Olfactory eavesdropping of predator alarm pheromone by sympatric but not allopatric prey

Abstract

Eavesdropping is predicted to evolve between sympatric, but not allopatric, predator and prey. The evolutionary arms race between Asian honey bees and their hornet predators has led to a remarkable defence, heat balling, which suffocates hornets with heat and carbon dioxide. We show that the sympatric Asian species, Apis cerana (Ac), formed heat balls in response to Ac and hornet (Vespa velutina) alarm pheromones, demonstrating eavesdropping. The allopatric species, Apis mellifera (Am), only weakly responded to a live hornet and Am alarm pheromone, but not to hornet alarm pheromone. We observed typical hornet alarm pheromone-releasing behaviour, hornet sting extension, when guard bees initially attacked. Once heat balls were formed, guards released honey bee sting alarm pheromones: isopentyl acetate, octyl acetate, (E)-2-decen-1-yl acetate and benzyl acetate. Only Ac heat balled in response to realistic bee alarm pheromone component levels (<1 bee-equivalent, 1 mg) of isopentyl acetate. Detailed eavesdropping experiments showed that Ac, but not Am, formed heat balls in response to a synthetic blend of hornet alarm pheromone. Only Ac antennae showed strong, consistent responses to hornet alarm pheromone compounds and venom volatiles. These data provide the first evidence that the sympatric Ac, but not the allopatric Am, can eavesdrop upon hornet alarm pheromone and uses this information, in addition to bee alarm pheromone, to heat ball hornets. Evolution has likely given Ac this eavesdropping ability, an adaptation that the allopatric Am does not possess.

Honey Bee Alarm Pheromone Mediates Communication in Plant–Pollinator–Predator Interactions

“…The Asian honey bee shows high electrophysiological responses to hornet alarm pheromone. Their guards are also easily recruited to attack [49]. So far, we still do not know how these hornet predators use honey bee alarm pheromone to trigger attacking or repelling in front of the bee hive.…”

Visual contagion in prey defence signals can enhance honest defence

“…This attraction was not due to the production of alarm pheromone (which we did not detect in SPME assays) or other odours because video playbacks of bees producing the ISY signal were sufficient to attract guards. Guards may produce attractive odours that we did not detect, but we previously used the same SPME technique and found that guards that extended their stingers produced clearly detectable alarm pheromone compounds (Dong et al., 2018). Moreover, the presence of a predator was not necessary since guards were attracted to the video playbacks of an ISY signaller but not its still image.…”

“…We waited until one only guard bee was on the designated test side of the nest (randomly chosen as right or left) and held this hornet at the corner and 10 cm in front of the chosen nest side. At this distance, Ac workers do not heat‐ball hornets (Dong et al., 2018), but will perform the ISY signal after detecting the hornet. Within a few seconds, the guard bee usually began to ISY signal, and the 5 min trial began.…”

Losing the Arms Race: Greater Wax Moths Sense but Ignore Bee Alarm Pheromones

“…Queen pheromones are used to maintain the social order of the colony [30]. Bee alarm pheromones play differential roles in different contexts, such as risk alerts to prevent hive mates from foraging at flowers with dangers [20], or to recruit bees to the entrance [31]. However, in the hive, the alarm pheromones are also used to defend against parasitoids [17].…”