Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, we have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. We investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. We found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid-parasitoid-hyperparasitoid interactions we studied. 5. We conclude that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. Our findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.