Our cage paradigm gives rise to a self-specialized dynamic of food distribution similar to what is observed in honey bee colonies. Natural foragers returning to the nest unload their crop to a single non-foraging receiving bee, only sharing with additional receivers if the crop load is more than can be imbibed by just one29. The receiving bee trophallaxes the nectar to other hive mates or deposits it in honey comb30. Correspondingly, caged individuals that were observed to forage at least once were seldom observed to share food with others, while bees that also had access to feeders but were never observed to forage were far more likely to engage in trophallaxis (Fig. 2a,b). For simplicity, we will henceforth refer to the first group as “foragers” and to the latter as “non-foragers.” Within the group of non-foragers, there was an inverse correlation between trophallaxis with bees restricted from feeders and trophallaxis with bees that had feeder access (Fig. 2c,f), suggesting a further subdivision of food sharing roles. These patterns indicate a cascade of trophallaxis in which foragers unload food to non-foragers specializing in receiving and distributing it to downstream non-foragers which in turn transfer food to the bees behind mesh.

In a natural hive, roles associated with food collection and distribution are marked by behavioural and physiological differences. Octopamine receptor AmOctαR1 is differentially expressed in the antennal lobes and subesophageal ganglion of same-aged foragers and non-foragers9. Sucrose responsiveness tends to increase with age; earlier work shows a difference between same-aged nurses and foragers10, but this was not measurable in a later study28. Although sucrose responsiveness has been often studied in relation to foraging behaviour, it has not previously been examined in the context of food sharing behaviours. To better understand the self-specialization that emerged inside cages, we quantified sucrose responsiveness as well as expression levels of AmOctαR1. Our results do not show differences in AmOctαR1 expression between foragers and non-foragers, suggesting that this is not necessary for the determination of foraging role in an artificial caged laboratory setting (Fig. 4). Similarly to the most recent findings in outdoor colonies28, we find no difference in sucrose responsiveness between foragers and non-foragers (Fig. 3a,b). However, in benign foraging conditions when food is unscented, we find that sucrose responsiveness is inversely related to trophallaxis with bees that have feeder access and positively correlated to trophallaxis with bees restricted from feeders (Fig. 3c,d). Aversive conditions and scent negate the correlations between trophallaxis and sucrose responsiveness. In the unscented benign condition, these opposite relationships with sucrose responsiveness could be driving the specialization for distributing food within the bottom compartment vs transferring food to bees restricted from feeders (Fig. 2c,f). Our observations did not reliably identify directionality of food transfer, so it is unclear whether the relationships with sucrose responsiveness are specific to donating food or to receiving it. Future studies will be necessary to resolve the causality of the relationship between food sharing and sucrose responsiveness.

Surprisingly, we find that foraging conditions and presence of scent change only the food sharing behaviour of non-foragers that were never observed directly experiencing the aversive conditions (Fig. 5). When food is scented, non-foragers in cages with aversive foraging conditions were more likely to trophallax with bees restricted from feeder access, without any difference in trophallaxis with bees that had feeder access. When food is unscented, aversive foraging conditions have the opposite effect, decreasing trophallaxis with bees restricted from feeder access. It is important to note that no other trophallaxis or foraging behaviours are altered, suggesting a specific effect on a particular type of social interaction rather than a global effect of stress (Fig. 5a,c–e). The dependence of the effect of aversive conditions on scent is ecologically relevant, as nectar in the wild is sometimes but not always scented25,26,31. The corresponding behaviour in a natural colony would be an increase or decrease in trophallaxis between receiver bees and younger nurse bees.

An inhibition of trophallaxis with younger nurse bees under threatening conditions aligns with the phenomenon in which some species of birds decrease their parental provisioning to redirect energy towards self-maintenance in stressful conditions32,33. On the evolutionary scale, unpredictable and poor environments lead to parents paying less attention to chicks’ begging and instead using cues such as body size to determine provisioning34. Aversive foraging conditions could have similar consequences for a honey bee colony; whether non-foragers experience stress through an unobserved direct encounter with aversive feeders or the stress is communicated via social interaction with foragers, this results in less social feeding of the bees lacking feeder access. Future studies could use observation hives to test our prediction that receivers trophallax unscented nectar less to young bees in aversive foraging conditions. More broadly, our results give rise to the question of whether food is shared less with the youngest members of a social group in times of environmental stress across vertebrate and invertebrate species besides birds and honey bees.

The presence of scent in food provides an adaptive opportunity to pass on information regarding danger. If trophallaxis between non-foragers and downstream bees can transmit a negative association with the nectar’s scent, future risk will be mitigated once the downstream bees initiate their own foraging decisions. Researchers have long known that trophallaxis likely serves communication purposes beyond the sharing of food; when trophallactic interactions in small groups of bees were studied, less than 5% of the interactions actually resulted in food transfer12. Social mammals such as rats35, mice36, Mongolian gerbils36,37, and spiny mice38 confer long-lasting food preference in conspecifics using semiochemicals found on the breath and in urine and faeces. Negative feedback that transmits food source aversion is less common. Lasius niger ants deposit less trail pheromone when a trail is crowded, thus creating a reduction in positive signal that serves as a mechanism of negative feedback39. Food receivers in colonies of the stingless bee Melipona seminigra food are vibrated on their thorax by foragers during unloading40, and in Melipona quadrifasciata scented food elicits stronger vibrations than unscented food during unloading41; the effect on receivers has not yet been discovered. Honey bee foragers that have had an aversive experience at a food source identity other foragers dancing to advertise a similarly scented location, and stop the dance with a vibrational “stop signal” to reduce recruitment18. In a laboratory setting, honey bees produce a hissing sound when presented with an odour they have learned to associate with electric shock42. It is not yet clear whether this hiss is similarly produced in the natural context of a hive and whether it acts as a social signal. Both the vibrational stop signal and the hiss are activated by aversively associated scents, providing a potential mechanism for how aversive conditions impact downstream bees’ behaviour when food is scented. One possibility is that foragers and/or non-foragers sense aversively associated scents while unloading scented sucrose from their own crops, which triggers a hiss, vibration, or some other informative social behaviour. We occasionally observed bees running at higher than usual speeds inside cages and vibrating against other bees, but it was not possible to identify the bees’ tag numbers during such rapid movement and video recording equipment was not used. It was also not possible to hear individual hisses through the plastic window covering cages due to interference from the air pump and the background noise of bees’ buzzing. Although further work is needed to reveal the mechanisms at play, our results suggest that aversively associated scented nectars not long increase non-foragers’ trophallaxis with downstream bees but also facilitate the transfer of information regarding nectar sources.

In order for an increase in trophallaxis of food collected in aversive conditions to be adaptive, downstream bees must exhibit subsequent aversion to the associated scent. This is particularly essential because foragers generally prefer food sources that smell like what they have been fed through trophallaxis earlier in their lives. Bees as young as a few days post- emergence are primed by the scented nectars foragers bring into the nest, forming positive associative memories that can be retrieved once they reach foraging age43. Adult bees prefer flowers smelling of nectars they have consumed in the nest16. Similarly, Camponotus mus ants that have received scented solution in a single trophallaxis event prefer this scent when tested in a Y-maze44. Thus, one might expect the maladaptive consequence of increased trophallaxis causing preference for riskier food sources unless the aversive association continues to be transferred through trophallaxis. After removing bees from cages, we tested all subjects’ proboscis extension responses to the scents that had been dissolved in food at aversive and benign feeders. We predicted that both bees with and without feeder access would exhibit proboscis extension to scents from benign feeders and not to scents from aversive feeders. However, aversive conditions had no effect on proboscis extension for bees in either compartment (Fig. 6). Although bees with feeder access did exhibit statistically significant preferential PER to the scent experienced in cages, regardless of aversive conditions, <30% of these bees displayed PER, suggesting that due to the accumulated stress of five days in cages followed by one day of restraint in harnesses, bees may not have been able to display PER even in the case of preference. For bees without feeder access, no significant preference was detected even in benign conditions, so the impact of aversive conditions was not clear. We hope that future studies using free-flying, less stressed subjects can test the idea that aversive conditions cause receiver bees to not only increase their rate of trophallaxis with nest bees, but also to pass on the aversive association, thus preparing as many bees as possible for dangerous food sources.

This study suggests that aversive conditions experienced during foraging can change downstream social food sharing, influencing pre-foraging individuals that have not yet experienced external conditions first-hand. We hope to spur future work exploring the impact of natural aversive foraging conditions, such as predation and con-specific competition, on social information transfer and subsequent foraging decisions.