Can biochemical tracers reveal ontogenetic trophic shift and individual prey selection in white sharks from Guadalupe Island, Northeast Pacific?

Refining the role of apex predators in marine food webs is a necessary step in predicting the consequences of their global decline under the footprint of fishing activities. White sharks (Carcharodon carcharias) are vulnerable predators, performing large migrations and able to forage on a variety of prey in different habitats. In the Northeast Pacific, juvenile and adult white sharks are found seasonally at the same aggregation sites, such as Guadalupe Island off Mexico. While adults are thought to target local pinniped colonies, very few prey-predator interactions have been documented and the diet of juveniles in this area remains poorly understood. Here we used carbon/nitrogen stable isotopes and fatty acids to characterize the trophic ecology of white sharks at Guadalupe Island. In contrast to the ontogenetic trophic shift paradigm, we detected no influence of size on muscle stable isotope and fatty acid composition, revealing no significant dietary variation between juvenile and adult sharks. Stable isotopes did not allow definitive conclusions to be drawn regarding the diet of white sharks at Guadalupe Island, due to significant variability in the contribution of different potential prey depending on the trophic discrimination factors used. However, most sharks were rich in polyunsaturated fatty acids (such as long-chain omega 3), suggesting a local diet of mainly pelagic prey (potentially large fish or cephalopods). A few individuals appeared to show recent consumption of pinnipeds, with higher proportions of saturated and monounsaturated fatty acids. These individual differences in fatty acid composition could reflect an ecological trade-off between consumption of prey rich in fat (marine mammals) versus prey rich in polyunsaturated fatty acids (pelagic prey), respectively meeting the energetic and physiological needs of white sharks. Although ontogenetic trophic changes were not able to be discerned, our results thus provide new insights into the physiological drivers of predator-prey interactions, which can benefit the definition of conservation strategies in a changing ocean.

Do marine protected areas influence mercury exposure? Insights from a shark community in the tropical Northeast Pacific.

Biomass depletion caused by overfishing is likely to alter the structure of food webs and impact mercury transfer to marine predators. Although marine protected areas (MPAs) are spared from fishing pressure, their influence on biota mercury levels is poorly understood. Here, we used carbon and nitrogen stable isotope compositions as well as mercury concentrations in fin clips to characterize foraging habitat and mercury exposure of a shark community composed of migratory and resident species of the Revillagigedo archipelago, an offshore MPA in the Northeast Pacific off Mexico. We found that the probability of finding migratory sharks in the isotopic niche of Revillagigedo-resident sharks was low, likely reflecting the use of habitats outside the archipelago by highly mobile species. Community-wide variations in mercury were primarily explained by shark length, revealing that bioaccumulation was the main driver of Hg concentrations. We failed to detect a clear effect of foraging habitat on shark mercury exposure, which may be related to migratory species using both exploited and protected areas when moving outside the Revillagigedo MPA. More similar studies on the potential mitigation of Hg contamination by MPAs are needed in the future if fishing pressure increases to satisfy the growing global human population.

Mercury stable isotopes suggest reduced foraging depth in oxygen minimum zones for blue sharks.

Oxygen minimum zones (OMZs) are currently expanding across the global ocean due to climate change, leading to a compression of usable habitat for several marine species. Mercury stable isotope compositions provide a spatially and temporally integrated view of marine predator foraging habitat and its variability with environmental conditions. Here, we analyzed mercury isotopes in blue sharks Prionace glauca from normoxic waters in the northeastern Atlantic and from the world's largest and shallowest OMZ, located in the northeastern Pacific (NEP). Blue sharks from the NEP OMZ area showed higher Δ199Hg values compared to sharks from the northeastern Atlantic, indicating a reduction in foraging depth of approximately 200 m. Our study suggests for the first time that blue shark feeding depth is altered by expanding OMZs and illustrates the use of mercury isotopes to assess the impacts of ocean deoxygenation on the vertical foraging habitat of pelagic predators.

Mercury concentrations, biomagnification and isotopic discrimination factors in two seabird species from the Humboldt Current ecosystem.

Assessing mercury (Hg) biomagnification requires the description of prey-predator relationships, for each species and ecosystem, usually based on carbon and nitrogen isotope analyses. Here, we analyzed two seabirds from the Humboldt Current ecosystem, the Guanay cormorant (Phalacrocorax bougainvillii) and the Peruvian booby (Sula variegata), as well as their main prey, the Peruvian anchovy (Engraulis ringens). We reported Hg concentrations, Hg biomagnification (BMF) and isotopic discrimination factors (Δ13C and Δ15N) in seabird whole blood. BMFs and Δ13C in our study (on wild birds where diet was not controlled) were similar to other piscivorous seabirds previously studied in captive settings, but Δ15N were lower than most captive experiments. We observed lower Hg concentrations in Humboldt seabirds compared to other oligotrophic ecosystems, possibly due to Hg biodilution in the high biomass of the first trophic levels. This work calls for a better characterization of Hg trophic dynamics in productive upwelling ecosystems.

Foraging plasticity diversifies mercury exposure sources and bioaccumulation patterns in the world's largest predatory fish.

Large marine predators exhibit high concentrations of mercury (Hg) as neurotoxic methylmercury, and the potential impacts of global change on Hg contamination in these species remain highly debated. Current contaminant model predictions do not account for intraspecific variability in Hg exposure and may fail to reflect the diversity of future Hg levels among conspecific populations or individuals, especially for top predators displaying a wide range of ecological traits. Here, we used Hg isotopic compositions to show that Hg exposure sources varied significantly between and within three populations of white sharks (Carcharodon carcharias) with contrasting ecology: the north-eastern Pacific, eastern Australasian, and south-western Australasian populations. Through Δ200Hg signatures in shark tissues, we found that atmospheric Hg deposition pathways to the marine environment differed between coastal and offshore habitats. Discrepancies in δ202Hg and Δ199Hg signatures among white sharks provided evidence for intraspecific exposure to distinct sources of marine methylmercury, attributed to population and ontogenetic shifts in foraging habitat and prey composition. We finally observed a strong divergence in Hg accumulation rates between populations, leading to three times higher Hg concentrations in large Australasian sharks compared to north-eastern Pacific sharks, and likely due to different trophic strategies adopted by adult sharks across populations. This study illustrates the variety of Hg exposure sources and bioaccumulation patterns that can be found within a single species and suggests that intraspecific variability needs to be considered when assessing future trajectories of Hg levels in marine predators.

Foraging depth depicts resource partitioning and contamination level in a pelagic shark assemblage: Insights from mercury stable isotopes.

The decline of shark populations in the world ocean is affecting ecosystem structure and function in an unpredictable way and new ecological information is today needed to better understand the role of sharks in their habitats. In particular, the characterization of foraging patterns is crucial to understand and foresee the evolution of dynamics between sharks and their prey. Many shark species use the mesopelagic area as a major foraging ground but the degree to which different pelagic sharks rely on this habitat remains overlooked. In order to depict the vertical dimension of their trophic ecology, we used mercury stable isotopes in the muscle of three pelagic shark species (the blue shark Prionace glauca, the shortfin mako shark Isurus oxyrinchus and the smooth hammerhead shark Sphyrna zygaena) from the northeastern Pacific region. The Δ199Hg values, ranging from 1.40 to 2.13‰ in sharks, suggested a diet mostly based on mesopelagic prey in oceanic habitats. We additionally used carbon and nitrogen stable isotopes (δ13C, δ15N) alone or in combination with Δ199Hg values, to assess resource partitioning between the three shark species. Adding Δ199Hg resulted in a decrease in trophic overlap estimates compared to those based on δ13C/δ15N alone, demonstrating that multi-isotope modeling is needed for accurate trophic description of the three species. Mainly, it reveals that they forage at different average depths and that resource partitioning is mostly expressed through the vertical dimension within pelagic shark assemblages. Concomitantly, muscle total mercury concentration (THg) differed between species and increased with feeding depth. Overall, this study highlights the key role of the mesopelagic zone for shark species foraging among important depth gradients and reports new ecological information on trophic competition using mercury isotopes. It also suggests that foraging depth may play a pivotal role in the differences between muscle THg from co-occurring high trophic level shark species.

The Twilight Zone as a Major Foraging Habitat and Mercury Source for the Great White Shark.

The twilight zone contains the largest biomass of the world's ocean. Identifying its role in the trophic supply and contaminant exposure of marine megafauna constitutes a critical challenge in the context of global change. The white shark (Carcharodon carcharias) is a threatened species with some of the highest concentrations of neurotoxin methylmercury (MeHg) among marine top predators. Large white sharks migrate seasonally from coastal habitats, where they primarily forage on pinnipeds, to oceanic offshore habitats. Tagging studies suggest that while offshore, white sharks may forage at depth on mesopelagic species, yet no biochemical evidence exists. Here, we used mercury isotopic composition to assess the dietary origin of MeHg contamination in white sharks from the Northeast Pacific Ocean. We estimated that a minimum of 72% of the MeHg accumulated by white sharks originates from the consumption of mesopelagic prey, while a maximum of 25% derives from pinnipeds. In addition to highlighting the potential of mercury isotopes to decipher the complex ecological cycle of marine predators, our study provides evidence that the twilight zone constitutes a crucial foraging habitat for these large predators, which had been suspected for over a decade. Climate change is predicted to expand the production of mesopelagic MeHg and modify the mesopelagic biomass globally. Considering the pivotal role of the twilight zone is therefore essential to better predict both MeHg exposure and trophic supply to white sharks, and effectively protect these key vulnerable predators.

Mercury isotopes as tracers of ecology and metabolism in two sympatric shark species.

In coastal ecosystems, top predators are exposed to a wide variety of nutrient and contaminant sources due to the diversity of trophic webs within inshore marine habitats. Mercury contamination could represent an additional threat to shark populations that are declining worldwide. Here we measured total mercury, carbon and nitrogen isotopes, as well as mercury isotopes, in two co-occurring shark species (the bull shark Carcharhinus leucas and the tiger shark Galeocerdo cuvier) and their potential prey from a coastal ecosystem of the western Indian Ocean (La Réunion Island). Our primary goals were to (i) determine the main trophic Hg sources for sharks and (ii) better characterize their diet composition and foraging habitat. Hg isotope signatures (Δ199Hg and δ202Hg) of shark prey suggested that bull sharks were exposed to methylmercury (MeHg) produced in offshore epipelagic waters, while tiger sharks were exposed to offshore mesopelagic MeHg with additional microbial transformation in slope sediments. Δ199Hg values efficiently traced the ecology of the two predators, demonstrating that bull sharks targeted coastal prey in shallow waters while tiger sharks were mainly foraging on mesopelagic species in the deeper waters of the island slope. Unexpectedly, we found a positive shift in δ202Hg (>1‰) between sharks and their prey, leading to high δ202Hg values in the two shark species (e.g. 1.91 ± 0.52‰ in bull sharks). This large shift in δ202Hg indicates that sharks may display strong MeHg demethylation abilities, possibly reflecting evolutionary pathways for mitigating their MeHg contamination.

Trophic resources and mercury exposure of two silvertip shark populations in the Northeast Pacific Ocean.

Worldwide shark populations have experienced rapid declines over the last decades, mainly due to overfishing. Marine protected areas (MPAs) have thus become an indispensable tool for the protection of these marine predators. Two recently-created MPAs in the Northeast Pacific Ocean, the Revillagigedo National Park and Clipperton Atoll, are characterized by different trophic structures potentially influencing the trophic niche and contaminant exposure of resident sharks in these two sites. In this context, we used carbon (δ13C) and nitrogen (δ15N) stable isotope analyzes as well as total mercury concentrations ([THg]) to assess the effect of foraging site on the trophic niche and Hg levels of juvenile silvertip (ST) sharks Carcharhinus albimarginatus. Analyzing fin clip samples from Revillagigedo and Clipperton, we found that shark δ15N varied spatially in relation to δ15N baselines, suggesting similar trophic position in both MPAs. Moreover, δ13C values indicated that ST sharks from Revillagigedo would feed on different food webs (i.e. both benthic and pelagic) while individuals from Clipperton would only rely on benthic food webs. These differences between MPAs led to a weak overlap of isotopic niches between the two populations, highlighting the site residency of juvenile ST sharks. Within each population, [THg] was not correlated with trophic tracers (δ15N and δ13C) and was also similar between populations. This study revealed no influence of site or food web in [THg] and raises the question of the origin of Hg exposure for reef shark populations in the Northeast Pacific Ocean.

Stable isotope analyses revealed the influence of foraging habitat on mercury accumulation in tropical coastal marine fish.

Bioaccumulation of toxic metal elements including mercury (Hg) can be highly variable in marine fish species. Metal concentration is influenced by various species-specific physiological and ecological traits, including individual diet composition and foraging habitat. The impact of trophic ecology and habitat preference on Hg accumulation was analyzed through total Hg concentration and stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) in the muscle of 132 fish belonging to 23 different species from the Senegalese coast (West Africa), where the marine ecosystem is submitted to nutrient inputs from various sources such as upwelling or rivers. Species-specific ecological traits were first investigated and results showed that vertical (i.e. water column distribution) and horizontal habitat (i.e. distance from the coast) led to differential Hg accumulation among species. Coastal and demersal fish were more contaminated than offshore and pelagic species. Individual characteristics therefore revealed an increase of Hg concentration in muscle that paralleled trophic level for some locations. Considering all individuals, the main carbon source was significantly correlated with Hg concentration, again revealing a higher accumulation for fish foraging in nearshore and benthic habitats. The large intraspecific variability observed in stable isotope signatures highlights the need to conduct ecotoxicological studies at the individual level to ensure a thorough understanding of mechanisms driving metal accumulation in marine fish. For individuals from a same species and site, Hg variation was mainly explained by fish length, in accordance with the bioaccumulation of Hg over time. Finally, Hg concentrations in fish muscle are discussed regarding their human health impact. No individual exceeded the current maximum acceptable limit for seafood consumption set by both the European Union and the Food and Agriculture Organization of the United Nations. However, overconsumption of some coastal demersal species analyzed here could be of concern regarding human exposure to mercury.

Metal subcellular partitioning determines excretion pathways and sensitivity to cadmium toxicity in two marine fish species.

Subcellular cadmium (Cd) partitioning was investigated in the liver of two marine fish species, the European sea bass Dicentrarchus labrax and the Senegalese sole Solea senegalensis, dietary exposed to an environmentally realistic Cd dose for two months followed by a two-month depuration. The two species displayed different handling strategies during the depuration period. Cd was largely bound to detoxifying fractions such as heat stable proteins (HSP) including metallothioneins (MT) in sea bass, while Cd was more linked to sensitive fractions such as organelles in sole. Whole liver concentrations and subcellular partitioning were also determined for essential elements. The greatest impairment of essential metal homeostasis due to Cd exposure was found in sole. These elements followed the Cd partitioning pattern, suggesting that they are involved in antioxidant responses against Cd toxicity. Cd consumption diminished sole growth in terms of body weight, probably due to lipid storage impairment. The contrasting partitioning patterns showed by the two species might imply different pathways for Cd elimination from the liver. In sea bass, MT-bound Cd would be excreted through bile or released into blood, crossing the cell membrane via a protein transporter. In sole, MRG-bound Cd would be sequestered by organelles before being released into the blood via vesicular exocytosis. These distinct strategies in cellular Cd handling in the liver might account for differential sensitivity to Cd toxicity and differential Cd excretion pathways between the two marine fish species.

Significance of metallothioneins in differential cadmium accumulation kinetics between two marine fish species.

Impacted marine environments lead to metal accumulation in edible marine fish, ultimately impairing human health. Nevertheless, metal accumulation is highly variable among marine fish species. In addition to ecological features, differences in bioaccumulation can be attributed to species-related physiological processes, which were investigated in two marine fish present in the Canary Current Large Marine Ecosystem (CCLME), where natural and anthropogenic metal exposure occurs. The European sea bass Dicentrarchus labrax and Senegalese sole Solea senegalensis were exposed for two months to two environmentally realistic dietary cadmium (Cd) doses before a depuration period. Organotropism (i.e., Cd repartition between organs) was studied in two storage compartments (the liver and muscle) and in an excretion vector (bile). To better understand the importance of physiological factors, the significance of hepatic metallothionein (MT) concentrations in accumulation and elimination kinetics in the two species was explored. Accumulation was faster in the sea bass muscle and liver, as inferred by earlier Cd increase and a higher accumulation rate. The elimination efficiency was also higher in the sea bass liver compared to sole, as highlighted by greater biliary excretion. In the liver, no induction of MT synthesis was attributed to metal exposure, challenging the relevance of using MT concentration as a biomarker of metal contamination. However, the basal MT pools were always greater in the liver of sea bass than in sole. This species-specific characteristic might have enhanced Cd biliary elimination and relocation to other organs such as muscle through the formation of more Cd/MT complexes. Thus, MT basal concentrations seem to play a key role in the variability observed in terms of metal concentrations in marine fish species.

Trophic ecology influence on metal bioaccumulation in marine fish: Inference from stable isotope and fatty acid analyses.

The link between trophic ecology and metal accumulation in marine fish species was investigated through a multi-tracers approach combining fatty acid (FA) and stable isotope (SI) analyses on fish from two contrasted sites on the coast of Senegal, one subjected to anthropogenic metal effluents and another one less impacted. The concentrations of thirteen trace metal elements (As, Cd, Co, Cr, Cu, Fe, Li, Mn, Ni, Pb, Sn, U, and Zn) were measured in fish liver. Individuals from each site were classified into three distinct groups according to their liver FA and muscle SI compositions. Trace element concentrations were tested between groups revealing that bioaccumulation of several metals was clearly dependent on the trophic guild of fish. Furthermore, correlations between individual trophic markers and trace metals gave new insights into the determination of their origin. Fatty acids revealed relationships between the dietary regimes and metal accumulation that were not detected with stable isotopes, possibly due to the trace metal elements analysed in this study. In the region exposed to metallic inputs, the consumption of benthic preys was the main pathway for metal transfer to the fish community while in the unaffected one, pelagic preys represented the main source of metals. Within pelagic sources, metallic transfer to fish depended on phytoplankton taxa on which the food web was based, suggesting that microphytoplankton (i.e., diatoms and dinoflagellates) were a more important source of exposition than nano- and picoplankton. This study confirmed the influence of diet in the metal accumulation of marine fish communities, and proved that FAs are very useful and complementary tools to SIs to link metal accumulation in fish with their trophic ecology.