The life histories of insect herbivores are affected by variation in host plant quality, with poor quality typically being associated with reduced herbivore fecundity, size and longevity. Plant pathogens are ubiquitous in nature and can alter host plant quality as experienced by insect herbivores. We asked how host plant infection by the widespread and economically important fungal pathogen Botrytis cinerea affected the life history traits of two aphid species. We found that the life history traits of the black bean aphid Aphis fabae were negatively affected by being reared on infected host plants, showing reduced fecundity, population growth rate, size, off-plant survival time and development rate. In contrast, we found that pea aphids Acyrthosiphon pisum benefitted from being reared on infected plants, and that the degree of benefit varied between pea aphid clonal lines. This work suggests that the ecological and economic consequences of plant pathogen infection on the dynamics of aphid pests could be difficult to predict.

Indirect effects are ubiquitous in nature, and have received much attention in terrestrial plant–insect herbivore–enemy systems. In such tritrophic systems, changes in plant quality can have consequential effects on the behavior and abundance of insect predators and parasitoids. Plant quality as perceived by insect herbivores may vary for a range of reasons, including because of infection by plant pathogens. However, plant diseases vary in their origin (viral, bacterial or fungal) and as a result may have differing effects on plant physiology. To investigate if the main groups of plant pathogens differ in their indirect effects on higher trophic levels, we performed a meta-analysis using 216 measured responses from 29 primary studies. There was no overall effect of plant pathogens on natural enemy traits as differences between pathogen types masked their effects. Infection by fungal plant pathogens showed indirect negative effects on the performance and preference of natural enemies via both chewing and piercing-sucking insect herbivore feeding guilds. Infection by bacterial plant pathogens had a positive effect on the natural enemies (parasitoids) of chewing herbivores. Infection by viral plant pathogens showed no clear effect, although parasitoid preference may be positively affected by their presence. It is important to note that given the limited volume of studies to date on such systems, this work should be considered exploratory. Plant pathogens are very common in nature, and tritrophic systems provide an elegant means to examine the consequences of indirect interactions in ecology. We suggest that further studies examining how plant pathogens affect higher trophic levels would be of considerable value.

Urbanization can change interactions in insect communities, and the few studies of tritrophic interactions in urban settings focus on interactions between plants, herbivorous insects and their mutualists and natural enemies. Plant pathogen infection is also widespread and common, and infection may also alter such interactions, but we have no understanding of whether the ecological consequences of pathogen infection vary with urbanization. Using replicated aphid colonies on experimental plants, we investigated how infection by the plant pathogen Botrytis cinerea influences interactions between plants, aphids and the aphid natural enemies and ant mutualists in highly urbanized, suburban and rural study sites. Aphid and natural enemy abundance were highest in the suburban site, while mutualist ants were most abundant in the urban site, reversing the usual positive density-dependent relationship between natural enemies and aphids. The effect of pathogen infection varied with trait and site, mediated by natural enemy preference for hosts or prey on uninfected plants. The effect of infection on aphid abundance was only seen in the suburban site, where natural enemies were most abundant on uninfected plants and aphid numbers were greatest on infected plants. In the urban site, there was no effect of infection, while in the rural site, aphid numbers were lower on infected plants. Uninfected plants were smaller than infected plants and differed between locations. This study suggests that the effects of urbanization on ecological interactions may become more complex and difficult to predict as we study ecological assemblages and communities at greater levels of structural complexity.

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