The influence of multiple environmental stressors on susceptibility to parasites: An experimental determination with oysters

Abstract

A large ‐scale field experiment was used to test whether exposure to a suite of potential environmental factors (flow speed, temperature, salinity, and low dissolved oxygen) influences the level of parasitic infection of the oyster Crassostrea virginica. The parasite was the protozoan Perkinsus marinus, which has decimated populations of oysters in estuaries of North America. The environmental factors were considered stressors because they influence the physiological condition of either the host or parasite. Between December 1994 and July 1995, flow speed, temperature, salinity, dissolved oxygen concentration (DO), Perkinsus infection, and mortality of oysters were monitored across 24 experimental oyster reefs in the Neuse River estuary, North Carolina. Eight reef treatments were created consisting of an orthogonal combination of three factors: water depth (3 m vs. 6 m deep), reef height (2 m vs. 1 m tall), and position on reef (base vs. crest). Principal component analysis revealed that there was clear separation of environmental factors among reefs and that a majority of the variation (96.2%) among treatments could be explained by two principal component axes (PCs): one (24.3% of variation explained) was formed by flow and the other (71.9% of variation explained) by temperature, salinity, and DO. Oysters with the highest proportion of individuals infected (prevalence), highest intensity of infection, and highest mortality were located at the base of reefs, where flow speeds and food quality were lowest and sedimentation rates highest. However, there was no significant effect of hydrographic conditions on Perkinsus infection or mortality of oysters, despite large differences in mean salinity, DO, and exposure to hypoxia ‐anoxia. Temperature did not vary among treatments. Correlation of disease responses (infection prevalence and intensity, and mortality) with the first two PCs showed that these response variables were significantly (and negatively) correlated with flow only. Oysters in low flow were hypothesized to have the greatest susceptibility to Perkinsus infection because of their poor physiological condition. The restoration of oyster reefs increases reef height and thus flow speeds (by elevating oysters higher above the boundary and by actively influencing flow), thereby reducing the negative effects of disease by restoring reef morphology to its natural size.