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.

ENSO Climate Forcing of the Marine Mercury Cycle in the Peruvian Upwelling Zone Does Not Affect Methylmercury Levels of Marine Avian Top Predators.

Climate change is expected to affect marine mercury (Hg) biogeochemistry and biomagnification. Recent modeling work suggested that ocean warming increases methylmercury (MeHg) levels in fish. Here, we studied the influence of El Niño Southern Oscillations (ENSO) on Hg concentrations and stable isotopes in time series of seabird blood from the Peruvian upwelling and oxygen minimum zone. Between 2009 and 2016, La Niña (2011) and El Niño conditions (2015-2016) were accompanied by sea surface temperature anomalies up to 3 °C, oxycline depth change (20-100 m), and strong primary production gradients. Seabird Hg levels were stable and did not co-vary significantly with oceanographic parameters, nor with anchovy biomass, the primary dietary source to seabirds (90%). In contrast, seabird Δ199Hg, proxy for marine photochemical MeHg breakdown, and δ15N showed strong interannual variability (up to 0.8 and 3‰, respectively) and sharply decreased during El Niño. We suggest that lower Δ199Hg during El Niño represents reduced MeHg photodegradation due to the deepening of the oxycline. This process was balanced by equally reduced Hg methylation due to reduced productivity, carbon export, and remineralization. The non-dependence of seabird MeHg levels on strong ENSO variability suggests that marine predator MeHg levels may not be as sensitive to climate change as is currently thought.

Persistent organic pollutants and trace metals in selected marine organisms from the Akanda National Park, Gabon (Central Africa).

Akanda National Park (ANP) is composed of mangrove ecosystems bordering Libreville, Gabon's capital. The contamination of aquatic resources from the ANP by persistent organic pollutants (POPs) and trace metals (TMs) was never evaluated. To provide a basis for their monitoring in the ANP, five species (two fish, two mollusks, and one crustacean) were analyzed from three sampling sites in 2017. Contamination levels for POPs and TMs were below maximum acceptable limits for seafood, including Cd and Pb. No DDT was found in any sample. Inter-specific differences were more obvious than the differences among sites, although the results may be biased by an unbalanced sampling design. The oyster Crassostrea gasar was the most contaminated species, making this species a good candidate to assess environmental contamination in the area. The studied species also contained essential elements, such as Fe, Zn and Mn at interesting levels in a nutritional point of view.

Predominant heterotrophic diazotrophic bacteria are involved in Sargassum proliferation in the Great Atlantic Sargassum Belt.

Since 2011, the Caribbean coasts have been subject to episodic influxes of floating Sargassum seaweed of unprecedented magnitude originating from a new area "the Great Atlantic Sargassum Belt" (GASB), leading in episodic influxes and mass strandings of floating Sargassum. For the biofilm of both holopelagic and benthic Sargassum as well as in the surrounding waters, we characterized the main functional groups involved in the microbial nitrogen cycle. The abundance of genes representing nitrogen fixation (nifH), nitrification (amoA), and denitrification (nosZ) showed the predominance of diazotrophs, particularly within the GASB and the Sargasso Sea. In both location, the biofilm associated with holopelagic Sargassum harboured a more abundant proportion of diazotrophs than the surrounding water. The mean δ15N value of the GASB seaweed was very negative (-2.04‰), and lower than previously reported, reinforcing the hypothesis that the source of nitrogen comes from the nitrogen-fixing activity of diazotrophs within this new area of proliferation. Analysis of the diversity of diazotrophic communities revealed for the first time the predominance of heterotrophic diazotrophic bacteria belonging to the phylum Proteobacteria in holopelagic Sargassum biofilms. The nifH sequences belonging to Vibrio genus (Gammaproteobacteria) and Filomicrobium sp. (Alphaproteobacteria) were the most abundant and reached, respectively, up to 46.0% and 33.2% of the community. We highlighted the atmospheric origin of the nitrogen used during the growth of holopelagic Sargassum within the GASB and a contribution of heterotrophic nitrogen-fixing bacteria to a part of the Sargassum proliferation.

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.

Lipid-correction models for δ13C values across small pelagic fishes (Clupeiformes) from the Atlantic Ocean.

The interpretation of δ13C values in trophic ecology requires standardization of the lipid content of organisms estimated through their C:N ratio. To avoid time-consuming lipid extractions, the use of mathematical corrections has been developed for many years, and the conclusions generally point in the direction of species-specific adjustment of the models. This study aimed at defining the maximum taxonomic level required to obtain the best corrected δ13C values in small pelagic fish of the order Clupeiformes. δ13C values of six species were analyzed bulk and lipid-free, and were used to fit and validate linear and mass-balance models at different taxonomic levels. Despite a species effect combined with the C:N ratio effect, the corrected δ13C values produced by a global model for the Clupeiformes were as good as or better when compared to lipid-free samples than those produced by species-specific models, paving the way for possible generalization to other species in this order. At the order level, the linear model outperformed the mass-balance model.

Mercury concentrations in tuna blood and muscle mirror seawater methylmercury in the Western and Central Pacific Ocean.

Understanding the relationship between mercury in seafood and the distribution of oceanic methylmercury is key to understand human mercury exposure. Here, we determined mercury concentrations in muscle and blood of bigeye and yellowfin tunas from the Western and Central Pacific. Results showed similar latitudinal patterns in tuna blood and muscle, indicating that both tissues are good candidates for mercury monitoring. Complementary tuna species analyses indicated species- and tissue- specific mercury patterns, highlighting differences in physiologic processes of mercury uptake and accumulation associated with tuna vertical habitat. Tuna mercury content was correlated to ambient seawater methylmercury concentrations, with blood being enriched at a higher rate than muscle with increasing habitat depth. The consideration of a significant uptake of dissolved methylmercury from seawater in tuna, in addition to assimilation from food, might be interesting to test in models to represent the spatiotemporal evolutions of mercury in tuna under different mercury emission scenarios.

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.

Trophic structure of a nektobenthic community exploited by a multispecific bottom trawling fishery in Northeastern Brazil.

We used complementary stable isotope (SIA) and stomach content (SCA) analyses to investigate feeding relationships among species of the nektobenthic communities and the potential ecological effects of the bottom trawling of a coastal ecosystem in northeastern Brazil. Carbon (δ13C) and nitrogen (δ15N) compositions were determined for five basal sources and 28 consumers, from zooplankton to shrimp and fish species. Fishes and basal sources showed a broad range of δ15N (fishes: 6.49-14.94‰; sources: 2.58-6.79‰) and δ13C values (fishes: -23.86 to -13.71‰; sources: -24.32 to -13.53‰), while shrimps and crabs exhibited similar nitrogen and carbon ratios. Six trophic consumer groups were determined among zooplankton, crustaceans and fishes by SIA, with trophic pathways associated mostly with benthic sources. SCA results indicated a preference for benthic invertebrates, mainly worms, crabs and shrimps, as prey for the fish fauna, highlighting their importance in the food web. In overall, differences between SCA and the SIA approaches were observed, except for groups composed mainly for shrimps and some species of high δ15N values, mostly piscivorous and zoobenthivores. Given the absence of regulation for bottom trawling activities in the area, the cumulative effects of trawling on population parameters, species composition, potentially decreasing the abundance of benthic preys (e.g., shrimps, worms and crabs) may lead to changes in the trophic structure potentially affect the food web and the sustainability of the fishery.

Benefit-risk associated with the consumption of fish bycatch from tropical tuna fisheries.

Mercury, omega-3 (docosahexaenoic acid, DHA and eicosapentaenoic acid, EPA) and macronutrients (fat and proteins) were quantified on a wet weight (ww) basis in 20 species of fish taken as bycatch in tropical tuna fisheries. Based on a hazard quotient taking into account mercury and omega-3 contents, a benefit-risk assessment for the consumption of these pelagic species was conducted for three people categories: young children, children and adults. All fish bycatch were found to be an excellent source of proteins (min‒max = 14.4-25.2 g/100 g fillet), had low omega-6/omega-3 ratios (<1, except for silky shark), and had mercury content below the safety limits defined by sanitary agencies. Silky shark and Istiophoridae had the highest mercury contents (min‒max = 0.029-0.317 ppm ww). Omega-3 contents were the lowest in silky shark (0.2 ± 0.2 mg/100 g fillet) and the highest in striped marlin (3.6 ± 3.2 g/100 g fillet). Billfishes (Istiophoridae, including striped marlin), minor tunas (Scombridae), and Carangidae had the highest omega-3 contents (min‒max = 0.68-7.28 g/100 g fillet). The highest hazard quotient values obtained for silky shark and great barracuda reflected a lower nutritional benefit (i.e., low omega-3 source) than risk (i.e., mercury exposure), making them not advisable for consumption. Eight species had low hazard quotients, and among them cottonmouth jack and flat needlefish were found of high health interest (high protein, moderate fat contents, and low omega-6/omega-3 ratio). A daily serving portion of 85-200 g (according to people category) can be recommended for these species. Batfish, and to a lower extent pompano dolphinfish and brassy chub, can also be consumed safely and would provide greater health benefits than risks. These results advocate for a better access of these species to local populations.

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.

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.

Accounting for age uncertainty in growth modeling, the case study of yellowfin tuna (Thunnus albacares) of the Indian Ocean.

Age estimates, typically determined by counting periodic growth increments in calcified structures of vertebrates, are the basis of population dynamics models used for managing exploited or threatened species. In fisheries research, the use of otolith growth rings as an indicator of fish age has increased considerably in recent decades. However, otolith readings include various sources of uncertainty. Current ageing methods, which converts an average count of rings into age, only provide periodic age estimates in which the range of uncertainty is fully ignored. In this study, we describe a hierarchical model for estimating individual ages from repeated otolith readings. The model was developed within a Bayesian framework to explicitly represent the sources of uncertainty associated with age estimation, to allow for individual variations and to include knowledge on parameters from expertise. The performance of the proposed model was examined through simulations, and then it was coupled to a two-stanza somatic growth model to evaluate the impact of the age estimation method on the age composition of commercial fisheries catches. We illustrate our approach using the sagittal otoliths of yellowfin tuna of the Indian Ocean collected through large-scale mark-recapture experiments. The simulation performance suggested that the ageing error model was able to estimate the ageing biases and provide accurate age estimates, regardless of the age of the fish. Coupled with the growth model, this approach appeared suitable for modeling the growth of Indian Ocean yellowfin and is consistent with findings of previous studies. The simulations showed that the choice of the ageing method can strongly affect growth estimates with subsequent implications for age-structured data used as inputs for population models. Finally, our modeling approach revealed particularly useful to reflect uncertainty around age estimates into the process of growth estimation and it can be applied to any study relying on age estimation.

Sequential isotopic signature along gladius highlights contrasted individual foraging strategies of jumbo squid (Dosidicus gigas).

BACKGROUND: Cephalopods play a major role in marine ecosystems, but knowledge of their feeding ecology is limited. In particular, intra- and inter-individual variations in their use of resources has not been adequatly explored, although there is growing evidence that individual organisms can vary considerably in the way they use their habitats and resources. METHODOLOGY/PRINCIPAL FINDINGS: Using δ(13)C and δ(15)N values of serially sampled gladius (an archival tissue), we examined high resolution variations in the trophic niche of five large (>60 cm mantle length) jumbo squids (Dosidicus gigas) that were collected off the coast of Peru. We report the first evidence of large inter-individual differences in jumbo squid foraging strategies with no systematic increase of trophic level with size. Overall, gladius δ(13)C values indicated one or several migrations through the squid's lifetime (∼8-9 months), during which δ(15)N values also fluctuated (range: 1 to 5‰). One individual showed an unexpected terminal 4.6‰ δ(15)N decrease (more than one trophic level), thus indicating a shift from higher- to lower-trophic level prey at that time. The data illustrate the high diversity of prey types and foraging histories of this species at the individual level. CONCLUSIONS/SIGNIFICANCE: The isotopic signature of gladii proved to be a powerful tool to depict high resolution and ontogenic variations in individual foraging strategies of squids, thus complementing traditional information offered by stomach content analysis and stable isotopes on metabolically active tissues. The observed differences in life history strategies highlight the high degree of plasticity of the jumbo squid and its high potential to adapt to environmental changes.