Animal pollinators support biodiversity and agricultural yields, and there is significant concern over the causes and consequences of declining bee populations. A key challenge for studying the health of social pollinators such as bees and the ecosystem services they provide is understanding both the proximate effects of environmental stressors on individual workers, as well as how these effects impact collective dynamics. Neonicotinoid pesticides are neuroactive compounds that disrupt cholinergic signaling in the insect central nervous system. While mounting evidence indicates these globally common pesticides can negatively affect bees, the specific behavioral mechanisms by which these neuroactive compounds impair colony growth remain unclear. Here, we develop a fully automated, robotic platform to continuously monitor behavior of individually-identified workers from multiple bumblebee (Bombus impatiens) colonies in parallel. We use this platform to study the temporal dynamics of worker behaviors (including nest maintenance and social thermoregulation) and their disruption by a common neonicotinoid pesticide (imidacloprid). Finally, we test the effects of imidacloprid exposure on bumblebee social thermoregulation performance in the field.
Results/Conclusions
We find that (a) worker behavior shows strong and stable circadian dynamics within bumblebee colonies, and that (b) exposure to field-realistic concentrations of imidacloprid (~6 ng/g) disrupts key aspects of worker behavior (including nursing). However, we find that the impacts of imidacloprid exposure are variable over the circadian cycle, with the strongest effects occurring at night. We also find strong evidence that field-realistic imidacloprid exposure impairs colony thermoregulation performance, in part by impairing the colony’s capacity to construct an insulating wax canopy. The effects of imidacloprid exposure on colony thermoregulation are non-linear and dynamic, suggesting the potential for potent interactions between climate stress and pesticide exposure. Our results reveal a novel behavioral mechanism by which sublethal neonicotinoid exposure may impair bee colony growth. Our findings also show that neonicotinoid pesticides impact worker behavior and colony performance through complex interactions with environmental conditions, highlighting the need for a more complete understanding of the physiological and neurobiological underpinnings of collective behavior in social pollinators, and their disruption by environmental stressors such as pesticides.