Cascading effects of herbivore protective symbionts on hyperparasitoids

AILSA H. C. MCLEAN,BENJAMIN J. PARKER,JAN HRČEK,H. CHARLES J. GODFRAY

doi:10.1111/een.12424

AILSA H. C. MCLEAN, BENJAMIN J. PARKER + Show 2 more

Open Access

https://doi.org/10.1111/een.12424

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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.

Highlights

Symbiotic associations with bacteria or fungi can allow animals to exploit otherwise inaccessible niches (Douglas, 2011; McFall-Ngai et al, 2013)
We investigated whether the protective effects of a defensive facultative symbiont in pea aphids can impact the hyperparasitoids two trophic levels above them, using two species of primary parasitoids and two species of hyperparasitoids
We found that both the protective symbiont and hyperparasitoids reduce the numbers of hatching primary parasitoids

Summary

Introduction

Symbiotic associations with bacteria or fungi can allow animals to exploit otherwise inaccessible niches (Douglas, 2011; McFall-Ngai et al, 2013). Microbial symbiosis is important in insects where it can allow the exploitation of otherwise nutrient-inadequate diets (Douglas, 2006, 2009) or lead to improved tolerance of heat shock and other abiotic challenges (Montllor et al, 2002). Acquisition of defensive capabilities through infection with a novel symbiont – perhaps from a ‘horizontal gene pool’ of potential symbionts with different defensive capabilities (Jaenike, 2012; Henry et al, 2013) – is likely to have consequences for the wider food web within which the insect is embedded through the direct and indirect effects of reducing the incidences of specific natural enemies. Protective symbionts could potentially alter community diversity and food web structure, but we currently have little idea of the magnitude or importance of these potential effects (McLean et al, 2016). Food web cascades have been reported in a variety of contexts and at different spatial

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