Factors influencing short-term parasitoid establishment and efficacy for the biological control of Halyomorpha halys with the samurai wasp Trissolcus japonicus.

BACKGROUND: Classical biological control has been identified as the most promising approach to limit the impact of the invasive pest species Halyomorpha halys (Heteroptera: Pentatomidae). This study investigated the parasitism rate at sites where the biocontrol agent Trissolcus japonicus (Hymenoptera: Scelionidae) was released and where its unintentional introduction took place, in the Trentino-South Tyrol region. The effect of land-use composition was studied to understand which factors favor the establishment of hosts and parasitoids, including native and exotic species. RESULTS: The released T. japonicus were detected a year after the start of the program, with a significant parasitoid impact and discovery, compared to control sites. Trissolcus japonicus was the most abundant H. halys parasitoid, and Trissolcus mitsukurii and Anastatus bifasciatus were recorded also. The efficacy of T. mitsukurii was lower in sites where T. japonicus was successfully established, suggesting a possible competitive interaction. Parasitism level by T. japonicus at the release sites was 12.5% in 2020 and 16.4% in 2021. The combined effect of predation and parasitization increased H. halys mortality up to 50% at the release sites. Landscape composition analysis showed that both H. halys and T. japonicus were more likely to be found at sites with lower altitude and with permanent crops, whereas other hosts and parasitoids preferred different conditions. CONCLUSION: Trissolcus japonicus showed a promising impact on H. halys, at release and adventive sites, with minor nontarget effects, mediated by landscape heterogeneity. The prevalence of T. japonicus in landscapes with permanent crops could support IPM in the future. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Assessing the Distribution of Exotic Egg Parasitoids of Halyomorpha halys in Europe with a Large-Scale Monitoring Program.

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.

Assemblage of the Egg Parasitoids of the Invasive Stink Bug Halyomorpha halys: Insights on Plant Host Associations.

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an invasive alien species and a key agricultural pest. Its native parasitoids (Trissolcus japonicus Ashmead and Tr. mitsukurii Ashmead) have been registered in several countries where H. halys brought dramatic economic losses and where biological control is considered to be the most effective long-term solution. By searching for stink bug egg masses and exposing sentinel egg masses, we monitored the distribution of native and exotic egg parasitoids in Trentino-Alto Adige (Italy), an area where both the host and parasitoids are in expansion. We recorded ten pentatomids, seven parasitoid species, with the first report of Tr. japonicus in this area and a hyperparasitoid. In the assemblage, Anastatus bifasciatus (Geoffroy) and Tr. mitsukurii were the dominant parasitoids, with a different distribution in terms of context and host plants. Sycamore was the host plant where the highest number of naturally laid parasitized egg masses (26%) were recorded. Trissolcus mitsukurii showed the highest parasitism rate, and was often found in apple orchards. The emergence of exotic parasitoids showed a temporal delay compared to native ones. Sequence analysis of 823 bp of the CO1 mitochondrial gene revealed that the recovered Tr. japonicus and Tr. mitsukurii harbored one single haplotype each. These haplotypes were previously found in 2018 in Northern Italy. While sentinel egg masses proved to be very effective in tracking the arrival of exotic Trissolcus species, the collection of stink bug egg masses provided fundamental data on the plant host species. The results lend strong support to the adaptation of exotic Trissolcus species to the environmental conditions of the range of introduction, providing new information on plant host-associations, fundamental for the development of biological control programs.

An Insight into the Role of Trissolcus mitsukurii as Biological Control Agent of Halyomorpha halys in Northeastern Italy.

Sustainable strategies such as classical or augmentative biological control are currently being evaluated for the long-term management of the alien invasive pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). A three-year study carried out in northeastern Italy was performed to investigate the distribution and field performance of the H. halys egg parasitoid Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae), in comparison with other parasitoid species. In the study area, adventive populations of T. mitsukurii were present since 2016, representing the earliest detection of this species in Europe. Trissolcus mitsukurii was the most abundant parasitoid and showed a higher "parasitoid impact" (i.e., number of parasitized eggs over the total number of field-collected eggs) compared to the other species, i.e., Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae), Trissolcus basalis (Wollaston) and Trissolcus kozlovi Rjachovskij (Hymenoptera: Scelionidae). The hyperparasitoid Acroclisoides sinicus (Huang and Liao) (Hymenoptera: Pteromalidae) was also recorded. Phylogenetic analysis of T. mitsukurii population distinguished two clades, one covering samples from Italy, Japan and China, the other from South Korea. The present study provides promising results for the biological control of a pest that is having a dramatic impact on a wide range of crops worldwide.