Foraging behavior of Ganaspis brasiliensis in response to temporal dynamics of volatile release by the fruit–Drosophila suzukii complex

The lineage G1 of Ganaspis brasiliensis is a larval parasitoid of the worldwide pest Drosophila suzukii and one of its most effective natural enemies in the native area. Because of its high degree of host specificity, G. brasiliensis G1 is considered a suitable species for introduction in areas invaded by D. suzukii following a classical biological control approach. Indeed, the release of the parasitoid is currently implemented in the USA and Italy. G1 females attack only host larvae developing in ripening fresh fruits on the plant and not larvae that develop in decaying fruits. To date, virtually no information is available on the cues regulating the foraging behavior of G1. In this study, we therefore aimed to find out whether chemical cues are exploited by G1 females to: (i) locate host fruits; (ii) locate suitable host larvae within infested fruit; (iii) discriminate between infested fresh fruits and infested rotting ones. We used a model system composed of blueberries and D. suzukii tested in two-choice olfactometer bioassays (with D. suzukii-infested fruits, healthy fruits, and pure air as odor targets), followed by the collection and the characterization of volatile organic compounds (VOCs) released by the tested targets. The results showed a clear time-dependent choice made by G1 females of infested versus healthy fruits related to the concomitant development of D. suzukii larvae and fruit degradation. Attraction to infested fruits was recorded during the early stages of infestation, followed by a repellent phase coinciding with fruits largely degraded by larval feeding. We found that the attractiveness of G. brasiliensis G1 towards fruits infested by young larvae was associated with the detection of VOCs released by the infested blueberries, and host’s cuticular hydrocarbons. Conversely, the repellence of older and deteriorated fruits hosting developed D. suzukii larvae was associated with the detection of a fermentation compound produced by microorganisms likely carried inside the fruit by the flies. The response of G1 females to the temporal dynamics of chemical cues emitted by the fruit–host larvae complex was consistent with the high degree of specificity of the parasitoid towards the ripening host fruits and towards D. suzukii.