Assemblage of the egg parasitoids of the invasive stink bug Halyomorpha halys: insights on plant host associations

Authors: ZAPPONI, LIVIA - Fondazione Edmund Mach; BON, MARIE-CLAUDE - European Biological Control Laboratory (EBCL); FOUANI, JALAL MELHEM - Fondazione Edmund Mach; ANFORA, GIANFRANCO - Fondazione Edmund Mach; SCHMIDT, SILVIA - Research Centre For Agriculture And Forestry Laimburg; FALAGIARDA, MARTINA - Research Centre For Agriculture And Forestry Laimburg

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/27/2020
Publication Date: 9/1/2020
Citation: Zapponi, L., Bon, M., Fouani, J., Anfora, G., Schmidt, S., Falagiarda, M. 2020. Assemblage of the egg parasitoids of the invasive stink bug Halyomorpha halys: insights on plant host associations. Insects. 11(9), 588. https://doi.org/10.3390/insects11090588.
DOI: https://doi.org/10.3390/insects11090588

Interpretive Summary: The brown marmorated stink bug (BMSB), Halyomorpha halys, which originated in Asia, has spread during the last decade, particularly in the US and Italy in Europe. This pest attacks a wide variety of economically important tree fruits, vegetables, and field crops, and potentially impacts trophic interactions among beneficial native insects, including bugs and parasitoids. Recently, in two regions in northern Italy, two native parasitoids, Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) have been recovered. In Trentino-Alto Adige in northern Italy, another region where BMSB is expanding rapidly, the distribution of BMSB and of native and exotic egg parasitoids was extensively monitored. This study recorded a total of ten pentatomids including BMSB and eight egg parasitoids including T. mitsukurii and T. japonicus. BMSB egg masses were found on 41 host plant species, mainly maple trees and apple trees. 26% of BMSB egg masses were collected on sycamore maple, on which the highest number of parasitized egg masses were found, all egg parasitoids considered. T. mitsukurii showed the highest parasitism rate and was often found in agricultural areas on apple trees. DNA-based barcode analyses revealed that the T. japonicus and T. mitsukurii recovered in this region are similar to those previously found during 2018 surveys for BMSB egg parasitoids in other regions in Northern Italy. This study confirmed the remarkable adaptation of at least two native egg parasitoids of BMSB to the environmental conditions in Europe. This research enables a more comprehensive understanding of the association of BMSB with these parasitoids, the spread of which is anticipated to increase biological control of BMSB.

Technical Abstract: Halyomorpha halys (Stål) (Hemiptera Pentatomidae), (BMSB) is an invasive key agricultural pest of Asian origin. In Europe where the pest brought dramatic economic losses and biological control is considered to be the most effective long-term solution, two of its native egg parasitoids, Trissolcus japonicus Ashmead and Trissolcus mitsukurii Ashmead have been recently recovered. In Trentino-Alto Adige in Italy, an area where both the populations of BMSB and its parasitoids are expanding, we monitored the distribution of stink bugs including BMSB, and native and exotic egg parasitoids by searching for stink bug egg masses and exposing sentinel egg masses. We recorded ten pentatomids and eight parasitoid species, and we first reported the presence of T. japonicus in this area. Anastatus bifasciatus and T. mitsukurii were the dominant parasitoids, showing a different distribution in terms of context and host plants. BMSB egg masses were found on 41 host plant species, mainly maple trees and apple trees. 26% of BMSB egg masses were collected on Acer pseudoplatanus, on which the highest number of parasitized egg masses were found, all egg parasitoid species considered. T. mitsukurii showed the highest parasitism rate and was often found in agricultural areas on Malus domestica. The phenology of exotic parasitoids was delayed compared to native ones . Sequence analysis of 823 bp of the CO1 mitochondrial gene revealed that the recovered T. japonicus and T. mitsukurii harbored one single haplotype each. These haplotypes were previously evidenced during the 2018 surveys for BMSB egg parasitoids in Northern Italy. The study confirmed the remarkable adaptation of two exotic Trissolcus species to the environmental conditions in Europe, and provided new important information about trophic associations, which are fundamental for the development of biological control programs against BMSB.