Using meta-analysis to explore the roles of global upwelling exposure and experimental design in bivalve responses to low pH.

Low pH conditions, associated with ocean acidification, represent threats to many commercially and ecologically important organisms, including bivalves. However, there are knowledge gaps regarding factors explaining observed differences in biological responses to low pH in laboratory experiments. Specific sources of local adaptation such as upwelling exposure and the role of experimental design, such as carbonate chemistry parameter changes, should be considered. Linking upwelling exposure, as an individual oceanographic phenomenon, to responses measured in laboratory experiments may further our understanding of local adaptation to global change. Here, meta-analysis is used to test the hypotheses that upwelling exposure and experimental design affect outcomes of individual, laboratory-based studies that assess bivalve metabolic (clearance and respiration rate) responses to low pH. Results show that while bivalves generally decrease metabolic activity in response to low pH, upwelling exposure and experimental design can significantly impact outcomes. Bivalves from downwelling or weak upwelling areas decrease metabolic activity in response to low pH, but bivalves from strong upwelling areas increase or do not change metabolic activity in response to low pH. Furthermore, experimental temperature, exposure time and magnitude of the change in carbonate chemistry parameters all significantly affect outcomes. These results suggest that bivalves from strong upwelling areas may be less sensitive to low pH. This furthers our understanding of local adaptation to global change by demonstrating that upwelling alone can explain up to 49 % of the variability associated with bivalve metabolic responses to low pH. Furthermore, when interpreting outcomes of individual, laboratory experiments, scientists should be aware that higher temperatures, shorter exposure times and larger changes in carbonate chemistry parameters may increase the chance of suppressed metabolic activity.

Behavioral and physiological effects of ocean acidification and warming on larvae of a continental shelf bivalve.

The negative impacts of ocean warming and acidification on bivalve fisheries are well documented but few studies investigate parameters relevant to energy budgets and larval dispersal. This study used laboratory experiments to assess developmental, physiological and behavioral responses to projected climate change scenarios using larval Atlantic surfclams Spisula solidissima solidissima, found in northwest Atlantic Ocean continental shelf waters. Ocean warming increased feeding, scope for growth, and biomineralization, but decreased swimming speed and pelagic larval duration. Ocean acidification increased respiration but reduced immune performance and biomineralization. Growth increased under ocean warming only, but decreased under combined ocean warming and acidification. These results suggest that ocean warming increases metabolic activity and affects larval behavior, while ocean acidification negatively impacts development and physiology. Additionally, principal component analysis demonstrated that growth and biomineralization showed similar response profiles, but inverse response profiles to respiration and swimming speed, suggesting alterations in energy allocation under climate change.

Energetic consequences of resource use diversity in a marine carnivore.

Understanding how intraspecific variation in the use of prey resources impacts energy metabolism has strong implications for predicting long-term fitness and is critical for predicting population-to-community level responses to environmental change. Here, we examine the energetic consequences of variable prey resource use in a widely distributed marine carnivore, juvenile sand tiger sharks (Carcharias taurus). We used carbon and nitrogen isotope analysis to identify three primary prey resource pools-demersal omnivores, pelagic forage, and benthic detritivores and estimated the proportional assimilation of each resource using Bayesian mixing models. We then quantified how the utilization of these resource pools impacted the concentrations of six plasma lipids and how this varied by ontogeny. Sharks exhibited variable reliance on two of three predominant prey resource pools: demersal omnivores and pelagic forage. Resource use variation was a strong predictor of energetic condition, whereby individuals more reliant upon pelagic forage exhibited higher blood plasma concentrations of very low-density lipoproteins, cholesterol, and triglycerides. These findings underscore how intraspecific variation in resource use may impact the energy metabolism of animals, and more broadly, that natural and anthropogenically driven fluctuations in prey resources could have longer term energetic consequences.

Host phenotype and microbiome vary with infection status, parasite genotype, and parasite microbiome composition.

A growing literature demonstrates the impact of helminths on their host gut microbiome. We investigated whether the stickleback host microbiome depends on ecoevolutionary variables by testing the impact of exposure to the cestode parasite Schistocephalus solidus with respect to infection success, host genotype, parasite genotype, and parasite microbiome composition. We observed constitutive differences in the microbiome of sticklebacks of different origin, and those differences increased when sticklebacks exposed to the parasite resisted infection. In contrast, the microbiome of successfully infected sticklebacks varied with parasite genotype. More specifically, we revealed that the association between microbiome and immune gene expression increased in infected individuals and varied with parasite genotype. In addition, we showed that S. solidus hosts a complex endomicrobiome and that bacterial abundance in the parasite correlates with expression of host immune genes. Within this comprehensive analysis we demonstrated that (i) parasites contribute to modulating the host microbiome through both successful and unsuccessful infection, (ii) when infection is successful, the host microbiome varies with parasite genotype due to genotype-dependent variation in parasite immunomodulation, and (iii) the parasite-associated microbiome is distinct from its host and impacts the host immune response to infection.

Population level differences in overwintering survivorship of blue crabs (Callinectes sapidus): A caution on extrapolating climate sensitivities along latitudinal gradients.

Winter mortality can strongly affect the population dynamics of blue crabs (Callinectes sapidus) near poleward range limits. We simulated winter in the lab to test the effects of temperature, salinity, and estuary of origin on blue crab winter mortality over three years using a broad range of crab sizes from both Great South Bay and Chesapeake Bay. We fit accelerated failure time models to our data and to data from prior blue crab winter mortality experiments, illustrating that, in a widely distributed, commercially valuable marine decapod, temperature, salinity, size, estuary of origin, and winter duration were important predictors of winter mortality. Furthermore, our results suggest that extrapolation of a Chesapeake Bay based survivorship model to crabs from New York estuaries yielded poor fits. As such, the severity and duration of winter can impact northern blue crab populations differently along latitudinal gradients. In the context of climate change, future warming could possibility confer a benefit to crab populations near the range edge that are currently limited by temperature-induced winter mortality by shifting their range edge poleward, but care must be taken in generalizing from models that are developed based on populations from one part of the range to populations near the edges, especially for species that occupy large geographical areas.

Regional variation in mercury bioaccumulation among NW Atlantic Golden (Lopholatilus chamaeleonticeps) and Blueline (Caulolatilus microps) Tilefish.

Mercury (Hg) concentrations in fishes from the NW Atlantic Ocean pose concern due to the importance of this region to U.S. fisheries harvest. In this study, total Hg (THg) concentrations and nitrogen stable isotope (δ15N) values were quantified in muscle tissues sampled from Golden (Lopholatilus chamaeleonticeps) and Blueline (Caulolatilus microps) Tilefish collected during a fishery-independent survey conducted in the NW Atlantic to compare bioaccumulation patterns between these species. Total Hg concentrations averaged (±SD) 0.4 ± 0.4 µg/g dry weight (d.w.) for L. chamaeleonticeps and 1.1 ± 0.7 µg/g d.w. for C. microps with <2% of all sampled fish, those >70 cm fork length, exceeding the most restrictive USEPA regulatory guidelines for human consumption (THg > 0.46 µg/g w.w.), when converted to wet weight concentrations. The THg concentrations reported here for individuals from the NW Atlantic stock are comparable to those reported for similarly sized individuals collected from the SW Atlantic stock but notably lower than those reported for Gulf of Mexico L. chamaeleonticeps, indicating different Hg exposure and assimilation kinetics for fish from the NW Atlantic, and highlights the broad geographic variability of Hg bioaccumulation among Tilefish stocks. Caulolatilus microps had higher δ15N values relative to L. chamaeleonticeps and a pattern of decreasing THg concentrations was also present from south to north across the study range. It is concluded that this trophic difference and spatial pattern in Tilefish THg concentrations emphasizes the habitat and resource partitioning mechanisms described for these sympatric species that permits their coexistence in the continental shelf environment. Importantly, regional variability in THg concentrations accentuate the possible roles of fine-scale biotic and abiotic processes that can act to regulate Hg bioaccumulation among individuals and species.

Separation of realized ecological niche axes among sympatric tilefishes provides insight into potential drivers of co-occurrence in the NW Atlantic.

Golden and Blueline Tilefish (Lopholatilus chamaeleonticeps and Caulolatilus microps) are keystone taxa in northwest (NW) Atlantic continental shelf-edge environments due to their biotic (trophic-mediated) and abiotic (ecosystem engineering) functional roles combined with high-value fisheries. Despite this importance, the ecological niche dynamics (i.e., those relating to trophic behavior and food-web interactions) of these sympatric species are poorly understood, knowledge of which may be consequential for maintaining both ecosystem function and fishery sustainability. We used stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) to build realized ecological niche hypervolumes to serve as proxies for diet and production use patterns of L. chamaeleonticeps and C. microps. We hypothesized that: (a) species exhibit ontogenetic shifts in diet and use of production sources; (b) species acquire energy from spatially distinct resource pools that reflect a sedentary life-history and differential use of the continental shelf-edge; and (c) species exhibit differentiation in one or more measured niche axes. We found evidence for ontogenetic shifts in diet (δ15N) but not production source (δ13C) in both species, suggesting a subtle expansion of measured ecological niche axes. Spatial interpolation of stable isotope ratios showed distinct latitudinal gradients; for example, individuals were 13C enriched in northern and 15N enriched in southern regions, supporting the assertion that tilefish species acquire energy from regional resource pools. High isotopic overlap was observed among species (≥82%); however, when hypervolumes included depth and region of capture, overlap among species substantially decreased to overlap estimates of 15%-77%. This suggests that spatial segregation could alleviate potential competition for resources among tilefish species inhabiting continental shelf-edge environments. Importantly, our results question the consensus interpretation of isotopic overlap estimates as representative of direct competition among species for shared resources or habitats, instead identifying habitat segregation as a possible mechanism for coexistence of tilefish species in the NW Atlantic.

Overwintering survivorship and growth of young-of-the-year black sea bass Centropristis striata.

Overwintering conditions have long been known to affect fish survival and year-class strength as well as determine the poleward range limit of many temperate fishes. Despite this known importance, mechanisms controlling overwintering mortality are poorly understood and the tolerance of marine fishes to the combined effects of winter temperature, salinity, and size is rarely quantified. In recent years, higher abundances of the temperate Serranid, black sea bass Centropristis striata, have been observed at latitudes further north than their traditional range suggesting that warming water temperatures, particularly during winter, may be facilitating the establishment of a population at more northern latitudes. To examine overwintering survival of C. striata, the combined effects of temperature, salinity and body mass were quantified in laboratory experiments. We identified 6°C as the lower incipient lethal temperature for C. striata, below which fish cease feeding, lose weight rapidly and die within 32 days. A short cold exposure experiment indicated that temperatures below 5°C resulted in mortality events that continued even as the temperature increased slowly to 10°C, indicating that even short cold snaps can impact survival and recruitment in this species. Importantly, fish in lower salinity lived significantly longer than fish at higher salinity at both 3°C and 5°C, suggesting that osmoregulatory stress plays a role in overwintering mortality in this species. Size was not a critical factor in determining overwintering survival of young-of-the-year (YOY) C. striata. Overwintering survival of YOY C. striata can be effectively predicted as a function of temperature and salinity and their interaction with an accelerated failure model to project future range limits. Identifying temperature thresholds may be a tractable way to incorporate environmental factors into population models and stock assessment models in fishes.

Endangered Atlantic Sturgeon in the New York Wind Energy Area: implications of future development in an offshore wind energy site.

Imminent development of offshore wind farms on the outer continental shelf of the United States has led to significant concerns for marine wildlife. The scarcity of empirical data regarding fish species that may utilize development sites, further compounded by the novelty of the technology and inherent difficulty of conducting offshore research, make identification and assessment of potential stressors to species of concern problematic. However, there is broad potential to mitigate putatively negative impacts to seasonal migrants during the exploration and construction phases. The goal of this study was to establish baseline information on endangered Atlantic Sturgeon in the New York Wind Energy Area (NY WEA), a future offshore development site. Passive acoustic transceivers equipped with acoustic release mechanisms were used to monitor the movements of tagged fish in the NY WEA from November 2016 through February 2018 and resulted in detections of 181 unique individuals throughout the site. Detections were highly seasonal and peaked from November through January. Conversely, fish were relatively uncommon or entirely absent during the summer months (July-September). Generalized additive models indicated that predictable transitions between coastal and offshore habitat were associated with long-term environmental cues and localized estuarine conditions, specifically the interaction between photoperiod and river temperature. These insights into the ecology of marine-resident Atlantic Sturgeon are crucial for both defining monitoring parameters and guiding threat assessments in offshore waters and represent an important initial step towards quantitatively evaluating Atlantic Sturgeon at a scale relevant to future development.

Temporal Changes in 137Cs Concentrations in Fish, Sediments, And Seawater off Fukushima Japan.

We analyzed publicly available data of Fukushima 137Cs concentrations in coastal fish, in surface and bottom waters, and in surface marine sediments and found that within the first year of the accident pelagic fish lost 137Cs at much faster rates (mean of ∼1.3% d-1) than benthic fish (mean of ∼0.1% d-1), with benthopelagic fish having intermediate loss rates (mean of ∼0.2% d-1). The loss rates of 137Cs in benthic fish in the first year were more comparable to the decline of 137Cs concentrations in sediments (0.03% d-1), and the declines in pelagic fish were more comparable to the declines in seawater. Retention patterns of 137Cs in pelagic fish were comparable to that in laboratory studies of fish in which there were no sustained 137Cs sources, whereas the benthopelagic and benthic fish species retained 137Cs to a greater extent, consistent with the idea that there is a sustained additional 137Cs source for these fish. These field data, based on 13 511 data points in which 137Cs was above the detection limit, are consistent with conclusions from laboratory experiments that demonstrate that benthic fish can acquire 137Cs from sediments, primarily through benthic invertebrates that contribute to the diet of these fish.

Biogeography of resistance to paralytic shellfish toxins in softshell clam, Mya arenaria (L.), populations along the Atlantic coast of North America.

Blooms of Alexandrium spp., the causative agent of paralytic shellfish poisoning (PSP), recur with varying frequency and intensity on the Northwest Atlantic coast of North America, from New York, USA, to northern Canadian waters. Along this latitudinal range blooms co-occur with abundant, intertidal populations of softshell clams, Mya arenaria. Prior work identified a naturally-occurring genetic mutation in Domain II α-subunit of the clams' voltage-gated sodium channels (NaV), which significantly reduces the binding affinity of the paralytic shellfish toxin, saxitoxin (STX). This mutation provides clams with resistance to the deleterious effects of STX, allowing them to continue feeding during Alexandrium spp. blooms and attain very high tissue toxicities. This study used genetic sequencing of the NaV mutation locus in clams from four coastal regions of the Bay of Fundy-Gulf of Maine and the mid-Atlantic to determine the percentage of clams in each region that possess the resistant NaV mutation. The genotype composition was related to the occurrence and magnitude of PSP outbreaks based on shellfish toxicity, primarily that of mussels, Mytilus edulis, used as a proxy for the prevalence and severity of Alexandrium blooms in each region. As hypothesized, the proportion of clams bearing the resistant mutation generally matched up well with the historical incidence and intensity of Alexandrium spp. blooms. The highest percentage of homozygote resistant clams (RR = 70.0%), and the lowest percentage of sensitive clams (SS = 4.5%) were found in eastern Gulf of Maine populations. Exceptions at a few sites where anomalously high numbers of M. arenaria with the resistant mutation were found despite the absence of blooms, may be attributable to larval gene flow. There was no evidence that Alexandrium blooms occurring in Northport Harbor, Long Island, have resulted in a shift in genotypic composition of the local clam population, presumably due to their low cell toxicity. Seasonal mismatch of highly vulnerable M. arenaria postset with toxic blooms at this latitude may also partly explain this result. This study provides strong supporting evidence that Alexandrium blooms can select for resistance to PSP-toxins in M. arenaria populations and proposes a mechanism for the persistence of the sensitive allele throughout the region. Implications for clam aquaculture (seeding) efforts, as well as for shellfish toxicity monitoring are discussed.

The influence of temperature stress on the physiology of the Atlantic surfclam, Spisula solidissima.

Atlantic surfclam populations have significantly declined in state and federal waters from the south shore of Long Island, New York to the Delmarva Peninsula since the early 2000s. Previous studies have demonstrated that surfclams in this geographic range show signs of physiological stress, suggested to be a result of increasing ocean temperatures. In this study, we examined the effect of 2 temperature regimes (19 °C and 23 °C) on surfclam physiology. These temperatures were chosen because they represent maximal (23 °C) and minimal (19 °C) temperatures prevailing in New York clamming areas during summer. Results demonstrated enhanced energy metabolism and significant reductions in filtration rate, scope for growth, and immune functions in clams exposed to the warmer temperature treatment. Although net energy gains remained positive in both treatments under our experimental conditions, the findings suggest that temperature stress is involved in the recent observations of surfclams in poor condition. The impact of elevated temperatures on phytoplankton quantity/quality and other environmental variables in combination with the direct impact on surfclam filtration and metabolic rates could lead to a negative energy balance. While some uncertainties remain about population-scale impacts of overall warming trends, we fear that future increases in temperature may lead to the collapse of the Atlantic surfclam between New York and Virginia, especially within inshore regions.

The relationship between observational scale and explained variance in benthic communities.

This study addresses the impact of spatial scale on explaining variance in benthic communities. In particular, the analysis estimated the fraction of community variation that occurred at a spatial scale smaller than the sampling interval (i.e., the geographic distance between samples). This estimate is important because it sets a limit on the amount of community variation that can be explained based on the spatial configuration of a study area and sampling design. Six benthic data sets were examined that consisted of faunal abundances, common environmental variables (water depth, grain size, and surficial percent cover), and sonar backscatter treated as a habitat proxy (categorical acoustic provinces). Redundancy analysis was coupled with spatial variograms generated by multiscale ordination to quantify the explained and residual variance at different spatial scales and within and between acoustic provinces. The amount of community variation below the sampling interval of the surveys (< 100 m) was estimated to be 36-59% of the total. Once adjusted for this small-scale variation, > 71% of the remaining variance was explained by the environmental and province variables. Furthermore, these variables effectively explained the spatial structure present in the infaunal community. Overall, no scale problems remained to compromise inferences, and unexplained infaunal community variation had no apparent spatial structure within the observational scale of the surveys (> 100 m), although small-scale gradients (< 100 m) below the observational scale may be present.

Exploration of Trends in Interspecific Abundance-Occupancy Relationships Using Empirically Derived Simulated Communities.

The interspecific abundance-occupancy relationship (AOR) is a widely used tool that describes patterns of habitat utilization and, when evaluated over time, may be used to identify large-scale changes in community structure. Our primary goal for this research was to validate the utility of AORs as temporal indicators of community state. We used long-term survey data in four regions of the northwest Atlantic coastal shelf (NWACS) to estimate the diversity of spatial behaviors in each community, which we modeled with negative binomial (NB) distributions. NB parameters were used to generate time series data for simulated communities, from which AORs were then estimated and evaluated for temporal trends. We found that AORs from simulated communities were similar in year-to-year variation to empirical relationships. In order to further understand the role of spatial diversity in the generation of AOR trends, we did additional simulations where NB parameters were manually manipulated. In one instance, we ran simulations while holding species' parameters constant over time. This treatment effectively removed trends, suggesting that temporal change in community relationships was the result of genuine variation in intraspecific spatial use. In another set of simulations, we conducted a case study to evaluate the impact of a select group of schooling and spatially aggregating species on an especially rapid shift in AORs in the Gulf of Maine from 1973 to 1983. Removals of these species reduced the magnitudes of most trends, demonstrating their importance to observed community changes. This research directly links variation in AORs to distribution and density-related processes and provides a potentially powerful framework to identify community-level change and to test ecological and mechanistic hypotheses.

Declining Mercury Concentrations in Bluefin Tuna Reflect Reduced Emissions to the North Atlantic Ocean.

Tunas are apex predators in marine food webs that can accumulate mercury (Hg) to high concentrations and provide more Hg (∼40%) to the U.S population than any other source. We measured Hg concentrations in 1292 Atlantic bluefin tuna (ABFT, Thunnus thynnus) captured in the Northwest Atlantic from 2004 to 2012. ABFT Hg concentrations and variability increased nonlinearly with length, weight, and age, ranging from 0.25 to 3.15 mg kg-1, and declined significantly at a rate of 0.018 ± 0.003 mg kg-1 per year or 19% over an 8-year period from the 1990s to the early 2000s. Notably, this decrease parallels comparably reduced anthropogenic Hg emission rates in North America and North Atlantic atmospheric Hg0 concentrations during this period, suggesting that recent efforts to decrease atmospheric Hg loading have rapidly propagated up marine food webs to a commercially important species. This is the first evidence to suggest that emission reduction efforts have resulted in lower Hg concentrations in large, long-lived fish.

Response of mollusc assemblages to climate variability and anthropogenic activities: a 4000-year record from a shallow bar-built lagoon system.

With their position at the interface between land and ocean and their fragile nature, lagoons are sensitive to environmental change, and it is reasonable to expect these changes would be recorded in well-preserved taxa such as molluscs. To test this, the 4000-year history of molluscs in Great South Bay, a bar-built lagoon, was reconstructed from 24 vibracores. Using x-radiography to identify shell layers, faunal counts, shell condition, organic content, and sediment type were measured in 325 samples. Sample age was estimated by interpolating 40 radiocarbon dates. K-means cluster analysis identified three molluscan assemblages, corresponding to sand-associated and mud-associated groups, and the third associated with inlet areas. Redundancy and regression tree analyses indicated that significant transitions from the sand-associated to mud-associated assemblage occurred over large portions of the bay about 650 and 294 years bp. The first date corresponds to the transition from the Medieval Warm Period to the Little Ice Age; this change in climate reduced the frequency of strong storms, likely leading to reduced barrier island breaching, greater bay enclosure, and fine-grained sediment accumulation. The second date marks the initiation of clear cutting by European settlers, an activity that would have increased runoff of fine-grained material. The occurrence of the inlet assemblage in the western and eastern ends of the bay is consistent with a history of inlets in these areas, even though prior to Hurricane Sandy in 2012, no inlet was present in the eastern bay in almost 200 years. The mud dominant, Mulinia lateralis, is a bivalve often associated with environmental disturbances. Its increased frequency over the past 300 years suggests that disturbances are more common in the bay than in the past. Management activities maintaining the current barrier island state may be contributing to the sand-mud transition and to the bay's susceptibility to disturbances.