Design, development, and implementation of IsoBank: A centralized repository for isotopic data.

Stable isotope data have made pivotal contributions to nearly every discipline of the physical and natural sciences. As the generation and application of stable isotope data continues to grow exponentially, so does the need for a unifying data repository to improve accessibility and promote collaborative engagement. This paper provides an overview of the design, development, and implementation of IsoBank (www.isobank.org), a community-driven initiative to create an open-access repository for stable isotope data implemented online in 2021. A central goal of IsoBank is to provide a web-accessible database supporting interdisciplinary stable isotope research and educational opportunities. To achieve this goal, we convened a multi-disciplinary group of over 40 analytical experts, stable isotope researchers, database managers, and web developers to collaboratively design the database. This paper outlines the main features of IsoBank and provides a focused description of the core metadata structure. We present plans for future database and tool development and engagement across the scientific community. These efforts will help facilitate interdisciplinary collaboration among the many users of stable isotopic data while also offering useful data resources and standardization of metadata reporting across eco-geoinformatics landscapes.

Absence of a functional gut microbiome impairs host amino acid metabolism in the Pacific spiny dogfish (Squalus suckleyi).

Nitrogen recycling and amino acid synthesis are two notable ways in which the gut microbiome can contribute to host metabolism, and these processes are especially important in nitrogen-limited animals. Marine elasmobranchs are nitrogen limited as they require substantial amounts of this element to support urea-based osmoregulation. However, following antibiotic-induced depletion of the gut microbiome, elasmobranchs are known to experience a significant decline in circulating urea and employ compensatory nitrogen conservation strategies such as reduced urea and ammonia excretion. We hypothesized that the elasmobranch gut microbiome transforms dietary and recycled nutrients into amino acids, supporting host carbon and nitrogen balance. Here, using stable isotope analyses, we found that depleting the gut microbiome of Pacific spiny dogfish (Squalus suckleyi) resulted in a significant reduction to the incorporation of supplemented dietary 15N into plasma amino acids, notably those linked to nitrogen handling and energy metabolism, but had no effect on gut amino acid transport. These results demonstrate the importance of gut microbes to host amino acid pools and the unique nitrogen handling strategy of marine elasmobranchs. More broadly, these results elucidate how the gut microbiome contributes to organismal homeostasis, which is likely a ubiquitous phenomenon across animal populations.

Accumulation of Per- and Polyfluoroalkyl Substances (PFAS) in Coastal Sharks from Contrasting Marine Environments: The New York Bight and The Bahamas.

Per- and polyfluoroalkyl substances (PFAS) enter the marine food web, accumulate in organisms, and potentially have adverse effects on predators and consumers of seafood. However, evaluations of PFAS in meso-to-apex predators, like sharks, are scarce. This study investigated PFAS occurrence in five shark species from two marine ecosystems with contrasting relative human population densities, the New York Bight (NYB) and the coastal waters of The Bahamas archipelago. The total detected PFAS (∑PFAS) concentrations in muscle tissue ranged from 1.10 to 58.5 ng g-1 wet weight, and perfluorocarboxylic acids (PFCAs) were dominant. Fewer PFAS were detected in Caribbean reef sharks (Carcharhinus perezi) from The Bahamas, and concentrations of those detected were, on average, ∼79% lower than in the NYB sharks. In the NYB, ∑PFAS concentrations followed: common thresher (Alopias vulpinus) > shortfin mako (Isurus oxyrinchus) > sandbar (Carcharhinus plumbeus) > smooth dogfish (Mustelus canis). PFAS precursors/intermediates, such as 2H,2H,3H,3H-perfluorodecanoic acid and perfluorooctanesulfonamide, were only detected in the NYB sharks, suggesting higher ambient concentrations and diversity of PFAS sources in this region. Ultralong-chain PFAS (C ≥ 10) were positively correlated with nitrogen isotope values (δ15N) and total mercury in some species. Our results provide some of the first baseline information on PFAS concentrations in shark species from the northwest Atlantic Ocean, and correlations between PFAS, stable isotopes, and mercury further contextualize the drivers of PFAS occurrence.

Long-term effects of climate change on juvenile bull shark migratory patterns.

Seasonal variability in environmental conditions is a strong determinant of animal migrations, but warming temperatures associated with climate change are anticipated to alter this phenomenon with unknown consequences. We used a 40-year fishery-independent survey to assess how a changing climate has altered the migration timing, duration and first-year survival of juvenile bull sharks (Carcharhinus leucas). From 1982 to 2021, estuaries in the western Gulf of Mexico (Texas) experienced a mean increase of 1.55°C in autumn water temperatures, and delays in autumn cold fronts by ca. 0.5 days per year. Bull shark migrations in more northern estuaries concomitantly changed, with departures 25-36 days later in 2021 than in 1982. Later, migrations resulted in reduced overwintering durations by up to 81 days, and the relative abundance of post-overwintering age 0-1 sharks increased by >50% during the 40-year study period. Yet, reductions in prey availability were the most influential factor delaying migrations. Juvenile sharks remained in natal estuaries longer when prey were less abundant. Long-term declines in prey reportedly occurred due to reduced spawning success associated with climate change based on published reports. Consequently, warming waters likely enabled and indirectly caused the observed changes in shark migratory behaviour. As water temperatures continue to rise, bull sharks in the north-western Gulf of Mexico could forgo their winter migrations in the next 50-100 years based on current trends and physiological limits, thereby altering their ecological roles in estuarine ecosystems and recruitment into the adult population. It is unclear if estuarine food webs will be able to support changing residency patterns as climate change affects the spawning success of forage species. We expect these trends are not unique to the western Gulf of Mexico or bull sharks, and migratory patterns of predators in subtropical latitudes are similarly changing at a global scale.

A new species of deep-sea Booralana Bruce, 1986 (Crustacea: Isopoda: Cirolanidae) from The Bahamas, Western North Atlantic.

Booralana nickorum sp. nov. is described from the deep-water slope of the Exuma Sound, The Bahamas, from depths of 540 to 560 metres. It is the fourth species to be assigned to the genus and the second species described from the Western North Atlantic. The species can be distinguished from Booralana tricarinata Camp and Heard, 1988 and the other species by the sub-triangular pleotelson and the uropodal exopod of mature males being far longer than endopod, with both rami extending well beyond the posterior margin of the pleotelson. Additionally, pleopods 3 and 4 lack a prominent angle at midpoint of ramus.

MFishBT: A global database of biogeochemical tags in migratory fish.

Humans have long been fascinated by the mysteries surrounding fish migrations and addressing these complex behaviors often requires large data sets. Biogeochemical tags, including trace elements and stable isotopes, are the most accessible biomarkers for tracking fish migrations. However, access to standardized biogeochemical tag data is rarely available for migratory fish, which limits our understanding of the evolutionary origins, drivers, timing, and corridors of migration. This precludes the development of conservation strategies and the implementation of management actions. Here, we present MFishBT, a global, open-access database of Migratory Fish's Biogeochemical Tags. As of April 2023, the MFishBT contains biogeochemical records from 1,305 studies, of which 53% used element-to-calcium (E/Ca) ratios, 34% used isotopic ratios, and 13% used both. The database covers 17,413 field sampling locations (inland 47% vs. marine 53%) around the globe, comprising 490 migratory fish species of four classes, 44 orders/suborders, and 137 families. In total, 77 trace elements and 11 isotope systems were measured across various fish biological archives, including otoliths, scales, eye lenses, and vertebrae. E/Ca ratios were examined more frequently than isotopic ratios, led by Sr/Ca, Mg/Ca, Ba/Ca, and 87 Sr/86 Sr, δ13 C, and δ18 O. The MFishBT compiles 27,030, 16,222, and 2,481,714 records with biogeochemical data detected in the core, edge, and core-to-edge transects for biological archives of migratory fish. This is the most globally comprehensive open-access database on biogeochemical tags in migratory fish to date, and can serve a variety of needs in scientific research, conservation, and management. We encourage researchers to add more data sets to this database in the future. This database is released for noncommercial use only. There are no copyright restrictions, and please cite this paper when using these data, or a subset of these data, for publication.

Emerging human-shark conflicts in the New York Bight: A call for expansive science and management.

Recent spikes in interactions between humans and sharks in the New York Bight have sparked widespread reporting of possible causalities, many of which lack empirical support. Here we comment on the current state of knowledge regarding shark biology and management in New York waters emphasizing that the possible drivers of increased human-shark interactions are confounded by a lack of historical monitoring data. We outline several key research avenues that should be considered to ensure the safe and sustainable coexistence of humans, sharks, and their prey, in an era of accelerated environmental change.

DNA metabarcoding of cloacal swabs provides insight into diets of highly migratory sharks in the Mid-Atlantic Bight.

The abundances of migratory shark species observed throughout the Mid-Atlantic Bight (MAB) during productive summer months suggest that this region provides critical habitat and prey resources to these taxa. However, the principal prey assemblages sustaining migratory shark biomass in this region are poorly defined. We applied high-throughput DNA metabarcoding to shark feces derived from cloacal swabs across nine species of Carcharhinid and Lamnid sharks to (1) quantify the contribution of broad taxa (e.g., invertebrates, fishes) supporting shark biomass during seasonal residency in the MAB and (2) determine whether the species displayed distinct dietary preference indicative of resource partitioning. DNA metabarcoding resulted in high taxonomic (species-level) resolution of shark diets with actinopterygian and elasmobranch fishes as the dominant prey categories across the species. DNA metabarcoding identified several key prey groups consistent across shark taxa that are likely integral for sustaining their biomass in this region, including Atlantic menhaden (Brevoortia tyrannus), Atlantic mackerel (Scomber scombrus), and benthic elasmobranchs, including skates. Our results are consistent with previously published stomach content data for the shark species of similar size range in the Northwest Atlantic Ocean, supporting the efficacy of cloacal swab DNA metabarcoding as a minimally invasive diet reconstruction technique. The high reliance of several shark species on Atlantic menhaden could imply wasp-waist food-web conditions during the summer months, whereby high abundances of forage fishes sustain a diverse suite of migratory sharks within a complex, seasonal food web.

Energetic connectivity of diverse elasmobranch populations - implications for ecological resilience.

Understanding the factors shaping patterns of ecological resilience is critical for mitigating the loss of global biodiversity. Throughout aquatic environments, highly mobile predators are thought to serve as important vectors of energy between ecosystems thereby promoting stability and resilience. However, the role these predators play in connecting food webs and promoting energy flow remains poorly understood in most contexts. Using carbon and nitrogen isotopes, we quantified the use of several prey resource pools (small oceanic forage, large oceanics, coral reef, and seagrass) by 17 species of elasmobranch fishes (n = 351 individuals) in The Bahamas to determine their functional diversity and roles as ecosystem links. We observed remarkable functional diversity across species and identified four major groups responsible for connecting discrete regions of the seascape. Elasmobranchs were responsible for promoting energetic connectivity between neritic, oceanic and deep-sea ecosystems. Our findings illustrate how mobile predators promote ecosystem connectivity, underscoring their functional significance and role in supporting ecological resilience. More broadly, strong predator conservation efforts in developing island nations, such as The Bahamas, are likely to yield ecological benefits that enhance the resilience of marine ecosystems to combat imminent threats such as habitat degradation and climate change.

Observations of hypomelanosis in the nurse shark Ginglymostoma cirratum.

Hypomelanosis refers to a suite of skin pigment abnormalities, including albinism, leucism and piebaldism. While documented across many vertebrate species, examples of hypomelanosis are rarely seen in chondrichthyans, with little insight into the potential effects on survival. Here, we report the first observation of abnormal skin pigmentation indicative of piebaldism in the Atlantic nurse shark Ginglymostoma cirratum, representing only the second reported case of skin aberrations for this species. This extremely rare observation is discussed in the broader context of fitness variation and long-term survival.

Tiger sharks support the characterization of the world's largest seagrass ecosystem.

Seagrass conservation is critical for mitigating climate change due to the large stocks of carbon they sequester in the seafloor. However, effective conservation and its potential to provide nature-based solutions to climate change is hindered by major uncertainties regarding seagrass extent and distribution. Here, we describe the characterization of the world's largest seagrass ecosystem, located in The Bahamas. We integrate existing spatial estimates with an updated empirical remote sensing product and perform extensive ground-truthing of seafloor with 2,542 diver surveys across remote sensing tiles. We also leverage seafloor assessments and movement data obtained from instrument-equipped tiger sharks, which have strong fidelity to seagrass ecosystems, to augment and further validate predictions. We report a consensus area of at least 66,000 km2 and up to 92,000 km2 of seagrass habitat across The Bahamas Banks. Sediment core analysis of stored organic carbon further confirmed the global relevance of the blue carbon stock in this ecosystem. Data from tiger sharks proved important in supporting mapping and ground-truthing remote sensing estimates. This work provides evidence of major knowledge gaps in the ocean ecosystem, the benefits in partnering with marine animals to address these gaps, and underscores support for rapid protection of oceanic carbon sinks.

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.

Bulk and amino acid nitrogen isotopes suggest shifting nitrogen balance of pregnant sharks across gestation.

Nitrogen isotope (δ15N) analysis of bulk tissues and individual amino acids (AA) can be used to assess how consumers maintain nitrogen balance with broad implications for predicting individual fitness. For elasmobranchs, a ureotelic taxa thought to be constantly nitrogen limited, the isotopic effects associated with nitrogen-demanding events such as prolonged gestation remain unknown. Given the linkages between nitrogen isotope variation and consumer nitrogen balance, we used AA δ15N analysis of muscle and liver tissue collected from female bonnethead sharks (Sphyrna tiburo, n = 16) and their embryos (n = 14) to explore how nitrogen balance may vary across gestation. Gestational stage was a strong predictor of bulk tissue and AA δ15N values in pregnant shark tissues, decreasing as individuals neared parturition. This trend was observed in trophic (e.g., Glx, Ala, Val), source (e.g., Lys), and physiological (e.g., Gly) AAs. Several potential mechanisms may explain these results including nitrogen conservation, scavenging, and bacterially mediated breakdown of urea to free ammonia that is used to synthesize AAs. We observed contrasting patterns of isotopic discrimination in embryo tissues, which generally became enriched in 15N throughout development. This was attributed to greater excretion of nitrogenous waste in more developed embryos, and the role of physiologically sensitive AAs (i.e., Gly and Ser) to molecular processes such as nucleotide synthesis. These findings underscore how AA isotopes can quantify shifts in nitrogen balance, providing unequivocal evidence for the role of physiological condition in driving δ15N variation in both bulk tissues and individual AAs.

Risk assessment for seafood consumers exposed to mercury and other trace elements in fish from Long Island, New York, USA.

We determined concentrations of Hg, Pb, Cd, Cr, As, Ni, Ag, Se, Cu, and Zn in muscle tissue of six commonly consumed Long Island fish species (black seabass, bluefish, striped bass, summer flounder, tautog, and weakfish, total sample size = 1211) caught off Long Island, New York in 2018 and 2019. Long-term consumption of these coastal fish could pose health risks largely due to Hg exposure; concentrations of the other trace elements were well below levels considered toxic for humans. By combining the measured Hg concentrations in the fish (means ranging from 0.11 to 0.27 mg/kg among the fish species), the average seafood consumption rate, and the current US EPA Hg reference dose (0.0001 mg/kg/d), it was concluded that seafood consumption should be limited to four fish meals per month for adults for some fish (bluefish, tautog) and half that for young children. Molar ratios of Hg:Se exceeded 1 for some black seabass, bluefish, tautog, and weakfish.

Complete mitochondrial genome of the Caribbean reef shark, Carcharhinus perezi (Carcharhinformes: Carcharhinidae).

The Caribbean reef shark (Carcharhinus perezi; Poey, 1876) is a medium to large-bodied coastal and reef-associated predator found throughout the subtropical and tropical waters of the Atlantic Ocean and Caribbean Sea, although its populations are increasingly threatened by overfishing. We describe the first mitochondrial genome sequence for this species, using Illumina MiSeq sequencing of an individual from The Bahamas. We report the mitogenome sequence of the Caribbean reef shark to be 16,709 bp and composed two rRNA genes, 22 tRNA genes, 13 protein-coding genes, 2 non-coding regions; the D-loop control region and the origin of light-strand replication. We discuss the implications of this new information on future monitoring efforts and conservation measures such as marine protected areas, and urge for greater application of mitochondrial studies of sharks in the Atlantic Ocean.

Are stable isotope ratios suitable for describing niche partitioning and individual specialization?

As concerns about anthropogenic and natural disturbance grow, understanding animal resource use patterns has been increasingly prioritized to predict how changes in environmental conditions, food web structure, and population dynamics will affect biological resilience. Among the tools used to assess resource use, stable isotope analysis has proliferated in ecological studies, particularly in relation to describing intra- and interspecific variation in trophic interactions. Despite a growing need to disseminate scientific information, the inherent limitations of stable isotope ratios and inappropriate synonymizing of distinct evolutionary and ecological processes may mislead ecological inferences in natural systems. This situation necessitates a re-evaluation of the utility of stable isotope ratios to address certain ecological questions. Here, we assess the efficacy of stable isotope ratios to describe two fundamental ecological processes, niche partitioning and individual specialization. Investigation of these processes has increased substantially in accordance with increased access to stable isotope data. This article discusses the circumstances and approaches that are necessary to evaluate niche partitioning and individual specialization, and outlines key considerations for the associated application of stable isotope ratios.

Shark tooth collagen stable isotopes (δ15 N and δ13 C) as ecological proxies.

The isotopic composition of tooth-bound collagen has long been used to reconstruct dietary patterns of animals in extant and palaeoecological systems. For sharks that replace teeth rapidly in a conveyor-like system, stable isotopes of tooth collagen (δ13 CTeeth & δ15 NTeeth ) are poorly understood and lacking in ecological context relative to other non-lethally sampled tissues. This tissue holds promise, because shark jaws may preserve isotopic chronologies from which to infer individual-level ecological patterns across a range of temporal resolutions. Carbon and nitrogen stable isotope values were measured and compared between extracted tooth collagen and four other non-lethally sampled tissues of varying isotopic turnover rates: blood plasma, red blood cells, fin and muscle, from eight species of sharks. Individual-level isotopic variability of shark tooth collagen was evaluated by profiling teeth of different ages across whole jaws for the shortfin mako shark Isurus oxyrinchus and sandbar shark Carcharhinus plumbeus. Measurements of δ13 CTeeth and δ15 NTeeth were positively correlated with isotopic values from the four other tissues. Collagen δ13 C was consistently 13 C-enriched relative to all other tissues. Patterns for δ15 N were slightly less uniform; tooth collagen was generally 15 N-enriched relative to muscle and red blood cells, but congruent with fin and blood plasma (values clustered around a 1:1 relationship). Significant within-individual variability was observed across whole shortfin mako shark (δ13 C range = 1.4‰, δ15 N range = 3.6‰) and sandbar shark (δ13 C range = 1.2‰-2.4‰, δ15 N range = 1.7‰-2.4‰) jaws, which trended with tooth age. We conclude that amino acid composition and associated patterns of isotopic fractionation result in predictable isotopic offsets between tissues. Within-individual variability of tooth collagen stable isotope values suggests teeth of different ages may serve as ecological chronologies, that could be applied to studies on migration and individual-level diet variation across diverse time-scales. Greater understanding of tooth replacement rates, isotopic turnover and associated fractionation of tooth collagen will help refine potential ecological inferences, outlining clear goals for future scientific inquiry.

Metal concentrations in coastal sharks from The Bahamas with a focus on the Caribbean Reef shark.

Over the last century anthropogenic activities have rapidly increased the influx of metals and metalloids entering the marine environment, which can bioaccumulate and biomagnify in marine top consumers. This may elicit sublethal effects on target organisms, having broad implications for human seafood consumers. We provide the first assessment of metal (Cd, Pb, Cr, Mn, Co, Cu, Zn, As, Ag, and THg) and metalloid (As) concentrations in the muscle tissue of coastal sharks from The Bahamas. A total of 36 individual sharks from six species were evaluated, spanning two regions/study areas, with a focus on the Caribbean reef shark (Carcharhinus perezi), and to a lesser extent the tiger shark (Galeocerdo cuvier). This is due their high relative abundance and ecological significance throughout coastal Bahamian and regional ecosystems. Caribbean reef sharks exhibited some of the highest metal concentrations compared to five other species, and peaks in the concentrations of Pb, Cr, Cu were observed as individuals reached sexual maturity. Observations were attributed to foraging on larger, more piscivorous prey, high longevity, as well a potential slowing rate of growth. We observed correlations between some metals, which are challenging to interpret but may be attributed to trophic level and ambient metal conditions. Our results provide the first account of metal concentrations in Bahamian sharks, suggesting individuals exhibit high concentrations which may potentially cause sublethal effects. Finally, these findings underscore the potential toxicity of shark meat and have significant implications for human consumers.

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.