Testing the multiple stressor hypothesis: chlorothalonil exposure alters transmission potential of a bumblebee pathogen but not individual host health.

Abstract

Numerous threats are putting pollinator health and essential ecosystem pollination services in jeopardy. Although individual threats are widely studied, their co-occurrence may exacerbate negative effects, as posited by the multiple stressor hypothesis. A prominent branch of this hypothesis concerns pesticide-pathogen co-exposure. A landscape analysis demonstrated a positive association between local chlorothalonil fungicide use and microsporidian pathogen (Nosema bombi) prevalence in declining bumblebee species (Bombus spp.), suggesting an interaction deserving further investigation. We tested the multiple stressor hypothesis with field-realistic chlorothalonil and N. bombi exposures in worker-produced B. impatiens microcolonies. Chlorothalonil was not avoided in preference assays, setting the stage for pesticide-pathogen co-exposure. However, contrary to the multiple stressor hypothesis, co-exposure did not affect survival. Bees showed surprising tolerance to Nosema infection, which was also unaffected by chlorothalonil exposure. However, previously fungicide-exposed infected bees carried more transmission-ready spores. Our use of a non-declining bumblebee and potential higher chlorothalonil exposures under some scenarios could mean stronger individual or interactive effects in certain field settings. Yet, our results alone suggest consequences of pesticide co-exposure for pathogen dynamics in host communities. This underlies the importance of considering both within- and between-host processes when addressing the multiple stressor hypothesis in relation to pathogens.