The Effects of Parasites on Coastal Marsh Ecosystem Structure and Functioning

Abstract

Recent experiments and comparative surveys in Southern US salt marshes revealed that a common larval trematode parasite, Parorchis acanthus, generated a trophic cascade that protected foundational marsh plants (Spartina alterniflora) from drought-associated overgrazing by suppressing the per capita grazing impacts of its host, the marsh periwinkle (Littoraria irrorata). While it is clear that parasites can play a positive role in mediating marsh ecosystem response to disturbance, there is still little known about the context dependency of this interaction, the role of definitive avian hosts in regulating parasite prevalence, and whether other commonly-occurring parasites may also modify processes that underpin ecosystem stability. The purpose of this project was to extend the current understanding of the roles played by parasites and their hosts in mediating marsh ecosystem stability. A field manipulation of Littoraria density in which infection prevalence with Parorchis acanthus was held at a constant value revealed that these parasites yielded positive impacts on Spartina aboveground biomass at middling densities of snails, but the positive effects of parasites were negligible at both low, and high snail densities. Surveys of drought-impacted marshes revealed that birds – the definitive hosts for trematode that infect Littoraria – congregated within die-off areas and that increased bird usage of die-off areas was associated with increased trematode parasitism in snails within grazer fronts, decreased per capita grazing rates of snails, and proportionate decreases in ecosystem die-off rate. Multi-site bird exclusion and mechanistic field studies experimentally confirmed that birds increased ecosystem resistance to drought-driven die-off by acting as the dispersive vectors for parasites that suppress Littoraria grazing. Finally, we explored how the trematode Cercaria opaca in ribbed mussels (Geukensia demissa) influenced the facultative mutualism between Guekensia and Spartina – an interaction that underlies marsh ecosystem resilience to drought-associated die-off. A field manipulation using experimentally infected mussels revealed that mutualistic benefits to Spartina decreased with increasing infection intensity in mussels. Subsequent mechanistic experiments demonstrated that increasing infection with C. opaca decreased mussel biodeposit production, the functional trait underlying mutualistic benefits to Spartina. Additionally, increasing parasite load was associated with decreased strength of both shells and byssal attachments, potentially explaining the relatively higher predation on heavily infected mussels in our field study. A survey of five North Carolina salt marshes revealed that infection intensity in mussels increased with proximity to die-off areas, indicating that C. opaca could influence marsh recovery following die-off events. Taken together, these results underscore the importance of parasitism’s influence on Southern salt marsh ecosystem stability and more generally show that parasites can be major arbiters of community structure and functioning.