Sublethal fungicide-insecticide co-exposure affects nest recognition and parental investment in a solitary bee

Fungicides may interact synergistically with insecticides. However, our understanding of the impacts of sublethal insecticide-fungicide combinations on solitary bees is mostly restricted to laboratory studies, providing no information about potential consequences on behavior and reproductive success. We analyzed the effects of a fungicide application, alone and in combination with sublethal levels of an insecticide, on the nesting behavior and reproductive output of the solitary bee Osmia cornuta. We released individually-marked females into oilseed rape field cages, and subsequently sprayed the plants with four treatments: control (water), fungicide (tebuconazole), insecticide (acetamiprid at a sublethal concentration), and mixture (fungicide + insecticide). We recorded nesting activity before and after the sprays and assessed post-spray individual reproductive success. Bees of the single pesticide treatments were unaffected by the sprays and did not differ from control bees in any of the parameters measured. The longevity of bees of the mixture treatment was unaffected. However, these bees showed reduced foraging activity, shorter in-nest pollen-nectar deposition times, and increased difficulty recognizing their nesting cavity, leading to a decrease in provisioning rate, parental investment, and offspring production. Our study demonstrates that co-exposure to a fungicide with otherwise harmless levels of an insecticide caused behavioral effects with consequences on reproductive success. Because longevity was unaffected, these effects would not have been easily detected in a chronic laboratory test. Our results have important implications for bee risk assessment, which should account for exposure to multiple compounds and address behavioral effects and reproductive output under semi-field and/or field conditions.