Abstract

Hidden trophic interactions are important in understanding food web ecology and evaluating the ecological risks and benefits associated with the introduction of exotic natural enemies in classical biological control programs. Although non-target risk is typically evaluated based on evidence of successful parasitism, parasitoid-induced host mortality not resulting in visible evidence of parasitism (i.e., nonreproductive effects) is often overlooked. The adventive establishment of Trissolcus japonicus, an exotic parasitoid of the introduced stink bug Halyomorpha halys, provides an opportunity to investigate the total impact of this parasitoid on target and non-target hosts in the field. We developed a new methodology to measure nonreproductive effects in this system, involving a species-specific diagnostic PCR assay for T. japonicus. We applied this methodology to field-deployed eggs of four pentatomid species, coupled with traditional rearing techniques. Nonreproductive effects were responsible for the mortality of an additional 5.6% of H. halys eggs due to T. japonicus, and were even more substantial in some of the non-target species (5.4-43.2%). The observed hidden mortality of native non-target species from an introduced parasitoid could change predictions about direct and indirect ecological interactions and the efficacy of biological control of the target pest.

Highlights

  • The accurate characterization of trophic interactions is important for several domains of applied ecology

  • As Trissolcus japonicus is the species of interest in the present study, we developed a set of species-specific polymerase chain reaction (PCR) primers for T. japonicus to allow rapid and cost-effective analysis of field samples

  • In each of the three simulations described below, we investigated the hypothesized direct and indirect population-level consequences of the levels of observed reproductive and non-reproductive effects measured in this study by varying three key parameters: attack rate, a; the proportion of parasitoid attacks resulting in parasitoid reproduction and host death, s; and the proportion of parasitoid attacks resulting in dead hosts but no parasitoid offspring emergence, μ

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Summary

Introduction

The accurate characterization of trophic interactions is important for several domains of applied ecology. Many classical biological control introductions have been declared successful, the practice has come under heavy criticism in recent years due to a minority of cases in which introduced natural enemies have had negative impacts on non-target native species [2,3]. These concerns have led to a strict regulatory process in most countries, whereby thorough host range studies are required to assess the physiological and ecological host range of a biological control agent prior to approval for release [4,5]. Hidden interactions, which may occur when natural enemies attack a host (e.g., Condon et al [6]), may be more common than is currently realized, and may be essential to understanding the ecological risk of introduced natural enemies as well as their broader role in trophic networks [7]

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