The Sublethal Effects of Pesticide Exposure on Aging, Behavior, and the Potential of Improved Dietary Lipid Supplementation in Honey Bees

Abstract

Honey bees (Apis mellifera), the most widely utilized commercial pollinator, have experienced rapid declines over the past two decades due to a synergy of stressors that include poor forage, pathogens, parasites, and pesticides. A major goal of honey bee research is to not only identify the presence and magnitude of these stressors, but to understand how stressors affect bees and to develop ways to mitigate their negative effects. Prior research has focused on identifying which pesticides have the greatest lethality, rather than identifying those that induce subtle, non-lethal effects. Sublethal effects may compromise metabolic homeostasis through continued activation of the stress response, a compounding effect that might eventually lead to colony failure. Here, we focus on insect growth regulators as a possible honey bee stressor. Insect growth regulators are a group of reportedly “pollinator-friendly” pesticides that affect development in target pests by hindering hormonal processes necessary to reach adulthood. While these pesticides are inherently more hazardous to juvenile insects, they may accelerate the degradation of fat body tissue in adult insects, an endocrine organ that acts as the primary internal lipid reserve. In worker honey bees, fat body degradation is linked to foraging onset. Accelerated fat body degradation is inferred to lower age at foraging onset, a phenomenon known as precocious foraging. Precocious foragers are reported to be less effective, as they exhibit higher mortality rates and complete fewer total foraging trips than non-precocious cohorts. It is unknown whether precocious foragers differ regarding the quantity and nutritional quality of their collected pollen. It is possible that they could be foraging for fattier, more nutritious pollen to compensate for reduced internal nutrient reserves. Understanding the physiology of stressed foragers may provide greater insight as to how endocrine disruption leads to observable changes in food-seeking behavior. We asked whether two common insect growth regulator pesticides (spirodiclofen, a fatty acid synthesis disruptor, and pyriproxyfen, a juvenile hormone mimic) accelerate fat body degradation in honey bees and release lipids into the hemolymph to fuel the stress response. I examined how these pesticides affect the survival and lipid metabolism of nurse-aged worker bees reared in laboratory cages (Appendix A). Field-realistic quantities of spirodiclofen did not affect the survival of nurse-aged bees, affirming that this pesticide was indeed non-lethal. Spirodiclofen also accelerated abdominal lipid depletion, whereas pyriproxyfen did not. We then asked whether bees treated with these pesticides would forage earlier and for fattier pollen to compensate for accelerated lipid degradation. I conducted in-hive observations of treated bees to determine if they foraged earlier and for more, fattier pollen (Appendix B). Pyriproxyfen lowered the average age of onset foraging, without accelerating lipid depletion, whereas spirodiclofen accelerated lipid depletion without affecting the average age of onset foraging. Additionally, spirodiclofen-treated bees foraged for less, yet more lipid-rich pollen, suggesting they might be compensating for accelerated lipid loss. Finally, we asked if increasing the lipid component of supplemental pollen diet could mitigate the deleterious effects of pesticide treatment. Lipid supplementation reduced hive weight loss among pesticide-treated hives, suggesting hive biomass might be sustained with improved diet design (Appendix C).