Hidden Host Mortality from an Introduced Parasitoid: Conventional and Molecular Evaluation of Non-Target Risk

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.

Assessing the Distribution of Exotic Egg Parasitoids of Halyomorpha halys in Europe with a Large-Scale Monitoring Program

“…The actual impact on native stink bugs should be evaluated with specifically designed field experiments, which should take into account hidden trophic interactions [ 40 ] as well. Further investigations are needed to assess whether behavioral barriers (such as phenology, habitat preference and interspecific competition) exist and could prevent non-target parasitism in the field [ 41 ].…”

Add Germany to the List—Adventive Population of Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) Emerges in Germany

“…Studies investigating fundamental and realized host ranges of candidate biocontrol agents typically focus on reproductive effects such as parasitism and emergence rates on target and non-target host species. Hepler et al [ 52 ] applied molecular forensics to assess the impact of mortality caused by non-reproductive effects, e.g., host feeding or aborted parasitoid development. They showed that the combined impact of reproductive and non-reproductive effects of a parasitoid on non-target species may be considerable depending on the host species and the evolutionary history of parasitoid and host species.…”

“…While unsuccessful parasitism by native egg parasitoid species still constitutes a form of biological control of H. halys in the broadest sense, such parasitism events of essentially unsuitable hosts present what has been termed an “evolutionary trap” [ 24 ]. Such evolutionary traps may have a negative effect on native stink bug parasitoid communities caused by parasitism of the unsuitable H. halys egg masses [ 24 , 52 , 53 ]. Immunological defenses of the developing stink bug embryos prevent successful parasitism by native egg parasitoid species.…”

Partial refuges from biological control due to intraspecific variation in protective host traits: a case study with the egg parasitoidTrissolcus japonicus

“…Host eggs that aborted for reasons other than unsuccessful parasitism versus because of unsuccessful parasitism cannot be readily distinguished without molecular diagnostic tools (e.g. Hepler et al 2020), but comparisons of abortion levels of eggs exposed to parasitoids with those in unexposed control egg masses can allow an estimate of how much host egg abortion is due to parasitoids (Abram et al 2016).…”

“…Although a number of non-target species are susceptible to attack by T. japonicus , interpretation of some results is hindered by the fact that parasitoid behaviour was not observed, or unexposed control egg masses were not included in experimental designs to estimate how many hosts were killed without parasitoid reproduction (i.e., non-reproductive effects; Abram et al 2016; Abram et al 2019). While T. japonicus is known to attack some non-target stink bugs (Milnes and Beers 2019; Hepler et al 2020), the population-level impact of this attack is not known (Kaser et al 2018; Abram et al 2020). Ecological refuges from parasitism (e.g.…”