The defensive behaviour of honey bees (Apis mellifera): individuality, social regulation, and neural mechanisms

Among all the different behaviours that animals exhibit, defensive behaviour lies at the intersection of survival of an individual, its kin, territory and resources. In both loosely aggregated and highly social animals, threats are initially detected by guarding individuals, and an alarm signal is then communicated via visual, chemical or vibrational means to warn conspecifics. Depending on the nature of the group and the territory they protect, defensive behaviour typically triggers either a `flight' or `fight' response. Animals that choose the `flight' response either escape or hide themselves for a short period due to their inability to attack physically. In contrast, those that choose the `fight' response defend against their predators by physically assaulting them until the threat is deterred. Although defensive behaviour appears straightforward, it is not – as conspecifics can lose a limb or even die while defending their group and territory.

The defensive behaviour in honey bees Apis mellifera operates similarly – individual bees sting their predators in an attempt to defend their colony; however, they die after stinging, creating a unique evolutionary paradox. To balance out colony defence against loss of colony workforce, we must look beyond the ‘collective spirit’ of the hive to understand regulation at the individual level. Bees process sensory information in their individual brains, integrating cues from both the threat and surrounding environment. This information is weighed against each bee's unique internal threshold, which incorporates both intrinsic predispositions and external factors, determining the individual's decision to either sting or not sting. This, in turn, results in an efficient colony defence. My PhD research focuses on this aspect, on how bees regulate their individual and social factors, in the broad context of collective defensive behaviour. I cover different aspects of this theme, namely olfaction, individuality, social factors, and neural mechanisms, as elucidated below.

In Chapter 2, I explore via a literature review how insects, both solitary and social, defend against intruders by using their sense of olfaction. I detail how insects detect threats, deploy chemical `weapons', and, in social insects, communicate danger through chemical signals called alarm pheromones. Further, I discuss the chemical properties of these alarm pheromones, their immediate behavioural as well as long-term physiological effects, along with their neural processing in the insect brain.

In Chapter 3, I ask whether individuals exhibit consistency in their stinging likelihood, which may suggest a predetermined bias to the threat, regardless of the defensiveness of the colony. I demonstrate that individual bees do vary in their stinging behaviours, and this variation persists in the presence of social factors. I further support these findings with explanations of an ‘internal state’. Moreover, I demonstrate that the stinging responsiveness of bees decreases upon exposure to the alarm pheromone over repeated trials, in contrast to their response to repeated visual stimuli of the threat. These findings suggest differential neurobiological mechanisms at the individual level for different stimuli. Finally, I confirm that group composition does not affect individual bees in their defensive decisions.

In Chapter 4, I investigate the neurobiological basis of defensive behaviour. Here, I focus on the biogenic amine, serotonin, which modulates aggression in a diverse range of invertebrates, including bees. Using high spatial resolution techniques such as immunostaining, I map serotonergic activity in the bee brain following alarm pheromone exposure and stinging behaviour. With pharmacological manipulations, I identify a putative serotonergic receptor mediating stinging responses, providing preliminary evidence for a neural circuit underlying defensive behaviour.

Overall, my thesis advances our understanding of defensive behaviour, which is one among the large behavioural repertoires of honey bees. My focus on behavioural and neurobiological perspectives in this topic have potential implications for understanding the evolution of social defense mechanisms in insects as well as other animals. Furthermore, it may also inform beekeeping practices on individual and colony defensiveness.