Role of powdery mildew in the behavior of parasitoid: A case study using whiteflies and Encarsia formosa on tomato plants

The current study was conducted to assess the impact of powdery mildew (Oidium neolycopersici) on plant-non-vector herbivore-parasitoid interactions, e.g. tomato plants, whiteflies (Trialeurodes vaporariorum) and parasitoid (Encarsia formosa). Encarsia females were significantly less attracted to powdery mildew infected tomato plants (PM) than healthy plants (Con.). Thus parasitism rates of whiteflies (WF) were significantly lower on powdery mildew (PM) plants as compared to Con. plants (17.5:41.5%). These differences disappeared when E. formosa females were forced to parasitize whiteflies on either PM or Con. The performance of the parasitoid was not significantly influenced when developing on whiteflies feeding on powdery mildew infected plants. In olfactometer bioassays, either naïve or experienced parasitoids significantly preferred healthy plants colonised by whiteflies as compared to powdery mildew infected plants colonised by whitefly (PMWF) (30.0:10.0% for naïve parasitoids; 41.4:15.2% for experienced parasitoids). In wind tunnel bioassays, volatiles emitting from WFs significantly increased upwind oriented flight and landing in Encarsia targets as compared to any other treatments. Volatiles from Con, PM, PMWF and WF were collected and analyzed by GC and GC-MS, revealing that both qualities and quantities of volatile compounds differed to a large extend. Plants significantly increased volatile emission after being attacked by whiteflies (275.3 mol h−1) or infected by powdery mildew (267.58 mol h−1). However, plants significantly reduced volatile emissions in PMWF co-existing systems (80.58 mol h−1). Our results demonstrate that volatiles released by either herbivore damaged plants, pathogen diseased plants or combinations of these agents, respectively, may influence the foraging behavior of the parasitoids while searching for their hosts, resulting in reduced efficacies of parasitoids. This, in turn, may impact the outcome of biological control systems, especially in greenhouse conditions.