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

Abstract

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.

The role of disease in bee foraging ecology

“…Given that various pathogens have been observed to impair the foraging ability of bees (see discussion above), it would seem likely that pollination services are also altered or impaired. Gillespie & Adler [64], for example, found a negative correlation between Nosema infection rates in bumble bees at different field sites, and seed set of Trifolium and Solanum plants. Lach et al [10] found that honey bees infected with N. apis collected less pollen, and infection intensity was negatively correlated with the amount of pollen grains carried on the body of foragers, suggesting a lower efficiency of highly infected workers as pollinators.…”

Pollination services enhanced with urbanization despite increasing pollinator parasitism

“…Bumblebees offer us an excellent model system to study the indirect effects of parasitism on mutualisms [ 20 ]. The majority of Bombus spp., are generalist pollinators, foraging on many native wild and crop plants in diverse terrestrial habitats in temperate regions [ 15 ].…”

The enemy of my enemy is my friend: Nematode infection of pollinating and non-pollinating fig wasps has net benefits for the fig-fig wasp pollination mutualism

“…It is likely (with increased sampling) that all other associated NPFW suffer fitness limitations due to infection, suggesting that nematode infection may remove a sizeable proportion of the total wasp-antagonist community in each generation. This may be explained as an indirect effect (Gillespie andAdler 2013, Guimarães et al 2017) or may represent a novel density-dependent facultative mutualism between Parasitodiplogaster nematodes, Pegoscapus pollinating wasps, and F. petiolaris. When more NPFWs exploit the mutualism they are more likely to encounter nematodes whose infection they are sensitive to, making them unlikely to arrive at a new fig and reproduce.…”