Biological control effects of non‐reproductive host mortality caused by insect parasitoids

Abstract

As the rate of spread of invasive species increases, consumer-resource communities are often populated by a combination of exotic and native species at all trophic levels. In parasitoid-host communities, these novel associations may lead to disconnects between parasitoid preference and performance, and parasitoid oviposition may result in death of the parasitoid offspring, death of the host, or death of both. Despite their relevance for biological control risk and efficacy assessments, the direct and indirect population-level consequences of parasitoids attacking and killing their hosts without successfully reproducing (non-reproductive mortality) are poorly understood. Non-reproductive mortality induced by egg parasitoids (parasitoid-induced host egg abortion) may be particularly important for understanding the population dynamics of the invasive agricultural pest Halyomorpha halys (Hemiptera: Pentatomidae) and endemic stink bugs in North America, which are attacked by a suite of both native and introduced egg parasitoids. It is unclear, however, how various factors controlling parasitoid foraging and developmental success manifest at the population level. We constructed two related versions of a two-host-one-parasitoid model to evaluate the population-level consequences of non-reproductive host mortality. Egg abortion can result in strong negative or positive enemy-mediated indirect effects, taking the form of apparent competition, apparent parasitism, apparent amensalism, or apparent commensalism. For parasitoids limited in their reproductive output by the number of eggs they can produce, higher non-reproductive host mortality can reduce the strength of the positive indirect effect in cases of apparent parasitism, and it can reduce the negative indirect effect on the more suitable host in cases of apparent competition. For time-limited parasitoids, unsuitable hosts with high levels of non-reproductive parasitoid-induced mortality can be strongly suppressed in the presence of a suitable host, while the suitable host is only negligibly impacted (i.e., apparent amensalism). We evaluate these model-derived hypotheses within the context of H. halys and its native and nonnative parasitoids in North America, and discuss their application to risk assessment in biological control programs.

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

“…However, molecular approaches can quantify parasitism that may be underestimated due to high levels of host mortality in traditional rearing [ 41 ]. Mortality due to nonreproductive effects may be more severe when a host and parasitoid do not share an evolutionary history (as is the case in classical biological control), as physiological incompatibilities may prevent successful parasitoid development [ 34 , 38 ]. Detection of DNA from dead, undeveloped Trissolcus eggs and larvae in an incompatible pentatomid host has been demonstrated previously [ 42 ].…”

“…To generate predictions regarding the direct and indirect ecological effects of nonreproductive effects, we used the first model (“Model 1”) described in detail in Kaser et al [ 34 ]. This model simulates a two-host, one parasitoid system and is based on difference equations outlined by Beddington [ 35 ] and further developed by Heimpel et al [ 36 ], Kaser and Heimpel [ 37 ], and Abram et al [ 9 ] to include the possibility of variation in host susceptibility and host mortality due to parasitism that does not result in parasitoid reproduction (parasitoid-induced host egg abortion, i.e., nonreproductive effects).…”

“…First, we ran simulations that included the upper levels of nonreproductive effects (NRE U ) observed in our study. a was set at a baseline value of 0.05 (based on sensitivity analyses in Kaser et al [ 34 ]) for H. halys based on the total observed parasitoid impact in the presence of nonreproductive effects, and then scaled for each non-target based on the relative levels of parasitoid impact observed in our study). s was calculated based on the proportion of estimated parasitoid impact that was due to reproductive effects for each host species, and μ was set according to the proportion of total parasitoid impact that was due to nonreproductive effects, NRE U .…”

An effective cold storage method for stockpilingHalyomorpha halyseggs for field surveys and laboratory rearing ofTrissolcus japonicus

“…Our results show that refrigeration at 8°C for 10-14 days also kills nymphs, removing this risk. Limitations of using frozen eggs include the likely underestimation of parasitism levels (Jones et al 2014;Panizzi et al 2018;McIntosh et al 2019) and omission of other parasitoid-induced host mortality (Kaser et al 2018;Stahl et al 2019b). Consequently, some researchers have increasingly begun using viable H. halys eggs as an alternative (e.g., Costi et al 2018).…”

Variation in levels of acceptance, developmental success, and abortion of Halyomorpha halys eggs by native North American parasitoids

“…In addition, when an invasive species that acts as an evolutionary trap for native parasitoids is the target of biological control programs, it may be important to consider, variation in the ability of parasitoids to kill the invasive host when they unsuccessfully attack it ("non-reproductive effects"; reviewed in Abram et al, 2019a) may be important to consider. The mortality of the invasive pest resulting from non-reproductive effects could theoretically contribute to biological control of the invasive pest via both direct and indirect ecological effects (Kaser et al, 2018;Abram et al, 2019a;Stahl et al, 2019a). Assessing intraspecific variation in native parasitoid acceptance, developmental success, and the ability to induce host mortality can provide insight into the potential for the adaptation of native species to new invasive hosts, while also forming and form the basis for genetic improvement through breeding programs for native biological control agents (Lommen et al, 2017;Kruitwagen et al, 2018).…”