Sulfoxaflor and nutritional deficiency synergistically reduce survival and fecundity in bumblebees

A range of anthropogenic factors are causing unprecedented bee declines. Among these drivers the usage of pesticides is believed to be crucial. While the use of key bee-harming insecticides, such as the neonicotinoids, has been reduced by regulatory authorities, novel, less studied substances have occupied their market niche. Understanding the threat of these chemicals to bees is, therefore, crucial to their conservation. Here we focus on sulfoxaflor, a novel insecticide, targeting the same neural receptor as the neonicotinoids. In stark contrast to the growing concerns around its negative impacts on bee health, a recent assessment has resulted in the extension of its authorisations across the USA. However, such assessments may underestimate risks by overlooking interactive impacts of multiple stressors. Here we investigated co-occurring, lethal and sublethal risks of sulfoxaflor and a dietary stress for bumblebees (Bombus terrestris), a key pollinator. Specifically, we employed a novel microcolony design, where, for the first time in bees, pesticide exposure mimicked natural degradation. We orally exposed workers to sulfoxaflor and a sugar-deficient diet in a fully factorial design. Field realistic, worst-case sulfoxaflor exposure caused a sharp increase in bee mortality. At sublethal concentrations, sulfoxaflor negatively affected bee fecundity, but not survival. Nutritional stress reduced bee fecundity and synergistically or additively aggravated impacts of sulfoxaflor on bee survival, egg laying and larval production. Our data show that non-mitigated label uses of sulfoxaflor may have major, yet severely neglected effects on bumblebee health, which may be exacerbated by nutritional stress. By unravelling mechanistic interactions of synergistic risks, our study highlights the need to overcome inherent limitations of Environmental Risk Assessment schemes, which, being based on a "single stressor paradigm", may fail to inform policymakers of the real risks of pesticide use.