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

Abstract

Simple SummaryThe Brown Marmorated Stink Bug (BMSB), Halyomorpha halys, is an invasive polyphagous species that causes extensive damage to fruits and vegetable crops. Available chemical treatments and mechanical measures are often insufficient to keep this pest under control. In the last decade, the scientific community has made several efforts in order to identify and select suitable natural enemies to use in biological control program. Several native and exotic parasitoid species attacking H. halys eggs have been registered in the invaded countries. In this study, the distribution of these parasitoids was examined in Trentino-Alto Adige, in Northern Italy, by combining two different methods. The research revealed the presence of seven parasitoid and one hyperparasitoid species, which are present in different contexts and on several host plants. The most abundant species, Anastatus bifasciatus and Trissolcus mitsukurii, showed different patterns in distribution, with a higher presence of A. bifasciatus in urban areas and Tr. mitsukurii in orchards. Our results proved that H. halys natural enemies are adapted to the environmental conditions of the study area. The gathered data on the plant host-associations will support the development of future biological control programs.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.