Consumption competition by a parasitoid wasp opens a window of survival under intraguild predation

Intraguild predation is a common type of omnivory that occurs when two competing consumers that share a resource also prey on each other. Theory predicts limited conditions under which species engaging in this interaction can coexist, but in nature intraguild predation is widespread. In asymmetrical intraguild predation one predator feeds on another but not vice-versa, and the dominant predator usually excludes the subordinate one, unless the latter is more efficient at exploiting the shared prey. Despite decades of research, the mechanisms enabling coexistence of such subordinate predators remain poorly understood. Here, we combine a long-term multigenerational experiment with behavioural tests to investigate the population dynamics of the parasitoid wasp Aphidius colemani, when sharing the aphid prey Myzus persicae with two dominant predators: the ladybird Adalia bipunctata and the brown lacewing Micromus angulatus. These predators act as dominant or intraguild predators because they can feed on both healthy and parasitized aphids. We found that in the presence of predators, the parasitoid had smaller population sizes and quicker extinction times. Unexpectedly, however, the parasitoid had a negative impact on the lacewing, but not on the ladybird. Behavioural experiments revealed that (1) late parasitoid stages (mummies) were seldom predated by intraguild predators, (2) the lacewing had lower consumption rates and (3) the ladybird preferentially consumed young parasitized aphids. These results suggest that the slower-feeding lacewing allowed parasitoids to develop into protected mummies and capitalize aphid resources, a case of consumption competition. The faster consumption rates of the ladybird narrowed the window of parasitoid survival, a limitation further exacerbated by this predator's aggressive behaviour that preferentially consumed early instars of its competing natural enemy. Consumption competition can therefore allow survival under intraguild predation and influence the persistence of species in communities with multiple natural enemies.