Parasites disrupt a keystone mutualism that underpins the structure, functioning, and resilience of a coastal ecosystem

Abstract Parasites can alter the traits or densities of mutualistic partners, potentially destabilizing mutualistic associations that underpin the structure, functioning, and stability of entire ecosystems. Despite the potentially wide‐ranging consequences of such disruptions, no studies have directly manipulated parasite prevalence and/or intensity in a mutualistic partner, nor quantified the resulting community‐level effects. Here, we investigated the effects of a common trematode parasite ( Cercaria opaca ) on the strength of a keystone facultative mutualism in western Atlantic salt marshes between the foundational marsh cordgrass, Spartina alterniflora , and the ribbed mussel, Geukensia demissa . Cordgrass increases mussel survivorship and growth through shading, while mussels enhance cordgrass growth by producing nutrient‐rich biodeposits. This mutualistic association also creates conditions that enhance biodiversity and ecosystem functioning, and mediates the ability of foundational plants to resist and recover from extreme drought. We used lab and field assays to show how increasing infection with trematode metacercariae negatively influenced mussel biodeposit production, as well as the strength of mussel shells and byssal attachments. By conducting a field manipulation using experimentally infected mussels, we demonstrated that the mutualistic benefits of mussels to cordgrass growth decreased with increasing trematode infection intensity—a pattern likely generated by reduced mussel biodeposition and enhanced mortality. Additionally, increasing parasite loads in mussels led to predictable decreases in the abundances of benthic invertebrates, as well as in key ecosystem characteristics and process rates (i.e., redox potential and sediment accretion). Finally, a survey of five North Carolina salt marshes demonstrated that infection with C. opaca was most common in mussels in areas experiencing cordgrass die‐off due to drought, and that infection intensity decreased with distance from die‐off areas. Because the mussel–cordgrass mutualism underpins marsh ecosystem resilience to drought‐associated die‐off, our results suggest that parasitism may depress recovery from these disturbances. Although this is the first experimental demonstration of parasites indirectly altering community structure and functioning by undermining an ecologically influential mutualism, this type of relationship could be common in nature, given that parasites frequently infect influential mutualists.