The world is a complicated place. Organisms typically interact with one another simultaneously and the strength of interactions can depend on what’s happening in the environment. As a number of organisms within a community increases, indirect interactions also increase exponentially (Abrahams 1992). As ecologists, we’re fascinated by the beauty of this complex world while we struggle to understand and predict how nature really works. Studying a pair-wise interaction is a good first step to tackle this challenge but it’s often not good enough to understand the real world.
Gillespie and Adler (2013) present a really cool multiple species interactions in nature in their recent Ecology paper. Using plants and bumble bee pollinators as a study system, they examined how antagonists (parasites and parasitoids in this case) affect their mutualistic interactions in the field. They focused on several species of parasitoid conopid flies and two common parasite of bumble bees, protozoa and microsporidium. Given that these parasitic species can negatively affect bumble bee performance, they predicted that 1) there would be a negative correlation between parasite infection levels in bumble bees and pollination service and 2) these correlations should be stronger for plant species that rely more on bumble bees for pollination than the one that rely less (i.e. generalist plant species).
What they did:
Between 2007 and 2008, they collected bumble bees from 26 sites and estimated the proportion of bees that were parasitized by flies, protozoans or microsporidium. On the same day that they collected bumble bees, they also conducted a field experiment to test pollination service on four different plant species: Two species that heavily rely on bumble bees for pollination and another two species that rely less on bumble bees (in other words, they are generalists). They placed these four species of greenhouse-reared plants to the field for a day and quantified pollinator visitation. Then they took the experimental plants back to the greenhouse and quantified total seed and seed mass.
What they found:
They found a negative relationship between parasitism by one of the parasites (microsporidium) and pollination service for two bumble bee-dependent plant species, consistent with their prediction. However, this pattern disappeared for other two generalist plants species that less dependent on bumble bees. Basically, bumble bee-dependent plant species experienced negative indirect effects by microsporidium, mediated by pollinators. Effects of flies and protozoans on any of the plant species were negligible or even positive though, presumably because they are less virulent parasites/parasitoids of bumble bees.
-Studying biotic interactions in a community context is super hard! I like how they looked at mutualism and antagonism simultaneously in the field (Figure 2 of the paper)
-I like how they examined four plant species that differ in their dependence on bumble bee pollinators. By doing so, they demonstrated that the magnitude of indirect negative effects on plants depends on the mutualism strength.
-In their discussion, Gillespie and Adler bring up an interesting point about trait-mediated indirect effects. What if parasites/parasitoids indirectly affects the behavior of bumble bees? For example, parasitized bees may fly less and increase inbreeding depression within a plant population. What a cool hypothesis!
Gillespie S. D. and L. S. Adler 2013. Indirect effects on mutualisms: parasitism of bumble bees and pollination service to plants. Ecology 94:454–464.