Effects of Co-Varying Diel-Cycling Hypoxia and pH on Growth in the Juvenile Eastern Oyster, Crassostrea virginica.

Shallow water provides important habitat for many species, but also exposes these organisms to daily fluctuations in dissolved oxygen (DO) and pH caused by cycles in the balance between photosynthesis and respiration that can contribute to repeated, brief periods of hypoxia and low pH (caused by elevated pCO2). The amplitude of these cycles, and the severity and duration of hypoxia and hypercapnia that result, can be increased by eutrophication, and are predicted to worsen with climate change. We conducted laboratory experiments to test the effects of both diel-cycling and constant low DO and pH (elevated pCO2) on growth of the juvenile eastern oyster (Crassostrea virginica), an economically and ecologically important estuarine species. Severe diel-cycling hypoxia (to 0.5 mg O2 L-1) reduced shell growth in juvenile oysters, as did constant hypoxia (1.2 and 2.0 mg O2 L-1), although effects varied among experiments, oyster ages, and exposure durations. Diel-cycling pH reduced growth only in experiments in which calcite saturation state cycled to ≤0.10 and only during the initial weeks of these experiments. In other cases, cycling pH sometimes led to increased growth rates. Comparisons of treatment effects across multiple weeks of exposure, and during a longer post-experiment field deployment, indicated that juvenile oysters can acclimate to, and in some cases compensate for initial reductions in growth. As a result, some ecosystem services dependent on juvenile oyster growth rates may be preserved even under severe cycling hypoxia and pH.

Effects of air-exposure gradients on spatial infection patterns of Perkinsus marinus in the eastern oyster Crassostrea virginica.

Spatial distributions of species can be shaped by factors such as parasites, mortality, and reproduction, all of which may be influenced by differences in physical factors along environmental gradients. In nearshore tidal waters, an elevational gradient in aerial exposure during low tide can shape the spatial distributions of benthic marine organisms. The eastern oyster Crassostrea virginica is an ecologically and economically important species that can dominate both subtidal and intertidal habitats along the east coast of the USA. Our goal was to determine whether prevalence and intensity of Perkinsus marinus (the causative agent of Dermo disease) infections vary along intertidal to subtidal gradients during summer. We used (1) field experiments conducted at 4 sites in the Chesapeake Bay and a Virginia coastal bay, (2) a controlled air-exposure experiment, and (3) field surveys from 7 sites ranging from Maine to North Carolina to test for effects of tidal exposure on infection. Results from our field surveys suggested that high intertidal oysters tend to have higher infection prevalence than subtidal oysters, but there was no effect on infection intensity. Field experiments rarely yielded significant effects of tidal exposure on infection prevalence and intensity. Overall, our study shows that exposure to air may not be a strong driver of infection patterns in this host-parasite system.

Landscape-level variation in disease susceptibility related to shallow-water hypoxia.

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.

Evaluating ecosystem response to oyster restoration and nutrient load reduction with a multispecies bioenergetics model.

Many of the world's coastal ecosystems are impacted by multiple stressors each of which may be subject to different management strategies that may have overlapping or even conflicting objectives. Consequently, management results may be indirect and difficult to predict or observe. We developed a network simulation model intended specifically to examine ecosystem-level responses to management and applied this model to a comparison of nutrient load reduction and restoration of highly reduced stocks of bivalve suspension feeders (eastern oyster, Crassostrea virginica) in an estuarine ecosystem (Chesapeake Bay, USA). Model results suggest that a 50% reduction in nutrient inputs from the watershed will result in lower phytoplankton production in the spring and reduced delivery of organic material to the benthos that will limit spring and summer pelagic secondary production. The model predicts that low levels of oyster restoration will have no effect in the spring but does result in a reduction in phytoplankton standing stocks in the summer. Both actions have a negative effect on pelagic secondary production, but the predicted effect of oyster restoration is larger. The lower effect of oysters on phytoplankton is due to size-based differences in filtration efficiency and seasonality that result in maximum top-down grazer control of oysters at a time when the phytoplankton is already subject to heavy grazing. These results suggest that oyster restoration must be achieved at levels as much as 25-fold present biomass to have a meaningful effect on phytoplankton biomass and as much as 50-fold to achieve effects similar to a 50% nutrient load reduction. The unintended effect of oyster restoration at these levels on other consumers represents a trade-off to the desired effect of reversing eutrophication.

Ecosystem engineers in the pelagic realm: alteration of habitat by species ranging from microbes to jellyfish.

Ecosystem engineers are species that alter the physical environment in ways that create new habitat or change the suitability of existing habitats for themselves or other organisms. In marine systems, much of the focus has been on species such as corals, oysters, and macrophytes that add physical structure to the environment, but organisms ranging from microbes to jellyfish and finfish that reside in the water column of oceans, estuaries, and coastal seas alter the chemical and physical environment both within the water column and on the benthos. By causing hypoxia, changing light regimes, and influencing physical mixing, these organisms may have as strong an effect as species that fall more clearly within the classical category of ecosystem engineer. In addition, planktonic species, such as jellyfish, may indirectly alter the physical environment through predator-mediated landscape structure. By creating spatial patterns of habitats that vary in their rates of mortality due to predation, planktonic predators may control spatial patterns and abundances of species that are the direct creators or modifiers of physical habitat.

Hypoxia, nitrogen, and fisheries: integrating effects across local and global landscapes.

Anthropogenic nutrient enrichment and physical characteristics result in low dissolved oxygen concentrations (hypoxia) in estuaries and semienclosed seas throughout the world. Published research indicates that within and near oxygen-depleted waters, finfish and mobile macroinvertebrates experience negative effects that range from mortality to altered trophic interactions. Chronic exposure to hypoxia and fluctuating oxygen concentrations impair reproduction, immune responses, and growth. We present an analysis of hypoxia, nitrogen loadings, and fisheries landings in 30 estuaries and semien-closed seas worldwide. Our results suggest that hypoxia does not typically reduce systemwide fisheries landings below what would be predicted from nitrogen loadings, except where raw sewage is released or particularly sensitive species lose critical habitat. A number of compensatory mechanisms limit the translation of local-scale effects of hypoxia to the scale of the whole system. Hypoxia is, however, a serious environmental challenge that should be considered in fisheries management strategies and be a direct target of environmental restoration.

Interspecific Competition and the Abundance of Nest Sites: Factors Affecting Sexual Selection.

The abundance of suitable nest sites and competition with other species for such sites appears to affect the intensity of intersexual selection in Coryphopterus nicholsi, a temperate goby that is a protogynous hermaphrodite. Field manipulations demonstrated that, within a population, the proportion of males that breed, and therefore the intensity of sexual selection, depends on the number of suitable nest rocks. The abundance of nest sites may also affect the timing of sex change in this species. Collections from areas with many suitable nest sites contained a higher proportion of males than collections from areas with few suitable nest sites. Aggression among males probably determines which individuals within the population can monopolize a suitable nest site and therefore are able to mate as a male. Field observations indicated that aggressive interactions occur frequently and that the larger individual of an interacting pair almost inevitably chases off the smaller individual during aggressive encounters. In field collections, males guarding eggs averaged larger in size than males not guarding eggs, and large males guarded nest sites that were superior to those guarded by small males. Competitors, including a large fish and several invertebrates, monopolize rocks otherwise suitable for Coryphopterus' use and thereby limit the number and proportion of breeding males in the goby's population. Field and laboratory observations and experiments indicated that a larger fish, Porichthys notatus, displaces Coryphopterus from nest sites and prevents Coryphopterus from using many of the large rocks on the reef. Other animals, including encrusting invertebrates and sea urchins, may also reduce the suitability and availability of rocks as nest sites. Such competition for nest sites reduces the opportunity of breeding by small males and increases the number of mates per large breeding male. Interspecific competition should, therefore, increase selection for protogynous hermaphroditism in Coryphopterus by increasing the reproductive advantage of large over small males. I discuss the possibility that interspecific competition may be an important selective force in resource-based mating systems of other animals and present potential examples from the literature.

Development of a subtidal epibenthic community: factors affecting species composition and the mechanisms of succession.

Macroinvertebrate grazers and temporal variability were found to strongly influence species composition of communities that developed subtidally on plexiglas panels. On panels exposed to the naturally high densities of sea urchins and sea stars, only grazer-resistant algal crusts, a diatom/blue-green algal film and short-lived filamentous algae became abundant. On those panels protected from grazers, however, other algae and sessile invertebrates were also common. Both the effects of grazing and the abundance of individual taxa differed on panels immersed at different times of the year.Resident species also affected subsequent recruitment. Some colonists were found more frequently on panels with established communities than on recently immersed plates. Others became more abundant on younger than on older panels. Considerable small-scale spatial variation in the abundance of species was also found among panels within treatments and appeared to persist throughout the 13 months of the study.I suggest that since the interactions that determine which mechanisms are important in succession occur between individuals (generalized here to species), not between successional stages, factors such as those examined that can determine which species will interact, indirectly determine the mechnaisms that are important in the development of a community. Models that deal with interactions between successional stages may lack the detail neccessary to predict or explain changes in species composition in diverse communities.