Co-exposure to a honeybee pathogen and an insecticide: synergistic effects in a new solitary bee host but not in <i>Apis mellifera</i>

Pesticides and pathogens are major drivers of bee declines. However, their potential interactions are poorly understood, especially for non-<i>Apis</i> bees. This study assessed the combined effects of infestation by the honeybee pathogen <i>Vairimorpha ceranae</i> and chronic exposure to the insecticide flupyradifurone on <i>Osmia bicornis</i> and <i>Apis mellifera</i>. We investigated whether <i>V. ceranae</i> could reproduce in a new solitary bee host (<i>O. bicornis</i>) and assessed sublethal and lethal effects of the pathogen and the pesticide, alone and in combination. We also analysed the interactive effects of the combined exposure on <i>V. ceranae</i> proliferation and bee survival in the two bee species. Newly emerged bees were orally infected with 100 000 spores of <i>V. ceranae</i> and then exposed ad libitum to flupyradifurone at field-realistic concentrations. We showed, for the first time to our knowledge, that <i>V. ceranae</i> can replicate in the midgut of <i>O. bicornis</i>, causing histological damage, impaired phototactic response, reduced food consumption and decreased longevity. The pathogen-pesticide combination caused a synergistic effect in <i>O. bicornis,</i> leading to an abrupt survival decline. In <i>A. mellifera</i>, <i>V. ceranae</i> and flupyradifurone showed antagonistic survival effects, but the pesticide promoted pathogen proliferation. Our results warn against the potential effects of pathogen spillover and multiple stressor exposure on non-<i>Apis</i> bees.