Keystone seabird may face thermoregulatory challenges in a warming Arctic.

Climate change affects the Arctic more than any other region, resulting in evolving weather, vanishing sea ice and altered biochemical cycling, which may increase biotic exposure to chemical pollution. We tested thermoregulatory impacts of these changes on the most abundant Arctic seabird, the little auk (Alle alle). This small diving species uses sea ice-habitats for foraging on zooplankton and resting. We equipped eight little auks with 3D accelerometers to monitor behavior, and ingested temperature recorders to measure body temperature (Tb). We also recorded weather conditions, and collected blood to assess mercury (Hg) contamination. There were nonlinear relationships between time engaged in different behaviors and Tb. Tb increased on sea ice, following declines while foraging in polar waters, but changed little when birds were resting on water. Tb also increased when birds were flying, and decreased at the colony after being elevated during flight. Weather conditions, but not Hg contamination, also affected Tb. However, given our small sample size, further research regarding thermoregulatory effects of Hg is warranted. Results suggest that little auk Tb varies with behavior and weather conditions, and that loss of sea ice due to global warming may cause thermoregulatory and energic challenges during foraging trips at sea.

A keystone avian predator faces elevated energy expenditure in a warming Arctic.

Climate change is transforming bioenergetic landscapes, challenging behavioral and physiological coping mechanisms. A critical question involves whether animals can adjust behavioral patterns and energy expenditure to stabilize fitness given reconfiguration of resource bases, or whether limits to plasticity ultimately compromise energy balance. In the Arctic, rapidly warming temperatures are transforming food webs, making Arctic organisms strong models for understanding biological implications of climate change-related environmental variability. We examined plasticity in the daily energy expenditure (DEE) of an Arctic seabird, the little auk (Alle alle) in response to variability in climate change-sensitive drivers of resource availability, sea surface temperature (SST) and sea ice coverage (SIC), and tested the hypothesis that energetic ceilings and exposure to mercury, an important neurotoxin and endocrine disrupter in marine ecosystems, may limit scope for plasticity. To estimate DEE, we used accelerometer data obtained across years from two colonies exposed to distinct environmental conditions (Ukaleqarteq [UK], East Greenland; Hornsund [HS], Svalbard). We proceeded to model future changes in SST to predict energetic impacts. At UK, high flight costs linked to low SIC and high SST drove DEE from below to above 4 × basal metabolic rate (BMR), a proposed energetic threshold for breeding birds. However, DEE remained below 7 × BMR, an alternative threshold, and did not plateau. Birds at HS experienced higher, relatively invariable SST, and operated above 4 × BMR. Mercury exposure was unrelated to DEE, and fitness remained stable. Thus, plasticity in DEE currently buffers fitness, providing resiliency against climate change. Nevertheless, modeling suggests that continued warming of SST may promote accelerating increases in DEE, which may become unsustainable.

In Vivo Mercury (De)Methylation Metabolism in Cephalopods under Different pCO2 Scenarios.

This work quantified the accumulation efficiencies of Hg in cuttlefish, depending on both organic (MeHg) and inorganic (Hg(II)) forms, under increased pCO2 (1600 µatm). Cuttlefish were fed with live shrimps injected with two Hg stable isotopic tracers (Me202Hg and 199Hg(II)), which allowed for the simultaneous quantification of internal Hg accumulation, Hg(II) methylation, and MeHg demethylation rates in different organs. Results showed that pCO2 had no impact on Hg bioaccumulation and organotropism, and both Hg and pCO2 did not influence the microbiota diversity of gut and digestive gland. However, the results also demonstrated that the digestive gland is a key organ for in vivo MeHg demethylation. Consequently, cuttlefish exposed to environmental levels of MeHg could exhibit in vivo MeHg demethylation. We hypothesize that in vivo MeHg demethylation could be due to biologically induced reactions or to abiotic reactions. This has important implications as to how some marine organisms may respond to future ocean change and global mercury contamination.

Mercury Contamination Challenges the Behavioral Response of a Keystone Species to Arctic Climate Change.

Combined effects of multiple, climate change-associated stressors are of mounting concern, especially in Arctic ecosystems. Elevated mercury (Hg) exposure in Arctic animals could affect behavioral responses to changes in foraging landscapes caused by climate change, generating interactive effects on behavior and population resilience. We investigated this hypothesis in little auks (Alle alle), a keystone Arctic seabird. We compiled behavioral data for 44 birds across 5 years using accelerometers while also quantifying blood Hg and environmental conditions. Warm sea surface temperature (SST) and low sea ice coverage reshaped time activity budgets (TABs) and diving patterns, causing decreased resting, increased flight, and longer dives. Mercury contamination was not associated with TABs. However, highly contaminated birds lengthened interdive breaks when making long dives, suggesting Hg-induced physiological limitations. As dive durations increased with warm SST, subtle toxicological effects threaten to increasingly constrain diving and foraging efficiency as climate change progresses, with ecosystem-wide repercussions.

Bioaccumulation of inorganic and organic mercury in the cuttlefish Sepia officinalis: Influence of ocean acidification and food type.

The bioaccumulation of mercury (Hg) in marine organisms through various pathways has not yet been fully explored, particularly in cephalopods. This study utilises radiotracer techniques using the isotope 203Hg to investigate the toxicokinetics and the organotropism of waterborne inorganic Hg (iHg) and dietary inorganic and organic Hg (methylHg, MeHg) in juvenile common cuttlefish Sepia officinalis. The effect of two contrasting CO2 partial pressures in seawater (400 and 1600 µatm, equivalent to pH 8.08 and 7.54, respectively) and two types of prey (fish and shrimp) were tested as potential driving factors of Hg bioaccumulation. After 14 days of waterborne exposure, juvenile cuttlefish showed a stable concentration factor of 709 ± 54 and 893 ± 117 at pH 8.08 and 7.54, respectively. The accumulated dissolved i203Hg was depurated relatively rapidly with a radiotracer biological half-life (Tb1/2) of 44 ± 12 and 55 ± 16 days at pH 8.08 and 7.54, respectively. During the whole exposure period, approximately half of the i203Hg was found in the gills, but i203Hg also increased in the digestive gland. When fed with 203Hg-radiolabelled prey, cuttlefish assimilated almost all the Hg provided (>95%) independently of the prey type. Nevertheless, the prey type played a major role on the depuration kinetics with Hg Tb1/2 approaching infinity in fish fed cuttlefish vs. 25 days in shrimp fed cuttlefish. Such a difference is explained by the different proportion of Hg species in the prey, with fish prey containing more than 80% of MeHg vs. only 30% in shrimp. Four days after ingestion of radiolabelled food, iHg was primarily found in the digestive organs while MeHg was transferred towards the muscular tissues. No significant effect of pH/pCO2 variation was observed during both the waterborne and dietary exposures on the bioaccumulation kinetics and tissue distribution of i203Hg and Me203Hg. Dietary exposure is the predominant pathway of Hg bioaccumulation in juvenile cuttlefish.

Hg concentrations and stable isotope variations in tropical fish species of a gold-mining-impacted watershed in French Guiana.

The aim of the study was to determine if gold-mining activities could impact the mercury (Hg) concentrations and isotopic signatures in freshwater fish consumed by riparian people in French Guiana. Total Hg, MeHg concentrations, and Hg stable isotopes ratios were analyzed in fish muscles from different species belonging to three feeding patterns (herbivorous, periphytophagous, and piscivorous). We compared tributaries impacted by gold-mining activities (Camopi, CR) with a pristine area upstream (Trois-Sauts, TS), along the Oyapock River. We measured δ15N and δ 13C to examine whether Hg patterns are due to differences in trophic level. Differences in δ 15N and δ 13C values between both studied sites were only observed for periphytophagous fish, due to difference of CN baselines, with enriched values at TS. Total Hg concentrations and Hg stable isotope signatures showed that Hg accumulated in fish from both areas has undergone different biogeochemical processes. Δ199Hg variation in fish (-0.5 to 0.2‰) was higher than the ecosystem baseline defined by a Δ199Hg of -0.66‰ in sediments, and suggested limited aqueous photochemical MeHg degradation. Photochemistry-corrected δ202Hg in fish was 0.7‰ higher than the baseline, consistent with biophysical and chemical isotope fractionation in the aquatic environment. While THg concentrations in periphytophagous fish were higher in the gold-mining area, disturbed by inputs of suspended particles, than in TS, the ensemble of Hg isotope shifts in fish is affected by the difference of biotic (methylation/demethylation) and abiotic (photochemistry) processes between both areas and did therefore not allow to resolve the contribution of gold-mining-related liquid Hg(0) in fish tissues. Mercury isotopes of MeHg in fish and lower trophic level organisms can be complementary to light stable isotope tracers.

Linking pollution and cancer in aquatic environments: A review.

Due to the interconnectedness of aquatic ecosystems through the highly effective marine and atmospheric transport routes, all aquatic ecosystems are potentially vulnerable to pollution. Whilst links between pollution and increased mortality of wild animals have now been firmly established, the next steps should be to focus on specific physiological pathways and pathologies that link pollution to wildlife health deterioration. One of the pollution-induced pathologies that should be at the centre of attention in ecological and evolutionary research is cancer, as anthropogenic contamination has resulted in a rapid increase of oncogenic substances in natural habitats. Whilst wildlife cancer research is an emerging research topic, systematic reviews of the many case studies published over the recent decades are scarce. This research direction would (1) provide a better understanding of the physiological mechanisms connecting anthropogenic pollution to oncogenic processes in non-model organisms (reducing the current bias towards human and lab-animal studies in cancer research), and (2) allow us to better predict the vulnerability of different wild populations to oncogenic contamination. This article combines the information available within the scientific literature about cancer occurrences in aquatic and semi-aquatic species. For the first aim, we use available knowledge from aquatic species to suggest physiological mechanisms that link pollution and cancer, including main metabolic detoxification pathways, oxidative damage effects, infections, and changes to the microbiome. For the second aim, we determine which types of aquatic animals are more vulnerable to pollution-induced cancer, which types of pollution are mainly associated with cancer in aquatic ecosystems, and which types of cancer pollution causes. We also discuss the role of migration in exposing aquatic and semi-aquatic animals to different oncogenic pollutants. Finally, we suggest novel research avenues, including experimental approaches, analysis of the effects of pollutant cocktails and long-term chronic exposure to lower levels of pollutants, and the use of already published databases of gene expression levels in animals from differently polluted habitats.

Drivers of variability in mercury and methylmercury bioaccumulation and biomagnification in temperate freshwater lakes.

The four largest freshwater lakes in southwestern France are of both ecological and economic importance. However, some of them are subjected to mercury (Hg) contamination, resulting in the ban of human consumption of piscivorous fish. Moreover, beyond predatory fish, little information exist regarding Hg levels in other species of these ecosystems. In this context, we used a food web analytical approach to investigate Hg bioaccumulation and biomagnification in relation to the trophic structure of these four lakes. More specifically, various organisms (macrophytes, epiphyton, invertebrates and fish) were collected at the four lakes and analysed for carbon and nitrogen stable isotopes as well as for total Hg (THg) and methylmercury (MeHg). A spatial variability of bioaccumulation in organisms was observed, particularly in carnivorous fish, with higher Hg levels being found in the two more northern lakes (median±SE: 3491 ± 474 and 1113 ± 209 ng THg.g-1 dw in lakes HC and L, respectively) than in the southern pair (600 ± 117 and 911 ± 117 ng THg.g-1 dw in lakes CS and PB, respectively). Methylmercury biomagnification was observed through the food webs of all four lakes, with different trophic magnification slopes (HC = 0.16; L = 0.33; CS = 0.27; PB = 0.27), even though the length of the food chains was similar between the lakes. Our results suggest that rather than the food web structure, anthropogenic inputs (sulfate in northern lakes and phosphorus inputs in southern ones) may have a strong impact, more or less directly, on Hg methylation in freshwater environments, and lead to concentrations exceeding environmental recommendations despite low Hg backgrounds in sediment and water.

Mercury contamination levels in the bioindicator piscivorous fish Hoplias aïmara in French Guiana rivers: mapping for risk assessment.

In French Guiana, native populations present high level of mercury contamination, which has been linked to the consumption of contaminated fishes. The goal of this study is to undertake a cartography of mercury contamination levels in fishes from the six main Guiana rivers. The selected species for this study is the ubiquitous piscivorous fish Hoplias aimara. A total number of 575 fishes from 134 discrete fishing sites are regrouped into 51 river sectors. Results from this study permits to rank the six main Guiana rivers by their mean level of contamination: Oyapock (0.548 mg kg-1), Comté (0.624 mg kg-1), Maroni (0.671 mg kg-1), Approuague (0.684 mg kg-1), Mana (0.675 mg kg-1), and Sinnamary (1.025 mg kg-1). The contamination is however not spatially homogenous along each river, and a map of the different levels of mercury contamination in fishes is provided. Sectors of low mean Hg contamination are observed both upstream (0.471 mg kg-1) and downstream (0.424 mg kg-1), corresponding to areas without any influence of gold mining activities and areas under the influence of estuarine dilution, respectively. Anoxia and gold mining activities are found to be the two main factors responsible for the high mercury concentration in fish muscles. While mean levels of mercury contaminations are higher in anoxia areas (1.029 mg kg-1), contaminations induced by gold mining activities (0.717 mg kg-1) present the most harmful consequences to human populations. No significant differences in Hg concentrations are observed between 2005 and 2014 for neither a pristine nor a gold mining area, while Hg concentration differences are observed between former (0.550 mg kg-1) and current gold mining sites (0.717 mg kg-1).

Biosensor for screening bacterial mercury methylation: example within the Desulfobulbaceae.

Mercury methylation and demethylation processes govern the fate of methylmercury in aquatic ecosystems. Under anoxic conditions, methylation activity is mainly of biological origin and is often the result of sulfate-reducing bacteria. In this study, the use of a luminescent biosensor for screening methylmercury production was validated by exposing the reporter strain to methylating or non-methylating Desulfovibrio strains. The sensitivity of the biosensor to methylmercury was shown to depend on sulfate-reducing bacterial growth conditions. Bioluminescence was measured using 1-10 mM of sulfides. As the sulfide level increased, luminescence decreased by 40-70%, respectively. Nevertheless, assuming an average of 5 mM of sulfide produced during sulfate-reducing growth, a mercury methylation potential of over 4% was detected when using 185 nM of inorganic mercury. Due to technical limitations, mercury speciation has, to date, only been investigated in a small number of bacterial strains, and no consistent phylogenetic distribution has been identified. Here, the biosensor was further used to assess the Hg methylation capacities of an additional 21 strains related to the Desulfobulbaceae. Seven of them were identified as methylmercury producers. Cultivation procedures combined with bacterial biosensors could provide innovative tools to identify new methylator clades amongst the prokaryotes.

Bacterial periphytic communities related to mercury methylation within aquatic plant roots from a temperate freshwater lake (South-Western France).

Macrophyte floating roots are considered as hotspots for methylmercury (MeHg) production in aquatic ecosystems through microbial activity. Nevertheless, very little is known about periphyton bacterial communities and mercury (Hg) methylators in such ecological niches. The ability to methylate inorganic Hg is broadly distributed among prokaryotes; however, sulfate-reducers have been reported to be the most important MeHg producers in macrophyte floating roots. In the present work, the periphyton bacterial communities colonizing Ludwigia sp. floating roots were investigated through molecular methods. Among the 244 clones investigated, anaerobic microorganisms associated with the sulfur biogeochemical cycle were identified. Notably, members of the sulfur-oxidizing prokaryotes and the anoxygenic, purple non-sulfur bacteria (Rhodobacteraceae, Comamonadaceae, Rhodocyclaceae, Hyphomicrobiaceae) and the sulfate reducers (Desulfobacteraceae, Syntrophobacteraceae, and Desulfobulbaceae) were detected. In addition, 15 sulfate-reducing strains related to the Desulfovibrionaceae family were isolated and their Hg-methylation capacity was tested using a biosensor. The overall results confirmed that Hg methylation is a strain-specific process since the four strains identified as new Hg-methylators were closely related to non-methylating isolates. This study highlights the potential involvement of periphytic bacteria in Hg methylation when favorable environmental conditions are present in such ecological micro-niches.

Specific Effects of Dietary Methylmercury and Inorganic Mercury in Zebrafish (Danio rerio) Determined by Genetic, Histological, and Metallothionein Responses.

A multidisciplinary approach is proposed here to compare toxicity mechanisms of methylmercury (MeHg) and inorganic mercury (iHg) in muscle, liver, and brain from zebrafish (Danio rerio). Animals were dietary exposed to (1) 50 ng Hg g(-1), 80% as MeHg; (2) diet enriched in MeHg 10000 ng Hg g(-1), 95% as MeHg; (3) diet enriched in iHg 10000 ng Hg g(-1), 99% as iHg, for two months. Hg species specific bioaccumulation pathways were highlighted, with a preferential bioaccumulation of MeHg in brain and iHg in liver. In the same way, differences in genetic pattern were observed for both Hg species, (an early genetic response (7 days) for both species in the three organs and a late genetic response (62 days) for iHg) and revealed a dissimilar metabolization of both Hg species. Among the 18 studied genes involved in key metabolic pathways of the cell, major genetic responses were observed in muscle. Electron microscopy revealed damage mainly because of MeHg in muscle and also in liver tissue. In brain, high MeHg and iHg concentrations induced metallothionein production. Finally, the importance of the fish origin in ecotoxicological studies, here the seventh descent of a zebrafish line, is discussed.

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.

Mercury bioaccumulation along food webs in temperate aquatic ecosystems colonized by aquatic macrophytes in south western France.

Mercury (Hg) is considered as an important pollutant for aquatic systems as its organic form, methylmercury (MeHg), is easily bioaccumulated and bioamplified along food webs. In various ecosystems, aquatic periphyton associated with macrophyte was identified as an important place for Hg storage and methylation by microorganisms. Our study concerns temperate aquatic ecosystems (South Western France) colonized by invasive macrophytes and characterized by high mercury methylation potentials. This work establishes original data concerning Hg bioaccumulation in organisms (plants, crustaceans, molluscs and fish) from five contrasting ecosystems. For low trophic level species, total Hg (THg) concentrations were low (from 27±2ngTHgg(-1)dw in asiatic clam Corbicula fluminea to 418±114ngTHgg(-1)dw in crayfish Procambarus clarkii). THg concentrations in some carnivorous fish (high trophic level) were close to or exceeded the International Marketing Level (IML) with values ranging from 1049±220ngTHgg(-1)dw in pike perch muscle (Sander lucioperca) to 3910±1307ngTHgg(-1)dw in eel muscle (Anguilla Anguilla). Trophic levels for the individuals were also evaluated through stable isotope analysis, and linked to Hg concentrations of organisms. A significant Hg biomagnification (r(2)= 0.9) was observed in the Aureilhan lake, despite the absence of top predator fish. For this site, Ludwigia sp. periphyton, as an entry point of Hg into food webs, is a serious hypothesis which remains to be confirmed. This study provides a first investigation of Hg transfer in the ecosystems of south western France and allows the assessment of the risk associated with the presence of Hg in aquatic food webs.

Incidence of invasive macrophytes on methylmercury budget in temperate lakes: central role of bacterial periphytic communities.

Several studies demonstrated high mercury (Hg) methylation and demethylation in the periphyton associated with floating roots in tropical ecosystems. The importance of aquatic plants on methylmercury production in three temperate ecosystems from south-western France was evaluated through Hg species concentrations, and Hg methylation/demethylation activities by using stable isotopic tracers ((199)Hg(II), Me(201)Hg). Hg accumulation and high methylation and demethylation yields were detected in plant roots and periphyton, whereas results for sediment and water were low to insignificant. The presence of sulfate reducing prokaryotes was detected in all compartments (T-RFLP based on dsrAB amplified through nested PCR) and their main role in Hg methylation could be demonstrated. In turn, sulfate reduction inhibition did not affect demethylation activities. The estimation of net MeHg budgets in these ecosystems suggested that aquatic rhizosphere is the principal location for methylmercury production and may represent an important source for the contamination of the aquatic food chain.

Influence of prey type on nickel and thallium assimilation, subcellular distribution and effects in juvenile fathead minnows (Pimephales promelas).

Because fish take up metals from prey, it is important to measure factors controlling metal transfer between these trophic levels so as to explain metal bioaccumulation and effects in fish. To achieve this, we exposed two types of invertebrates, an oligochaete (Tubifex tubifex) and a crustacean (Daphnia magna), to environmentally relevant concentrations of two important contaminants, nickel (Ni) and thallium (Tl), and fed these prey to juvenile fathead minnows (Pimephales promelas). We then measured the assimilation efficiency (AE), subcellular distribution and effects of these metals in fish. Fish assimilated dietary Tl more efficiently from D. magna than from T. tubifex, and more efficiently than Ni, regardless of prey type. However, the proportion of metal bound to prey subcellular fractions that are likely to be trophically available (TAM) had no significant influence on the efficiency with which fish assimilated Ni or Tl. In fish, the majority of their Ni and Tl was bound to subcellular fractions that are purportedly detoxified, and prey type had a significant influence on the proportion of detoxified Ni and Tl in fish. We measured higher activities of cytochrome C oxidase and glutathione S-transferase in fish fed D. magna compared to fish fed T. tubifex, regardless of the presence or absence of Ni or Tl in prey. However, we measured decreased activities of glutathione S-transferase and nucleoside diphosphate kinase in fish fed Tl-contaminated D. magna compared to fish from the three other treatment levels.