Bee-associated fungi mediate effects of fungicides on bumble bees

Bumble bees are important pollinators that face threats from multiple sources, including agrochemical application. Declining bumble bee populations have been linked to fungicide application, which could directly affect the fungi often found in the stored food and GI tract of healthy bumble bees. Here, we test the hypothesis that fungicides impact bee health by disrupting bee-fungi interactions. We examine the interactive effects of the fungicide propiconazole and fungal supplementation on the survival, reproduction, and microbiome composition of microcolonies (queenless colonies) using two species, Bombus vosnesenskii and B. impatiens . We found that both bee species benefitted from fungi, but were differentially affected by fungicides. In B. vosnesenskii , fungicide exposure decreased survival while fungal supplementation mitigated fungicide effects. For B. impatiens , fungicide application had no effect, but fungal supplementation improved survival and offspring production. Fungicides reduced fungal abundance in B. vosnesenskii microcolonies, but not in B. impatiens , where instead fungal addition decreased fungal abundance. In B. vosnesenskii , the abundance of the pathogen Ascosphaera was negatively associated with survival, while the yeast Zygosaccharomyces was positively associated with survival. Our results highlight species-specific differences in response to fungicides and the nature of bee-fungi associations, and caution the use of results obtained using one species to predict responses of other species. These results demonstrate that fungicides can alter bee-fungi interactions with consequences for bee survival and reproduction, and suggest that exploring the mechanisms of such interactions, including interactions among fungi in the bee GI tract, may offer insights into bumble bee biology and conservation strategies. Significance statement Wild bumble bee populations are declining globally, and a major predictor of these declines is agricultural fungicide application. We test the hypothesis that bee-associated fungi mediate fungicide effects on bees, examining how fungicide exposure and subsequent fungal supplementation impact bumble bee survival and microbiome. Fungal supplementation enhanced survival in both bumble bee species tested here, with fungi mediating effects of fungicide exposure in one species. Differences in bee survival were associated with changes in the gut mycobiome: negatively with the pathogen Ascosphaera and positively with Zygosaccharomyces yeasts. This study highlights the importance of the mycobiome in bumble bee health both as a mechanism by which fungicides impact bumble bees and as an avenue of further research on beneficial bee-associated fungi.