Diel-cycling hypoxia is widespread in shallow portions of estuaries and lagoons, especially in systems with high nutrient loads resulting from human activities. Far less is known about the effects of this form of hypoxia than deeper-water seasonal or persistent low dissolved oxygen. We examined field patterns of diel-cycling hypoxia and used field and laboratory experiments to test its effects on acquisition and progression of Perkinsus marinus infections in the eastern oyster, Crassostrea virginica, as well as on oyster growth and filtration. P. marinus infections cause the disease known as Dermo, have been responsible for declines in oyster populations, and have limited success of oyster restoration efforts. The severity of diel-cycling hypoxia varied among shallow monitored sites in Chesapeake Bay, and average daily minimum dissolved oxygen was positively correlated with average daily minimum pH. In both field and laboratory experiments, diel-cycling hypoxia increased acquisition and progression of infections, with stronger results found for younger (1-year-old) than older (2-3-year-old) oysters, and more pronounced effects on both infections and growth found in the field than in the laboratory. Filtration by oysters was reduced during brief periods of exposure to severe hypoxia. This should have reduced exposure to waterborne P. marinus, and contributed to the negative relationship found between hypoxia frequency and oyster growth. Negative effects of hypoxia on the host immune response is, therefore, the likely mechanism leading to elevated infections in oysters exposed to hypoxia relative to control treatments. Because there is considerable spatial variation in the frequency and severity of hypoxia, diel-cycling hypoxia may contribute to landscape-level spatial variation in disease dynamics within and among estuarine systems.
Diel-cycling hypoxia co-occurs with diel-cycling pH in shallow waters that are typically considered as refuge from deep-water hypoxia and are, therefore, targeted for restoration. These areas also tend to be heavily impaired by eutrophication from nutrient over-enrichment which increases the occurrence and severity of hypoxia and pH cycles. We used laboratory experiments to investigate the effects of diel-cycling dissolved oxygen (DO) and co-varying diel-cycling pH on infections of Perkinsus spp. and hemocyte activity in the eastern oyster Crassostrea virginica. Perkinsus marinus is the protistan parasite that causes Dermo disease in oysters. Severe diel-cycling DO increased the acquisition and progression of Perkinsus infections during exposure, and had a legacy effect the next year. Diel-cycling pH did not significantly affect infection dynamics either on its own or in combination with diel-cycling DO. Diel-cycling DO and pH both individually and in conjunction stimulated hemocyte activity, although this stimulated activity may not be effective at preventing Perkinsus infection. The magnitude of cycling conditions is an important consideration when choosing restoration sites, as severe cycling may hinder the reestablishment of oysters by creating areas that serve as reservoirs for parasites that can infect nearby populations.
Acidification research has exploded in recent years, however, experiments testing effects of co-cycling hypoxia and pH on ecological and physiological processes are rare, despite the pervasiveness and potential importance of co-varying fluctuations in these parameters. Co-cycling dissolved oxygen (DO) and pH are difficult to precisely control, as gases used for manipulation influence both parameters. We successfully developed a LabVIEW TM -based system capable of monitoring and controlling co-varying DO and pH in raw seawater flow-through aquaria. Using feedback from Oxyguard DO probes and Honeywell ion sensitive field effect transistor Durafet pH sensors, our system controls ratios of nitrogen, oxygen, carbon dioxide, atmospheric air, and CO 2 -stripped air within a total gas flow rate through mass flow controllers, to achieve target co-cycling DO and pH values in five treatments. Our system performed well in two long-term experiments investigating effects of diel-cycling hypoxia and pH on eastern oyster (Crassostrea virginica) feeding, growth, fecundity, Perkinsus sp. (Dermo) infection dynamics and immune response. In our 2013 adult oyster experiment, the severe low DO treatment averaged only 0.04 mg L 21 higher than the 0.50 mg L 21 target, and the moderate hypoxia averaged only 0.05 mg L 21 higher than the 1.30 mg L 21 target over 48 d of cycles. Mean pH for the hypercapnia plateau was within 0.02 above the 7.00 target. In our 2013 spat experiment, daily minimum DO in the severe and moderate hypoxia treatments were both within 0.06 mg L 21 of the 0.50 and 1.3 mg L 21 targets, respectively; hypercapnia plateau pH values were within 0.01 of our 7.00 target.There is increasing interest in the combined effects of hypoxia (low dissolved oxygen [DO] concentrations) and acidification of estuaries and coastal waters where anthropogenic CO 2 emissions and nutrient loads potentially exacerbate natural diel, tidal, and seasonal cycles of DO and pH (Doney et al. 2009a,b;Duarte et al. 2013;Melzner et al. 2013). In shallow estuarine systems, the magnitude of diel fluctuations can be very large; DO can range from anoxia to supersaturation, and pH can vary by a full pH unit or more ( Fig.
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