Foraging experiences durably modulate honey bees’ sucrose responsiveness and antennal lobe biogenic amine levels

Authors: FINKELSTEIN, ABBY - Arizona State University; Brent, Colin; GIURFA, MARTIN - University Of Toulouse; AMDAM, GRO - Arizona State University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/13/2019
Publication Date: 4/1/2019
Citation: Finkelstein, A.B., Brent, C.S., Giurfa, M., Amdam, G.V. 2019. Foraging experiences durably modulate honey bees’ sucrose responsiveness and antennal lobe biogenic amine levels. Scientific Reports. 9:5393.

Interpretive Summary: Foraging exposes organisms to both rewards and hazards, providing an advantage for learning to maximize the former while minimizing the latter. Honey bees (Apis mellifera) can learn to associate environmental stimuli, like scents and visual cues, with their foraging experiences. Individual variation in sensitivity to foraging stimuli can also shape the foraging preferences. Because sensitivity to stimuli can be changed by manipulating neurotransmitter levels, we propose that foraging experiences act on neurotransmitter pathways to induce enduring changes that produce a learned preference. To simulate varied foraging conditions, freely-moving bees were housed in cages where feeders offered combinations of sugar solution, floral scents, and electric shock. Temporary effects were excluded by providing bees with free access to food for three days prior to all subsequent assays. Under benign conditions, bees exposed to a scent became less interested in the sugar solution compared to those given no scent. This effect was negated if the bees were also shocked when feeding, indicative of an adaptive tuning process which maximizes preference for high quality, non-hazardous food sources. Foraging conditions also influenced brain neurotransmitter levels, suggesting that an individuals’ foraging experiences durably modify neurochemistry and shape future foraging behaviour.

Technical Abstract: Foraging exposes organisms to rewarding and aversive encounters, 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 ad libitum food 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 when presented with aversive stimuli, 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 an individuals’ foraging experiences durably modify neurochemistry and shape future foraging behaviour.