Vector-borne plant pathogens modify top-down and bottom-up effects on insect herbivores

Ecological theory predicts that host-plant traits affect herbivore population growth rates, which in turn modulates predator-prey interactions. However, while vector-borne plant pathogens often alter traits of both host plants and vectors, a few studies have assessed how pathogens may act as interaction modifiers within tri-trophic food webs. By applying a food web motif framework, we assessed how a vector-borne plant pathogen (Pea-enation mosaic virus, PEMV) modified both bottom-up (plant-herbivore) and top-down (predator-prey) interactions. Specifically, we assessed trophic interactions with PEMV-infectious Acyrthosiphon pisum (pea aphid) vectors compared to non-infectious aphids in a factorial experiment that manipulated predator and plant communities. We show that PEMV altered bi-trophic relationships, whereby on certain plant species, PEMV reduced vector performance but also increased their susceptibility to predators. However, on other plant species, PEMV weakened top-down control or increased vector performance. Our results suggest that vector-borne plant pathogens are important interaction modifiers for plant-herbivore-predator dynamics: host-plant response to viruses can decrease herbivore abundance by reducing herbivore performance, but also increase herbivore abundance by weakening top-down control. Broadly speaking, trophic interactions that regulate herbivore outbreaks appear to be modified for herbivores actively transmitting viruses to host plants. Consequently, management and monitoring of outbreaking herbivores should consider the infection status of focal populations.