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

SIMPLE SUMMARY: The brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive pest that causes losses to many crops in different parts of the world. Biological control programs using the egg parasitoids Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) have been proposed as sustainable strategies to control this pest. Acroclisoides sinicus (Huang and Liao) is another parasitoid that frequently emerged from H. halys egg masses, hypothesized to be a hyperparasitoid of Trissolcus spp. that can have a potentially negative effect on the outcome of biological control programs. Under laboratory conditions, we investigated the impact of A. sinicus on the two primary parasitoids of H. halys, assessing its host preference and exploitation capacity. Acroclisoides sinicus demonstrated a clear preference in parasitizing T. mitsukurii, while the impact on T. japonicus was relatively low. Acroclisoides sinicus can use volatiles emitted by egg masses to distinguish between those parasitized by T. mitsukurii from those parasitized by T. japonicus or unparasitized ones. The results obtained here suggest that the presence of the hyperparasitoid can affect the composition of H. halys parasitoid complex. 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.