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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Phylotranscriptomic Insights into the Diversification of Endothermic Thunnus Tunas.

Birds, mammals, and certain fishes, including tunas, opahs and lamnid sharks, are endothermic, conserving internally generated, metabolic heat to maintain body or tissue temperatures above that of the environment. Bluefin tunas are commercially important fishes worldwide, and some populations are threatened. They are renowned for their endothermy, maintaining elevated temperatures of the oxidative locomotor muscle, viscera, brain and eyes, and occupying cold, productive high-latitude waters. Less cold-tolerant tunas, such as yellowfin tuna, by contrast, remain in warm-temperate to tropical waters year-round, reproducing more rapidly than most temperate bluefin tuna populations, providing resiliency in the face of large-scale industrial fisheries. Despite the importance of these traits to not only fisheries but also habitat utilization and responses to climate change, little is known of the genetic processes underlying the diversification of tunas. In collecting and analyzing sequence data across 29,556 genes, we found that parallel selection on standing genetic variation is associated with the evolution of endothermy in bluefin tunas. This includes two shared substitutions in genes encoding glycerol-3 phosphate dehydrogenase, an enzyme that contributes to thermogenesis in bumblebees and mammals, as well as four genes involved in the Krebs cycle, oxidative phosphorylation, ß-oxidation, and superoxide removal. Using phylogenetic techniques, we further illustrate that the eight Thunnus species are genetically distinct, but found evidence of mitochondrial genome introgression across two species. Phylogeny-based metrics highlight conservation needs for some of these species.

Studying animal niches using bulk stable isotope ratios: an updated synthesis.

The development of the isotopic niche, an n-dimensional hypervolume (with n being the number of isotopes) occupied by a population in delta space, has revolutionized the study of animal interactions in wild populations. While the isotopic niche offers a useful means to understand interactions at many ecological resolutions (e.g., individual, population, community, ecosystem), a variety of intrinsic and extrinsic factors drive isotopic variability and influence the ultimate geometry of observed niche dimensions. Here, we provide an updated synthesis to guide the application of bulk stable isotope ratios to study ecological niches. We summarize progress in the application of bulk stable isotope ratios for evaluating niches to synthesize a formal definition of the isotopic niche. We identify six broad categories to describe drivers of isotopic variance introduced by the animal, its environment, and the researcher, and provide recommendations to account for such variations before, during, and after sample collection and data analyses. Our synthesis illustrates the considerations that should be made before employing the isotopic niche to broader ecological contexts, and offers guidance for the use and interpretation of isotopic niche dynamics in future studies.

Are you really what you eat? Stomach content analysis and stable isotope ratios do not uniformly estimate dietary niche characteristics in three marine predators.

Calculation of dietary niche characteristics using stable isotopes has become a popular approach to understand the functional role of taxa across food webs. An underlying assumption of this approach is that stable isotopes accurately reflect the dietary breadth of a species over a temporal duration defined by tissue-specific isotopic turnover rates. In theory, dietary niche estimates derived from fast turnover rate tissues (e.g., blood plasma and liver) may augment stomach content-derived estimates more agreeably than slower turnover rate tissues (e.g., muscle or fin). We tested this hypothesis by comparing commonly used dietary niche estimates derived from stomach contents (nicheSCA: Levins', Shannon-Wiener's, and Smith's), with those estimated using stable isotopes [nicheSIA: standard ellipse area (SEA), convex hull total area (TA), theta (θ), and ellipse eccentricity (E)] of liver and muscle tissue. Model species were three large-bodied sharks: white (Carcharodon carcharias), dusky (Carcharhinus obscurus), and scalloped hammerhead (Sphyrna lewini). Within-technique comparisons for nicheSCA and nicheSIA metrics (i.e., SEA vs. TA) were often correlated; however, we did not observe any statistically significant correlations between nicheSCA and liver/muscle tissue nicheSIA (i.e., Levins' vs. SEA). We conclude that nicheSCA and nicheSIA do not provide comparable estimates of dietary niche, at least for the three predator species examined. This fundamental discrepancy highlights technique-specific limitations to estimating organismal dietary niche and identifies a need for the use of clearly defined niche metrics, i.e., the standardized use and reporting of the term isotopic niche as proposed by Newsome et al. (Front Ecol Environ 5:429-436, 2007). Finally, further investigation into the factors underpinning nicheSIA is required to better contextualize this popular ecological metric when compared to nicheSCA.

Resource-use dynamics of co-occurring chondrichthyans from the First Coast, North Florida, USA.

Recent studies on shark assemblages on the northeast Florida and southeast Georgia coast (hereafter referred to collectively as the "First Coast") have demonstrated differences in species and age-class composition of catch from previously characterized estuaries and newly surveyed area beaches, demonstrating that these regions may provide a critical habitat to different segments (i.e., life stages) of local shark populations. In this study, carbon and nitrogen stable isotopes (δ13 C and δ15 N) from muscle tissue and blood plasma were used to examine trophic dynamics (and temporal variability thereof) of the three dominant co-occurring species found along First Coast beaches (the Atlantic Sharpnose shark Rhizoprionodon terraenovae, Blacknose shark Carcharhinus acronotus and Blacktip shark Carcharhinus limbatus) to determine if they exhibit overlap in resource use along with spatial and temporal habitat use. Although considered spatially segregated from the beach species, a dominant, age-class species found in First Coast estuaries (juvenile Sandbar sharks Carcharhinus plumbeus) was also included in this analysis for comparison. Temporal variability of resource-use characteristics was detected at the species level. Resource-use overlap among species varied by tissue type and was generally higher for blood plasma, suggesting greater resource sharing over more recent time periods. Over longer time periods Atlantic Sharpnose and Blacktip sharks exhibited resource-use expansion, whereas Blacknose sharks exhibited a narrowing in resource use, suggesting a more specialized foraging strategy compared to the other species. The resource-use breadth of Sandbar sharks also expanded between blood plasma and muscle tissue. Significant size relationships were detected in Blacktip and Sandbar sharks, indicating ontogenetic resource shifts for both species. A diversity of highly productive resource pools likely support shark populations along the First Coast such that resource-use differentiation is not required to facilitate species co-occurrence. This work may shed light on understanding patterns of species co-occurrence as well as aid in future conservation efforts.

Wound healing in an elasmobranch fish is not impaired by high-CO2 exposure.

The purpose of this study was to test the effects of high CO2 exposure on wound healing rates in an elasmobranch fish (Urobatis jamaicensis). Small dermal injuries (8 mm biopsy) closed by 22 days post wounding with a decrease in haematocrit. High CO2 exposure (ΔpH = 1.4) did not influence healing rate or haematocrit. Combined, these data provide evidence that minimally invasive scientific procedures have short-term impacts on elasmobranch fishes even during exposure to a chronic stressor. Therefore, wound healing rates may not be strongly impacted by ocean acidification (ΔpH = 0.4).

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.

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.

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.