Co-infection is linked to infection prevalence and intensity in oysters amidst high environmental and spatial variation

Co-infecting parasites modify infection outcomes in the wild. However, it is unclear how multiple environmental factors influence co-infection. The Chesapeake Bay metapopulation of the eastern oyster, Crassostrea virginica, provides an opportunity to test the importance of co-infection across heterogeneous environments because multiple parasites infect oysters across a broad salinity gradient. This study leverages Maryland and Virginia oyster monitoring for a large-scale survey of four co-infecting organisms, including two tissue parasites and two shell bio-eroding parasites. We diagnosed infection in 440 oysters across 16 paired harvested and unharvested reefs and tested the importance of co-infecting organisms for each parasite relative to environmental conditions, host traits, and marine spatial management. Microscopic visual methods were used to diagnose prevalence and intensity of tissue infections with Perkinsus marinus (the causative agent of dermo disease) and Haplosporidium nelsoni (the causative agent of MSX disease). Macroscopic visual methods were used to diagnose prevalence and intensity of shell infections with Cliona boring sponges and blister-inducing Polydora worms. For the three oyster parasites that were detected [H. nelsoni infections were absent in all oysters], salinity was the overall strongest predictor, corresponding to bay-wide patterns of parasite prevalence and/or intensity. Despite high environmental and spatial variation, co-infections corresponded to altered prevalence and/or intensity for all three oyster parasites. The correlational patterns suggest that P. marinus acts as a lynchpin in co-infection, as its intensity increased with Cliona sponge prevalence and P. marinus co-infection predicted higher Polydora blister intensity. Oyster shell height, reef habitat, and harvest status also predicted parasite prevalence and intensity, further reflecting the multivariate drivers of infections in this system. Unharvested reefs had greater vertical habitat structure and higher intensities of Cliona sponge infections, but no differences in the prevalence of any of the three parasites. Spatial patterns unexpectedly show that reef-level predictors of parasite patterns were more important than differences between tributaries. This correlational survey provides novel insights through the statistical relationships between the three oyster parasites, environmental conditions, host traits, and human resource management. New and more detailed scenarios are needed to expand disease ecological theory to encompass co-infection in anthropogenically impacted wildlife populations.