Indirect effects on mutualisms: parasitism of bumble bees and pollination service to plants

Researchers increasingly recognize the important role of mutualisms in structuring communities and view positive interactions in a community context rather than as simple pairwise interactions. Indirect effects, such as those that predators have on lower trophic levels, are a key process in community ecology. However, such top-down indirect effects have rarely been extended to mutualisms. Antagonists of one mutualist have the potential to negatively affect the second mutualist through negative effects on their partner, and the magnitude of such effects should vary with mutualism strength. Bumble bees are ecologically and economically important pollinators that are an ideal system to determine if such indirect effects play an important role in mutualisms. Bumble bees are attacked by an array of parasites and predators, and they interact with a range of plants that vary in their dependence on bumble bees for reproduction. We tested whether variation in parasitism rates by Nosema bombi, Crithidia bombi, and conopid flies correlated with reproduction of greenhouse-raised plants placed in the field. At multiple sites over two years, we studied four plant species that varied in reliance on bumble bees as pollinators. We found a consistent negative relationship between Nosema parasitism and measures of pollination for Trifolium pratense and Solanum carolinense, plant species with high bumble bee visitation, whereas Rudbeckia hirta and Daucus carota, plant species with generalized pollination, experienced no impacts of Nosema. However, both Crithidia and conopids showed inconsistent relationships with pollination service. Although these patterns are correlational, they provide evidence that parasites of bumble bees may have negative indirect effects on plants, and that mutualism strength can moderate the magnitude of such effects.