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

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.