Honey bee inhibitory signaling is tuned to threat severity and can act as a colony alarm signal

Alarm communication is a key adaptation that helps social groups resist predation and rally defenses. In Asia, the world's largest hornet, Vespa mandarinia, and the smaller hornet, Vespa velutina, prey upon foragers and nests of the Asian honey bee, Apis cerana. We attacked foragers and colony nest entrances with these predators and provide the first evidence, in social insects, of an alarm signal that encodes graded danger and attack context. We show that like A. mellifera, A. cerana possesses a vibrational "stop signal", which can be triggered by predator attacks upon foragers, and inhibits waggle dancing. Large hornet attacks were more dangerous and resulted in higher bee mortality. Per attack at the colony-level, large hornets elicited more stop signals than small hornets. Unexpectedly, stop signals elicited by large hornets (SS large hornet) had a significantly higher vibrational fundamental frequency than those elicited by small hornets (SS small hornet) and were more effective at inhibiting waggle dancing. Stop signals resulting from attacks upon the nest entrance (SS nest) were produced by foragers and guards and were significantly longer in pulse duration than stop signals elicited by attacks upon foragers (SS forager). Unlike SS forager, SS nest were targeted at dancing and non-dancing foragers and had the common effect, tuned to hornet threat level, of inhibiting bee departures from the safe interior of the nest. Meanwhile, nest defenders were triggered by bee alarm pheromone and live hornet presence to heatball the hornet. In A. cerana, the waggle dance, sophisticated recruitment communication that encodes food location, is therefore matched with an inhibitory/alarm signal that encodes information about the context of danger and its threat level.

警报通讯是帮助社会群体抵御捕食、集结防御的关键适应性行为。在亚洲，世界体型最大的胡蜂——金环胡蜂（Vespa mandarinia）与体型较小的黄脚胡蜂（Vespa velutina）会捕食东方蜜蜂（Apis cerana）的采集蜂与蜂巢。我们针对这两种捕食者对采集蜂及蜂巢入口发起攻击实验，并首次在社会性昆虫中发现了能够编码不同危险等级与攻击场景的警报信号。研究表明，与西方蜜蜂（Apis mellifera）类似，东方蜜蜂拥有由捕食者攻击采集蜂所触发的振动“停止信号”，该信号可抑制摆尾舞行为。大胡蜂的攻击更具危险性，会导致更高的蜜蜂死亡率。在蜂群层面的单次攻击中，大胡蜂诱导产生的停止信号数量多于小胡蜂。出乎意料的是，大胡蜂诱导产生的停止信号（SS大胡蜂）相较小胡蜂诱导产生的停止信号（SS小胡蜂），其振动基频显著更高，且在抑制摆尾舞行为方面效果更强。由蜂巢入口攻击所诱导产生的停止信号（SS蜂巢）由采集蜂与守卫蜂产生，其脉冲时长显著长于由采集蜂攻击所诱导的停止信号（SS采集蜂）。与SS采集蜂不同，SS蜂巢信号会针对正在进行摆尾舞与未进行摆尾舞的采集蜂，且会根据胡蜂的威胁等级调整作用效果，共同抑制蜜蜂从安全的蜂巢内部向外出发。与此同时，蜂巢守卫蜂会被蜜蜂告警信息素与活体胡蜂的存在所激活，通过抱团热杀的方式应对胡蜂。在东方蜜蜂中，作为编码食物位置的复杂招募通讯行为的摆尾舞，与能够编码危险场景及其威胁等级的抑制性/警报信号形成了匹配机制。