Combining Irradiation and Biological Control against Brown Marmorated Stink Bug: Are Sterile Eggs a Suitable Substrate for the Egg Parasitoid Trissolcus japonicus?

The brown marmorated stink bug (BMSB), Halyomorpha halys, is a phytophagous invasive pest native to south-eastern Asia, and it is now distributed worldwide. This species is considered to be one of the most damaging insect pests in North America and in Europe. In agriculture, the predominant approach to managing BMSB is based on the use of insecticides, specifically pyrethroids and neonicotinoids. Unfortunately, the biology of the species and its facility to develop mechanisms of resistance to available pesticides has induced farmers and scientists to develop different, least-toxic, and more effective strategies of control. In a territorial area-wide approach, the use of a classical biological control program in combination with other least-toxic strategies has been given prominent consideration. Following exploratory surveys in the native range, attention has focused on Trissolcus japonicus, a small scelionid egg parasitoid wasp that is able to oviposit and complete its larval development in a single egg of H. halys. A common method for detecting egg parasitoids in the native range involves the placement of so-called 'sentinel' egg masses of the pest in the environment for a short period, which are then returned to the laboratory to determine if any of them are parasitized. Outside of the area of origin, the use of fertile sentinel eggs of the alien species may lead to the further release of the pest species; an alternative is to use sterile sentinel eggs to record the presence of new indigenous egg parasitoids or to detect the dispersal of alien species (in this case, T. japonicus) released in a new environment to control the target insect pest species. This study evaluated the performance of three types of sterile sentinel eggs as a suitable substrate for the oviposition and larval development of the egg parasitoid T. japonicus in a context of combining classical biological control with a Sterile Insect Technique (SIT) approach.

Orientus ishidae (Hemiptera: Cicadellidae): Biology, Direct Damage and Preliminary Studies on Apple Proliferation Infection in Apple Orchard.

The mosaic leafhopper, Orientus ishidae (Matsumura), is an Asian species widespread in Europe that can cause leaf damage in wild trees and transmit disease phytoplasmas to grapevines. Following an O. ishidae outbreak reported in 2019 in an apple orchard in northern Italy, the biology and damage caused by this species to apples were investigated during 2020 and 2021. Our studies included observations on the O. ishidae life cycle, leaf symptoms associated to its trophic activity, and its capability to acquire "Candidatus Phytoplasma mali," a causal agent of Apple Proliferation (AP). The results indicate that O. ishidae can complete the life cycle on apple trees. Nymphs emerged between May and June, and adults were present from early July to late October, with the peak of flight between July and early August. Semi-field observations allowed for an accurate description of leaf symptoms that appeared as a distinct yellowing after a one-day exposure. In field experiments, 23% of the leaves were found damaged. In addition, 16-18% of the collected leafhoppers were found carrying AP phytoplasma. We conclude that O. ishidae has the potential to be a new apple tree pest. However, further studies are required to better understand the economic impact of the infestations.

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.

Extending the vibroscape to agroecosystems: investigating the influence of abiotic factors and monitoring insect vibrational signaling.

Environmental conditions are crucial factors that influence communication systems and affect animal behavior. Research in the field of biotremology has improved our understanding of insect behavior, ecology, and evolution. However, the interactions between vibrational signaling and environmental factors are less studied, mainly because of technical issues faced in field trials. We therefore developed and tested an approach to investigate the effect of abiotic factors on insect vibrational signaling and explored its implementation as a monitoring tool for insect vibrational signals, using a vineyard as an agroecosystem model. Our results showed a significant decrease in insect signaling activity during unsuitable conditions of high temperature and wind velocity. We determined for the first time, the daily signaling pattern of the two insect pests, Scaphoideus titanus and Halyomorpha halys, in natural conditions. Biotremology techniques could be profitably used to monitor not only the presence of target pest species but also the biodiversity associated with vibrational signaling insects. In particular, the method implemented in this study could be used as a tool to compare the quality of cultivated areas under different management systems.

Attraction of Egg Parasitoids Trissolcus mitsukurii and Trissolcus japonicus to the chemical cues of Halyomorpha halys and Nezara viridula.

Trissolcus mitsukurii and Trissolcus japonicus are two Asian egg parasitoids associated with different pentatomids such as Halyomorpha halys. Adventive populations of T. mitsukurii were found in Northern Italy, suggesting its employment as a biological control agent (BCA) against H. halys. Nevertheless, to reduce the latter's population, T. japonicus was released in Italy. Releasing an exotic parasitoid requires investigating the interaction between the BCA and the environment to avoid negative impacts on the entomofauna of the new habitat. Trissolcus mitsukurii is mainly associated with Nezara viridula in its native area. Therefore, we investigated and compared the ability of female T. mitsukurii and T. japonicus to distinguish between naturally released cues of H. halys and N. viridula. A single parasitoid was exposed to contact kairomones of both pests to evaluate its modifications in orthokinetic and locomotory behaviour. The behaviour of female T. mitsukurii was also tested on synthetic compounds simulating the cues of the two pentatomids. When naturally released cues were used, T. japonicus preferred the traces of H. halys, while T. mitsukurii preferred N. viridula's cues. Moreover, the attraction of T. mitsukurii to N. viridula's cues was confirmed with synthetic cues. Additional studies are needed to judge if this parasitoid can be used as a BCA.

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.