Are tunas relevant bioindicators of mercury concentrations in the global ocean?

Humans are exposed to toxic methylmercury mainly by consuming marine fish. The Minamata Convention aims at reducing anthropogenic mercury releases to protect human and ecosystem health, employing monitoring programs to meet its objectives. Tunas are suspected to be sentinels of mercury exposure in the ocean, though not evidenced yet. Here, we conducted a literature review of mercury concentrations in tropical tunas (bigeye, yellowfin, and skipjack) and albacore, the four most exploited tunas worldwide. Strong spatial patterns of tuna mercury concentrations were shown, mainly explained by fish size, and methylmercury bioavailability in marine food web, suggesting that tunas reflect spatial trends of mercury exposure in their ecosystem. The few mercury long-term trends in tunas were contrasted and sometimes disconnected to estimated regional changes in atmospheric emissions and deposition, highlighting potential confounding effects of legacy mercury, and complex reactions governing the fate of mercury in the ocean. Inter-species differences of tuna mercury concentrations associated with their distinct ecology suggest that tropical tunas and albacore could be used complementarily to assess the vertical and horizontal variability of methylmercury in the ocean. Overall, this review elevates tunas as relevant bioindicators for the Minamata Convention, and calls for large-scale and continuous mercury measurements within the international community. We provide guidelines for tuna sample collection, preparation, analyses and data standardization with recommended transdisciplinary approaches to explore tuna mercury content in parallel with observation abiotic data, and biogeochemical model outputs. Such global and transdisciplinary biomonitoring is essential to explore the complex mechanisms of the marine methylmercury cycle.

Revealing the environmental pollution of two estuaries through histopathological biomarkers in five fishes from different trophic guilds of northeastern Brazil.

Estuaries in Brazil are mostly anthropically affected due to the discharge of industrial and domestic effluents. In two of them, the Santa Cruz Channel Estuary (ITAP) and Sirinhaém River Estuary (SIR), historically affected by mercury pollution and sugarcane industry in Northeast Brazil, we assessed environmental pollution using liver and gill histopathological biomarkers in fish from different trophic levels. Liver samples exhibited serious damages such as hepatic steatosis, necrosis, and infiltration. The gills showed moderate to severe changes, such as lifting of epithelial cells, lamellar aneurysm, and rupture of lamellar epithelium. Most of the changes in the liver and gills were reported for species Centropomus undecimalis and the Gobionellus stomatus, which were considered as good sentinels of pollution. The combination of biomarker methodologies was efficient in diagnosing the serious damage to the species, reinforcing the need for monitoring the health of the ecosystems evaluated.

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.

Evidence that Pacific tuna mercury levels are driven by marine methylmercury production and anthropogenic inputs.

Pacific Ocean tuna is among the most-consumed seafood products but contains relatively high levels of the neurotoxin methylmercury. Limited observations suggest tuna mercury levels vary in space and time, yet the drivers are not well understood. Here, we map mercury concentrations in skipjack tuna across the Pacific Ocean and build generalized additive models to quantify the anthropogenic, ecological, and biogeochemical drivers. Skipjack mercury levels display a fivefold spatial gradient, with maximum concentrations in the northwest near Asia, intermediate values in the east, and the lowest levels in the west, southwest, and central Pacific. Large spatial differences can be explained by the depth of the seawater methylmercury peak near low-oxygen zones, leading to enhanced tuna mercury concentrations in regions where oxygen depletion is shallow. Despite this natural biogeochemical control, the mercury hotspot in tuna caught near Asia is explained by elevated atmospheric mercury concentrations and/or mercury river inputs to the coastal shelf. While we cannot ignore the legacy mercury contribution from other regions to the Pacific Ocean (e.g., North America and Europe), our results suggest that recent anthropogenic mercury release, which is currently largest in Asia, contributes directly to present-day human mercury exposure.

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.

Lipid-free tuna muscle samples are suitable for total mercury analysis.

Tropical tunas are largely consumed worldwide, providing major nutritional benefits to humans, but also representing the main exposure to methylmercury, a potent neurotoxin that biomagnifies along food webs. The combination of ecological tracers (nitrogen and carbon stable isotopes, δ15N and δ13C) to mercury concentrations in tunas is scarce yet crucial to better characterize the influence of tuna foraging ecology on mercury exposure and bioaccumulation. Given the difficulties to get modern and historical tuna samples, analyses have to be done on available and unique samples. However, δ13C values are often analysed on lipid-free samples to avoid bias related to lipid content. While lipid extraction with non-polar solvents is known to have no effect on δ15N values, its impact on mercury concentrations is still unclear. We used white muscle tissues of three tropical tuna species to evaluate the efficiency and repeatability of different lipid extraction protocols commonly used in δ13C and δ15N analysis. Dichloromethane was more efficient than cyclohexane in extracting lipids in tuna muscle, while the automated method appeared more efficient but as repeatable as the manual method. Lipid extraction with dichloromethane had no effect on mercury concentrations. This may result from i) the affinity of methylmercury to proteins in tuna flesh, ii) the low lipid content in tropical tuna muscle samples, and iii) the non-polar nature of dichloromethane. Our study suggests that lipid-free samples, usually prepared for tropical tuna foraging ecology research, can be used equivalently to bulk samples to document in parallel mercury concentrations at a global scale.

Otolith chemical fingerprints of skipjack tuna (Katsuwonus pelamis) in the Indian Ocean: First insights into stock structure delineation.

The chemical composition of otoliths (earbones) can provide valuable information about stock structure and connectivity patterns among marine fish. For that, chemical signatures must be sufficiently distinct to allow accurate classification of an unknown fish to their area of origin. Here we have examined the suitability of otolith microchemistry as a tool to better understand the spatial dynamics of skipjack tuna (Katsuwonus pelamis), a highly valuable commercial species for which uncertainties remain regarding its stock structure in the Indian Ocean. For this aim, we have compared the early life otolith chemical composition of young-of-the-year (<6 months) skipjack tuna captured from the three main nursery areas of the equatorial Indian Ocean (West, Central and East). Elemental (Li:Ca, Sr:Ca, Ba:Ca, Mg:Ca and Mn:Ca) and stable isotopic (δ13C, δ18O) signatures were used, from individuals captured in 2018 and 2019. Otolith Sr:Ca, Ba:Ca, Mg:Ca and δ18O significantly differed among fish from different nurseries, but, in general, the chemical signatures of the three nursery areas largely overlapped. Multivariate analyses of otolith chemical signatures revealed low geographic separation among Central and Eastern nurseries, achieving a maximum overall random forest cross validated classification success of 51%. Cohort effect on otolith trace element signatures was also detected, indicating that variations in chemical signatures associated with seasonal changes in oceanographic conditions must be well understood, particularly for species with several reproductive peaks throughout the year. Otolith microchemistry in conjunction with other techniques (e.g., genetics, particle tracking) should be further investigated to resolve skipjack stock structure, which will ultimately contribute to the sustainable management of this stock in the Indian Ocean.

Stable mercury concentrations of tropical tuna in the south western Pacific ocean: An 18-year monitoring study.

Global anthropogenic mercury (Hg) emissions to the atmosphere since industrialization are widely considered to be responsible for a significant increase in surface ocean Hg concentrations. Still unclear is how those inputs are converted into toxic methylmercury (MeHg) then transferred and biomagnified in oceanic food webs. We used a unique long-term and continuous dataset to explore the temporal Hg trend and variability of three tropical tuna species (yellowfin, bigeye, and skipjack) from the southwestern Pacific Ocean between 2001 and 2018 (n = 590). Temporal trends of muscle nitrogen (δ15N) and carbon (δ13C) stable isotope ratios, amino acid (AA) δ15N values and oceanographic variables were also investigated to examine the potential influence of trophic, biogeochemical and physical processes on the temporal variability of tuna Hg concentrations. For the three species, we detected significant inter-annual variability but no significant long-term trend for Hg concentrations. Inter-annual variability was related to the variability in tuna sampled lengths among years and to tuna muscle δ15N and δ13C values. Complementary AA- and model-estimated phytoplankton δ15N values suggested the influence of baseline processes with enhanced tuna Hg concentrations observed when dinitrogen fixers prevail, possibly fuelling baseline Hg methylation and/or MeHg bioavailability at the base of the food web. Our results show that MeHg trends in top predators do not necessary capture the increasing Hg concentrations in surface waters suspected at the global oceanic scale due to the complex and variable processes governing Hg deposition, methylation, bioavailability and biomagnification. This illustrates the need for long-term standardized monitoring programs of marine biota worldwide.

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.