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. 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.

中文翻译：

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kairomone 反应中基于年龄的变化介导了无刺蜜蜂士兵（Tetragonisca angustula）的任务分配

集体防御是社会群体最普遍的行为之一。由于其重要性，复杂的社会可能会聘请一组防御专家，其身体和/或神经学属性经过调整以防御特定入侵者。然而，这些策略必须平衡，需要灵活应对不同的威胁级别和来源。昆虫社会在防御环境中严重依赖嗅觉进行检测和交流。因此，我们询问通过嗅觉进行的威胁检测是否专门针对入侵者特定的线索，以及如何将其整合到防御任务专业化中。无刺蜂 Tetragonisca angustula 的群体部署了一个形态不同的体型较大的工人（士兵）亚种姓，以进行群体防御。这些士兵随着年龄的增长在两种不同的守卫任务之间转换，从在巢穴入口附近的盘旋位置守卫到在巢穴入口管上的站立位置守卫。悬停和常备警卫拦截不同类型的入侵者：分别主要是异种和同种。我们询问悬停和站立守卫行为是否受到对入侵者相关嗅觉刺激的不同敏感性的调节；然后我们将他们对这些线索的反应与主要执行非防御任务的小型工人的反应进行了比较。我们在野外和实验室条件下将蜜蜂暴露在柠檬醛中，柠檬醛是一种由专性异种巢穴强盗产生的凯罗酮，主要由盘旋的守卫拦截。符合他们的角色，在 Y 型迷宫中，与站立的守卫或体型较小的蜜蜂相比，盘旋的守卫更有可能向柠檬醛移动。我们还向野外巢穴的守卫展示了同种与异种入侵者类型的假人，不同的是它们是否包括柠檬醛气味。站立的警卫比徘徊的警卫对同种入侵者场景更敏感，但异种反应因柠檬醛的存在而异。当柠檬醛不存在时，站立和盘旋警卫的反应比例相似，但添加柠檬醛导致站立警卫参与率略有下降。我们的结果可能证明了与这些真社会社会中的形态任务专业化和年龄多伦理性相对应的差异化线索特异性反应。群体防御是任何社会都普遍存在的功能，但威胁往往是多种多样的。尽管防御与非防御任务的专业化已经得到了很好的研究，但人们对特定威胁何时以及如何进行细分的了解较少。我们询问了无刺蜜蜂中年龄分化的士兵亚型在对与巢穴入侵者类型相关的嗅觉线索的先天反应方面有何不同。与行为角色一致，年轻士兵对专性异种寄生虫的气味更敏感，而年长的士兵对同种入侵者的气味更敏感。这表明学习的转变或离散的线索敏感性介导了防御性亚专业化。这是第一项比较不同年龄特定士兵亚型对嗅觉刺激的行为反应的研究。