Most plant viruses rely on vectors for transmission. Consequently, an understanding of virus-vector interactions is crucial to predict and mitigate large-scale viral outbreaks in agroecosystems. However, viruses and vectors interact in complex ecosystems. Non-vector community members may have significant impact on the success of both vector and pathogen; conversely, plant pathogens may have consequences for non-vector community members. Here, we present evidence of two-way interactions between a non-vector herbivore and a plant virus.
Peas, a commercial crop cultivated in eastern Washington, are attacked by the pea aphid, Acyrthosiphon pisum, which often transmits pea enation mosaic virus (PEMV). Peas are also defoliated by the pea leaf weevil, Sitona lineatus, a non-vector of PEMV.
To determine the effect of PEMV on S. lineatus, we recorded herbivory rates on PEMV-infected versus healthy plants from commercial fields. Greenhouses assays were conducted to determine how viral infection influences weevil feeding success and host selection.
We tested the influence of S. lineatus on PEMV by releasing PEMV-infected aphids into microcosm cages with/without weevils and measuring viral dispersal. In greenhouse assays, viral titer was measured in weevil-damaged and undamaged plants. Aphid fitness assays were also conducted to determine how weevils and PEMV may influence vector fitness.
Results/Conclusions
PEMV-infected plants experienced higher rates of weevil herbivory in commercial pea fields. Although infection did not influence weevil feeding success in single-plant assays, when presented with a choice weevils preferred to feed on infected plants.
In caged microcosms, PEMV dispersal was enhanced by the presence of weevils, despite the fact that weevils arrested vector movement. Weevil damage did not influence infection severity or inoculation success in plants challenged with PEMV. In single-plant assays, viruliferous aphid fitness was enhanced only when weevils were present. PEMV did not enhance vector fitness when weevils were absent from the system.
These results indicate that plant pathogens have wide-ranging impacts that extend beyond their vectors. By influencing the success and behavior of multiple feeding guilds, pathogens may induce broad shifts in community structure. Equally, community composition has implications for pathogens. Non-vector community members may indirectly influence pathogen spread by mediating the fitness and behavior of vector species. Consequently, we propose that a community-centric approach is necessary to understanding the dynamics of complex pathosystems.