Time-accuracy trade-off and task partitioning of hygienic behavior among honey bee (Apis mellifera) workers

Behavioral specialization and cooperation are fundamental in the organization and success of social groups. Honey bee workers display hygienic behavior, defined as the detection, uncapping, and removal of unhealthy brood. We present detailed analyses of behavioral specialization and task partitioning among hygienic worker bees, focusing on uncapping of brood cells and removal of the cells' content in freeze-killed brood assays. We demonstrate specialization of hygienic workers on either uncapping or removal and task partitioning among multiple individuals. Speed of hygiene decreases with the number of behavioral instances, suggesting a time cost for cooperation of multiple individuals. Additional analyses of an individual agent-based simulation of hygienic removal of Varroa-mite-infested brood demonstrate that erroneous removal of healthy brood can be reduced by task partitioning due to collective decision-making. Combined, our results indicate a speed-accuracy trade-off in the collective performance of hygienic behavior: Hygienic behavior may take longer when many individuals contribute and specialize on different tasks, but this organization of work also can prevent costly mistakes. This trade-off may explain the observed combination of elite workers and numerous other workers that contribute only little. Significance statement Honey bees and other social animals form successful groups that are characterized by individual specialization on different tasks. Hygienic behavior of honey bees removes unhealthy brood from the nest and is important for the health of honey bee colonies. Here, we observed that individual worker bees specialize on either of the two main tasks involved in hygienic behavior: uncapping cells or removing brood. We also found that a few individuals perform the majority of the work and that the speed of hygienic behavior is higher when one individual works continuously instead of multiple individuals. Additionally, we show in computer simulations that the number of erroneous brood removals is decreased when separate workers contribute to the different aspects of hygienic behavior. Thus, our study indicates that a speed-accuracy trade-off might drive the evolution of task partitioning in hygienic behavior.