Abstract

Eusocial insects divide their labour so that individuals working inside the nest are affected by external conditions through a cascade of social interactions. Honey bees (Apis mellifera) transfer food and information via mouth-to-mouth social feeding, ie trophallaxis, a process known to be modulated by the rate of food flow at feeders and familiarity of food’s scent. Little is understood about how aversive foraging conditions such as predation and con-specific competition affect trophallaxis. We hypothesized that aversive conditions have an impact on food transfer inside the colony. Here we explore the effect of foragers’ aversive experience on downstream trophallaxis in a cage paradigm. Each cage contained one group of bees that was separated from feeders by mesh and allowed to feed only through trophallaxis, and another group that had access to feeders and self-specialized to either forage or distribute food. Our results show that aversive foraging conditions increase non-foragers’ trophallaxis with bees restricted from feeder access when food is scented, and have the opposite effect when food is unscented. We discuss potential behavioural mechanisms and implications for the impact of aversive conditions such as malaise inducing toxins, predation, and con-specific competition.

Highlights

  • Honey bees, Apis mellifera, perform a wide array of behaviours inside and outside the nest

  • Considering that foragers can communicate aspects of their foraging experience and that non-foraging receivers unload nectar to downstream bees at a rate positively correlated with the rate at which it was originally received, we were intrigued by the possibility that aversive foraging experiences could be transmitted to bees downstream the network of food sharing

  • Non-foragers further specialized to produce a strong inverse correlation between trophallaxis with bees in their own compartment and trophallaxis with bees restricted from feeders, in each of the four foraging conditions (Spearman Rank Correlations: benign, non-scented (n = 26) − rs = −0.723, p = 2.98e-005; benign, scented (n = 17) − rs = −0.779, p = 0.003; aversive, scented (n = 18) − rs = −0.693, p = 0.001; aversive, non-scented (n = 18) − rs = −0.541, p = 0.02) (Fig. 2c–f)

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Summary

Introduction

Apis mellifera, perform a wide array of behaviours inside and outside the nest. Trophallaxis, the mouth-to-mouth exchange of liquid, is a primary mechanism of food and appetitive information transfer inside a honey bee colony. The stop signal occurs when returning foragers identify dancing bees sharing samples of nectar that has an aversively associated scent, and vibrate against the dancer’s thorax to halt the dance[18,23]. As a first step toward understanding the relationship between foraging conditions and downstream social food transfer, we designed cages in which the top compartment held honey bees fed only through trophallaxis and the bottom compartment held bees with access to feeders offering different foraging conditions. Afterwards, long-term recall assays used the proboscis extension response to test bees’ preference for scents associated with different foraging conditions, to determine associations made either directly or through social means. Sucrose responsiveness and gene expression assays allowed us to explore inter-individual variation associated with the self-organized division of labour that emerged in cages

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