The impact of honey bee (Apis mellifera) group size on hygienic behavior performance

Abstract

The size of animal groups has profound effects on individual and collective behavior, particularly in social insect colonies. Larger colonies are predicted to be more complex with more specialization among members. However, the empirical support of this theoretical expectation is limited. Hygienic behavior of honey bees is a complex cooperative behavior of workers detecting, uncapping, and removing unhealthy brood. It is an important defense against brood diseases, including the ectoparasitic mite Varroa destructor. We support the prediction that hygienic behavior increases with group size using a simulation model. To also test this prediction empirically, we performed five experiments, to compare the hygienic performance of small and large honey bee groups at four different scales, roughly representing four orders of magnitude. Hygienic performance qualitatively increased across the different scales, but different methodologies limit quantitative comparisons across experiments. Within experiments, group size was also positively related to hygienic behavior. The strongest effects of group size were measured in groups that were smaller than what honey bees adopt under natural conditions. The group-size effect on hygienic performance decreased with increasing scale and at the full colony scale, group size was unrelated to hygienic assay scores. Therefore, colony size is unlikely to confound the hygienic evaluation of colonies in apicultural practice although we demonstrate clear effects of group size on hygienic behavior. Direct observations of individual behavior that were performed in two small scale experiments did not support our prediction of increased individual specialization in larger groups. Thus, our study supports the notion of performance benefits of larger groups in the context of social immunity, although the mechanisms of how group size enhances hygienic behavior remain to be investigated further.

Significance Statement

Social insects owe their ecological success partly to their efficient division of labor and behavioral specialization of colony members. Empirical support for the theoretical argument that group performance increases with group size is insufficient. Hygienic behavior is an important defense against brood pests and diseases that threaten honey bee health. Yet, it has not been investigated with respect to group size. Here, we analyze a simulation model, demonstrating theoretically that group size is predicted to increase hygienic behavior. We then provide experimental support for this prediction across a range of group sizes, though results of some experiments are equivocal and sample sizes are limited, constraining our empirical conclusions. In small groups, we find support for the theoretical idea that hygienic performance increases with group size, but our study also indicates that this effect is not very important under apiculturally relevant group size conditions. We find no support for higher individual specialization in larger groups. Furthermore, our study indicates that beekeepers can disregard deviations in colony size when assessing their stock for hygienic behavior.