The brown marmorated stink bug Halyomorpha halys is an invasive agricultural pest with a worldwide distribution. Classical biological control has been identified as the most promising method to reduce the populations of H. halys. Adventive populations of two candidates for releases, Trissolcus japonicus and Trissolcus mitsukurii, have recently been detected in Europe. To assess their distribution and abundance, a large-scale survey was performed. From May to September 2019, a wide area covering northern Italy and parts of Switzerland was surveyed, highlighting the expanding distribution of both Tr. japonicus and Tr. mitsukurii. Within four years after their first detection in Europe, both species have rapidly spread into all types of habitats where H. halys is present, showing a wide distribution and continuous expansion. Both exotic Trissolcus showed high levels of parasitism rate towards H. halys, while parasitization of non-target species was a rare event. The generalist Anastatus bifasciatus was the predominant native parasitoid of H. halys, while the emergence of native scelionids from H. halys eggs was rarely observed. The presence of the hyperparasitoid Acroclisoides sinicus was also recorded. This study provided fundamental data that supported the development of the first inoculative release program of Tr. japonicus in Europe.

Halyomorpha halys(Stål) (Hemiptera, Pentatomidae) was accidentally introduced to North America and Europe, becoming a key pest of many important crops. In its native range, it is attacked by egg parasitoids, includingTrissolcus japonicus(Ashmead), considered to be the main species, andT. mitsukurii(Ashmead) (Hymenoptera, Scelionidae).Trissolcus japonicuswas detected in North America in 2014 and Europe in 2017, whileT. mitsukuriiwas detected in Australia in the early 20^thcentury and in Europe in 2016. Both species now appear established in the new areas. The present study used the MaxEnt algorithm to clarify the geographic dimension of the potential interaction betweenH. halysand these two parasitoid species, and to indicate where the release of one or the other parasitoid species is more likely to be effective. We found that the suitability for the two parasitoids overlaps theH. halysnative range completely. In invaded areas,T. japonicusshowed higher potential habitat suitability at the global scale, compared toT. mitsukurii, and also higher potential suitability at lower latitudes at continental and national scales. These results can substantially improve the effectiveness of biological control againstH. halys, by targeting the releases of parasitoids to the areas where each species is most likely to succeed.

The highly destructive Asian brown marmorated stink bug (Halyomorpha halys, BMSB) invaded Europe, Caucasus region, and North and South America. Efforts to control it are ongoing in the Palearctic European-Mediterranean Basin and North America by introducing and redistributing two Asian stenophagous scelionid egg parasitoids (Trissolcus japonicus and T. mitsukurii) that are attacked by an adventive oligophagous pteromalid Asian hyperparasitoid (Acroclisoides sinicus). Large BMSB nymphs and adults may be parasitized by new associations of oligophagous tachinid flies and immature stages by egg parasitoids and predators. The terms stenophagous and oligophagous are commonly used to define narrow and wider ranges, respectively, of food eaten, but here they refer to the range of hosts attacked by adult female parasitoids. A holistic weather-driven physiologically based demographic model (PBDM) of the tritrophic interactions was developed to evaluate prospectively the impact of natural enemies on the biological control of BMSB under current and climate change weather. Our study focuses on the European-Mediterranean region, with the results for the USA, Mexico, and Central America reported as supplementary information. The PBDM analysis suggests that biotypes of the egg parasitoids T. japonicus and T. mitsukurii with high search capacity could suppress BMSB regionally, but the requisite levels of parasitism by these parasitoids for economic control are not observed in their native range nor in invaded areas. The model suggests that the action of T. japonicus is greater than that of T. mitsukurii, but that joint interactions of the two egg parasitoids would provide higher mortality of BMSB. Field data and model results suggest that the egg hyperparasitoid A. sinicus has a modest negative impact on the suppression of BMSB. Moreover, tachinid parasitoids of adults could have an important supplemental role in suppressing BMSB densities. Analysis suggests that new biotypes of egg parasitoids and species of tachinid parasitoids of large nymphs and adults be sought.

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.