Cascading effects of herbivore protective symbionts on hyperparasitoids

Abstract

Abstract. 1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity.2. This study 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. It was 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. It is concluded 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. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.

Hyperparasitoids as new targets in biological control in a global change context

“…Protective symbionts in pests may have effects that extend to higher trophic levels, including hyperparasitoids (Oliver and Martinez, 2014;Ye et al, 2018). For example, in populations of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) that are protected by the bacterial endosymbiont Hamiltonella defensa against primary parasitism, there is a reduction in hyperparasitoid emergence not by a direct effect of the endosymbiont on the hyperparasitoid, but through indirect cascading effect resulting from the reduction of specific hosts available for primary parasitism (Mclean et al, 2017). In this sense, protection by endosymbionts is an additional type of bottom-up effect that influences the composition of a parasitoid-hyperparasitoid community (Rothacher et al, 2016;van Nouhuys et al, 2016;Ye et al, 2018).…”

Positive association between the diversity of symbionts and parasitoids of aphids in field populations

“…We assume that if parasitoid and symbiont diversity influence each other, such an effect should predominantly occur in primary parasitoids which are directly affected by possible symbionts. However, it is possible that some effects are carried over to secondary parasitoids or that they are influenced by primary parasitoid composition (McLean et al 2017).…”

Tri‐trophic interactions: bridging species, communities and ecosystems

“…This includes free‐living microbes in the rhizosphere (Venturi & Keel ), endosymbiotic bacteria in insects (e.g. Rothacher et al ; Mclean et al ), and endophytic fungi (Van Bael et al ), all of which have the potential to affect plant and arthropod traits of relevance to TTIs. Isolating and testing the effects of volatile compounds mediating below‐ and aboveground microbe‐mediated TTIs will be of key importance.…”