Virus infection decreases the attractiveness of white clover plants for a non-vectoring herbivore.

Tamara Van Molken,Josef F Stuefer,Cornelis A Hordijk,Hannie De Caluwe,Tjeerd A L Snoeren,Nicole M Van Dam,Antonio Leon-Reyes

doi:10.1007/s00442-012-2322-z

Abstract

Plant pathogens and insect herbivores are prone to share hosts under natural conditions. Consequently, pathogen-induced changes in the host plant can affect herbivory, and vice versa. Even though plant viruses are ubiquitous in the field, little is known about plant-mediated interactions between viruses and non-vectoring herbivores. We investigated the effects of virus infection on subsequent infestation by a non-vectoring herbivore in a natural genotype of Trifolium repens (white clover). We tested whether infection with White clover mosaic virus (WClMV) alters (1) the effects of fungus gnat feeding on plant growth, (2) the attractiveness of white clover for adult fungus gnat females, and (3) the volatile emission of white clover plants. We observed only marginal effects of WClMV infection on the interaction between fungus gnat larvae and white clover. However, adult fungus gnat females clearly preferred non-infected over WClMV-infected plants. Non-infected and virus-infected plants could easily be discriminated based on their volatile blends, suggesting that the preference of fungus gnats for non-infected plants may be mediated by virus-induced changes in volatile emissions. The compound β-caryophyllene was exclusively detected in the headspace of virus-infected plants and may hence be particularly important for the preference of fungus gnat females. Our results demonstrate that WClMV infection can decrease the attractiveness of white clover plants for fungus gnat females. This suggests that virus infections may contribute to protecting their hosts by decreasing herbivore infestation rates. Consequently, it is conceivable that viruses play a more beneficial role in plant–herbivore interactions than generally thought.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-012-2322-z) contains supplementary material, which is available to authorized users.

Highlights

Under natural conditions, plants are likely to be exposed to simultaneous attacks by pathogens and insect herbivores
We determined whether White clover mosaic virus (WClMV) infection alters the attractiveness of T. repens to adult fungus gnats. This may be Herbivorous insects can effectively discriminate between different bouquets of volatile organic compounds (VOCs; Smart and Blight 1997; Mewis et al 2002; Quiroz et al 2005; van Dam 2009), and chemical cues are predominantly responsible for the selection of oviposition sites by female herbivores (Renwick 1989)
In Trifolium repens, WClMV decreases the attractiveness of the host plant for adult fungus gnat females

Summary

Introduction

Plants are likely to be exposed to simultaneous attacks by pathogens and insect herbivores. Previous greenhouse studies have provided circumstantial evidence for interactive effects of WClMV and larvae of non-vectoring fungus gnats (Bradysia sp.; Fig. 1c) on the growth of T. repens plants (Van Molken, unpublished results). Herbivorous insects can effectively discriminate between different bouquets of volatile organic compounds (VOCs; Smart and Blight 1997; Mewis et al 2002; Quiroz et al 2005; van Dam 2009), and chemical cues are predominantly responsible for the selection of oviposition sites by female herbivores (Renwick 1989) The results of these experiments provide information about the possible influence of virus infections on the interaction between a non-vectoring insect herbivore and a non-crop plant species suggesting that, under certain conditions, host plants may indirectly benefit from virus infections (Roossinck 2011)

Materials and methods

10 Control

Findings

Discussion