Different Species of Mercury in the Livers of Tropical Dolphins
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1 Analytical Letters, 41: , 2008 Copyright # Taylor & Francis Group, LLC ISSN: print/ x online DOI: / CHEMICAL SPECIATION Different Species of Mercury in the Livers of Tropical Dolphins H.A. Kehrig, 1 T.G. Seixas, 2 E.A. Palermo, 1 A.P.M. Di Beneditto, 3 C.M.M. Souza, 3 and O. Malm, 1 1 Laboratorio de Radioisotopos Eduardo Penna Franca, IBCCF, Universidade Federal do Rio de Janeiro Brazil 2 Departamento de Química, PUC-Rio, Brazil 3 Laboratorio de Ciências Ambientais, CBB, Universidade Estadual Norte Fluminense, Brazil Abstract: Four kinds of mercury species (inorganic mercury (Hg inorg ), methylmercury (MeHg), total organic mercury (RHg org ), and insoluble mercury, deemed to be mercuric selenide (HgSe), were determined in the livers of dolphins from the Brazilian coast. The MeHg was identified and quantified in the toluene layer on a Gas Chromatograph with an Electron Capture Detector (GC-ECD). The RHg org was isolated by acid leaching (H 2 SO 4 -KBr-CuSO 4 ) and then extracted into CH 2 Cl 2. The RHg org and Hg inorg were determined by Cold-Vapor Atomic Absorption Spectroscopy (CV-AAS). The MeHg was the smallest fraction of Hg tot, with a median of 9%, whereas the highest fraction of the Hg tot was as HgSe, corresponding to 53%. The fractions of Hg inorg and RHg org corresponded to 30% and 39%, respectively. The lowest fraction of MeHg and the highest fraction of HgSe in the liver of all animals are related to different capacities or strategies of detoxification of methylmercury in this organ. Keywords: Inorganic mercury, insoluble mercury, liver, methylmercury, total organic mercury, tropical dolphin Received 11 October 2007; accepted 28 February Address correspondence to H.A. Kehrig, Laboratorio de Radioisotopos Eduardo Penna Franca, IBCCF, Universidade Federal do Rio de Janeiro, , Brazil. kehrig@biof.ufrj.br 1690
2 Species of Mercury in Dolphin Livers 1691 INTRODUCTION Mercury occurs in different chemical and physical forms. The most abundant are elemental Hg (Hg ), divalent mercury (Hg þ2 ), methylmercury (MeHg, CH 3 Hg þ ), dimethylmercury (DMHg, CH 3 HgCH 3 ), and ethylmercury (EtHg, CH 3 CH 2 Hg þ ), each of which is unique with regard to exposure pattern, metabolism, and toxic effects. The toxicity of mercury compounds depends not only on the form of mercury and the route of entry, but also on dosage (Gibiěar et al. 2007). Mercury compounds can affect productivity, reproduction, and survival of coastal and marine animals, and can be hazardous to human health (WHO 1989). Mercury species present as mercuric selenide appear to be quite inert in the mammalian liver (Wagemann et al. 2000), while methylmercury is a potent neurotoxin. Probably, the toxicities of the other forms of mercury, such as inorganic mercury and organic mercury other than methylmercury, fall between the toxicity of mercuric selenide and methylmercury, which represent the extremes of the toxicity mercury compounds (Wagemann et al. 2000). In the marine environment, almost all of the mercury in the muscle of aquatic mammals is methylated, as methylmercury (Joiris et al. 2001; Kehrig et al. 2004). However, the major part of mercury accumulated in their internal organs, especially in the liver, exists as inorganic mercury, suggesting that demethylation of methylmercury is possible (Wagemann et al. 2000; Joiris et al. 2001; Kehrig et al. 2004). The liver of marine mammals appears to be the preferential organ for mercury accumulation. These high hepatic mercury concentrations are probably related to the role played by the liver in terms of pollutant biotransformation (Frodello et al. 2000). The literature has proposed that the liver of the aquatic mammals may act as an organ for mercury demethylation and=or the sequestration of both organic and inorganic forms of this element from the body (Wagemann et al. 2000; Endo et al. 2002). More importantly, the literature reported that selenium is involved in both the demethylation and the immobilization of mercury in aquatic mammals, suggesting mercury selenide (HgSe) formation (Caurant et al. 1996; Nigro and Leonzio 1996). In order to assess the importance of the liver in the regulation of mercury accumulation, four mercury species, inorganic mercury (Hg inorg ), methylmercury (MeHg), total organic mercury (RHg org ), and insoluble mercury, deemed to be mercuric selenide (HgSe), were determined in this organ of tropical dolphins. Samples were collected after entanglement in gill-net fisheries on the northern coast of Rio de Janeiro state, Brazil. This study also quantifies the contribution of each mercury species to the total mercury burden in the liver.
3 1692 H.A. Kehrig et al. EXPERIMENTAL Samples The livers of 29 specimens of Sotalia guianensis (van Bénéden, 1862), a small coastal dolphin endemic to the western South Atlantic, were analyzed for total mercury, methylmercury, total organic mercury, inorganic mercury, and insoluble mercury, deemed to be mercuric selenide. The specimens of dolphin analyzed in the present study were collected after entanglement in gill-net fisheries, from 1998 to 2005, on the northern coast of Rio de Janeiro state. After the liver samples were freeze-dried, they lost around 70% of their water content. The concentrations of the analyzed four mercury species are presented in a dry-weight basis (dry wt). Instrumentation Samples were analyzed for total mercury, inorganic mercury, and total organic mercury with a cold vapor atomic absorption spectrometer with a Flow Injection Mercury System (FIMS) FIAS 400 (Perkin Elmer) with auto sampler AS90 (Perkin Elmer). The carrier gas was argon (99,998%) at a flow rate of 75 ml min 1. For methylmercury analysis, the chromatographic system used was a 14 B Shimadzu gas chromatograph (GC) with a pulsed current 63 Ni electron-capture detector-ecd (Kyoto, Japan) equipped with a Shimadzu C-R6A Chromatopac integrator and a GC silane-treated glass column of 1 m 3 mm i.d. (GL Sciences Japan) with Hg-20A as stationary phase on mesh Uniport HP (GL Sciences, Japan). On the top of column, nearest the injection port, 0.2 g of NaCl crystals were added to enhance the methylmercury detection. This method is based on the fact that methylmercury dithizonate in the final solution in toluene is converted into its chloride form as soon as it passes through the NaCl on the top of the columns (Akagi and Nishimura 1991; Kehrig et al. 2006). The column oven, detector, and injector temperature were maintained at 150 C, 250 C, and 180 C, respectively. The carrier gas was nitrogen (99,999%) at a flow rate of 40 ml min 1. Analytical Methodologies Total Mercury Determination in the Liver of the Dolphin Dried liver samples (0.05 g) were acid digested with 3 ml of H 2 SO 4 :HNO 3 (1:1v=v) (Merck p.a.) and 1 ml of conc. H 2 O 2 (Merck p.a.) in a 50 ml centrifuge tube at 60 C in water bath for 45 min. After
4 Species of Mercury in Dolphin Livers 1693 addition of 5 ml of 5% KMnO 4 (Merck p.a.) solution, the digested sample was allowed to stand overnight. Total mercury concentrations in the acid digested solution were determined by CVAAS (FIMS-system) with NaBH 4 (Merck p.a.) as a reducing agent. A detailed description of the method used is given elsewhere (Kehrig et al. 2006). Methylmercury Determination in the Liver of the Dolphin For methylmercury, we used an analytical procedure developed at the National Institute for Minamata Disease (NIMD) laboratory and adapted at the Universidade Federal do Rio de Janeiro (UFRJ) laboratory. The methylmercury determination in the liver of the dolphins was made by a combination of the dithizone-toluene extraction and GC-ECD analysis (Akagi and Nishimura 1991; Kehrig et al. 2006). Dried tissue (0.05 g) was digested with 10 ml of 1 mol L 1 alcoholic potassium hydroxide solution in a 50 ml screw-capped centrifuge tube at 100 C in a water bath for 45 min. The digested sample was slightly acidified with 10 ml of 1 mol L 1 HCl (Merck p.a.). After washing the digested acid sample with 5 ml of n-hexane (Tedia ABSOLV), the methylmercury was extracted with 10 ml of 0.05% dithizone (Merck p.a.) in toluene (Tedia ABSOLV) purified with an equal volume of 0.1 mol L 1 NaOH just before use. The organic layer was then washed twice with 5 ml of 1 mol L 1 NaOH to remove the excess dithizone. An aliquot (5 ml) of the organic layer was back-extracted with 2 ml of 0.01% Na 2 S in 0.1 mol L 1 NaOH=ethanol (1:1v=v). The excess sulphite ions from the methylmercury solution were eliminated with continuous bubbling (50 ml min 1 ) with N 2 gas and some drops of 1 mol L 1 HCl for a further 5 min. To the sample solution, 2 ml of Walpole s Buffer (ph ¼ 3.0) was added. Walpole s Buffer was made with 600 ml of Milli Q water þ 200 ml of 1 mol L 1 CH 3 COONa þ 200 ml of 1 mol L 1 HCl. The methylmercury from this inorganic layer was re-extracted with 1 ml of 0.05% purified dithizone-toluene. The organic layer was then washed twice with 2 ml of 1 mol L 1 NaOH to remove the excess dithizone and subsequently with 5 ml of distilled water and was then acidified with a few drops of 1 mol L 1 HCl, followed by GC-ECD (Kehrig et al. 2006). Total Organic Mercury, Inorganic Mercury, and Mercuric Selenide Determination in the Liver of the Dolphin Dried tissue (0.05 g) was placed in a screw-capped 50 ml Teflon vial for 15 min at room temperature with a mixture of 5 ml 5% H 2 SO 4,18%
5 1694 H.A. Kehrig et al. KBr, and 1 ml 1 mol L 1 CuSO 4 solution (Merck p.a.). The RHg org,hg i- norg, and HgSe in the liver samples were isolated by acid leaching. Then, 10 ml of CH 2 Cl 2 (Tedia ABSOLV) was added to each vial, and the samples were shaken vigorously for 15 min. The samples were then centrifuged for 5 min at 3200 rpm (Gibiěar et al. 2007). So, three phases were formed: organic phase (a), aqueous phase (b), and solid phase (c). The organic phase (up layer) (a) was separated in a Teflon separating funnel, and 1 ml of the CH 2 Cl 2 phase was transferred to a 50 ml centrifuge tube containing 5 ml of an HNO 3 -H 2 SO 4 mixture (1:4 v=v) and heated at 60 C in water bath for 45 min. The organic solvent mixture evaporated without detectable loss of RHg org (Wagemann et al. 2000). The remaining aqueous phase was digested and analyzed for total mercury. The RHg org concentration found included MeHg and other organic mercury forms. The Hg inorg remained in the aqueous bottom phase of the Teflon separating funnel (b) and HgSe remained in the solid phase (c). A 1 ml aliquot of the aqueous phase (b) was transferred to a 50 ml centrifuge tube containing 3 ml of H 2 SO 4 : HNO 3 (1:1v=v) (Merck p.a.) and heated at 60 C in water bath for 45 min (Wagemann et al. 2000). Then, the digested acid solution that contains Hg inorg was analyzed as for Hg tot. The concentration of HgSe corresponded to the difference between Hg tot, RHg org, and Hg inorg found in each liver sample. A mass balance of the mercury species (Hg inorg, MeHg, RHg org, and HgSe) was established, indicating how much individual mercury species contribute to the total mercury burden in the liver. RESULTS AND DISCUSSION Validation of the Analytical Methods Precision and accuracy of the analytical methods were determined and monitored using certified material from the International Atomic Energy Agency (IAEA 350-Tuna fish sample) and National Research Council- Canada (DORM-2, Dogfish muscle sample and TORT-2 Lobster hepatopancreas). Results for total mercury DORM-2 (N ¼ 12) were mg kg 1, and the CRM has a certified Hg tot value of mg kg 1. For TORT-2 (N ¼ 10), total mercury found was mg kg 1, and the CRM has a certified Hg tot value of mg kg 1.Recovery of Hg tot in the DORM-2 and TORT-2 samples was from 90 to 105%. Our results for RHg org and Hg inorg DORM-2 were mg kg 1 (N ¼ 7) and mg kg 1 (N ¼ 7), respectively. The sum of RHg org and Hg inorg results for the
6 Species of Mercury in Dolphin Livers 1695 DORM-2 sample was 4.76 mg kg 1, corresponding to the CRM Hg tot value of mg kg 1. In the muscle sample, DORM-2, 100% of the total organic mercury is as methylmercury (MeHg); that CRM value is mg kg 1. The mean of our RHg org results for the DORM-2 sample corresponded to 98% of the CRM MeHg certified value. Our results for RHg org and Hg inorg TORT-2 were mg kg 1 (N ¼ 5) and mg kg 1 (N ¼ 5), respectively. The sum of RHg org and Hg inorg results for the TORT-2 sample was mg kg 1, corresponding to the CRM Hg tot value of mg kg 1. The mean of our RHg org results for the TORT-2 sample corresponded to 95% of the CRM MeHg certified value. Recovery of RHg org in the DORM-2 and TORT-2 samples was from 85 to 108%. Our routine methylmercury results for reference sample IAEA 350 (N ¼ 39) were mg kg 1, while the CRM MeHg value was mg kg 1. Recovery of MeHg in the IAEA 350 sample was from 92 to 107%. The coefficient of variation (standard deviation=mean) for the duplicate samples was less than 10%. Liver Samples Total mercury concentrations (Hg tot ) (in a dry weight basis) ranged from 0.84 to mg kg 1 (Table 1). It is well-known that mercury accumulates preferentially in the liver of marine mammals, which is probably related to the role played by the liver in terms of pollutant biotransformation, metabolizing nutrients and essential elements as well as removing some nonessential elements and toxins from the bloodstream (Frodello et al. 2000). As a result, hepatic cells can have more concentrated amounts of elements relative to other tissues. This pattern was also observed in previous studies with dolphins from Argentina (Gerpe et al. 2002) and Brazil (Kehrig et al. 2004; Seixas et al. 2007). Table 1. The median and range of the concentrations of total mercury (Hg tot )ina dry-weight basis, and the percentage of methylmercury (% MeHg), total organic mercury (% RHg org ), inorganic mercury (% Hg inorg ), and mercuric selenide (% HgSe), to total mercury in the liver of Sotalia guianensis Hg tot (mg kg 1 ) % MeHg % % RHg org (RHg org MeHg) % % Hg inorg HgSe
7 1696 H.A. Kehrig et al. Methylmercury concentrations (MeHg) ranged from 0.23 to 6.51 mg kg 1, corresponding to the smallest fraction of total mercury (% MeHg) presented in the liver of all analyzed animals, with a median of 9% (see Table 1). In a previous study (Kehrig et al. 2004), Sotalia guianensis from Guanabara Bay (Rio de Janeiro, Brazil) presented lower percentages of methylmercury (%MeHg) in the liver (median 5%) than the specimens analyzed in this study. Differences found between the amount of MeHg in both studies on the same marine mammal species were probably due to the preferred prey, bioavailability of mercury in each marine environment, and environment variables, such as net primary production. The concentration of RHg org found in this study ranged from 0.49 to 9.67 mg kg 1, corresponding to 39% of the fraction of total mercury (%RHg org ) (see Table 1). It is important to observe that the concentration of RHg org found included MeHg and other organic mercury forms. The highest fraction of the total mercury in the liver was as HgSe, corresponding to a median of 53% (Table 1). However, the highest % MeHg (28%) and the lowest % HgSe ( 0%) occurred in the liver that presented the total mercury concentration below 1.0 mg kg 1 dry wt (Fig. 1a). Furthermore, the highest % HgSe (83%) occurred in the liver sample that presented the highest hepatic total mercury concentration (87.92 mg kg 1 dry wt) (Fig. 1b). In this study, all specimens of S. guianensis that presented total hepatic mercury concentration above 5.5 mg kg 1 dry wt showed the highest amount of HgSe (ranging from 44% to 89%) and the lowest amount of MeHg (ranging 2% to 7%) in their livers. Wagemann et al. (2000) reported similar results regarding the fractions of Hg tot as MeHg and HgSe in the liver samples of ringed seals Figure 1. The amount of Hg inorg, MeHg, (RHg org -MeHg), and HgSe presented in the liver samples of two specimens of Sotalia guianensis: (a) example of the sample with the lowest hepatic Hg tot concentration and (b) example of the sample with the highest hepatic Hg tot concentration.
8 Species of Mercury in Dolphin Livers 1697 from the Canadian Arctic. However, the ringed seals presented lower percentages of RHg org and higher percentages of Hg inorg than the results found in the same organ of the dolphins from the Brazilian coast. The relatively low fraction of methylmercury in the liver of all analyzed species found by us (always 28%) and by others (Palmisano et al. 1995; Wagemann et al. 2000; Kehrig et al. 2004) and also the increase of the fraction of mercuric selenide, indicate that the liver may act as an organ for mercury demethylation and=or the sequestration of both organic and inorganic forms of this element from the body. It is important to note that total mercury is accumulated in the liver as inorganic mercury, since this organ presents a small fraction of total mercury as methylmercury (Wagemann et al. 2000). According to Joiris et al. (2001), the accumulation of high concentrations of inorganic mercury in the liver was probably due to a slow demethylation process, implying the formation of HgSe (mercuric selenide). Demethylation, the transformation of organic mercury into the less toxic inorganic form, is believed to occur in the liver of marine mammals (Endo et al. 2002). Mercury is stored in a permanent and continuous manner in the mammalian liver in the form of insoluble mercuric selenide (Frodello et al. 2000; Wagemann et al. 2000). The ultrastructural investigation done on liver sections of different dolphin species from the Italian coast revealed the presence of dense and abundant granules containing mercury and selenium (Nigro and Leonzio 1996). The biosynthesis of mineral granules containing mercury and selenium in top marine predators is a common feature among these animals, and the existence of elimination pathways for the excretion of organic mercury might influence the amount of mercury and selenium storage as mineral granules in a particular species (Nigro and Leonzio 1996). CONCLUSIONS Probably, the lowest fraction of MeHg and the highest fraction of HgSe in the liver of all animals analyzed in this study are related to different capacities or strategies of detoxification of methylmercury in this organ. Approximately half of the total mercury in the liver, as HgSe, was potentially inert and apparently nontoxic mercury. REFERENCES Akagi, H. and Nishimura, H Speciation of mercury in the environment. In T. Suzuki, I. Nobumassa, and T.W. Clarkson (Eds.), Advances in mercury toxicology, (pp ). New York: Plenum.
9 1698 H.A. Kehrig et al. Caurant, F., Navarro, M., and Amiard, J.-C Mercury in pilot whales: Possible limits to the detoxification process. Science of the Total Environment, 186: Endo, T., Haraguchi, K., and Sakata, M Mercury and selenium concentrations in the internal organs of toothed whales and dolphins marketed for human consumption in Japan. Science of the Total Environment, 300: Frodello, J.P., Roméo, M., and Viale, D Distribution of mercury in the organs and tissues of five toothed-whale species of the Mediterranean. Environmental Pollution, 108: Gerpe, M.S., Rodriguez, D.H., Moreno, V.J., Bastida, R.O., and Moreno, J.A.E Accumulation of heavy metals in the franciscana (Pontoporia blainvillei) from Buenos Aires Province, Argentina. The Latin American Journal of Aquatic Mammals, 1: Gibiěar, D., Logar, M., Horvat, N., Marn-Pernat, A., Ponikvar, R., and Horvat, M Simultaneous determination of trace levels of ethylmercury and methylmercury in biological samples and vaccines using sodium tetra (n-propyl) borate as derivatizing agent. Analytical and Bioanalytical Chemistry, 388: Joiris, C.R., Holsbeek, L., Bolba, D., Gascard, C., Stanev, T., Komakhidzes, A., Baumgärtner, W., and Birkun, A Total and organic mercury in the Black Sea Harbour Porpoise Phocoena phocoena relicta. Marine Pollution Bulletin, 42: Kehrig, H.A., Costa, M., Moreira, I., and Malm, O Total and methylmercury in different species of mollusks from two estuaries in Rio de Janeiro state. Journal of the Brazilian Chemical Society, 17: Kehrig, H.A., Seixas, T.G., Baêta, A., Lailson-Brito, Jr., J., Moreira, I., and Malm, O Total mercury, methylmercury and selenium in the liver and muscle of different fishes and a marine mammal from a tropical estuary-brazil. Journal RMZ-Materials and Geoenvironment, 51: Nigro, M. and Leonzio, C Intracellular storage of mercury and selenium in different marine vertebrates. Marine Ecology Progress Series, 135: Palmisano, F., Cardellicchio, N., and Zambonin, P.G Speciation of mercury in dolphin liver: A two-stage mechanism for the demethylation accumulation process and role of selenium. Marine Environmental Research, 40: Seixas, T.G., Kehrig, H.A., Fillmann, G., Di Beneditto, A.P.M., Souza, C.M.M., Secchi, E.R., Moreira, I., and Malm, O Ecological and biological determinants of trace elements accumulation in liver and kidney of Pontoporia blainvillei. Science of the Total Environment, 385: Wagemann, R., Trebacs, E., Boila, G., and Lockhart, W.L Mercury species in the liver of ringed seals. Science of the Total Environment, 261: WHO Mercury. Environmental aspects Criteria N 86. World Health Organization, Geneva, Switzerland.
This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and
This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution
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