A mismatch in the emergence of Torymus sinensis may affect the effectiveness of this biocontrol agent?

Abstract

The biocontrol agent Torymus sinensis Kamijo is considered as one of the most successful examples of classical biological control programs. This parasitoid represented a feasible option to obtain sufficient, sustainable, and long-term control of the Asian chestnut gall wasp (ACGW), Dryocosmus kuriphilus Yasumatsu. Recently, an unusual presence of galls was recorded in a few chestnut orchards of Northern Italy, although T. sinensis was released in previous years. We hypothesized that the increase in infestation rate over the years was related to a mismatch in the parasitoid/host phenology, resulting in a decrease in biocontrol effectiveness. Investigations were performed in the five-year period 2018–2022 in six chestnut orchards, selected according to the ACGW infestation level, and divided in two categories: non-critical sites (negligible presence of ACGW galls) and critical sites (high presence of galls with suppression of bud growth). We evaluated T. sinensis’s parasitism rate and phenology by dissecting chestnut galls, comparing non-critical sites versus critical sites. Temperatures were monitored in all the orchards with data loggers. In non-critical sites the parasitism rate by T. sinensis was stable and/or growing in all years, accounting from 77% to 99% (i.e., total number of T. sinensis divided by total number of larval chambers). Conversely, the parasitism rate in critical sites experienced a severe decline, reaching values under 50% in all sites in 2021–2022. Specifically, parasitism on average was reduced by 44% when comparing 2019 versus 2022. The dissection of the galls recorded in non-critical sites in winter (February) highlighted that on average most T. sinensis were larvae and immature pupae (about 70%). Conversely, in critical sites most of the individuals were black mature pupae (76%), with presence of newly formed adults (12%). In 2019–2022, the mean temperature recorded in critical sites was 2.72 °C and 2.34 °C higher in January and February respectively, when compared to non-critical sites. Moreover, in critical sites the early emergence of the biocontrol agent (late February-early March) was recorded when current-year ACGW fresh galls were not available. No variation in the phenological cycle of the ACGW was ever observed, in all sites and years. Our results suggest that the asynchrony between T. sinensis and the ACGW heavily affected the role of the released agent in the suppression of the pest’s outbreaks. Future studies are needed to clarify whether this event is increasing in relevance, also in a climate change perspective.