Trophic niche partitioning of five sympatric shark species in the tropical eastern Pacific Ocean revealed by multi-tissue fatty acid analysis.

Fatty acid (FA) analysis of consumer tissues has recently shown utility in drawing further inferences about trophic niche dynamics of marine predators such as sharks. In this study, we examined liver, plasma, and muscle FAs in five coexisting pelagic sharks (blue (Prionace glauca), silky (Carcharhinus falciformis), bigeye thresher (Alopias superciliosus), pelagic thresher (Alopias pelagicus), and smooth hammerhead (Sphyrna zygaena)) inhabiting the tropical eastern Pacific Ocean. Results showed complex inter- and intra-individual and tissue variation among the five shark species. Based on multivariate analysis of the muscle FAs, P. glauca and C. falciformis have the largest FA niche widths, indicating diverse feeding habits or habitat isolation, whereas A. pelagicus and S. zygaena occupied a narrower niche width, reflecting increased trophic specialization. High percentages of muscle FA niche overlap indicated strong resource competition between S.zygaena and C. falciformis and a degree of dietary isolation by P. glauca. Interpretations of feeding ecology differed based on the analysis of plasma FAs, which could be attributed to higher dietary FA turnover rates. The liver was deemed unsuitable to examine FA niche metrics based on high and unexplained intra-specific variance in liver FAs as well as the unique lipid metabolism in chondrichthyans. Overall, our multi-tissue approach revealed the magnitude of potential competitive interactions among coexisting tropical shark species. It also expanded our understanding of inter-tissue variability and best practices when using FA analysis to estimate trophic niche metrics of sharks.

Mercury bioaccumulation in thresher sharks from the eastern tropical Pacific: Influences of body size, maturation stage, and feeding habitat.

Sharks, as top order predators, provide a guidance on how contaminants such as mercury bioaccumulate in marine environments. This study assessed the bioaccumulation of mercury (total mercury, THg) in the muscle, liver, red blood cells (RBC), and plasma of pelagic and bigeye thresher sharks (Alopias pelagicus and A. superciliosus) from eastern tropical Pacific. Additionally, the concentration of methylmercury (MeHg) in muscle was also determined to assess risks for human consumption. For both species, muscle THg concentrations (4.05 ± 2.15 and 4.12 ± 1.84 µg g-1 dry weight for pelagic and bigeye thresher shark) were higher than that in other tissues. THg concentrations for all tissues were significantly correlated with precaudal length, with higher accumulation rates after maturity in pelagic than bigeye thresher sharks, suggesting an associated dietary shift at maturation. Correlations among tissues in both species suggested similar transportation and distribution patterns in internal tissues. The δ13C values in muscle, RBC and plasma suggested that habitat shifts influenced Hg accumulation, whereas trophic position, estimated by δ15N values, had limited effects on patterns of Hg bioaccumulation. Diet shifts towards prey more cephalopods that content higher Hg than small fishes (large fishes: 1.77 µg g-1; cephalopods: 0.66 µg g-1 and small fishes 0.48 µg g-1, dry weight) increased Hg accumulation rates in adult pelagic thresher sharks. Concentrations of MeHg in the muscle of both thresher shark (3.42 ± 1.68 µg g-1 in A. pelagicus and 3.78 ± 2.13 µg g-1 in A. superciliosus) exceeded the recommended levels for human consumption. This research provides insight into the factors influencing mercury bioaccumulation in thresher sharks, which are essential for the management and conservation of these species.

Fatty acid profiles of more than 470 marine species from the Southern Hemisphere.

Lipid and fatty acid datasets are commonly used to assess the nutritional composition of organisms, trophic ecology, and ecosystem dynamics. Lipids and their fatty acid constituents are essential nutrients to all forms of life because they contribute to biological processes such as energy flow and metabolism. Assessment of total lipids in tissues of organisms provides information on energy allocation and life-history strategies and can be an indicator of nutritional condition. The analysis of an organism's fatty acids is a widely used technique for assessing nutrient and energy transfer, and dietary interactions in food webs. Although there have been many published regional studies that assessed lipid and fatty acid compositions, many only report the mean values of the most abundant fatty acids. There are limited individual records available for wider use in intercomparison or macro-scale studies. This dataset consists of 4856 records of individual and pooled samples of at least 470 different marine consumer species sampled from tropical, temperate, and polar regions around Australia and in the Southern, Indian, and Pacific Oceans from 1989 to 2018. This includes data for a diverse range of taxa (zooplankton, fish, cephalopods, chondrichthyans, and marine mammals), size ranges (0.02 cm to ~13 m), and that cover a broad range of trophic positions (2.0-4.6). When known, we provide a record of species name, date of sampling, sampling location, body size, relative (%) measurements of tissue-specific total lipid content and abundant fatty acids, and absolute content (mg 100 g-1 tissue) of eicosapentaenoic acid (EPA, 20:5n3) and docosahexaenoic acid (DHA, 22:6n3) as important long-chain (≥C20 ) polyunsaturated omega-3 fatty acids. These records form a solid basis for comparative studies that will facilitate a broad understanding of the spatial and temporal distribution of marine lipids globally. The dataset also provides reference data for future dietary assessments of marine predators and model assessments of potential impacts of climate change on the availability of marine lipids and fatty acids. There are 480 data records within our data file for which the providers have requested that permission for reuse be granted, with the likely condition that they are included as a coauthor on the reporting of the dataset. Records with this condition are indicated by a "yes" under "Conditions_of_data_use" in Data S1: Marineconsumer_FAdata.csv (see Table 2 in Metadata S1 for more details). For all other data records marked as "No" under "Conditions_of_data_use," there are no copyright restrictions for research and/or teaching purposes. We request that users acknowledge use of the data in publications, research proposals, websites, and other outlets via formal citation of this work and original data sources as applicable.

Effect of body size, feeding ecology and maternal transfer on mercury accumulation of vulnerable silky shark Carcharhinus falciformis in the eastern tropical pacific.

The silky shark Carcharhinus falciformis is a large pelagic species distributed in the global oceans and was recently listed as "Vulnerable" by the IUCN because of its decline in population due to overfishing. As an apex predator, the silky shark can accumulate elevated quantities of mercury (Hg), posing a potential risk to its remaining population. In this study, total Hg (THg) concentrations were determined in silky shark muscle, liver, dermis, red blood cells (RBC) and plasma sampled from the eastern tropical Pacific, and δ15N values were measured to explore the influence of feeding ecology on Hg accumulation. The highest THg concentrations were in muscle (7.81 ± 6.70 µg g-1 dry weight (dw) or 2.14 ± 1.83 µg g-1 wet weight (ww)) and liver (7.88 ± 10.22 µg g-1 dw or 4.66 ± 6.04 µg g-1 ww) rather than dermis, RBC and plasma. The THg concentrations in all tissue types were significantly correlated with fork length and showed faster accumulation rates after maturity. Maternal THg transfer was observed in silky sharks with embryos having 33.16% and 1.98% in muscle and liver compared with their respective mothers. The potentially harmful THg concentrations in silky shark tissues and embryos may lead to health problems of sharks and consumers. THg concentrations were negatively correlated with δ15N values for all tissues, indicating likely baseline variations in δ15N values that reflect changes in the foraging habitats or regions of silky sharks with size or age. Lastly, strong correlations were observed among THg concentrations of all tissue types, indicating that nonlethal sampling of muscle and dermis tissue can be used effectively to quantify THg concentration of other internal tissues.

Improving Marine Ecosystem Models with Biochemical Tracers.

Empirical data on food web dynamics and predator-prey interactions underpin ecosystem models, which are increasingly used to support strategic management of marine resources. These data have traditionally derived from stomach content analysis, but new and complementary forms of ecological data are increasingly available from biochemical tracer techniques. Extensive opportunities exist to improve the empirical robustness of ecosystem models through the incorporation of biochemical tracer data and derived indices, an area that is rapidly expanding because of advances in analytical developments and sophisticated statistical techniques. Here, we explore the trophic information required by ecosystem model frameworks (species, individual, and size based) and match them to the most commonly used biochemical tracers (bulk tissue and compound-specific stable isotopes, fatty acids, and trace elements). Key quantitative parameters derived from biochemical tracers include estimates of diet composition, niche width, and trophic position. Biochemical tracers also provide powerful insight into the spatial and temporal variability of food web structure and the characterization of dominant basal and microbial food web groups. A major challenge in incorporating biochemical tracer data into ecosystem models is scale and data type mismatches, which can be overcome with greater knowledge exchange and numerical approaches that transform, integrate, and visualize data.

Energy metabolism in mobile, wild-sampled sharks inferred by plasma lipids.

Evaluating how predators metabolize energy is increasingly useful for conservation physiology, as it can provide information on their current nutritional condition. However, obtaining metabolic information from mobile marine predators is inherently challenging owing to their relative rarity, cryptic nature and often wide-ranging underwater movements. Here, we investigate aspects of energy metabolism in four free-ranging shark species (n = 281; blacktip, bull, nurse, and tiger) by measuring three metabolic parameters [plasma triglycerides (TAG), free fatty acids (FFA) and cholesterol (CHOL)] via non-lethal biopsy sampling. Plasma TAG, FFA and total CHOL concentrations (in millimoles per litre) varied inter-specifically and with season, year, and shark length varied within a species. The TAG were highest in the plasma of less active species (nurse and tiger sharks), whereas FFA were highest among species with relatively high energetic demands (blacktip and bull sharks), and CHOL concentrations were highest in bull sharks. Although temporal patterns in all metabolites were varied among species, there appeared to be peaks in the spring and summer, with ratios of TAG/CHOL (a proxy for condition) in all species displaying a notable peak in summer. These results provide baseline information of energy metabolism in large sharks and are an important step in understanding how the metabolic parameters can be assessed through non-lethal sampling in the future. In particular, this study emphasizes the importance of accounting for intra-specific and temporal variability in sampling designs seeking to monitor the nutritional condition and metabolic responses of shark populations.

Spatial Patterns and Temperature Predictions of Tuna Fatty Acids: Tracing Essential Nutrients and Changes in Primary Producers.

Fatty acids are among the least understood nutrients in marine environments, despite their profile as key energy components of food webs and that they are essential to all life forms. Presented here is a novel approach to predict the spatial-temporal distributions of fatty acids in marine resources using generalized additive mixed models. Fatty acid tracers (FAT) of key primary producers, nutritional condition indices and concentrations of two essential long-chain (≥C20) omega-3 fatty acids (EFA) measured in muscle of albacore tuna, Thunnus alalunga, sampled in the south-west Pacific Ocean were response variables. Predictive variables were: location, time, sea surface temperature (SST) and chlorophyll-a (Chla), and phytoplankton biomass at time of catch and curved fork length. The best model fit for all fatty acid parameters included fish length and SST. The first oceanographic contour maps of EFA and FAT (FATscapes) were produced and demonstrated clear geographical gradients in the study region. Predicted changes in all fatty acid parameters reflected shifts in the size-structure of dominant primary producers. Model projections show that the supply and availability of EFA are likely to be negatively affected by increases in SST especially in temperate waters where a 12% reduction in both total fatty acid content and EFA proportions are predicted. Such changes will have large implications for the availability of energy and associated health benefits to high-order consumers. Results convey new concerns on impacts of projected climate change on fish-derived EFA in marine systems.

Lipid, fatty acid and energy density profiles of white sharks: insights into the feeding ecology and ecophysiology of a complex top predator.

Lipids are major sources of metabolic energy in sharks and are closely linked to environmental conditions and biological cycles, such as those related to diet, reproduction and migration. In this study, we report for the first time, the total lipid content, lipid class composition and fatty acid profiles of muscle and liver tissue of white sharks, Carcharodon carcharias, of various lengths (1.5-3.9 m), sampled at two geographically separate areas off southern and eastern Australia. Muscle tissue was low in total lipid content (<0.9% wet mass, wm) and was dominated by phospholipids (>90% of total lipid) and polyunsaturated fatty acids (34±12% of total fatty acids). In contrast, liver was high in total lipid which varied between 51-81% wm and was dominated by triacylglycerols (>93%) and monounsaturated fatty acids (36±12%). With knowledge of total lipid and dry tissue mass, we estimated the energy density of muscle (18.4±0.1 kJ g-1 dm) and liver (34.1±3.2 kJ g-1 dm), demonstrating that white sharks have very high energetic requirements. High among-individual variation in these biochemical parameters and related trophic markers were observed, but were not related to any one biological or environmental factor. Signature fatty acid profiles suggest that white sharks over the size range examined are generalist predators with fish, elasmobranchs and mammalian blubber all contributing to the diet. The ecological applications and physiological influences of lipids in white sharks are discussed along with recommendations for future research, including the use of non-lethal sampling to examine the nutritional condition, energetics and dietary relationships among and between individuals. Such knowledge is fundamental to better understand the implications of environmental perturbations on this iconic and threatened species.