Cucumber mosaic virus infection in squash influences interactions with non-vector herbivores and predators

Plant viruses are common in many plant communities, but the role of these organisms in modifying plant phenotype and insect dynamics is not well understood. Here we used a common non-persistently transmitted virus, Cucumber mosaic virus, to study the indirect effects of virus infection on the attraction and retention of herbivorous and predatory insects to cultivated squash (Cucurbita pepo cv. ‘Dixie’) in a central Pennsylvania agroecosystem. Cucumber mosaic virus has previously been shown to disrupt carbohydrate to amino acid ratios in non-vascular cells, reduce phloem nutrient levels, decrease plant size, and increase the emission of constitutive squash volatile cues. We found that virus infection reduces the likelihood of herbivorous insects arresting and feeding on plants. In particular, virus infection drastically reduced numbers of a damaging specialist squash herbivore (Anasa tristis) on plants in the field, and deterred oviposition in choice tests with healthy plants in the lab. This preference is likely driven by disruptions in taste cues rather than a reduced quality of the plant for this herbivore, since bugs developed at a similar rate on both infected and healthy plants in a growth assay. While virus infection resulted in reduced damage from herbivores, we also found that infection had little effect on visitation rates and the ability to locate prey (aphids) by predatory and parasitic insects. Our results demonstrate that virus infection is associated with reduced herbivore pressure, but that when herbivores are present (aphid prey), predators are just as effective at locating and foraging on virus-infected plants relative to healthy plants. These results indicate that plants infected with CMV may derive certain benefits from infection when herbivore pressure is high.