Unraveling the Vibrational Communication of Halyomorpha halys and the Insecticidal Impact on its Key Parasitoid Trissolcus japonicus: Implications for Integrated Pest Management and Biological Control

Biological invasions are currently a growing phenomenon at the global scale, orchestrated by invasive alien species, which are deemed harmful both economically and ecologically. One notorious invasive insect pest is the brown marmorated stink bug, Halyomorpha halys, which is causing significant economic losses in crop quality in Europe and the United States of America. A peculiar aspect of pentatomids, and therefore of H. halys, is the ability to communicate through low-frequency vibrations transmitted along the substrate. The current control measures for H. halys within integrated pest management (IPM), include agronomic practices (e.g., net protection), biorational control (e.g., pheromonal/vibrational traps), biological control (i.e., releasing natural enemies), and chemical control (i.e., insecticides). However, for a successful IPM strategy for H. halys, the synergistic use of the last two control techniques is imperative. Although this pest is intensively studied, knowledge gaps are still present regarding the diel rhythm of its vibrational communication as well as its post-diapause biology, which could be crucial for the integrated management of this pest. For that reason, the effect of different temperature scenarios on the post-diapause signaling, motility, and survival of H. halys was investigated. The overwintered adults became active immediately after the termination of diapause at 25 oC but lived significantly less than those at 18 oC which took longer to be vibrationally active. At 10 oC no vibrational activity was detected, yet the highest survival level was found. These results provide a foundation for bioclimatic modeling of climate change effects on H. halys and insights into the use of vibrational playbacks for monitoring and mass trapping as control techniques. The diel pattern of vibrational communication of H. halys was studied in semi-field and laboratory conditions. The acquired knowledge on diel activity was then tested for sustainable control strategies by extending playback periods of bimodal (i.e., pheromones + vibrational playbacks) traps to 24 hours, and compared it to the base trap model (solar panel) and the control (no power supply). Interestingly, H. halys exhibited a diel vibrational calling pattern without significant differences in cumulative signaling durations between the photophase or the scotophase. Moreover, females were predominately active within nocturnal and adjacent diurnal hours. The adult captures from bimodal traps that were power-supplied for 24 hour periods were significantly higher compared to the other groups. This suggests that the nocturnal vibrational activity of H. halys could be exploited within IPM strategies. For that purpose, the activation of bimodal traps during the scotophase should not be disregarded. In relation to the synergy between chemical and biological control techniques, the impact of four insecticides and an adjuvant commonly used in hazelnut crops was assessed on Trissolcus japonicus, the main egg parasitoid of H. halys. The lethal effects on female parasitoids were investigated after exposure for 1, 6, and 24 hours to residues applied to Munger cells using a Potter spray tower to determine mortality levels. Additionally, sublethal effects were investigated in terms of reproduction, foraging behavior on host footprints, and circadian locomotor activity. The toxicity levels exhibited variation depending on the chemical group of the tested insecticides, with the highest mortality observed for nicotinic acetylcholine receptor modulators, whereas a proteobacterial insecticide caused the lowest mortality. Nonetheless, the latter caused the highest reproduction impairment. Moreover, the presumably inert adjuvant caused significant reduction in circadian locomotor activity which could be translated to serious implications for the success of parasitoid wasps in field conditions, such as a limited success in finding host egg masses and/or food sources. The results suggest that the absence of lethal effects from a specific insecticide does not preclude the occurrence of significant sublethal effects, such as reduced reproduction capacity or circadian locomotor activity. They also illustrate how sensor data acquisition and behavioral analysis software can be utilized to detect important sublethal effects in non-target minute parasitoids.