Age-based changes in kairomone response mediate task partitioning in stingless bee soldiers (Tetragonisca angustula)

Abstract: Collective defense is one of the most ubiquitous behaviors performed by social groups. Because of its importance, complex societies may engage a set of defensive specialists, with physical and/or neurological attributes tuned for defense against specific invaders. These strategies must be balanced, however, with the need to flexibly respond to different threat levels and sources. Insect societies rely heavily on olfaction for detecting and communicating in the context of defense. We therefore asked whether threat detection via olfaction is specialized towards invader-specific cues and how this may be integrated into defense task specialization. Colonies of the stingless bee, Tetragonisca angustula, deploy a morphologically distinct sub-caste of larger-bodied workers (soldiers) for colony defense. These soldiers transition between two different guarding tasks as they age, progressing from guarding in a hovering position near the nest entrance to guarding in a standing position on the nest entrance tube. Hovering and standing guards intercept different types of invaders: primarily heterospecific versus conspecific, respectively. We asked whether hovering and standing guarding behaviors were modulated by differential sensitivity to invader-associated olfactory stimuli; then we compared their responses to these cues to those of smaller workers that perform predominantly non-defense tasks. We exposed bees under both field and lab conditions to citral, a kairomone produced by an obligate heterospecific nest robber, primarily intercepted by hovering guards. Consistent with their roles, hovering guards were more likely to move towards citral than were either standing guards or small-bodied bees within a Y-maze. We also presented guards at field nests with dummies of conspecific versus heterospecific invader types, varying whether they included citral odors. Standing guards were more responsive to conspecific intruder scenarios than hovering guards, but heterospecific response differed by presence of citral. Standing and hovering guards responded in similar proportions when citral was absent, but the addition of citral produced a marginally non-significant reduction in standing guard participation. Our results potentially demonstrate differentiated cue-specific responses that correspond to morphological task specialization and age polyethism in these eusocial societies. Significance statement: Group defense is a ubiquitous function of any society, but threats are often diverse. Though defense versus non-defense task specialization has been well studied, when and how individuals sub-specialize on particular threats is less understood. We asked how age-differentiated soldier sub-types in a stingless bee differ in their innate responsiveness to olfactory cues associated with nest invader type. Consistent with behavioral roles, younger soldiers were more innately reactive to odors of an obligate heterospecific parasite, and older soldiers were more reactive to odors of conspecific intruders. This suggests that either transitions in learning or discrete cue sensitivity mediate defensive sub-specialization. This is the first study to compare behavioral responsiveness to olfactory stimuli across age-specialized soldier sub-types. Results suggest benefits of flexible allocation and prompt further studies exploring the topic of defensive sub-specialization.