Hybridization and adaptive introgression in a marine invasive species in native habitats.

Hybridization of distinct populations or species is an important evolutionary driving force. For invasive species, hybridization can enhance their competitive advantage as a source of adaptive novelty by introgression of selectively favored alleles. Using single-nucleotide polymorphism (SNP) microarrays we assess genetic diversity and population structure in the invasive ctenophore Mnemiopsis leidyi in native habitats. Hybrids are present at the distribution border of two lineages, especially in highly fluctuating environments including very low salinities, while hybrids occur at lower frequency in stable high-saline habitats. Analyses of hybridization status suggest that hybrids thriving in variable environments are selected for, while they are selected against in stable habitats. Translocation of hybrids might accelerate invasion success in non-native habitats. This could be especially relevant for M. leidyi as low salinity limits its invasion range in western Eurasia. Although hybridization status is currently disregarded, it could determine high-risk areas where ballast water exchange should be prevented.

Legacy of past exposure to hypoxia and warming regulates an ecosystem service provided by oysters.

Climate change is having substantial impacts on organism fitness and ability to deliver critical ecosystem services, but these effects are often examined only in response to current environments. Past exposure to stress can also affect individuals via carryover effects, and whether these effects scale from individuals to influence ecosystem function and services is unknown. We explored within-generation carryover effects of two coastal climate change stressors-hypoxia and warming-on oyster (Crassostrea virginica) growth and nitrogen bioassimilation, an important ecosystem service. Oysters were exposed to a factorial combination of two temperature and two diel-cycling dissolved oxygen treatments at 3-months-old and again 1 year later. Carryover effects of hypoxia and warming influenced oyster growth and nitrogen storage in complex and context-dependent ways. When operating, carryover effects of single stressors generally reduced oyster nitrogen bioassimilation and relative investment in tissue versus shell growth, particularly in warm environments, while early life exposure to multiple stressors generally allowed oysters to perform as well as control oysters. When extrapolated to the reef scale, carryover effects decreased nitrogen stored by modeled oyster reefs in most conditions, with reductions as large as 41%, a substantial decline in a critical ecosystem service. In some scenarios, however, carryover effects increased nitrogen storage by modeled oyster reefs, again highlighting the complexity of these effects. Hence, even brief exposure to climate change stressors early in life may have persistent effects on an ecosystem service 1 year later. Our results show for the first time that within-generation carryover effects on individual phenotypes can impact processes at the ecosystem scale and may therefore be an overlooked factor determining ecosystem service delivery in response to anthropogenic change.

Context-dependent carryover effects of hypoxia and warming in a coastal ecosystem engineer.

Organisms are increasingly likely to be exposed to multiple stressors repeatedly across ontogeny as climate change and other anthropogenic stressors intensify. Early life stages can be particularly sensitive to environmental stress, such that experiences early in life can "carry over" to have long-term effects on organism fitness. Despite the potential importance of these within-generation carryover effects, we have little understanding of how they vary across ecological contexts, particularly when organisms are re-exposed to the same stressors later in life. In coastal marine systems, anthropogenic nutrients and warming water temperatures are reducing average dissolved oxygen (DO) concentrations while also increasing the severity of naturally occurring daily fluctuations in DO. Combined effects of warming and diel-cycling DO can strongly affect the fitness and survival of coastal organisms, including the eastern oyster (Crassostrea virginica), a critical ecosystem engineer and fishery species. However, whether early life exposure to hypoxia and warming affects oysters' subsequent response to these stressors is unknown. Using a multiphase laboratory experiment, we explored how early life exposure to diel-cycling hypoxia and warming affected oyster growth when oysters were exposed to these same stressors 8 weeks later. We found strong, interactive effects of early life exposure to diel-cycling hypoxia and warming on oyster tissue : shell growth, and these effects were context-dependent, only manifesting when oysters were exposed to these stressors again two months later. This change in energy allocation based on early life stress exposure may have important impacts on oyster fitness. Exposure to hypoxia and warming also influenced oyster tissue and shell growth, but only later in life. Our results show that organisms' responses to current stress can be strongly shaped by their previous stress exposure, and that context-dependent carryover effects may influence the fitness, production, and restoration of species of management concern, particularly for sessile species such as oysters.

Declining oxygen in the global ocean and coastal waters.

Oxygen is fundamental to life. Not only is it essential for the survival of individual animals, but it regulates global cycles of major nutrients and carbon. The oxygen content of the open ocean and coastal waters has been declining for at least the past half-century, largely because of human activities that have increased global temperatures and nutrients discharged to coastal waters. These changes have accelerated consumption of oxygen by microbial respiration, reduced solubility of oxygen in water, and reduced the rate of oxygen resupply from the atmosphere to the ocean interior, with a wide range of biological and ecological consequences. Further research is needed to understand and predict long-term, global- and regional-scale oxygen changes and their effects on marine and estuarine fisheries and ecosystems.

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.

Millennial-scale sustainability of the Chesapeake Bay Native American oyster fishery.

Estuaries around the world are in a state of decline following decades or more of overfishing, pollution, and climate change. Oysters (Ostreidae), ecosystem engineers in many estuaries, influence water quality, construct habitat, and provide food for humans and wildlife. In North America's Chesapeake Bay, once-thriving eastern oyster (Crassostrea virginica) populations have declined dramatically, making their restoration and conservation extremely challenging. Here we present data on oyster size and human harvest from Chesapeake Bay archaeological sites spanning ∼3,500 y of Native American, colonial, and historical occupation. We compare oysters from archaeological sites with Pleistocene oyster reefs that existed before human harvest, modern oyster reefs, and other records of human oyster harvest from around the world. Native American fisheries were focused on nearshore oysters and were likely harvested at a rate that was sustainable over centuries to millennia, despite changing Holocene climatic conditions and sea-level rise. These data document resilience in oyster populations under long-term Native American harvest, sea-level rise, and climate change; provide context for managing modern oyster fisheries in the Chesapeake Bay and elsewhere around the world; and demonstrate an interdisciplinary approach that can be applied broadly to other fisheries.

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.

Human-induced marine ecological degradation: micropaleontological perspectives.

We analyzed published downcore microfossil records from 150 studies and reinterpreted them from an ecological degradation perspective to address the following critical but still imperfectly answered questions: (1) How is the timing of human-induced degradation of marine ecosystems different among regions? (2) What are the dominant causes of human-induced marine ecological degradation? (3) How can we better document natural variability and thereby avoid the problem of shifting baselines of comparison as degradation progresses over time? The results indicated that: (1) ecological degradation in marine systems began significantly earlier in Europe and North America (∼1800s) compared with Asia (post-1900) due to earlier industrialization in European and North American countries, (2) ecological degradation accelerated globally in the late 20th century due to post-World War II economic growth, (3) recovery from the degraded state in late 20th century following various restoration efforts and environmental regulations occurred only in limited localities. Although complex in detail, typical signs of ecological degradation were diversity decline, dramatic changes in total abundance, decrease in benthic and/or sensitive species, and increase in planktic, resistant, toxic, and/or introduced species. The predominant cause of degradation detected in these microfossil records was nutrient enrichment and the resulting symptoms of eutrophication, including hypoxia. Other causes also played considerable roles in some areas, including severe metal pollution around mining sites, water acidification by acidic wastewater, and salinity changes from construction of causeways, dikes, and channels, deforestation, and land clearance. Microfossils enable reconstruction of the ecological history of the past 10(2)-10(3) years or even more, and, in conjunction with statistical modeling approaches using independent proxy records of climate and human-induced environmental changes, future research will enable workers to better address Shifting Baseline Syndrome and separate anthropogenic impacts from background natural variability.

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.