Meta-Analysis Suggests Differing Indirect Effects of Viral, Bacterial, and Fungal Plant Pathogens on the Natural Enemies of Insect Herbivores

SIMPLE SUMMARY: Plants suffer from disease, caused by fungal, bacterial and viral pathogens. Some insect herbivores avoid diseased plants, while others are attracted to them, often depending on how infection changes the quality of the plant. In turn, the herbivores are attacked by enemies, such as insect predators and parasitoids. Few studies have investigated how plant pathogens affect the herbivores’ insect natural enemies. Using a statistical technique called meta-analysis, we examined 216 measured responses from 29 studies, to see if we could find any patterns. The effect on natural enemies depended on the cause of the disease and type of natural enemy. Fungal pathogens had negative effects on the preference and performance of insect natural enemies, mainly through the disease reducing the quality of their insect herbivore prey. Bacterial pathogens had a positive effect on insect natural enemies, possibly caused by changes in host plant traits. We found no clear effect with viral diseases. We show that the causes of plant disease may have very different effects on ecological interactions between insect herbivores and their enemies, particularly parasitic wasps. This will help us understand how disease can change the patterns of interactions between species in natural and agricultural ecosystems. ABSTRACT: 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.