Raspberry viruses manipulate the behaviour of their insect vectors

Abstract

AbstractMany insect herbivores and plant pathogens influence each other via plant‐mediated mechanisms. Although there is speculation that these interactions may be important in structuring terrestrial food webs, few studies have empirically demonstrated the mechanisms by which pathogens manipulate the behaviour of their insect vectors. We investigated how infection of red raspberry, Rubus idaeus L. (Rosaceae), with two viral pathogens, black raspberry necrosis virus (BRNV) and raspberry leaf mottle virus (RLMV), affected the behaviour of their vector, the large raspberry aphid, Amphorophora idaei Börner (Hemiptera: Aphididae: Macrosiphini). As semi‐persistently transmitted viruses, comparatively little is known about how such viruses affect vector biology. We also examined the effect of infection on plant volatile emissions and amino acid content, which could drive changes in aphid behaviour and performance. Virus‐infected plants were initially more attractive to the aphid and the insects remained on infected plants for 30 min, but were found equally on uninfected plants 12 h after inoculation. Twenty‐seven volatile compounds were identified. Two green leaf volatiles were emitted at higher concentrations by infected plants: (Z)‐3‐hexenyl acetate and 2‐hexenal. In dose‐response assays, (Z)‐3‐hexenyl acetate was attractive to the aphid at concentrations of 50 ng ml−1. When reared on infected plants, aphids took more than 3 days longer to reach adulthood compared with those on uninfected plants, although the number of offspring remained the same. Soluble amino acid (essential and non‐essential) concentrations in raspberry leaves increased more than two‐fold with virus infection. Amino acid composition was dominated by glutamate, accounting for 64 and 77% of the total in uninfected and infected leaves, respectively. Excessive glutamate may have underpinned the negative effects of viral infection on aphid performance. These results demonstrate the capacity of viruses to alter their host plant to manipulate vector behaviour, which may have evolved to be consistent with the transmission requirements of the virus.