenic amine pathways, and these physiological responses continue to shape individual behaviour after acute effects have subsided. We predicted that bees that had experienced different feeder conditions would exhibit divergent sucrose responsiveness, antennal lobe biogenic amine titers, and receptor expression in the subesophageal zone and antennal lobes, the same regions implicated in a worker’s transition from nurse to forager behaviours
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