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

PLoS Biol. 2016 Mar 25;14(3):e1002423. doi: 10.1371/journal.pbio.1002423. eCollection 2016 Mar.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animal Communication*
  • Animals
  • Bees*
  • Pheromones
  • Predatory Behavior
  • Vibration
  • Wasps

Substances

  • Pheromones

Grants and funding

This work was supported by the Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, and the CAS 135 program (XTBGT01) of Chinese Academy of Science, China National Research Fund (31260585) to KT and a CAS Visiting Fellowship to JCN. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.