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

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.

Aphids show interspecific and intraspecific variation in life history responses to host plant infection by the fungal pathogen Botrytis cinerea

“…There is increasing evidence showing that plant pathogens play important roles in determining the interaction between insects and their host plants, and indeed these effects can ramify through communities (Grunseich et al 2020;Srisakrapikoop et al 2020). In this study, we find that two aphid species respond in different directions to the same plant pathogen-host system.…”

“…Fungal plant pathogen infection can alter host plant quality as experienced by herbivores by inducing biochemical defense responses inside the host plant. These biochemical responses can also negatively affect herbivorous insects (Fernandez-Conradi et al 2018;Ederli et al 2021) and indeed could also affect species at higher trophic levels (Ngah et al 2018;Srisakrapikoop et al 2020). Nevertheless, the effect of plant pathogen infection might also benefit some insect herbivores (Tack & Dicke 2013), and herbivores could differ in their responses to host plants infected by different plant pathogens (e.g.…”

Does This Look Infected? Hidden Host Plant Infection by the Pathogen Botrytis cinerea Alters Interactions between Plants, Aphids and Their Natural Enemies in the Field

“…On the other hand, symptomatic and asymptomatic plants showed a similar effect in reducing the numbers of predatory insects compared to uninfected plants. While previous studies have found that symptomatic plant pathogen infection affects natural enemy foraging behaviour [71], our findings suggest that variation in plant quality resulting from either symptomatic or asymptomatic infection by B. cinerea influences the foraging behaviour of insect natural enemies [72][73][74][75].…”

Herbaria Reveal Herbivory and Pathogen Increases and Shifts in Senescence for Northeastern United States Maples Over 150 Years

“…Both insect and pathogen damage increased over the time period of the study, with leaf area removal associated with an increase in the probability of other pathogen damage on a specimen and vice versa (Table 2). Experimental studies have demonstrated that some insect herbivores can be attracted to diseased host plants if infection increases the nutritional quality of the plant or alters chemical defenses (Stout et al, 2006;Srisakrapikoop et al, 2020). Herbivory also causes wounding of plant foliar tissue, which can introduce microbial pathogens or cause further damage (Savatin et al, 2014).…”