Site- and species-specific metal concentrations, mobility, and bioavailability in sediment, flora, and fauna of a southeastern United States salt marsh.

Salt marshes are highly productive and valuable coastal ecosystems that act as filters for nutrients and pollutants at the land-sea interface. The salt marshes of the mid-Atlantic United States often exhibit geochemical behavior that varies significantly from other estuaries around the world, but our understanding of metal mobility and bioavailability remains incomplete for these systems. We sampled abiotic (water and sediment) and native biotic (three halophyte and two bivalve species) compartments of a southeastern United States salt marsh to understand the site- and species-specific metal concentrations, fractionation, and bioavailability for 16 metals and metalloids, including two naturally occurring radionuclides. Location on the marsh platform greatly influenced metal concentrations in sediment and metal bioaccumulation in halophytes, with sites above the mean high-water mark (i.e., high marsh zone) having lower concentrations in sediment but plants exhibiting greater biota sediment accumulation factors (BSAFs). Transition metal concentrations in the sediment were an average of 6× higher in the low marsh zone compared to the high marsh zone and heavy metals were on average 2× higher. Tissue- and species-specific preferential accumulation in bivalves provide opportunities for tailored biomonitoring programs. For example, mussel byssal threads accumulated ten of the sixteen studied elements to significantly greater concentrations compared to soft tissues and oysters had remarkably high soft tissue zinc concentrations (~5000 mg/kg) compared to all other species and element combinations studied. Additionally, some of our results have important implications for understanding metal mobility and implementing effective remediation (specifically phytoremediation) strategies, including observations that (1) heavy metals exhibit distinct concentration spatial distributions and metal fractionation patterns which vary from the transition metals and (2) sediment organic matter fraction appears to play an important role in controlling sediment metal concentrations, fractionation, and plant bioavailability.

Predicting diet in brachyuran crabs using external morphology.

Morphological traits have often been used to predict diet and trophic position of species across many animal groups. Variation in gut size of closely related animals is known to be a good predictor of dietary habits. Species that are more herbivorous or that persist on low-quality diets often have larger stomachs than their carnivorous counterparts. This same pattern exists in crabs and in most species, individuals exhibit external markings on the dorsal side of their carapace that appear to align with the position and size of their gut. We hypothesized that these external markings could be used as an accurate estimate of the crab's cardiac stomach size, allowing an approximation of crab dietary strategies without the need to sacrifice and dissect individual animals. We used literature values for mean diet and standardized external gut size markings taken from crab photographs across 50 species to show that percent herbivory in the diet increases non-linearly across species of brachyuran crab with the external estimate of gut size. We also used data from dissections in four species to show that external gut markings were positively correlated with gut sizes, though the strength of this correlation differed across species. We conclude that when rough approximations of diet quality such as percent herbivory will suffice, measuring external carapace markings in crabs presents a quick, free, non-lethal alternative to dissections. Our results also provide important insights into tradeoffs that occur in crab morphology and have implications for crab evolution.

Tissue-Specific Toxicokinetics of Aqueous Radium-226 in an Estuarine Mussel, Geukensia demissa.

Radiological contamination of coastal habitats poses potential risk for native fauna, but the bioavailability of aqueous radium (Ra) and other dissolved metals to marine bivalves remains unclear. This study was the first to examine the tissue-specific disposition of aqueous 226Ra in a coastal mussel, specifically the Atlantic ribbed mussel Geukensia demissa. Most organ groups reached steady-state concentrations within 7 days during experimental exposure, with an average uptake rate constant of 0.0013 mL g-1 d-1. When moved to Ra-free synthetic seawater, mussels rapidly eliminated aqueous 226Ra (average elimination rate constant 1.56 d-1). The biological half-life for aqueous 226Ra ranged from 8.9 h for the gills and labial palps to 15.4 h for the muscle. Although previous field studies have demonstrated notable 226Ra accumulation in the soft tissues of marine mussels and that, for freshwater mussels, tissue-incorporated 226Ra derives primarily from the aqueous phase, our tissue-specific bioconcentration factors (BCFs) were on the order of (8.3 ± 1.5) × 10-4 indicating low accumulation potential of aqueous 226Ra in estuarine mussels. This suggests marine and estuarine mussels obtain 226Ra from an alternate route, such as particulate-sorbed Ra ingested during filter-feeding or from a contaminated food source.

Increasing tidal inundation corresponds to rising porewater nutrient concentrations in a southeastern U.S. salt marsh.

Salt marshes are ecologically and economically important features of coastal environments that are vulnerable to sea level rise, the rate of which has accelerated in recent decades along the southeastern US Atlantic coast. Increased flooding frequency and duration across the marsh platform is predicted to impact vegetation community structure and overall marsh persistence, but the effect of changing inundation patterns on biogeochemical processes in marsh sediments remains largely unexplored. As part of a long-term monitoring effort to assess how marshes are responding to sea level rise in North Inlet estuary (South Carolina, USA), we collected data on porewater nutrient concentrations from a series of permanent monitoring plots across multiple transects spanning the marsh elevation gradient during the growing season from 2009 to 2019. Additionally, we calculated time inundated for each plot using local water level data and high-resolution elevation measurements to assess the change in time flooded at each plot. Our results indicate that both NH4 and PO4 nutrient concentrations have increased in most permanent plots over the 11-year study period and that nutrient concentrations are higher with increasing proximity to the creek. Spatial patterns in nutrient increases through time are coincident with considerable increases in tidal inundation observed over the marsh platform. Across plots located in the low marsh, porewater NH4 and PO4 concentrations have risen at average rates of 8.96 µM/year and 0.86 µM/year, respectively, and have reached rates as high as 27.25 µM/year and 3.13 µM/year. We suggest that increased inundation time due to rising sea level has altered biogeochemical conditions influencing nutrient availability in marsh porewater, resulting in increases that likely have relevance for larger scale nutrient cycles as well as marsh ecosystem stability and function.

Conspecific cues, not starvation, mediate barren urchin response to predation risk.

Prey state and prey density mediate antipredator responses that can shift community structure and alter ecosystem processes. For example, well-nourished prey at low densities (i.e., prey with higher per capita predation risk) should respond strongly to predators. Although prey state and density often co-vary across habitats, it is unclear if prey responses to predator cues are habitat-specific. We used mesocosms to compare the habitat-specific responses of purple sea urchins (Strongylocentrotus purpuratus) to waterborne cues from predatory lobsters (Panulirus interruptus). We predicted that urchins from kelp forests (i.e., in well-nourished condition) tested at low densities typically observed in this habitat would respond more strongly to predation risk than barren urchins (i.e., in less nourished condition) tested at high densities typically observed in this habitat. Indeed, when tested at densities associated with respective habitats, urchins from forests, but not barrens, reduced kelp grazing by 69% when exposed to lobster risk cues. Barren urchins that were unresponsive to predator cues at natural, high densities suddenly responded strongly to lobster cues when conspecific densities were reduced. Strong responses of low densities of barren urchins persisted across feeding history (i.e. 0-64 days of starvation). This suggests that barren urchins can respond to predators but typically do not because of high conspecific densities. Because high densities of urchins in barrens should weaken the non-consumptive effects of lobsters, urchins in these habitats may continue to graze in the presence of predators thereby providing a feedback that maintains urchin barrens.

Transient dynamics during kelp forest recovery from fishing across multiple trophic levels.

Outcomes of management efforts to recover or restore populations of harvested species can be highly dependent on environmental and community context. Predator-prey interactions can alter recovery trajectories, and the timing of management actions within multi-trophic level harvest scenarios may influence the dynamics of recovery and lead to management trade-offs. Recent work using a generalist predator-prey model suggests that management promoting synchronized recovery of predators and prey leads to faster and less variable recovery trajectories than sequential recovery (predator or prey first). However, more complex communities may require different management actions to minimize recovery time and variability. Here, we use a tri-trophic level rocky reef community dynamics model with size-structure and fisheries at multiple trophic levels to investigate the importance of three ecological processes to recovery of fished communities: (1) size-structured predation, (2) non-consumptive effects of predators on prey behavior, and (3) varying levels of recruitment. We also test the effects of initiating recovery from community states associated with varying degrees of fishery-induced degradation and develop a simulation in which the basal resource (kelp) is harvested. In this system, a predator-first closure generally leads to the least volatile and quickest recovery, whether from a kelp forest, urchin barren, or intermediate community state. The benefits gained by selecting this strategy are magnified when recovering from the degraded community, the urchin barren, because initial conditions in the degraded state lead to lengthy recovery times. However, the shape of the size-structured predation relationship can strongly affect recovery volatility, where the differences between alternate management strategies are negated with size-independent predation. External recruitment reduces return times by bolstering the predatory lobster population. These results show that in a tightly linked tri-trophic level food web with top-down control, a predator-first fishery closure can be the most effective strategy to reduce volatility and shorten recovery, particularly when the system is starting from the degraded community state. Given the ubiquity of top predator loss across many ecosystems, we highlight the value of incorporating insights from community ecology into ecosystem management.

Predator type influences the frequency of functional responses to prey in marine habitats.

The functional response of a consumer to a gradient of resource density is a widespread and consistent framework used to quantify the importance of consumption to population dynamics and stability. Within benthic marine ecosystems, both crustaceans and fishes can provide strong top-down pressure on prey populations. Taxon-specific differences in biomechanics or habitat use, among other factors, may lead to variable functional response forms or parameter values (attack rate, handling time). Based on a review of 189 individual functional response fits, we find that these predator guilds differ in their frequency distribution of functional response types, with crustaceans exhibiting nearly double the proportion of sigmoidal, density-dependent functional responses (Holling type III) as predatory fishes. The implications of this finding for prey population stability are significant because type III responses allow prey persistence while type II responses are de-stabilizing and can lead to extinction. Comparing per capita predation rates across diverse taxa can provide integrative insights into predatory effects and the ability of predation to drive community structure.

Experiments reveal limited top-down control of key herbivores in southern California kelp forests.

Predator responses to gradients in prey density have important implications for population regulation and are a potential structuring force for subtidal marine communities, particularly on rocky reefs where herbivorous sea urchins can drive community state shifts. On rocky reefs in southern California where predatory sea otters have been extirpated, top-down control of sea urchins by alternative predators has been hypothesized but rarely tested experimentally. In laboratory feeding assays, predatory spiny lobsters (Panulirus interruptus) demonstrated a saturating functional response to urchin prey, whereby urchin proportional mortality was inversely density-dependent. In field experiments on rocky reefs near San Diego, California, predators (primarily the labrid fish California sheephead, Semicossyphus pulcher) inflicted highly variable mortality on purple urchin (Strongylocentrotus purpuratus) prey across all density levels. However, at low to moderate densities commonly observed within kelp forests, purple urchin mortality increased to a peak at a density of ~11 urchins/m2 . Above that level, at densities typical of urchin barrens, purple urchin mortality was density-independent. When larger red urchins (Mesocentrotus franciscanus) were offered to predators simultaneously with purple urchins, mortality was density-independent. Underwater videography revealed a positive relationship between purple urchin density and both the number and richness of fish predators, but these correlations were not observed when red urchins were present. Our results demonstrate highly variable mortality rates across prey densities in this system and suggest that top-down control of urchins can occur only under limited circumstances. Our findings provide insight into the dynamics of alternate community states observed on rocky reefs.

Interactive effects of predator and prey harvest on ecological resilience of rocky reefs.

A major goal of ecosystem-based fisheries management is to prevent fishery-induced shifts in community states. This requires an understanding of ecological resilience: the ability of an ecosystem to return to the same state following a perturbation, which can strongly depend on species interactions across trophic levels. We use a structured model of a temperate rocky reef to explore how multi-trophic level fisheries impact ecological resilience. Increasing fishing mortality of prey (urchins) has a minor effect on equilibrium biomass of kelp, urchins, and spiny lobster predators, but increases resilience by reducing the range of predator harvest rates at which alternative stable states are possible. Size-structured predation on urchins acts as the feedback maintaining each state. Our results demonstrate that the resilience of ecosystems strongly depends on the interactive effects of predator and prey harvest in multi-trophic level fisheries, which are common in marine ecosystems but are unaccounted for by traditional management.