Honey robbing causes coordinated changes in foraging and nest defence in the honey bee, Apis mellifera

Individuals and social groups balance foraging activities with other energetically demanding behaviours. In honey bee colonies, foraging and nest defence behaviours are performed by similar-aged bees, and so hives must adjust their workforce investment to fulfil both tasks. We investigate this balance in the context of honey robbing, a tactic in which foragers invade a victim hive, kill worker bees and steal honey stores. Robbing is highly beneficial because stored honey is a plentiful, concentrated food resource. However, robbing requires a large workforce to overwhelm the defences of the victim hive; it is unknown how robbing hives adjust other behaviours to accommodate this demand. We developed a method to provoke a hive to engage in simulated robbing and measured rapid changes in foraging activity and nest defence. Surprisingly, robbing hives increased both behaviours. Guards, the individuals responsible for nest defence, specifically increased defensiveness towards their own nestmates as they returned from a robbing trip. We found that increased foraging activity and changes in forager odour profiles from prolonged exposure to victim hive honeycomb were insufficient to explain robbing-induced changes in guard defensiveness. However, brain gene expression profiles of robbing foragers suggest these bees are unusually aggressive, and thus more likely to provoke aggression from nestmate guards. Increased forager aggression occurred even in the absence of direct competition with victim bees. Thus, although increased guard defensiveness may be costly in terms of increased nestmate mortality, because the ecological conditions that promote robbing simultaneously increase the likelihood a hive will become a robbing target, guards may use cues from returning nestmates to determine invasion risk and adjust their defensiveness accordingly. These results suggest that colonies use social information to dynamically optimize both foraging and defensiveness in order to maximize the benefits and minimize the costs of this high-risk tactic.