Global mercury concentrations in biota: their use as a basis for a global biomonitoring framework.

An important provision of the Minamata Convention on Mercury is to monitor and evaluate the effectiveness of the adopted measures and its implementation. Here, we describe for the first time currently available biotic mercury (Hg) data on a global scale to improve the understanding of global efforts to reduce the impact of Hg pollution on people and the environment. Data from the peer-reviewed literature were compiled in the Global Biotic Mercury Synthesis (GBMS) database (>550,000 data points). These data provide a foundation for establishing a biomonitoring framework needed to track Hg concentrations in biota globally. We describe Hg exposure in the taxa identified by the Minamata Convention: fish, sea turtles, birds, and marine mammals. Based on the GBMS database, Hg concentrations are presented at relevant geographic scales for continents and oceanic basins. We identify some effective regional templates for monitoring methylmercury (MeHg) availability in the environment, but overall illustrate that there is a general lack of regional biomonitoring initiatives around the world, especially in Africa, Australia, Indo-Pacific, Middle East, and South Atlantic and Pacific Oceans. Temporal trend data for Hg in biota are generally limited. Ecologically sensitive sites (where biota have above average MeHg tissue concentrations) have been identified throughout the world. Efforts to model and quantify ecosystem sensitivity locally, regionally, and globally could help establish effective and efficient biomonitoring programs. We present a framework for a global Hg biomonitoring network that includes a three-step continental and oceanic approach to integrate existing biomonitoring efforts and prioritize filling regional data gaps linked with key Hg sources. We describe a standardized approach that builds on an evidence-based evaluation to assess the Minamata Convention's progress to reduce the impact of global Hg pollution on people and the environment.

Shark conservation requires mortality-limiting regulations amid global change.

Despite anti-finning laws aimed at conserving sharks, Worm et al. have revealed that global shark mortality rates have surprisingly risen over the past decade, driven in large part by increased demand for meat. Here, we discuss the importance of this study, underscoring the need for broader regulations addressing overall shark mortality amid threats from global change.

Animal migration in the Anthropocene: threats and mitigation options.

Animal migration has fascinated scientists and the public alike for centuries, yet migratory animals are facing diverse threats that could lead to their demise. The Anthropocene is characterised by the reality that humans are the dominant force on Earth, having manifold negative effects on biodiversity and ecosystem function. Considerable research focus has been given to assessing anthropogenic impacts on the numerical abundance of species/populations, whereas relatively less attention has been devoted to animal migration. However, there are clear linkages, for example, where human-driven impacts on migration behaviour can lead to population/species declines or even extinction. Here, we explore anthropogenic threats to migratory animals (in all domains - aquatic, terrestrial, and aerial) using International Union for the Conservation of Nature (IUCN) Threat Taxonomy classifications. We reveal the diverse threats (e.g. human development, disease, invasive species, climate change, exploitation, pollution) that impact migratory wildlife in varied ways spanning taxa, life stages and type of impact (e.g. from direct mortality to changes in behaviour, health, and physiology). Notably, these threats often interact in complex and unpredictable ways to the detriment of wildlife, further complicating management. Fortunately, we are beginning to identify strategies for conserving and managing migratory animals in the Anthropocene. We provide a set of strategies that, if embraced, have the potential to ensure that migratory animals, and the important ecological functions sustained by migration, persist.

A novel intrauterine satellite transmitter to identify parturition in large sharks.

Determining where and when animals give birth is critical for establishing effective conservation management that protects vulnerable life stages (e.g., pregnant females and newborns) and places (e.g., nursery grounds). To date, this information has been elusive in the case of highly migratory sharks in the wild. Here, we report on the deployment a of novel intrauterine satellite tag implanted in two highly mobile apex predators, the tiger shark (Galeocerdo cuvier) and the scalloped hammerhead (Sphyrna lewini), that remotely documented the location and timing of birth by a highly migratory oceanic animal in the wild. This novel technology will be especially valuable for the protection of threatened and endangered shark species, where protection of pupping and nursery grounds is a conservation priority.

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.

3D visualization processes for recreating and studying organismal form.

The study of biological form is a vital goal of evolutionary biology and functional morphology. We review an emerging set of methods that allow scientists to create and study accurate 3D models of living organisms and animate those models for biomechanical and fluid dynamic analyses. The methods for creating such models include 3D photogrammetry, laser and CT scanning, and 3D software. New multi-camera devices can be used to create accurate 3D models of living animals in the wild and captivity. New websites and virtual reality/augmented reality devices now enable the visualization and sharing of these data. We provide examples of these approaches for animals ranging from large whales to lizards and show applications for several areas: Natural history collections; body condition/scaling, bioinspired robotics, computational fluids dynamics (CFD), machine learning, and education. We provide two datasets to demonstrate the efficacy of CFD and machine learning approaches and conclude with a prospectus.

The role of context in elucidating drivers of animal movement.

Despite its consequences for ecological processes and population dynamics, intra-specific variability is frequently overlooked in animal movement studies. Consequently, the necessary resolution to reveal drivers of individual movement decisions is often lost as animal movement data are aggregated to infer average or population patterns. Thus, an empirical understanding of why a given movement pattern occurs remains patchy for many taxa, especially in marine systems. Nonetheless, movement is often rationalized as being driven by basic life history requirements, such as acquiring energy (feeding), reproduction, predator-avoidance, and remaining in suitable environmental conditions. However, these life history requirements are central to every individual within a species and thus do not sufficiently account for the high intra-specific variability in movement behavior and hence fail to fully explain the occurrence of multiple movement strategies within a species. Animal movement appears highly context dependent as, for example, within the same location, the behavior of both resident and migratory individuals is driven by life history requirements, such as feeding or reproduction, however different movement strategies are utilized to fulfill them. A systematic taxa-wide approach that, instead of averaging population patterns, incorporates and utilizes intra-specific variability to enable predictions as to which movement patterns can be expected under a certain context, is needed. Here, we use intra-specific variability in elasmobranchs as a case study to introduce a stepwise approach for studying animal movement drivers that is based on a context-dependence framework. We examine relevant literature to illustrate how this context-focused approach can aid in reliably identifying drivers of a specific movement pattern. Ultimately, incorporating behavioral variability in the study of movement drivers can assist in making predictions about behavioral responses to environmental change, overcoming tagging biases, and establishing more efficient conservation measures.

Serum Protein Electrophoresis Reference Intervals for Six Species of Wild-Sampled Sharks in South Florida.

Serum proteins found in the blood have been used as diagnostic markers in both human and animal medicine. Evaluating proteins in the blood of sharks may be a valuable way to assess shark health. The purpose of this study was to perform serum protein electrophoresis from non-lethal blood samples of wild sharks and establish baseline values for six species off South Florida: blacknose (Carcharhinus acronotus), blacktip (C. limbatus), bull (C. leucas), lemon (Negaprion brevirostris), sandbar (C. plumbeus), and tiger shark (Galeocerdo cuvier). Two hundred and fifty-one serum samples were collected between 2015-2018 along with sex determination and morphometric measurements. Agarose gel analysis was performed using mammalian protein fraction delimits albumin, alpha 1-globulins, alpha 2-globulins, beta globulins, and gamma globulins alternatively defined as fractions 1-5. Reference electrophoretic profiles were established for each species, revealing the dominance of protein fractions 3 and 4. The fraction 3:4 ratio was determined for each shark and reference intervals for total solids, protein fractions, and fraction 3:4 ratio are reported for each species. There were no significant differences in total solids or protein fractions between males and females of any species. In both blacktip sharks and bull sharks, total solids were positively correlated with body size, but not in the other species evaluated. In blacknose sharks, the fraction 3:4 ratio was positively correlated with body condition. Results suggest that there may be differences in total solids values across dry and wet seasons for some species. Newly established reference intervals can now be utilized in future research to evaluate the health of captive sharks and to investigate the health status of individuals in the wild as well as relate health measures to environmental conditions.

Predator-prey landscapes of large sharks and game fishes in the Florida Keys.

Interspecific interactions can play an essential role in shaping wildlife populations and communities. To date, assessments of interspecific interactions, and more specifically predator-prey dynamics, in aquatic systems over broad spatial and temporal scales (i.e., hundreds of kilometers and multiple years) are rare due to constraints on our abilities to measure effectively at those scales. We applied new methods to identify space-use overlap and potential predation risk to Atlantic tarpon (Megalops atlanticus) and permit (Trachinotus falcatus) from two known predators, great hammerhead (Sphyrna mokarran) and bull (Carcharhinus leucas) sharks, over a 3-year period using acoustic telemetry in the coastal region of the Florida Keys (USA). By examining spatiotemporal overlap, as well as the timing and order of arrival at specific locations compared to random chance, we show that potential predation risk from great hammerhead and bull sharks to Atlantic tarpon and permit are heterogeneous across the Florida Keys. Additionally, we find that predator encounter rates with these game fishes are elevated at specific locations and times, including a prespawning aggregation site in the case of Atlantic tarpon. Further, using machine learning algorithms, we identify environmental variability in overlap between predators and their potential prey, including location, habitat, time of year, lunar cycle, depth, and water temperature. These predator-prey landscapes provide insights into fundamental ecosystem function and biological conservation, especially in the context of emerging fishery-related depredation issues in coastal marine ecosystems.

Effects of urbanization on the nutritional ecology of a highly active coastal shark: Preliminary insights from trophic markers and body condition.

The synergistic effects of coastal urbanization have dramatically impacted biological communities. Yet, few studies have investigated how urbanization can influence the diet quality and trophic ecology of coastal sharks. In a preliminary study, we examined for spatial variation in the nutritional ecology of a highly active marine predator, the blacktip (Carcharhinus limbatus) exposed to regional differences in coastal urbanization in southeast Florida. We used medium-term nutritional indicators (i.e., body condition and whole blood stable isotopes [δ15N and δ13C]) and short-term dietary markers (i.e., plasma fatty acid profiles) to test the hypothesis that blacktip sharks sampled within highly urbanized areas (hereafter, 'urban sharks') would exhibit higher body condition, but lower diet quality, compared to conspecifics sampled in areas exposed to relatively low levels of urbanization (hereafter, 'urban sharks'). Our initial results showed that urban blacktip sharks exhibited relatively higher body condition, blood δ15N levels, and percentages of saturated fatty acids compared to non-urban sharks. Collectively, these results suggest a possible positive alteration in the amount of food consumed by blacktip sharks in the study region and/or in the caloric value of their prey. We also found lower percentages of bacterial markers and higher values of dinoflagellate markers in urban sharks. Accordingly, we did not detect an expected reduction in diet quality (in terms of essential fatty acids) in this highly active species exposed to urbanization, as has been previously reported in a resident shark species (Ginglymostoma cirratum). Therefore, it is possible that lifestyle and feeding behavior influence the quality of food consumed by urban sharks. We suspect that impacts of urbanization are more pronounced in resident, sedentary and benthic species.

Ocean warming alters the distributional range, migratory timing, and spatial protections of an apex predator, the tiger shark (Galeocerdo cuvier).

Given climate change threats to ecosystems, it is critical to understand the responses of species to warming. This is especially important in the case of apex predators since they exhibit relatively high extinction risk, and changes to their distribution could impact predator-prey interactions that can initiate trophic cascades. Here we used a combined analysis of animal tracking, remotely sensed environmental data, habitat modeling, and capture data to evaluate the effects of climate variability and change on the distributional range and migratory phenology of an ectothermic apex predator, the tiger shark (Galeocerdo cuvier). Tiger sharks satellite tracked in the western North Atlantic between 2010 and 2019 revealed significant annual variability in the geographic extent and timing of their migrations to northern latitudes from ocean warming. Specifically, tiger shark migrations have extended farther poleward and arrival times to northern latitudes have occurred earlier in the year during periods with anomalously high sea-surface temperatures. A complementary analysis of nearly 40 years of tiger shark captures in the region revealed decadal-scale changes in the distribution and timing of shark captures in parallel with long-term ocean warming. Specifically, areas of highest catch densities have progressively increased poleward and catches have occurred earlier in the year off the North American shelf. During periods of anomalously high sea-surface temperatures, movements of tracked sharks shifted beyond spatial management zones that had been affording them protection from commercial fishing and bycatch. Taken together, these study results have implications for fisheries management, human-wildlife conflict, and ecosystem functioning.

Loss of an apex predator in the wild induces physiological and behavioural changes in prey.

Predators can impact prey via predation or risk effects, which can initiate trophic cascades. Given widespread population declines of apex predators, understanding and predicting the associated ecological consequences is a priority. When predation risk is relatively unpredictable or uncontrollable by prey, the loss of predators is hypothesized to release prey from stress; however, there are few tests of this hypothesis in the wild. A well-studied predator-prey system between white sharks (Carcharodon carcharias) and Cape fur seals (Arctocephalus pusillus pusillus) in False Bay, South Africa, has previously demonstrated elevated faecal glucocorticoid metabolite concentrations (fGCMs) in seals exposed to high levels of predation risk from white sharks. A recent decline and disappearance of white sharks from the system has coincided with a pronounced decrease in seal fGCM concentrations. Seals have concurrently been rafting further from shore and over deeper water, a behaviour that would have previously rendered them vulnerable to attack. These results show rapid physiological and behavioural responses by seals to release from predation stress. To our knowledge, this represents the first demonstration in the wild of physiological changes in prey from predator decline, and such responses are likely to increase given the scale and pace of apex predator declines globally.

Space use patterns of sharks in relation to boat activity in an urbanized coastal waterway.

Aquatic ecosystems face numerous anthropogenic threats associated with coastal urbanization, with boat activity being among the most prevalent. The present study aimed to evaluate a potential relationship between boat activity and shark space use in Biscayne Bay, Florida (USA), a coastal waterway exposed to high levels of boating. Spatiotemporal patterns in boat density and traffic were determined from aerial surveys and underwater acoustic recorders, respectively. These data were then compared with residency patterns of bull (Carcharhinus leucas), nurse (Ginglymostoma cirratum) and great hammerhead (Sphyrna mokarran) sharks quantified through passive acoustic telemetry. Results were mixed, with no detectable relationship between boat density and shark residency for any of the species. Hourly presence of G. cirratum decreased with increasing boat traffic, a relationship not seen in the other two species. Explanations for these results include habituation of sharks to the high levels of chronic boat activity in the study area and interspecific differences in hearing sensitivity.

Physiological markers suggest energetic and nutritional adjustments in male sharks linked to reproduction.

Energetic condition is one of the most important factors that influence fitness and reproductive performance in vertebrates. Yet, we lack evidence on how energetic states change in response to reproduction in large marine vertebrates. In the present study, we used a non-lethal approach to assess relationships among reproductive stage, circulating steroid hormones (testosterone and relative corticosteroid levels), plasma fatty acids, and the ketone body ß-hydroxybutyrate in male sharks of two species with divergent ecologies, the benthic nurse shark (Ginglymostoma cirratum) and the epipelagic blacktip shark (Carcharhinus limbatus). We found higher relative corticosteroid levels in adult nurse sharks during the pre-mating period and in blacktip sharks during the mating period. Higher levels of ß-hydroxybutyrate were found in adult nurse sharks during the mating period, but concentrations of this ketone body did not significantly vary across reproductive stages in blacktip sharks. We also detected reduced percentages of essential fatty acids during the mating period of both nurse and blacktip sharks. Taken together, our findings suggest that nurse and blacktip sharks differ in their energetic strategy to support reproduction, however, they likely rely on physiologically important fatty acids during mating, to support spermatogenesis.

Metabolic and nutritional condition of juvenile tiger sharks exposed to regional differences in coastal urbanization.

How varying levels of human activity, such as proximity and size of the nearest market (i.e., market gravity), influence the nutritional ecology and physiological condition of highly migratory marine predators is poorly understood. In the present study, we used a non-lethal approach to compare the concentration of metabolic hormones (i.e. corticosteroids and thyroid hormones) and plasma fatty acids between juvenile female tiger sharks (Galeocerdo cuvier) sampled in two areas of the subtropical north Atlantic, which differed markedly in their levels of coastal urbanization, Florida and the Bahamas (high versus low, respectively). We hypothesized that juvenile female tiger sharks sampled in water surrounding high coastal urbanization (Florida), would exhibit evidence of lower prey quality and higher energetic demands as compared to individuals sampled in relatively less urbanized areas of Northern Bahamas. Results revealed that relative corticosteroid levels (a proxy for energy mobilization) were higher in juvenile female tiger sharks sampled in Florida; however, no differences were found in concentrations of thyroid hormones (proxies of energetic adjustments) between the two locations. We found higher percentages of omega-3 polyunsaturated fatty acids (indicative of high prey quality) in juvenile tiger sharks from Florida, whereas higher percentages of bacterial markers (often indicative of domestic sewage effluent) were detected in the individuals sampled in the Bahamas. Taken together, these findings do not suggest that the differences in nutritional quality and metabolic condition found between the two sampling locations can be fully attributed to foraging in areas exposed to differing levels of urbanization. We speculate that these patterns may be due to the highly migratory nature and generalist feeding strategy of this species, even at the juvenile life stage, as well as proximity of sampling locations from shore.

Negative metal bioaccumulation impacts on systemic shark health and homeostatic balance.

Contamination by metals is among the most pervasive anthropogenic threats to the environment. Despite the ecological importance of marine apex predators, the potential negative impacts of metal bioaccumulation and biomagnification on the health of higher trophic level species remains unclear. To date, most toxicology studies in sharks have focused on measuring metal concentrations in muscle tissues associating human consumption and food safety, without further investigating potential impacts on shark health. To help address this knowledge gap, the present study evaluated metal concentrations in the gills, muscle, liver and rectal gland of coastal sharks opportunistically sampled from Brazilian waters and tested for potential relationships between metal bioaccumulation and general shark health and homeostatic balance metrics. Results revealed high metal concentrations in all four tissue types, with levels varying in relation to size, sex, and life-stage. Metal concentrations were also associated with serum biomarkers (urea, lactate, ALT, triglycerides, alkaline phosphatase, and phosphorus) and body condition, suggesting potential negative impacts on organismal health.

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.

Bacterial Communities in Multiple Tissues Across the Body Surface of Three Coastal Shark Species.

Bacteria are known to have explicit roles within the microbiomes of host tissues, therefore examining these communities may prove useful in assessing host health and responses to environmental change. The present study contributes to the emerging, yet understudied, field of microbiome research in elasmobranchs. We provide a screening of the culturable bacteria communities found on multiple tissue sites on the body surface of blacktip (Carcharhinus limbatus), bull (Carcharhinus leucas), and tiger (Galeocerdo cuvier) sharks near Miami, Florida. Tissue sites include mouth, gills, skin, and any visible wounds. The study adds to our understanding of the diversity of bacteria present on sharks in comparison to their natural environment. We also compare bacterial groups found within wounds in shark skin to healthy tissue sites on the same individual. Results indicate that wounds on an individual may allow for opportunistic bacteria to invade or overgrow where they would not normally be found, which may have potential health consequences for sharks that become wounded due to fishing practices. Identified bacteria belonged to the Actinobacteria, Firmicutes, and Proteobacteria phyla, known to be prominent bacterial groups associated with marine organisms. Results indicate shark species-specific differences in bacterial communities, including the presence of bacteria belonging to Planococcaceae exclusively on the skin of tiger sharks. To our knowledge, this is the first report of this family in any elasmobranch. While most tissue sites displayed commensal bacteria identified in similar studies, known pathogens belonging to Vibrionaceae and Staphylococcaceae were identified in the wounds of blacktip and bull sharks. Some bacteria may be normal residents, but the loss of protective dermal denticles due to a wound may allow colonization by pathogens. Continued research is needed to explore microbial communities associated with sharks and their influence on host health.

Variation of body condition and plasma energy substrates with life stage, sex, and season in wild-sampled nurse sharks Ginglymostoma cirratum.

Reported here are the relationships among morphological (i.e., body condition) and biochemical (i.e., plasma concentrations of triglycerides, cholesterol, free fatty acids, and ketone bodies and ketone body ratios) parameters related to energy storage and use, as well as the variation of such parameters, for 107 free-ranging nurse sharks Ginglymostoma cirratum sampled off South Florida. Immature G. cirratum exhibited a higher variance in body condition, plasma free fatty acid concentrations and ketone body ratios compared to adults. Mature female G. cirratum had significantly higher body condition than mature males, driven by a seasonal increase in mature female body condition during the wet season. Mature male G. cirratum showed a decrease in the ketone body ß-hydroxybutyric acid during the dry season. Taken together, this study provides a baseline assessment of body condition and internal physiological state for a data-poor marine species and demonstrates significant ontogenetic, sexual and seasonal variation in G. cirratum energetic state. As concluded by other studies of energy metabolism in free-ranging sharks, this research highlights the importance of considering intraspecific patterns and sampling context for inferring the drivers of variation.