Virus infection influences host plant interactions with non‐vector herbivores and predators

Abstract

Summary Viruses are widespread in both natural and agricultural plant communities and can significantly alter diverse traits of their host plants that mediate key interactions with other organisms. Yet, the impacts of plant viruses on broader community dynamics remain little studied. Here, we explore the effects of Cucumber mosaic virus, a common non‐persistently transmitted plant virus, on short‐ and long‐term interactions of herbivorous and predatory insects with squash (Cucurbita pepo) plants in a weedy field setting, as well as virus‐induced changes in plant phenotypes that mediate these interactions. Cucumber mosaic virus has previously been shown to have numerous effects on host plants that likely influence interactions with arthropods, including reduced plant size, increased volatile emissions, and diminished plant quality and palatability for aphid vectors. Infection reduced the likelihood of many herbivorous insects arresting and feeding on plants, as well as the apparency of plants to herbivores that base in‐flight foraging on visual cues. In particular, infection drastically reduced numbers of a specialist squash herbivore (Anasa tristis) on plants in the field – a pattern likely driven by a reduction of phagostimulatory sugar levels in leaf tissue and concurrent increase in amino acid levels, as nymphal development was not obviously impacted by infection status. Relative to effects on herbivores, virus infection had little impact on the ability of predatory insects to locate aphid prey, although an experiment examining plant visitation in the absence of aphids revealed reduced numbers of foraging Syrphidae (Diptera) and Coccinellidae (Coleoptera) on infected plants but increased visitation and oviposition by Chrysopidae (Neuroptera). CMV infection may reduce overall herbivore pressure on infected plants through effects on palatability and apparency, yet predators appear to locate herbivorous prey that do occur on infected plants as efficiently as those on healthy plants. Virus infection can significantly influence plant interactions with the insect community (including non‐vector as well as vector insects) with potential implications both for disease spread and for broader community dynamics.