Sharing stress, shifting strategies: Social context during stress shifts collective thermoregulation behaviors in honeybees

Abstract

Collective behaviors can buffer environmental challenges, but stress may disrupt the coordination required for group function. We tested whether social context during stress alters collective thermoregulation in honey bees (Apis mellifera). Fanner bees were exposed for 18 h to either control (30°C) or heat-stress (37°C) conditions while housed alone or in groups of 2, 12, or 25, and fanning behavior was assessed. After control conditions, bees frequently engaged in Nasonov fanning at lower temperatures before thermoregulatory fanning, consistent with a role in coordinating collective action before direct heat mitigation. After heat stress, groups skipped Nasonov fanning and directly engaged in thermoregulatory fanning, indicating a reorganization from communication to immediate action. Importantly, this shift depended on prior social context. Groups that experienced a stable social environment between treatment and assay maintained thermoregulatory performance after heat stress, whereas more socially disrupted groups showed reduced fanning. Follow-up experiments showed that this buffering effect was explained by group size stability rather than persistent social bonds among individuals. Unexpectedly, when Nasonov fanning was retained despite heat stress, it was associated with enhanced thermoregulatory performance, revealing a previously unrecognized role for this pheromone-signaling behavior in collective thermoregulation. Together, these findings show that stress does not simply impair collective behavior; instead, it reorganizes behavioral strategies in a socially dependent manner, linking individual plasticity to emergent group-level resilience in a changing world.