Herbivores can benefit both plants and their pathogens through selective herbivory on diseased tissue

Abstract

Abstract Infectious disease can shape community structure, particularly when pathogens affect foundation species. Seagrasses are foundation species that form meadows along coasts worldwide, controlling sediment deposition and biogeochemical cycling while supporting a diverse community of fish and invertebrates. These plants are hosts to wasting diseases that cause necrotic tissue lesions, which could alter seagrass value as food, habitat and mediators of ecosystem processes. However, such biotic interactions and influences on disease dynamics are still not well understood. We investigated whether a common herbivore affected the development of wasting disease on eelgrass. We measured the severity and prevalence of eelgrass wasting disease in a meadow across two summers through repeated field surveys. We assessed the role of the eelgrass herbivore on disease spread and growth using microcosm and mesocosm experiments. We further explored herbivore feeding preferences in a choice trial, which was paired with chemical analysis of plant tissue and analysed using a structural equation model. While the herbivore facilitates the growth of new disease lesions among isolated leaves, on balance they reduce lesion severity by more than 50% in comparison with no‐herbivore controls in field‐realistic settings. This was likely because the herbivore strongly prefers to eat diseased rather than healthy tissue, consuming nearly twice as much lesion area in choice trials. This preference arises from pathogen‐driven changes in the host plant; lesioned tissue requires less force to penetrate than non‐lesioned tissue. Additionally, as lesions increase in size, their polyphenolic concentrations drop, which further increases the magnitude of preference for lesioned tissue. Synthesis: These results suggest that these herbivores could help maintain disease in this system at a high prevalence (by facilitating disease development) but low severity (through preferential consumption), which is consistent with our field observations of nearly 100% prevalence and low severity in a natural bed where herbivore density is high. Describing such multi‐species interactions in marine systems will advance our predictions of future disease states, as current understandings focus primarily on how environmental change contributes to pathogen outbreaks.