The majority of plant viruses are transmitted by insect vectors. These vectors interact with individuals of many species as they forage within food webs, although it remains unclear how multiple trophic interactions affect vector dispersal and virus spread. In the Palouse region of the Pacific Northwestern US, pea aphids are the primary vector of several plant viruses that infect wild and managed legumes (vetch, clover, pea, lentil). These pathogens, such as pea enation mosaic virus (PEMV), can devastate crop production and may impact populations of wild legume species. Within both managed and natural food webs, pea aphids interact with multiple legume host-plant species, competing herbivores, and predators. Our work seeks to characterize how interactions between aphid vectors other species across multiple trophic levels affects the spread of the PEMV pathogen. Specifically, we focused on pea aphid interactions with ladybird predators, weedy alternative host-plant species (common vetch), and a non-vector herbivore (pea leaf weevils). In a large-scale experiment with field-collected insects, we quantified effects of tri-trophic interactions on vector movement, population growth, and resulting impacts on the spread of PEMV through a host plant population.
Results/Conclusions
We observed three dominant indirect effects that contributed to the rate of spread of PEMV through a host population of pea plants. First, ladybird beetles suppressed total aphid abundance, which diminished aphid movement to new host plants. These natural enemies consequently reduced incidence of PEMV in plants. Second, alternative host-plant species (vetch) increased total aphid abundance, and increased dispersal to new host plants, leading to a higher incidence of PEMV. This effect occurred despite vetch being a poor host for aphids, because aphids rapidly dispersed off vetch, potentially reducing intraspecific competition. Third, pea leaf weevils dramatically increased plant susceptibility to this aphid-borne pathogen, even after accounting for bottom-up and top-down effects on aphid populations. Overall, the two most important contributors to increased spread of PEMV appear to be outbreaks of competing herbivores and the presence of weedy alternative hosts that facilitate aphid movement. Further work will examine if conservation biological control targeting ladybird beetles, weed control, and suppression of pea leaf weevils could become effective management strategies for reducing the impact of PEMV in dry pea crops.