Why aquatic scientists should use sulfur stable isotope ratios (ẟ34S) more often.

Over the last few decades, measurements of light stable isotope ratios have been increasingly used to answer questions across physiology, biology, ecology, and archaeology. The vast majority analyse carbon (δ13C) and nitrogen (δ15N) stable isotopes as the 'default' isotopes, omitting sulfur (δ34S) due to time, cost, or perceived lack of benefits and instrumentation capabilities. Using just carbon and nitrogen isotopic ratios can produce results that are inconclusive, uncertain, or in the worst cases, even misleading, especially for scientists that are new to the use and interpretation of stable isotope data. Using sulfur isotope values more regularly has the potential to mitigate these issues, especially given recent advancements that have lowered measurement barriers. Here we provide a review documenting case studies with real-world data, re-analysing different biological topics (i.e. niche, physiology, diet, movement and bioarchaeology) with and without sulfur isotopes to highlight the various strengths of this stable isotope for various applications. We also include a preliminary meta-analysis of the trophic discrimination factor (TDF) for sulfur isotopes, which suggest small (mean -0.4 ± 1.7 ‰ SD) but taxa-dependent mean trophic discrimination. Each case study demonstrates how the exclusion of sulfur comes at the detriment of the results, often leading to very different outputs, or missing valuable discoveries entirely. Given that studies relying on carbon and nitrogen stable isotopes currently underpin most of our understanding of various ecological processes, this has concerning implications. Collectively, these examples strongly suggest that researchers planning to use carbon and nitrogen stable isotopes for their research should incorporate sulfur where possible, and that the new 'default' isotope systems for aquatic science should now be carbon, nitrogen, and sulfur.

Feeding behavior of yellowfin tuna around two insular regions of the western Atlantic Ocean.

The yellowfin tuna is a very abundant tropical tuna species in the western equatorial Atlantic Ocean and an important fishery resource for the Brazilian tuna fleet. In this study we performed stable isotope analysis to better understand the spatial trophodynamics and dietary changes in yellowfin tuna around two insular marine protected areas in Brazil. A total of 65 yellowfin tuna specimens measuring between 47 and 138 cm LT (total length) were sampled around the archipelagos of Fernando de Noronha (FNA; n = 34) and Saint Peter and Saint Paul (SPSPA; n = 31) between July 2018 and September 2019. Bayesian mixing models and generalized additive models were used to investigate the contributions of four different prey items (zooplankton, cephalopods, fish larvae, and flying fish) to yellowfin tuna diet in each area and their potential changes in relation to predator growth. The four prey items were found to have different overall contributions between the two studied areas, with zooplankton being the most important prey in FNA, whereas flying fish was the most relevant prey to the species' diet in SPSPA. Significant changes in the species diet by size were also found, with fish smaller than 90 cm (TL) having a more generalist diet and larger animals relying more on consuming larger and more nutritious prey (i.e., flying fish). Our results suggest that these two marine protected areas play an important role in ocean dynamics, providing important and different foraging grounds for the development of this predator species.

Bull Shark (Carcharhinus leucas) Occurrence along Beaches of South-Eastern Australia: Understanding Where, When and Why.

Unprovoked shark bites have increased over the last three decades, yet they are still relatively rare. Bull sharks are globally distributed throughout rivers, estuaries, nearshore areas and continental shelf waters, and are capable of making long distance movements between tropical and temperate regions. As this species is implicated in shark bites throughout their range, knowledge of the environmental drivers of bull shark movements are important for better predicting the likelihood of their occurrence at ocean beaches and potentially assist in reducing shark bites. Using the largest dataset of acoustically tagged bull sharks in the world, we examined the spatial ecology of 233 juvenile and large (including sub-adult and adult) bull sharks acoustically tagged and monitored over a 5.5-year period (2017-2023) using an array of real-time acoustic listening stations off 21 beaches along the coast of New South Wales, Australia. Bull sharks were detected more in coastal areas of northern NSW (<32° S) but they travelled southwards during the austral summer and autumn. Juveniles were not detected on shark listening stations until they reached 157 cm and stayed north of 31.98° S (Old Bar). Intra-specific diel patterns of occurrence were observed, with juveniles exhibiting higher nearshore presence between 20:00 and 03:00, whilst the presence of large sharks was greatest from midday through to 04:00. The results of generalised additive models revealed that large sharks were more often found when water temperatures were higher than 20 °C, after >45 mm of rain and when swell heights were between 1.8 and 2.8 m. Understanding the influence that environmental variables have on the occurrence of bull sharks in the coastal areas of NSW will facilitate better education and could drive shark smart behaviour amongst coastal water users.

Ontogenetic changes in the tooth morphology of bull sharks (Carcharhinus leucas).

Teeth are an integral component of feeding ecology, with a clear link between tooth morphology and diet, as without suitable dentition prey cannot be captured nor broken down for consumption. Bull sharks, Carcharhinus leucas, undergo an ontogenetic niche shift from freshwater to marine habitats, which raises the question: does tooth morphology change with ontogeny? Tooth shape, surface area and thickness were measured using both morphometrics and elliptic Fourier analysis to determine if morphology varied with position in the jaw and if there was an ontogenetic change concordant with this niche shift. Significant ontogenetic differences in tooth morphology as a function of position in the jaw and shark total length were found, with upper and lower jaws of bull sharks presenting two different tooth morphologies. Tooth shape and thickness fell into two groupings, anterior and posterior, in both the upper and lower jaws. Tooth surface area, however, indicated three groupings, mesial, intermediate and distal, in both the upper and lower jaws. While tooth morphology changed significantly with size, showing an inflection at sharks of 135 cm total length, each morphological aspect retained the same tooth groupings throughout. These ontogenetic differences in tooth morphologies reflect tooth strength, prey handling and heterodonty.

Forecasting intraspecific changes in distribution of a wide-ranging marine predator under climate change.

Globally, marine animal distributions are shifting in response to a changing climate. These shifts are usually considered at the species level, but individuals are likely to differ in how they respond to the changing conditions. Here, we investigate how movement behaviour and, therefore, redistribution, would differ by sex and maturation class in a wide-ranging marine predator. We tracked 115 tiger sharks (Galeocerdo cuvier) from 2002 to 2020 and forecast class-specific distributions through to 2030, including environmental factors and predicted occurrence of potential prey. Generalised Linear and Additive Models revealed that water temperature change, particularly at higher latitudes, was the factor most associated with shark movements. Females dispersed southwards during periods of warming temperatures, and while juvenile females preferred a narrow thermal range between 22 and 23 °C, adult female and juvenile male presence was correlated with either lower (< 22 °C) or higher (> 23 °C) temperatures. During La Niña, sharks moved towards higher latitudes and used shallower isobaths. Inclusion of predicted distribution of their putative prey significantly improved projections of suitable habitats for all shark classes, compared to simpler models using temperature alone. Tiger shark range off the east coast of Australia is predicted to extend ~ 3.5° south towards the east coast of Tasmania, particularly for juvenile males. Our framework highlights the importance of combining long-term movement data with multi-factor habitat projections to identify heterogeneity within species when predicting consequences of climate change. Recognising intraspecific variability will improve conservation and management strategies and help anticipate broader ecosystem consequences of species redistribution due to ocean warming.

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.

Overcoming multi-year impacts of maternal isotope signatures using multi-tracers and fast turnover tissues in juvenile sharks.

Stable isotopes are often used to determine the ecological role of different age classes of animals, but particularly for young animals this approach may be compromised. During gestation and or incubation body tissues of the young are derived directly from the mother. In neonates or post hatching, there is a period of transformation as the young grow and forage independently, but during this period different organs will continue to reflect the maternal isotopic signature as a function of their turnover rate. How long this maternal hangover persists remains poorly understood. We applied a multi-tracer approach (δ15N, δ13C and δ34S) to stable isotope signatures in juvenile bull sharks (Carcharhinus leucas) up to 6.5 years post parturition. We found that maternal provisioning was detectable for up to 3.5 years after birth in muscle but only detectable in young-of-the-year for liver. Inclusion of sulphur revealed when maternal signatures disappeared from low-turnover tissue, while also identifying the spatial and trophic ecology patterns from fast-turnover tissue. These results reveal the importance of sampling fast turnover tissues to study the trophic ecology of juvenile elasmobranchs, and how the use of only δ15N and δ13C isotopes is likely to make maternal patterns more difficult to detect.

Physiological Impairment as a Result of Bile Accumulation in an Apex Predator, the Tiger Shark (Galeocerdo cuvier Péron & Lesueur, 1822).

Physiological adaptations have evolved to help sharks face rapid periods of feast. Tiger sharks are generalist apex predators that rely on a high-lipid/protein diet. To achieve a satisfactory nutritional condition, proper lipid absorption and hepatic storage are needed. Bile secretion in sharks is low and sporadic but increases during short periods of fasting. The present study describes a physiological impairment caused by bile accumulation in juvenile tiger sharks, possibly due to prolonged fasting. These evidences suggest that, even though sharks have adaptations that prevent them from dying from starvation, alarming physiological alterations might occur. Future studies are needed to assess how such a condition can affect wild populations, as well as possible sublethal consequences that could impact their long-term survival.

Thermal Imaging Reveals Changes in Body Surface Temperatures of Blacktip Sharks (Carcharhinus limbatus) during Air Exposure.

Fish physiology is significantly affected by temperature variability. During fisheries interactions, fish are often exposed to air and subjected to rapid temperature changes. Fish thermal dynamics during such exposure, and the possible outcomes to their physiology, depend on how heat is distributed across their bodies, the speed at which their body temperatures change, and the size of the individual. Nevertheless, such thermal patterns remain unknown for sharks. This study employed a novel application of thermal imaging to evaluate external body temperature profiles of blacktip sharks (Carcharhinus limbatus) above-water exposure after capture. We found that above-water exposure duration, shark total length, and air temperature on the day of capture significantly influenced body surface temperatures of the analyzed sharks ([Formula: see text]). Body surface temperature significantly increased with increasing exposure; however, thermal profiles of immature sharks (<140 cm) were significantly warmer than those of mature sharks. Moreover, blacktip surface body temperatures were significantly higher during days when air temperatures were at least 2.5°C warmer than water temperatures. We discuss these results as they relate to the ecology of blacktip sharks and their potential vulnerability to fisheries capture due to such changes in peripheral body temperature.

Bioecology and movements of bull sharks, Carcharhinus leucas, caught in a long-term longline survey off northeastern Brazil

A robust understanding of habitat usage by coastal shark species, and how it overlaps with human presence in densely-populated regions is needed to inform the development of efficient conservation strategies for these important top predators. An intensive longline survey conducted in nearshore waters off northeastern Brazil from 2004 through 2014 caught a total of 18 bull sharks (Carcharhinus leucas) (male-female ratio = 0.63:1), which can be dangerous to humans. Although most sharks were sexually mature, there was no evidence that this region could be used as a parturition or nursery area. Prey items identified in the guts of the sharks comprised teleosts, mollusks and elasmobranchs. Additionally, one satellite-tagged bull shark covered a great distance (> 3,000 km) in 75 days at liberty, making most use of shallow waters (< 20 m depth) and presumably also entering an estuarine area. Although bull sharks are not an important fishery resource in this region, such a reduced abundance coupled with its affinity for coastal and inshore habitats highlights the potential vulnerability of C. leucas to deleterious anthropic interferences off northeastern Brazil.(AU)

Um melhor entendimento sobre a utilização de hábitat das espécies de tubarões costeiros, e como ela se sobrepõe à presença humana em regiões altamente populosas, se faz necessário a fim de subsidiar o desenvolvimento de eficientes medidas de conservação para esses importantes predadores de topo. Um estudo intensivo utilizando espinhel, conduzido em águas costeiras do nordeste do Brasil entre os anos de 2004 e 2014, capturou um total de 18 tubarões cabeça-chata (Carcharhinus leucas) (proporção macho-fêmea = 0,63:1), os quais podem ser perigosos para humanos. Apesar da maioria dos tubarões estarem sexualmente maduros, não houve evidências de que essa região esteja sendo utilizada como uma área de parto ou berçário. Entre os itens alimentares identificados foram encontrados teleósteos, moluscos e elasmobrânquios. Além disso, um tubarão cabeça-chata marcado com um transmissor satélite percorreu uma grande distância (> 3.000 km) em 75 dias em liberdade, fazendo o uso de águas superficiais (< 20 m profundidade) e presumivelmente entrando em uma área estuarina. Apesar de os tubarões cabeça-chata não corresponderem a um recurso pesqueiro importante nessa região, tal reduzida abundância juntamente com a sua afinidade por hábitats costeiros reforçam a potencial vulnerabilidade de C. leucas às interferências antrópicas deletérias ao longo da costa nordeste do Brasil.(AU)