Honey Bee Inhibitory Signaling Is Tuned to Threat Severity and Can Act as a Colony Alarm Signal

摘要

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 Apis 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 the bee alarm pheromone and live hornet presence to heat-ball the hornet. In A . cerana , sophisticated recruitment communication that encodes food location, the waggle dance, is therefore matched with an inhibitory/alarm signal that encodes information about the context of danger and its threat level. Honey bees possess a vibrational alarm signal that encodes information about the level of danger at food and at the nest entrance. Author Summary Asian honey bees are attacked by formidable predators, giant hornets, at food sources and at their nests. We show that one species of honey bee, Apis cerana , has evolved an alarm signal, the stop signal, which warns nestmates of this danger. The stop signal consists of a brief vibrational pulse that encodes information about the danger level in signal frequency and the danger context in signal duration. Each danger level and danger context results in a distinctive signal. Receivers of these signals respond appropriately, stopping recruitment for the dangerous food location or remaining inside the safety of the nest, according to the encoded danger level and context. This is the first known example of such a complex alarm signal in an insect and demonstrates a new level of sophistication in bee communication.