Plant traits and reproduction in a multitrophic system: The role of aphids, parasitoids, and hyperparasitoids

Hyperparasitoids, which prey on parasitoids developing inside herbivorous hosts, can disrupt top-down control of herbivores in multitrophic food chains. Hyperparasitism releases herbivores from their natural enemies, thereby potentially increasing plant damage and reducing plant performance. However, how hyperparasitoids impact plant fitness under field conditions has not been studied. In this study, we performed a field mesocosm experiment in which we manipulated the presence of aphids Myzus persicae Sulzer (Hemiptera: Aphididae), parasitoids Aphidius colemani Viereck (Hymenoptera: Braconidae), and hyperparasitoids Alloxysta fuscicornis Hartig (Hymenoptera: Figitidae) on wild mustard plants Sinapis arvensis L. (Brassicales: Brassicaceae) to quantify their effects on plant performance and fitness.Parasitoids effectively suppressed aphid populations, but this control was weakened in the presence of hyperparasitoids. In addition, aphid parasitism rates by parasitoids were lower in the presence of hyperparasitoids. However, none of the treatments significantly affected plant traits such as leaf number, flowering time, seed weight and survival. In the absence of natural enemies, aphids marginally reduced seed production compared to plants exposed to aphids, parasitoids and hyperparasitoids, but this effect was weak. Overall, our results suggest that while parasitoids exert strong top-down control on aphids, S. arvensis can tolerate aphid herbivory. Consequently, the net fitness benefit of indirect defence via parasitoid recruitment – and its disruption by hyperparasitoids – appears to be limited in this system, potentially due to the rapid life cycle and tolerance strategy of S. arvensis.