Many herbivorous insects die of pathogen infections, though the role of plant traits in promoting the persistence of these pathogens as an indirect interaction is poorly understood. We tested whether winter leaf retention of bush lupines (Lupinus arboreus) promotes the persistence of nucleopolyhedroviruses, thereby increasing the infection risk of caterpillars (Arctia virginalis) feeding on the foliage during spring. We also investigated whether winter leaf retention reduces viral exposure of younger caterpillars that live on the ground, as leaf retention prevents contaminated leaves from reaching the ground. We surveyed winter leaf retention of 248 lupine bush canopies across twelve sites and examined how it related to caterpillar infection risk, herbivory, and inflorescence density. We also manipulated the amount of lupine litter available to young caterpillars in a feeding experiment to emulate litterfall exposure in the field. Greater retention of contaminated leaves from the previous season increased infection rates of caterpillars in early spring. Higher infection rates reduced herbivory and increased plant inflorescence density by summer. Young caterpillars exposed to less litterfall were more likely to starve to death but less likely to die from infection, further suggesting foliage-mediated exposure to virus. We speculate that longer leaf life span may be an unrecognized trait that indirectly mediates top-down control of herbivores by facilitating epizootics.

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