Ganaspis kimorum as a classical biological control agent for Drosophila suzukii: from laboratory studies to field assessments

Agriculture forms the foundation of human society, providing one of the few essential resources we really need in life, food. However, agricultural production faces constant threats from emerging pests. While globalization facilitates access to agricultural products worldwide, it also opens the door to the spread of new invasive pests, leading to significant economic losses. One of the most emblematic examples of such event, is given by the spotted wing Drosophila, Drosophila suzukii. Native from East Asia, this fly colonized three continents in less than a decade. Its ability to oviposit in ripening fruit causes severe damage to berry and stone fruit crops. Current management relies heavily on pesticides, but growing interest in sustainable solutions has spurred research into biological control agents (BCAs). Since native pupal parasitoids proved ineffective at controlling the pest below acceptable thresholds, research recently shifted toward larval parasitoids from its native range. With classical biological control gaining momentum, European countries and American states collaborated to identify the most suitable candidate for release, ultimately selecting the figitid wasp Ganaspis kimorum as a classical biological control agent. Prior to its release, extensive studies were conducted under quarantine conditions to evaluate its specificity, biology, and parasitization rate. However, key aspects regulating host-parasitoid communication and those requiring exposure to natural conditions in the introduction areas remained unexplored. The main objective of this thesis was to assess the efficacy of G. kimorum as classical biological control agent in the newly introduced area through comprehensive laboratory and field assessments. The first part of this work focused to evaluating BCA establishment and ecological interactions. Pre and post-release monitoring assessed establishment, recapture rates, and interactions with non-target species (Chapter 2). Results showed that G. kimorum successfully established in 50% of study sites, exhibited high specificity toward D. suzukii in ripening fruits and demonstrated the ability to survive the winter in some of the introduced habitats. Monitoring also revealed the abundant presence of the adventive larval parasitoid, Leptopilina japonica. Exposure in the field of G. kimorum-parasitized hosts showed that the BCA experiences significant competitive pressure, leading to an average 62% reduction in emergence, likely due to secondary infestation by Drosophila spp. and multiparasitism by Leptopilina spp (Chapter 3). To investigate overwintering dynamics, G. kimorum was exposed to variable temperature regimes across seven sites in Switzerland and Northern Italy (Chapter 4). Consecutive dissections conducted throughout the winter revealed that G. kimorum was diapausing as first larval instar (L1) residing within early pupal stage of D. suzukii. A coefficient of variation (CV) and degree day (DD) analysis confirmed this hypothesis, suggesting a lower thermal threshold (TL) for development of 9°C and an average post-diapause DD accumulation of 329±6. The parasitoids were able to overwinter in four out of the seven sites under study, and temperatures played a major role to regulate survival rates that ranged from 0.4 to 17.6%. Host-searching mechanisms of G. kimorum were investigated in both medium and short range (Chapters 5-7). Olfactometry and volatile organic compound (VOC) analyses showed that parasitoids attraction toward the host was time-dependent (Chapter 5). While G. kimorum females were attracted by host’s cuticular hydrocarbons present in fruits infested with young larvae, they were repelled by fermentation compounds found in older and deteriorated fruits. Vibrational assays revealed that D. suzukii larvae produce incidental vibrations in the form of a series of broad band pulses (frequency range of 0.1–2 kHz and amplitude range of 12.1- 946 µm/s) (Chapter 6). Behavioral assays suggested that G. kimorum uses these cues to detect larvae inside infested fruit (Chapter 7). When larvae were killed inside berries and vibrational cues were absent, oviposition behavior was significantly diminished, with extrusion and insertion times reduced by 54% and 78% respectively. The project also assessed G. kimorum’s integration into the agroecosystem. In particular we assessed its susceptibility to insecticides commonly used against D. suzukii (Chapters 8). Laboratory topical exposures showed that Spinosad and λ-cyhalothrin were the most toxic active ingredients, while Cyantraniliprole exhibited the least toxicity. Field residual exposures confirmed these findings, with Spinosad and Deltamethrin causing 92% mortality immediately after application compared to the 52% caused by Cyantraniliprole. In conclusion, this thesis confirmed the efficacy of G. kimorum as biological control agent of D. suzukii in its newly introduced area (Trentino-Alto Adige). Post-release studies demonstrated its ability to establish and persist in natural environments, with successful overwintering observed in several sites despite the challenges posed by low temperatures. However, this thesis also identifies significant biotic and abiotic stressors limiting its establishment, in particular interspecific competition and winter survival. Overall, these findings provide valuable insights for the ongoing classical biological control program and help refine future risk assessments.