Hyperparasitism of Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) on Two Biological Control Agents of Halyomorpha halys

Abstract

Halyomorpha halys (Stål) is an invasive Asian pest that causes severe crop losses on various crops. Nowadays, management strategies against this pest mainly rely on pesticide use, but biological control with egg parasitoids is considered the most promising long-term and sustainable solution. Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) are Asian egg parasitoids already present in Europe and are the most effective biological control agents of H. halys. Therefore, these two species are considered for biological control programs in Europe and other parts of the world. Acroclisoides sinicus (Huang and Liao) is a pteromalid parasitoid wasp that frequently emerged from H. halys egg masses collected in northern Italy. This species has been hypothesized to be a hyperparasitoid of Trissolcus spp. parasitoids. This study was carried out under laboratory conditions where A. sinicus was tested in no-choice and two-choice experiments to assess the host preference between T. japonicus and T. mitsukurii. Olfactory responses of A. sinicus from volatiles emitted from different potential hosts were also tested. In all trials, A. sinicus showed a clear preference for parasitizing H. halys eggs previously parasitized by T. mitsukurii compared to T. japonicus. In no-choice experiments, the impact of the hyperparasitoid on T. japonicus was low, showing an exploitation rate of 4.0%, while up to a 96.2% exploitation rate was observed on T. mitsukurii. Acroclisoides sinicus was also attracted by volatiles emitted by egg masses parasitized by T. mitsukurii, while no response was observed to egg masses parasitized by T. japonicus or not parasitized. Therefore, according to the results obtained here, A. sinicus could limit the population development of T. mitsukurii, while lesser effects are expected on T. japonicus.

Tritrophic analysis of the prospective biological control of brown marmorated stink bug, Halyomorpha halys, under extant weather and climate change

“…Giovannini et al (2021) reared A. sinicus on both T. japonicus and T. mitsukurii, and though not designed to test for host preference, ~ 2.7 times as many A. sinicus were produced under similar conditions on T. mitsukurii than on T. japonicus. Laboratory studies by Mele et al (2021) found > 20:1 preference for T. mitsukurii compared to T. japonicus using a colony of A. sinicus derived from and maintained on T. mitsukurii parasitized BMSB eggs. However, growing evidence indicates that genetic variation in behavior and conditioning during the adult stage in insects can contribute to preference for the host on which the insect developed (Barron 2001).…”

“…In parasitoid wasps, conditioning during "critical periods" during the adult stage may have a profound impact on host selection behavior (van Emden et al 1996;Bjorksten and Hoffmann 1998;Barron 2001). Hence, the strong laboratory host preferences demonstrated in A. sinicus by Mele et al (2021) may not be applicable to the field where hyperparasitism levels are low (Mele et al 2022). In the model, we assumed equal preference for T. japonicus and T. mitsukurii, but the capacity to incorporate unequal preference is a component.…”

“…Acroclisoides sinicus has been successfully reared on both T. japonicus and T. mitsukurii, though ~ 2.7-fold higher emergence occurred on T. mitsukurii in rearing studies (Giovannini et al 2021). Laboratory studies by Mele et al (2021) found a > 20:1 A. sinicus preference for T. mitsukurii over T. japonicus when A. sinicus was reared on T. mitsukurii (see discussion section). However, in field studies in northeastern Italy when only T. mitsukurii was present (see Zapponi et al 2021), A. sinicus parasitism rates on T. mitsukurii were ~ 7.5% (Mele et al 2022) suggesting a low search rate ( As α).…”

“…The lower thermal threshold for development is 12.65 °C, and the upper threshold is ~ 35 °C. The nonlinear developmental rate As R(T) at mean temperature T is At time t, the population demand for primary parasitoid hosts (Mele et al 2021) is where i is age in days after a 2-day preoviposition period, As sr is the sex ratio, and the symmetrical concave scalar As (T) corrects for the effects of temperature on oviposition in the range 15-33.5 °C. In laboratory studies, the sex ratio of A. sinicus offspring from T. mitsukurii-parasitized eggs ranged from 62 to 91% females and 50-80% females from T. japonicus (Giovannini et al 2021).…”