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.

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.

Mercury isotopes of key tissues document mercury metabolic processes in seabirds.

Seabirds accumulate significant amounts of mercury (Hg) due to their long-life span together with their medium to high trophic position in marine food webs. Hg speciation and Hg isotopic analyses of total Hg in different tissues (pectoral muscles, liver, brain, kidneys, blood and feathers) were assessed to investigate their detoxification mechanisms. Three species with contrasted ecological characteristics were studied: the Antarctic prion (zooplankton feeder), the white-chinned petrel (pelagic generalist consumer) and the southern giant petrel (scavenger on seabirds and marine mammals). The difference of mass-dependent fractionation (MDF, δ202Hg) values between liver and muscles (up to 0.94 ‰) in all three seabirds strongly suggests hepatic demethylation of the isotopically lighter methylmercury (MeHg) and subsequent redistribution of the isotopically heavier fraction of MeHg towards the muscles. Similarly, higher δ202Hg values in feathers (up to 1.88 ‰) relative to muscles and higher proportion of MeHg in feathers (94-97%) than muscles (30-70%) likely indicate potential MeHg demethylation in muscle and preferential excretion of MeHg (isotopically heavier) in the growing feathers during moult. The extents of these key detoxification processes were strongly dependent on the species-specific detoxification strategies and levels of dietary MeHg exposure. We also found higher mass-independent fractionation (MIF, Δ199Hg) values in feathers relative to internal tissues, possibly due to different integration times of Hg exposure between permanently active organs and inert tissues as feathers. Hg isotope variations reported in this study show evidence of detoxification processes in seabirds and propose a powerful approach for deep investigation of the Hg metabolic processes in seabirds.

A "seabird-eye" on mercury stable isotopes and cycling in the Southern Ocean.

Since mercury (Hg) biogeochemistry in the Southern Ocean is minimally documented, we investigated Hg stable isotopes in the blood of seabirds breeding at different latitudes in the Antarctic, Subantarctic and Subtropical zones. Hg isotopic composition was determined in adult penguins (5 species) and skua chicks (2 species) from Adélie Land (66°39'S, Antarctic) to Crozet (46°25'S, Subantarctic) and Amsterdam Island (37°47'S, Subtropical). Mass-dependent (MDF, δ202Hg) and mass-independent (MIF, Δ199Hg) Hg isotopic values separated populations geographically. Antarctic seabirds exhibited lower δ202Hg values (-0.02 to 0.79 ‰, min-max) than Subantarctic (0.88 to 2.12 ‰) and Subtropical (1.44 to 2.37 ‰) seabirds. In contrast, Δ199Hg values varied slightly from Antarctic (1.31 to 1.73 ‰) to Subtropical (1.69 to 2.04 ‰) waters. The extent of methylmercury (MeHg) photodemethylation extrapolated from Δ199Hg values was not significantly different between locations, implying that most of the bioaccumulated MeHg was of mesopelagic origin. The larger increase of MDF between the three latitudes co-varies with MeHg concentrations. This supports an increasing effect of specific biogenic Hg pathways from Antarctic to Subtropical waters, such as Hg biological transformations and accumulations. This "biogenic effect" among different productive southern oceanic regions can also be related to different mixed layer depth dynamics and biological productivity turnover that specifically influence the vertical transport between the mesopelagic and the photic zones. This study shows the first Hg isotopic data of the Southern Ocean at large scale and reveals how regional Southern Ocean dynamics and productivity control marine MeHg biogeochemistry and the exposure of seabirds to Hg contamination.

Contrasting Spatial and Seasonal Trends of Methylmercury Exposure Pathways of Arctic Seabirds: Combination of Large-Scale Tracking and Stable Isotopic Approaches.

Despite the limited direct anthropogenic mercury (Hg) inputs in the circumpolar Arctic, elevated concentrations of methylmercury (MeHg) are accumulated in Arctic marine biota. However, the MeHg production and bioaccumulation pathways in these ecosystems have not been completely unraveled. We measured Hg concentrations and stable isotope ratios of Hg, carbon, and nitrogen in the feathers and blood of geolocator-tracked little auk Alle alle from five Arctic breeding colonies. The wide-range spatial mobility and tissue-specific Hg integration times of this planktivorous seabird allowed the exploration of their spatial (wintering quarters/breeding grounds) and seasonal (nonbreeding/breeding periods) MeHg exposures. An east-to-west increase of head feather Hg concentrations (1.74-3.48 µg·g-1) was accompanied by significant spatial trends of Hg isotope (particularly Δ199Hg: 0.96-1.13‰) and carbon isotope (δ13C: -20.6 to -19.4‰) ratios. These trends suggest a distinct mixing/proportion of MeHg sources between western North Atlantic and eastern Arctic regions. Higher Δ199Hg values (+0.4‰) in northern colonies indicate an accumulation of more photochemically impacted MeHg, supporting shallow MeHg production and bioaccumulation in high Arctic waters. The combination of seabird tissue isotopic analysis and spatial tracking helps in tracing the MeHg sources at various spatio-temporal scales.

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.

Using blood and feathers to investigate large-scale Hg contamination in Arctic seabirds: A review.

Mercury (Hg), because of its deleterious effects on wildlife and its high concentrations in polar regions, has been widely studied in the Arctic. This provided important information regarding food web contamination, spatial and temporal trends of Hg in ecosystems or risk assessments for wildlife and Humans. Among the Arctic biota, seabirds have been among the most studied species due to their sensitivity to this toxicant, their role as bioindicators of the contamination status of their environment, and their consumption by Arctic communities. However, most studies that investigated Hg in Arctic seabirds focused on measurements in internal organs or in eggs, while few investigations have been performed on blood and feathers, despite the relevant and complementary information they provide. Here, we first provide a detailed overview of the specific information blood and feathers can bring when investigating Hg contamination of Arctic seabirds, including new knowledge on the poorly studied non-breeding period. Second, we perform a comprehensive review of the use of blood and feathers as non-lethal tissues to study Hg in Arctic seabirds. This review demonstrates important interspecific variations in Hg blood concentrations according to seabird trophic status, with seaducks generally presenting the lowest Hg concentrations while auks have the highest ones. However, all the observed Hg concentrations are below the admitted toxicity thresholds. Hg concentrations in feathers follow similar trends and gulls appear to be the most contaminated species, likely as a consequence of contrasting migratory and overwintering strategies. This review also confirms strong spatial variations with higher concentrations found in the Canadian Arctic and Pacific waters than in Greenland and the European Arctic. It also identifies some major understudied areas such as West Greenland, Aleutian Islands and Russia. Finally, we provide a thorough review of the current knowledge regarding molting patterns in Arctic seabirds, which is an essential information to interpret Hg concentrations measured in feathers. Overall, our results point out the importance of blood and feathers in seabird ecotoxicological assessments and highlight the need for large scale international collaborations and research programs.

Identification of sources and bioaccumulation pathways of MeHg in subantarctic penguins: a stable isotopic investigation.

Seabirds are widely used as bioindicators of mercury (Hg) contamination in marine ecosystems and the investigation of their foraging strategies is of key importance to better understand methylmercury (MeHg) exposure pathways and environmental sources within the different ecosystems. Here we report stable isotopic composition for both Hg mass-dependent (e.g. δ202Hg) and mass-independent (e.g. Δ199Hg) fractionation (proxies of Hg sources and transformations), carbon (δ13C, proxy of foraging habitat) and nitrogen (δ15N, proxy of trophic position) in blood of four species of sympatric penguins breeding at the subantarctic Crozet Islands (Southern Indian Ocean). Penguins have species-specific foraging strategies, from coastal to oceanic waters and from benthic to pelagic dives, and feed on different prey. A progressive increase to heavier Hg isotopic composition (δ202Hg and Δ199Hg, respectively) was observed from benthic (1.45 ± 0.12 and 1.41 ± 0.06‰) to epipelagic (1.93 ± 0.18 and 1.77 ± 0.13‰) penguins, indicating a benthic-pelagic gradient of MeHg sources close to Crozet Islands. The relative variations of MeHg concentration, δ202Hg and Δ199Hg with pelagic penguins feeding in Polar Front circumpolar waters (1.66 ± 0.11 and 1.54 ± 0.06‰) support that different MeHg sources occur at large scales in Southern Ocean deep waters.

Seabird Tissues As Efficient Biomonitoring Tools for Hg Isotopic Investigations: Implications of Using Blood and Feathers from Chicks and Adults.

Blood and feathers are the two most targeted avian tissues for environmental biomonitoring studies, with mercury (Hg) concentration in blood and body feathers reflecting short and long-term Hg exposure, respectively. In this work, we investigated how Hg isotopic composition (e.g., δ202Hg and Δ199Hg) of blood and feathers from either seabird chicks (skuas, n = 40) or adults (penguins, n = 62) can accurately provide information on exposure to Hg in marine ecosystems. Our results indicate a strong correlation between blood and feather Hg isotopic values for skua chicks, with similar δ202Hg and Δ199Hg values in the two tissues (mean difference: -0.01 ± 0.25 ‰ and -0.05 ± 0.12 ‰, respectively). Since blood and body feathers of chicks integrate the same temporal window of Hg exposure, this suggests that δ202Hg and Δ199Hg values can be directly compared without any correction factors within and between avian groups. Conversely, penguin adults show higher δ202Hg and Δ199Hg values in feathers than in blood (mean differences: 0.28 ± 0.19‰ and 0.25 ± 0.13‰), most likely due to tissue-specific Hg temporal integration. Since feathers integrate long-term (i.e., the intermoult period) Hg accumulation, whereas blood reflects short-term (i.e., seasonal) Hg exposure in adult birds, the two tissues provide complementary information on trophic ecology at different time scales.

Assessment of mercury speciation in feathers using species-specific isotope dilution analysis.

Seabirds are considered as effective sentinels of environmental marine contamination and their feathers are extensively used as non-lethal samples for contaminant biomonitoring. This tissue represents the main route for mercury (Hg) elimination in seabirds and contains predominantly methylmercury (MeHg). In this work, we developed a robust analytical technique for precise and accurate simultaneous quantification of MeHg, inorganic Hg (iHg) and consequently total Hg (THg), in feathers by gas-chromatography (GC)-ICPMS analyses using species-specific isotope dilution technique. An optimisation of the extraction method was carried out by testing different extraction systems, reagents and spiking procedures using an internal reference feather sample. The procedure was validated for MeHg and THg concentrations with a human hair certified reference material. Microwave nitric acid extraction with spike addition before the extraction provided the best recovery and was chosen as the most appropriate species simultaneous extraction method (SSE). An additional assessment was performed by comparison of our developed extraction method and a MeHg specific extraction technique (MSE) classically used for Hg speciation studies on feathers. The developed method was applied to feather samples from a large number of seabirds from the Southern Ocean (penguins, albatrosses, petrels and skuas) to investigate the variability of Hg speciation across a large range of Hg exposure conditions and concentrations. In all cases, MeHg accounted for > 90% of THg, thus verifying the predominance of organic Hg over iHg in feathers.

Specific Pathways of Dietary Methylmercury and Inorganic Mercury Determined by Mercury Speciation and Isotopic Composition in Zebrafish (Danio rerio).

An original approach is proposed to investigate inorganic (iHg) and methylmercury (MeHg) trophic transfer and fate in a model fish, Danio rerio, by combining natural isotopic fractionation and speciation. Animals were exposed to three different dietary conditions: (1) 50 ng Hg g(-1), 80% as MeHg; (2) diet enriched in MeHg 10,000 ng Hg g(-1), 95% as MeHg, and (3) diet enriched in iHg 10,000 ng Hg g(-1), 99% as iHg. Harvesting was carried out after 0, 7, 25, and 62 days. Time-dependent Hg species distribution and isotopic fractionation in fish organs (muscle, brain, liver) and feces, exhibited different patterns, as a consequence of their dissimilar metabolization. The rapid isotopic re-equilibration to the new MeHg-food source reflects its high bioaccumulation rate. Relevant aspects related to Hg excretion are also described. This study confirms Hg isotopic fractionation as a powerful tool to investigate biological processes, although its deconvolution and fully understanding is still a challenge.