Powdery mildew suppresses herbivore-induced plant volatiles and interferes with parasitoid attraction in Brassica rapa

The co-occurrence of different antagonists on a plant can greatly affect infochemicals with ecological consequences for higher trophic levels. Here we investigated how the presence of a plant pathogen, the powdery mildew Erysiphe cruciferarum, on Brassica rapa affects (1) plant volatiles emitted in response to damage by a specialist herbivore, Pieris brassicae; (2) the attraction of the parasitic wasp Cotesia glomerata and (3) the performance of P. brassicae and C. glomerata. Plant volatiles were significantly induced by herbivory in both healthy and mildew-infected plants, but were quantitatively 41% lower for mildew-infected plants compared to healthy plants. Parasitoids strongly preferred Pieris-infested plants to dually-infested (Pieris+mildew) plants, and preferred dually infested plants over only mildew-infected plants. The performance of P. brassicae was unaffected by powdery mildew, but C. glomerata cocoon mass was reduced when parasitized caterpillars developed on mildew-infected plants. Thus, avoidance of mildew-infested plants may be adaptive for C. glomerata parasitoids, whereas P. brassicae caterpillars may suffer less parasitism on mildew-infected plants in nature. From a pest management standpoint, the concurrent presence of multiple plant antagonists can affect the efficiency of specific natural enemies, which may in turn have a negative impact on the regulation of pest populations. The co-occurrence of different antagonists on a plant can have multitrophic consequences at the community level. Here we show that infection by a fungal pathogen, the powdery mildew Erysiphe cruciferarum, on Brassica rapa strongly reduces plant volatiles emitted in response to damage by the insect herbivore Pieris brassicae, and reduces plant attractiveness to the main natural enemy of P. brassicae, the parasitic wasp Cotesia glomerata. Herbivore performance was unaffected by the presence of powdery mildew, but parasitoid performance was negatively affected (decreased cocoon mass). From a pest management standpoint, the presence of powdery mildew on Brassica plants may affect the foraging efficiency of natural enemies, which may in turn have a negative impact on the regulation of pest populations.