Parental host species affects behavior and parasitism by the pentatomid egg parasitoid, Trissolcus japonicus (Hymenoptera: Scelionidae)

Highlights

• Separate parasitoid lines were established using two pentatomid species as hosts.

• Behavioral assay results suggest T. japonicus exhibits some degree of host fidelity.

• Host parasitism rates and host suitability were dependent on exposed host species.

• T. japonicus hind tibia length and body weight were dependent on host species.

Abstract

The samurai wasp, Trissolcus japonicus, is the primary natural enemy of the invasive brown marmorated stink bug, Halyomorpha halys, in its native range of Asia. Laboratory tests have found that the wasp can parasitize numerous native pentatomid species in North America, yet many potentially influential factors involved with T. japonicus host acceptance and host suitability are understudied. In this study we evaluated the effects of host-related semiochemicals and parental host species on T. japonicus host foraging behavior and host parasitism. To address possible influences of parental host species, separate parasitoid lines were established using H. halys and native predatory pentatomid Podisus maculiventris eggs as hosts. Female T. japonicus from both host types were exposed to soybean (Glycine max) leaf surfaces contaminated by adult kairomones of either host species in behavioral assays. Females from each host type were also subject to no-choice tests in which they were exposed to either H. halys or P. maculiventris egg masses in large mesh cages. Each female used in the no-choice tests was weighed and their right hind tibiae were measured to identify possible phenotypic plasticity. Results from the behavioral assays suggest that T. japonicus exhibits some degree of host fidelity while searching for hosts. Females which emerged from P. maculiventris eggs resided for equal amounts of time on leaves contaminated with kairomones from either stink bug species. Differences in no-choice test performance were not found between the two host types, as parasitism rates and host suitability were determined to be dependent on exposed host species and not the parasitoid parental host species. T. japonicus which emerged from H. halys possessed longer right hind tibiae and weighed roughly twice as much as wasps which emerged from P. maculiventris.

Introduction

The brown marmorated stink bug (BMSB), Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is a highly polyphagous insect native to eastern Asia and currently considered a serious nuisance and agricultural pest across North America and Europe (Hoebeke and Carter, 2003, Wermelinger et al., 2008, Rice et al., 2014). Halyomorpha. halys was initially discovered in the United States in 1996 and has since spread to 44 states, many of which have reported significant economic damages to agriculture (NE IPM, 2019). Its polyphagy, as well as its mobility, classify H. halys as a landscape-level pest, enabling it to colonize urban, natural, and agricultural habitats (Lee et al., 2013, Joseph et al., 2014), and evade current management strategies to suppress local populations (Morrison et al., 2015).

The introduction of natural enemies (i.e., classical biological control) of H. halys is considered a promising long-term strategy for managing the pest’s populations at a landscape level (Rice et al., 2014). The Asian egg parasitoid, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae) is the primary natural enemy of H. halys in its native range, where it has been documented to parasitize 50 to 80% of H. halys egg masses found in the field (Qui et al., 2007, Yang et al., 2009, Talamas et al., 2013, Zhang et al., 2017). For this reason, T. japonicus is recognized as the key candidate biological control agent for H. halys and has been the subject of intensive USDA-ARS quarantine host specificity studies (Buffington et al., 2018). To date, results from host range experimentation have provided a baseline understanding of T. japonicus fundamental host range. Although T. japonicus shows a clear preference for H. halys in laboratory host range tests, the wasp is physiologically capable of successful development within several native stink bug species (Hedstrom et al., 2017).

The value of biological control programs’ host specificity evaluations has been questioned by a number of scientists (Howarth, 1983, Hawkins and Marino, 1997, Strong and Pemberton, 2001, Louda et al., 2003). They claim that an exotic agent’s host range is exceedingly difficult to accurately assess using simplistic laboratory procedures. The majority of host range tests conducted for T. japonicus have measured only the direct interaction between the parasitoid and potential host, and therefore exclude the ecologically vital steps of the egg parasitoid host foraging process (Godfray, 1994). This host foraging process is mediated by a parasitoid’s perception of various host-related chemical cues (i.e. semiochemicals) which not only relay crucial information regarding the general habitat and location of a prospective host, but may also offer the parasitoid detailed information concerning a host’s suitability (Vet and Dicke, 1992, Fatouros et al., 2008). By integrating semiochemicals into current T. japonicus host specificity testing regimes, a more accurate prediction of the wasp’s ecological host range may be obtained.

Egg parasitoids rely heavily on the presence of semiochemicals in their environment to bridge the immense spatial gap between them and their often inconspicuous hosts (Conti and Colazza, 2012). Also known as the infochemical detour strategy (Vet & Dicke, 1992), the ability of egg parasitoids to exploit a variety of chemical compounds associated with non-host life stages is crucial for successful host location (Vinson et al., 1998). Chemicals deposited on plant substrates (e.g., contact kairomones), such as low-volatility residues left by adults and immature host stages, further motivate parasitoids to search intensively for a host in their local vicinity (Meiners and Peri, 2013). Laboratory studies that exposed scelionid parasitoids to HIPVs (Moraes et al., 2005, Michereff et al., 2013), pheromones (Bruni, 2000, Conti et al., 2003), and host species adult contact kairomones (Colazza et al., 1999, Peri et al., 2006, Salerno et al., 2006) were able to elicit characteristic egg parasitoid host recognition behaviors. These behaviors included parasitoid arrestment or periods of motionlessness, decreased flight responses, slower walking velocities, and increased turning rates (Colazza et al., 1999). Quantifying the magnitude of semiochemical-induced behaviors is an effective technique for determining an egg parasitoid’s preference to search for one suitable host over another (Conti et al., 2004). For instance, Trissolcus spp. have displayed dissimilar behavioral responses when exposed to semiochemicals from coevolved hosts versus non-coevolved hosts (Salerno et al., 2006, Boyle et al., 2019). Comparative analyses of T. japonicus behavioral responses to semiochemicals from H. halys and from selected physiologically suitable native pentatomids would provide valuable knowledge concerning the wasp’s host foraging preferences, and ultimately expand our understanding of its host specificity.

The manipulation of a parasitoid’s informational and physiological state is another approach that would enhance the ecological complexity of current T. japonicus host range evaluations and strengthen the parasitoid’s non-target risk assessment (Withers & Browne, 2004). In particular, a parasitoid’s parental host species has been shown to influence its phenotypic traits (Abram et al., 2016), associative learning (Hastings and Godfray, 1999), lifetime fecundity (Turlings et al., 1993), and host preferences (Orr et al., 2000). Currently, parental host species effects have not been adequately identified for T. japonicus. Previous studies suggest positive intraspecific correlations between egg parasitoid size and reproductive traits such as female egg loads and total offspring produced (Boivin, 2010, Boivin and Martel, 2012). An egg parasitoid’s vagility, or propensity to move throughout its environment in search of hosts, was also positively correlated with the body size of certain egg parasitoid species (Bennett and Hoffmann, 1998, Abram et al., 2016). Allahyari et al. (2004) examined parental host effects on egg parasitoid fitness parameters for Trissolcus grandis when reared on its coevolved host versus a non-coevolved host, concluding that the observed increases in host handling time for smaller T. grandis females reared on the non-coevolved host could indicate reductions in the parasitoid’s lifetime fecundity. Since T. japonicus parasitizes pentatomid species other than H. halys in its native range and can also successfully develop in several North American species, understanding the influences that the parental host species may have on T. japonicus host preferences is necessary for a comprehensive non-target risk assessment (Hedstrom et al., 2017, Zhang et al., 2017, Botch and Delfosse, 2018).

Here, we have simulated a non-target parasitism event for T. japonicus and examined its influence on the parasitoid’s host specificity. Specifically, our present study tested how the parental host species of T. japonicus affects its host foraging behaviors and its capacity to successfully locate and parasitize a suitable host. To do so, we reared the parasitoid on its coevolved host, H. halys, and on a native, physiologically suitable host, Podisus maculiventris (Say) (Pentatomidae: Asopinae). P. maculiventris is an important generalist predator of many agricultural pests, and is thought to be distributed among habitats that overlap with those of H. halys (McPherson, 1980, Culliney, 1986, Wiedenmann et al., 1994). Our previous research revealed that T. japonicus (reared on H. halys) spent more time on different leaf substrates with H. halys adult kairomones than on substrates with P. maculiventris adult kairomones (Boyle et al. 2019). With these results in mind, our current study exposed T. japonicus reared on either of those two hosts to plant substrates contaminated by H. halys or P. maculiventris adult kairomones in order to determine whether the host species from which T. japonicus emerges affects the wasp’s kairomone-induced behavioral responses.

To expand our investigation of parental host influence, we then conducted no-choice host range tests for each T. japonicus line in larger, more complex arenas so that their abilities to successfully locate and parasitize H. halys and P. maculiventris could be more holistically evaluated. By comparing the performance of the two T. japonicus strains, we hoped to acquire novel insight into how non-target parasitism events and parental host species may impact the host specificity and ecological host range of T. japonicus. We hypothesized that T. japonicus that emerged from P. maculiventris eggs would subsequently respond more to that species’ kairomones and parasitize its eggs more successfully the following generation, as previously observed in non-target host range experiments conducted by Botch & Delfosse (2018). If true, this would suggest that T. japonicus could have greater non-target impacts on the valued native predatory stink bug than would be anticipated solely on the basis of the no-choice and choice laboratory tests.