Assessment of treatment-specific tethering survival bias for the juvenile blue crab Callinectes sapidus in a simulated salt marsh.

The blue crab (Callinectes sapidus) is ecologically and economically important in Chesapeake Bay. Nursery habitats, such as seagrass beds, disproportionately contribute individuals to the adult segment of populations. Salt marshes dominated by smooth cordgrass Spartina alterniflora are intertidal nursery habitats which may serve as a refuge from predation for juvenile blue crabs. However, the effects of various characteristics of salt marshes on nursery metrics, such as survival, have not been quantified. Comparisons of juvenile survival between salt marshes and other habitats often employ tethering to assess survival. Although experimental bias when tethering juvenile prey is well recognized, the potential for habitat-specific bias in salt marshes has not been experimentally tested. Using short-term mesocosm predation experiments, we tested if tethering in simulated salt marsh habitats produces a habitat-specific bias. Juvenile crabs were tethered or un-tethered and randomly allocated to mesocosms at varying simulated shoot densities and unstructured sand. Tethering reduced survival, and its effect was not habitat specific, irrespective of shoot density, as evidenced by a non-significant interaction effect between tethering treatment and habitat. Thus, tethering juvenile blue crabs in salt marsh habitat did not produce treatment-specific bias relative to unvegetated habitat across a range of shoot densities; survival of tethered and un-tethered crabs was positively related to shoot density. These findings indicate that tethering is a useful method for assessing survival in salt marshes, as with other nursery habitats including seagrass beds, algae and unstructured sand.

Non-native red alga Gracilaria vermiculophylla compensates for seagrass loss as blue crab nursery habitat in the emerging Chesapeake Bay ecosystem.

Non-native species can become deleterious or potentially beneficial as components of novel ecosystems. The non-native red macroalga Gracilaria vermiculophylla may provide nursery habitat where eelgrass Zostera marina has been extirpated in Chesapeake Bay. A mensurative experiment was conducted monthly May-October 2013 and 2014 in the York River, Chesapeake Bay, to evaluate hypotheses that Gracilaria (1) can compensate for the loss of seagrass nurseries by colonizing habitats where seagrass has been eliminated by environmental stress, and (2) is utilized by juvenile blue crabs (Callinectes sapidus) as nursery habitat. We quantified Gracilaria presence, percent cover, and biomass as a function of region (upriver, midriver, and downriver) and seagrass presence or absence using stratified random sampling, 20-m transects, and 0.0625-m2 quadrats. Gracilaria volume was measured and converted to dry weight. Effects of the factors and covariates temperature, salinity, dissolved oxygen, month, and year were analyzed using generalized linear models. Juvenile blue crab density was quantified in summer 2013 using suction sampling in Gracilaria and seagrass. A model with the collective effect of region and seagrass presence or absence (downriver seagrass, downriver unvegetated bottom, midriver unvegetated bottom) best predicted Gracilaria abundance. Gracilaria presence, percent cover, and biomass were highest in downriver seagrass, followed by downriver unvegetated bottom, and then midriver unvegetated bottom, where seagrass has been extirpated, supporting hypothesis (1). Gracilaria did not occur upriver, likely due to a lack of recruitment. Seagrass and Gracilaria housed similar densities of juvenile blue crabs, supporting hypothesis (2). We estimated that a single 40-ha cove system with Gracilaria could house 200,000 juvenile crabs as would a single 2.4-ha seagrass bed. Consequently, the numerous midriver and downriver cove systems in the York River could support millions of young juvenile blue crabs and thereby compensate for the loss of seagrass in the river and in other areas of Chesapeake Bay. At present, Gracilaria has no widespread negative impacts on seagrass in the York River or most regions of Chesapeake Bay, likely because percent cover and biomass are not excessively high at present. We posit that Gracilaria has become an important alternative nursery habitat for the blue crab in Chesapeake Bay and can potentially mitigate impacts of climate change on seagrass nursery habitats.

Pattern formation in marsh ecosystems modeled through the interaction of marsh vegetation, mussels and sediment.

Spatial self-organization, a common feature of multi-species communities, can provide important insights into ecosystem structure and resilience. As environmental conditions gradually worsen (e.g., resource depletion, erosion intensified by storms, drought), some ecological systems collapse to an irreversible state once a tipping point is reached. Spatial patterning may be one way for them to cope with such changes. We use a mathematical model to describe self-organization of an eroding marsh shoreline based on three-way interactions between sediment volume and two ecosystem engineers - smooth cordgrass Spartina alterniflora and ribbed mussels Geukensia demissa. Our model indicates that scale-dependent interactions between multiple ecosystem engineers drive the self-organization of eroding marsh edges and regulate the spatial scale of shoreline morphology. Spatial self-organization of the marsh edge increases the system's productivity, allows it to withstand erosion, and delays degradation that otherwise would occur in the absence of strong species interactions. Further, changes in wavelength and variance of the spatial patterns give insight into marsh recession. Finally, we find that the presence of mussels in the system modulates the spatial scale of the patterns, generates patterns with shorter wavelengths, and allows the system to tolerate a greater level of erosion. Although previous studies suggest that self-organization can emerge from local interactions and can result in increased ecosystem persistence and stability in various ecosystems, our findings extend these concepts to coastal salt marshes, emphasizing the importance of the ecosystem engineers, smooth cordgrass and ribbed mussels, and demonstrating the potential value of self-organization for ecosystem management and restoration.

Nitrogen reductions have decreased hypoxia in the Chesapeake Bay: Evidence from empirical and numerical modeling.

Seasonal hypoxia is a characteristic feature of the Chesapeake Bay due to anthropogenic nutrient input from agriculture and urbanization throughout the watershed. Although coordinated management efforts since 1985 have reduced nutrient inputs to the Bay, oxygen concentrations at depth in the summer still frequently fail to meet water quality standards that have been set to protect critical estuarine living resources. To quantify the impact of watershed nitrogen reductions on Bay hypoxia during a recent period including both average discharge and extremely wet years (2016-2019), this study employed both statistical and three-dimensional (3-D) numerical modeling analyses. Numerical model results suggest that if the nitrogen reductions since 1985 had not occurred, annual hypoxic volumes (O2 < 3 mg L-1) would have been ~50-120% greater during the average discharge years of 2016-2017 and ~20-50% greater during the wet years of 2018-2019. The effect was even greater for O2 < 1 mg L-1, where annual volumes would have been ~80-280% greater in 2016-2017 and ~30-100% greater in 2018-2019. These results were supported by statistical analysis of empirical data, though the magnitude of improvement due to nitrogen reductions was greater in the numerical modeling results than in the statistical analysis. This discrepancy is largely accounted for by warming in the Bay that has exacerbated hypoxia and offset roughly 6-34% of the improvement from nitrogen reductions. Although these results may reassure policymakers and stakeholders that their efforts to reduce hypoxia have improved ecosystem health in the Bay, they also indicate that greater reductions are needed to counteract the ever-increasing impacts of climate change.

Corrigendum to "Bistability in a differential equation model of oyster reef height and sediment accumulation" [J. Theor. Biol. 289 (2011) 1-11].

There was a mistake in the Matlab code we used to generate time series solutions of our model, Eqs. (16)-(18). The corrected text below replaces one paragraph on p. 7, and the figures below replace Figs. 4-5 on p. 8. There is no qualitative change to our results. However, there is a quantitative change in the initial dead oyster shell volume B(0) needed for reef survival. The corrected threshold B(0), about 0.40 m3 per m2 of sea floor, is more consistent with a recently experimentally estimated threshold of 0.30 m (Colden, Latour, and Lipcius, Mar Ecol Prog Ser 582: 1-13, 2017) than was our old incorrect threshold of about 0.12 m3.

Successful recruitment, survival and long-term persistence of eastern oyster and hooked mussel on a subtidal, artificial restoration reef system in Chesapeake Bay.

Restoration efforts with native eastern oyster, Crassostrea virginica, in Chesapeake Bay and elsewhere have been limited by shell availability, necessitating the use of alternative structures as subtidal reefs, yet these have rarely been evaluated quantitatively. We quantified population structure, density, abundance and biomass of eastern oyster and hooked mussel, Ischadium recurvum, on a concrete modular reef (75 m2 surface area over 5 m2 of river bottom) deployed subtidally at 7 m depth in the Rappahannock River, Virginia during October, 2000. After nearly 5 y (May 2005), we took 120 stratified random samples over the reef. The reef was heavily colonized by 28-168 oysters and 14-2177 mussels m-2 surface area. These densities translate to 1085 oysters and 8617 mussels m-2 river bottom, which are the highest recorded for artificial oyster reefs. Size structure of oysters reflected four year classes, with over half of oysters more than 1 y old and of reproductive age. Oyster biomass (1663 g dry mass m-2 river bottom) and condition index were equally high, whereas parasite prevalence and intensity were low. Oyster density correlated positively in a sigmoid fashion with mussel density up to high densities, then declined. This modular reef is one of the most successful artificial reefs for eastern oyster and hooked mussel restoration, and details features that are conducive for successful settlement, growth and survival in subtidal habitats.

Gear and survey efficiency of patent tongs for oyster populations on restoration reefs.

Surveys of restored oyster reefs need to produce accurate population estimates to assess the efficacy of restoration. Due to the complex structure of subtidal oyster reefs, one effective and efficient means to sample is by patent tongs, rather than SCUBA, dredges, or bottom cores. Restored reefs vary in relief and oyster density, either of which could affect survey efficiency. This study is the first to evaluate gear (the first full grab) and survey (which includes selecting a specific half portion of the first grab for further processing) efficiencies of hand-operated patent tongs as a function of reef height and oyster density on subtidal restoration reefs. In the Great Wicomico River, a tributary of lower Chesapeake Bay, restored reefs of high- and low-relief (25-45 cm, and 8-12 cm, respectively) were constructed throughout the river as the first large-scale oyster sanctuary reef restoration effort (sanctuary acreage > 20 ha at one site) in Chesapeake Bay. We designed a metal frame to guide a non-hydraulic mechanical patent tong repeatedly into the same plot on a restored reef until all oysters within the grab area were captured. Full capture was verified by an underwater remotely-operated vehicle. Samples (n = 19) were taken on nine different reefs, including five low- (n = 8) and four high-relief reefs (n = 11), over a two-year period. The gear efficiency of the patent tong was estimated to be 76% (± 5% standard error), whereas survey efficiency increased to 81% (± 10%) due to processing. Neither efficiency differed significantly between young-of-the-year oysters (spat) and adults, high- and low-relief reefs, or years. As this type of patent tong is a common and cost-effective tool to evaluate oyster restoration projects as well as population density on fished habitat, knowing the gear and survey efficiencies allows for accurate and precise population estimates.

The demographic consequences of growing older and bigger in oyster populations.

Structured population models, particularly size- or age-structured, have a long history of informing conservation and natural resource management. While size is often easier to measure than age and is the focus of many management strategies, age-structure can have important effects on population dynamics that are not captured in size-only models. However, relatively few studies have included the simultaneous effects of both age- and size-structure. To better understand how population structure, particularly that of age and size, impacts restoration and management decisions, we developed and compared a size-structured integral projection model (IPM) and an age- and size-structured IPM, using a population of Crassostrea gigas oysters in the northeastern Pacific Ocean. We analyzed sensitivity of model results across values of local retention that give populations decreasing in size to populations increasing in size. We found that age- and size-structured models yielded the best fit to the demographic data and provided more reliable results about long-term demography. Elasticity analysis showed that population growth rate was most sensitive to changes in the survival of both large (>175 mm shell length) and small (<75 mm shell length) oysters, indicating that a maximum size limit, in addition to a minimum size limit, could be an effective strategy for maintaining a sustainable population. In contrast, the purely size-structured model did not detect the importance of large individuals. Finally, patterns in stable age and stable size distributions differed between populations decreasing in size due to limited local retention and populations increasing in size due to high local retention. These patterns can be used to determine population status and restoration success. The methodology described here provides general insight into the necessity of including both age- and size-structure into modeling frameworks when using population models to inform restoration and management decisions.

Evidence of eelgrass (Zostera marina) seed dispersal by northern diamondback terrapin (Malaclemys terrapin terrapin) in lower Chesapeake Bay.

The initial discovery in May 2009 of eelgrass (Zostera marina) seeds in fecal samples of wild-caught northern diamondback terrapins (Malaclemys terrapin terrapin) was the first field evidence of eelgrass seed ingestion in this species. This finding suggested the potential of terrapins as seed dispersers in eelgrass beds, which we sampled for two additional years (2010 and 2011). Seeds were only found in feces of terrapins captured prior to June 8 in all three years, coinciding with eelgrass seed maturation and release. Numbers of seeds in terrapin feces varied annually and decreased greatly in 2011 after an eelgrass die off in late 2010. The condition of seeds in terrapin feces was viable-mature, germinated, damaged, or immature. Of terrapins captured during time of seed release, 97% were males and juvenile females, both of which had head widths <30 mm. The fraction of individuals with ingested seeds was 33% for males, 35% for small females, and only 6% for large (mature) females. Probability of seed ingestion decreased exponentially with increasing terrapin head width; only males and small females (head width <30 mm) were likely to be vectors of seed dispersal. The characteristic that diamondback terrapins have well-defined home ranges allowed us to estimate the number of terrapins potentially dispersing eelgrass seeds annually. In seagrass beds of the Goodwin Islands region (lower York River, Virginia), there were 559 to 799 terrapins, which could disperse between 1,341 and 1,677 eelgrass seeds annually. These would represent a small proportion of total seed production within a single seagrass bed. However, based on probable home range distances, terrapins can easily traverse eelgrass meadow boundaries, thereby dispersing seeds beyond the bed of origin. Given the relatively short dispersion distance of eelgrass seeds, the diamondback terrapin may be a major source of inter-bed seed dispersal and genetic diversity.

Bistability in a differential equation model of oyster reef height and sediment accumulation.

Native oyster populations in Chesapeake Bay have been the focus of three decades of restoration attempts, which have generally failed to rebuild the populations and oyster reef structure. Recent restoration successes and field experiments indicate that high-relief reefs persist, likely due to elevated reef height which offsets heavy sedimentation and promotes oyster survival, disease resistance and growth, in contrast to low-relief reefs which degrade in just a few years. These findings suggest the existence of alternative stable states in oyster reef populations. We developed a mathematical model consisting of three differential equations that represent volumes of live oysters, dead oyster shells (=accreting reef), and sediment. Bifurcation analysis and numerical simulations demonstrated that multiple nonnegative equilibria can exist for live oyster, accreting reef and sediment volume at an ecologically reasonable range of parameter values; the initial height of oyster reefs determined which equilibrium was reached. This investigation thus provides a conceptual framework for alternative stable states in native oyster populations, and can be used as a tool to improve the likelihood of success in restoration efforts.

Unprecedented restoration of a native oyster metapopulation.

Native oyster species were once vital ecosystem engineers, but their populations have collapsed worldwide because of overfishing and habitat destruction. In 2004, we initiated a vast (35-hectare) field experiment by constructing native oyster reefs of three types (high-relief, low-relief, and unrestored) in nine protected sanctuaries throughout the Great Wicomico River in Virginia, United States. Upon sampling in 2007 and 2009, we found a thriving metapopulation comprising 185 million oysters of various age classes. Oyster density was fourfold greater on high-relief than on low-relief reefs, explaining the failure of past attempts. Juvenile recruitment and reef accretion correlated with oyster density, facilitating reef development and population persistence. This reestablished metapopulation is the largest of any native oyster worldwide and validates ecological restoration of native oyster species.

A sex-specific metabolite identified in a marine invertebrate utilizing phosphorus-31 nuclear magnetic resonance.

Hormone level differences are generally accepted as the primary cause for sexual dimorphism in animal and human development. Levels of low molecular weight metabolites also differ between men and women in circulating amino acids, lipids and carbohydrates and within brain tissue. While investigating the metabolism of blue crab tissues using Phosphorus-31 Nuclear Magnetic Resonance, we discovered that only the male blue crab (Callinectes sapidus) contained a phosphorus compound with a chemical shift well separated from the expected phosphate compounds. Spectra obtained from male gills were readily differentiated from female gill spectra. Analysis from six years of data from male and female crabs documented that the sex-specificity of this metabolite was normal for this species. Microscopic analysis of male and female gills found no differences in their gill anatomy or the presence of parasites or bacteria that might produce this phosphorus compound. Analysis of a rare gynandromorph blue crab (laterally, half male and half female) proved that this sex-specificity was an intrinsic biochemical process and was not caused by any variations in the diet or habitat of male versus female crabs. The existence of a sex-specific metabolite is a previously unrecognized, but potentially significant biochemical phenomenon. An entire enzyme system has been synthesized and activated only in one sex. Unless blue crabs are a unique species, sex-specific metabolites are likely to be present in other animals. Would the presence or absence of a sex-specific metabolite affect an animal's development, anatomy and biochemistry?

Periodic dynamics in a two-stage Allee effect model are driven by tension between stage equilibria.

Single species difference population models can show complex dynamics such as periodicity and chaos under certain circumstances, but usually only when rates of intrinsic population growth or other life history parameter are unrealistically high. Single species models with Allee effects (positive density dependence at low density) have also been shown to exhibit complex dynamics when combined with over-compensatory density dependence or a narrow fertility window. Here we present a simple two-stage model with Allee effects which shows large amplitude periodic fluctuations for some initial conditions, without these requirements. Periodicity arises out of a tension between the critical equilibrium of each stage, i.e. when the initial population vector is such that the adult stage is above the critical value, while the juvenile stage is below the critical value. Within this area of parameter space, the range of initial conditions giving rise to periodic dynamics is driven mainly by adult mortality rates. Periodic dynamics become more important as adult mortality increases up to a certain point, after which periodic dynamics are replaced by extinction. This model has more realistic life history parameter values than most 'chaotic' models. Conditions for periodic dynamics might arise in some marine species which are exploited (high adult mortality) leading to recruitment limitation (low juvenile density) and might be an additional source of extinction risk.