This project was unique in its multidisciplinary and comprehensive ‘One Health’ approach – integrating marine ecologists, oceanographers, epidemiologists, molecular biologists, modelers, and parasitologists to investigate the ecology of zoonotic pathogens in the marine environment. Our goal was to develop a mechanistic understanding of the marine transmission dynamics of Toxoplasma gondii, an important cause of parasitic disease in marine mammals, particularly Southern sea otters (Photo 1), and humans. We investigated a novel paradigm and showed that although California sea lions (Photo 2) shed T. gondii-like oocysts in their feces, these oocysts were molecularly distinct, previously unrecognized coccidian parasites. Therefore, evidence to date confirms that wild and domestic felids are the only known definitive hosts of T. gondii. Our molecular surveillance of 959 wild-caught mussels demonstrated higher than previously reported T. gondii contamination of California coastlines as well as novel strains of the parasite (Photo 3). Epidemiological field investigations coupled with laboratory transport experiments showed that the distribution of oocysts in marine habitats is a function of oocyst loading from domestic and wild felids via freshwater run-off (Photo 4: Coastal freshwater run-off) and oocyst transport dynamics that are governed by association with aggregates (marine snow) and sticky polymers. Particle aggregation affects both the spatial distribution and bioavailability of oocysts to invertebrates that can serve as a source of infection for marine mammals and potentially humans. In addition to being incorporated in aggregates, T. gondii (and potentially other pathogens) adhere to sticky polysaccharides, called excreted polymeric substances (EPS) that enhance their association with sinking aggregates and incorporation into biofilms (Photo 5). Gelatinous polymers including EPS are fundamental to biophysical processes in aquatic habitats, including mediating aggregation processes and functioning as the matrix of biofilms. The ramifications of our findings extend the role of aquatic polymers in oceanic processes and show that invisible colloids, biofilms and food webs play an important role in disease ecology in marine environments. We further demonstrated that EPS facilitate the acquisition, concentration, and retention of T. gondii by kelp-grazing snails, which can transmit T. gondii to threatened southern sea otters.  Freshwater sources that may transport pathogens to coastal waters are often delivered to piers, coral reefs, kelp beds, and tide pools – habitats known to contain rich EPS-producing biota. Thus, coastal waters that receive contaminated runoff may also contain high levels of polymers that could mediate critical disease transmission mechanisms, including the spatial distribution and fate of terrestrial pathogens in nearshore habitats. Finally, our refined understanding of T. gondii oocyst transport dynamics facilitated an unprecedented modeling effort that links space-time patterns in pathogen distributions and otter movement, yielding a mechanism-based estimate of otter disease risk that can be compared with epidemiologically established risk patterns. This achievement will aid future research and relevant stake holders by making more accurate projections of how disease risk may change due to alterations in watershed pollutant loading, climate variability, land use, estuarine habitat quality, kelp forest dynamics, and coastal ocean circulation. Overall, findings from this project benefit the threatened southern sea otter population, which is struggling to recover, as well as other marine mammals and humans sharing the coastal environment.

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