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

Murray, Naomi1

Research facility: University of California, Davis
Published Oct 26, 2022; Updated Apr 02, 2024 on Dryad. https://doi.org/10.25338/B8805V

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Oct 26, 2022 version files 29.81 KB
Dec 06, 2022 version files 32.31 KB
Apr 02, 2024 version files 37.91 KB

Abstract

Infectious disease can be a key driver of 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 affected by wasting diseases that cause necrotic tissue lesions. These lesions could alter seagrass value as food, habitat, and mediators of ecosystem processes, though biotic influences on disease dynamics are still not well understood. We explored the role of one eelgrass herbivore in affecting the development of wasting disease.

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 a common eelgrass herbivore in affecting disease spread and growth using microcosm and mesocosm experiments. We further explored herbivore preference in a choice feeding trial, which was paired with chemical analysis of plant tissue and analyzed using a structural equation model.

While this herbivore facilitates the growth of new lesions among isolated leaves, on balance they reduce lesion severity by more than 50% in comparison to no-herbivore controls in field-realistic settings. This was likely because this herbivore strongly prefers to eat diseased rather than healthy tissue, consuming nearly twice as much lesion area in choice trials. This preference results 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.   Understanding such multi-species interactions in marine systems will advance our predictions of future disease states beyond current understanding, which focuses primarily on the influence of environmental change on pathogen outbreaks.