Bee‐associated fungi mediate effects of fungicides on bumble bees

Abstract

1. 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 gastrointestinal (GI) tract of healthy bumble bees.2. We test the hypothesis that fungicides impact bee health by disrupting bee-fungi interactions. We examined 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.3. We found that 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.4. Fungicides reduced fungal abundance in B. vosnesenskii microcolonies, but not in B. impatiens, where instead fungal addition decreased fungal abundance (ITS copy number). Fungal composition varied between treatments but differently between bee species. In B. impatiens, fungal addition increased microbiome diversity. In B. vosnesenskii, the abundance of the pathogen Ascosphaera was negatively associated with survival, while the yeast Zygosaccharomyces was positively associated with survival. 5. Our results highlight that bumble bee species differ in response to fungicides and in the nature of bee-fungi associations. Fungicides can alter bee-fungi interactions with consequences for bee survival and reproduction, and 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.

Effects of spinetoram and glyphosate on physiological biomarkers and gut microbes in Bombus terrestris

“…In addition to containing a large number of gut bacteria, the bee gut is rich in fungi, which have antibacterial and antioxidant activities, and probiotic potential ( Hsu et al, 2021 ; Cui et al, 2022 ; Rutkowski et al, 2022 ). However, the effects of pesticide exposure on the gut fungi of bees are often overlooked.…”

Bees just wanna have fungi: a review of bee associations with nonpathogenic fungi

“…In all but one published instance, yeast-containing flowers or nectars increased visitation or consumption by bumble bees over uncolonized or bacteria-colonized nectars (Herrera et al 2013 , Schaeffer and Irwin 2014 , Schaeffer et al 2017a , 2019 , Yang et al 2019 ). As an exception, B. vosnesenskii did not prefer yeast-inoculated nectar volatiles over those of control nectar in a microcolony study (Rutkowski et al 2022 ). In contrast to most bumble bee responses, honeybees show no attraction to nectar yeasts or even display reduced visitation to nectar colonized by floral fungi (Kevan et al 1987 , Rering et al 2018 , 2020 , 2021 , Crowley-Gall et al 2022 , Schaeffer et al 2022 ).…”

“…infection levels in honeybees (Škerl and Gajger 2022 ). In Bombus impatiens , consumption of the nectar yeast Metschnikowia reukaufii did not affect colony survival or brood production (Schaeffer et al 2017a ), but addition of the yeasts Starmerella sorbosivorans, Zygosaccharomyces rouxii , and Debaroymyces hansenii —which are typically present within the colony environment—improved worker survival and offspring production (Rutkowski et al 2022 ). In the bumble bee B. terrestris, M. gruessii , and W. bombiphila increased colony development rates and the number of offspring produced, though other fungal species tested were not as beneficial (Pozo et al 2019 ).…”

“…Fungicides reduce the growth of floral and bee-associated fungi (Alvarez-Perez et al 2016 , Bartlewicz et al 2016 , Schaeffer et al 2017b ), which may alter bee–fungi interactions. In bumble bees, exposure to the fungicides chlorothalonil and propiconazole reduced colony biomass, worker production, and worker survival (Bernauer et al 2015 , Steffan et al 2017 , Rutkowski et al 2022 ). These effects on bee health were accompanied by changes in the fungal abundance and communities of nest provisions and bee guts, with a decrease in common bee associates like Cladosporium, Aspergillus, Penicillium , and Zygosaccharomyces , while other groups, including the pathogen-containing Ascosphaerales, increase in prevalence (Yoder et al 2013 , Steffan et al 2017 , Rutkowski et al 2022 ).…”

“…In bumble bees, exposure to the fungicides chlorothalonil and propiconazole reduced colony biomass, worker production, and worker survival (Bernauer et al 2015 , Steffan et al 2017 , Rutkowski et al 2022 ). These effects on bee health were accompanied by changes in the fungal abundance and communities of nest provisions and bee guts, with a decrease in common bee associates like Cladosporium, Aspergillus, Penicillium , and Zygosaccharomyces , while other groups, including the pathogen-containing Ascosphaerales, increase in prevalence (Yoder et al 2013 , Steffan et al 2017 , Rutkowski et al 2022 ). In one case, applying the azole fungicide propiconazole to Bombus vosnesenskii microcolonies reduced worker survival, but supplementation with bee-associated fungi ( Penicillium, Starmerella , and Zygosaccharomyces ) back into the nest following fungicide exposure eliminated negative effects of fungicide on survival, suggesting that fungicide effects could be mediated through disruption of nest fungi communities (Rutkowski et al 2022 ).…”