Trophic transfer and accumulation of mercury in ray species in coastal waters affected by historic mercury mining (Gulf of Trieste, northern Adriatic Sea)

Abstract

Total mercury (Hg) and monomethylmercury (MMHg) were analysed in the gills, liver and muscle of four cartilaginous fish species (top predators), namely, the eagle ray (Myliobatis aquila), the bull ray (Pteromylaeus bovinus), the pelagic stingray (Dasyatis violacea) and the common stingray (Dasyatis pastinaca), collected in the Gulf of Trieste, one of the most Hg-polluted areas in the Mediterranean and worldwide due to past mining activity in Idrija (West Slovenia). The highest Hg and MMHg concentrations expressed on a dry weight (d.w.) basis were found in the muscle of the pelagic stingray (mean, 2.529 mg/kg; range, 1.179–4.398 mg/kg, d.w.), followed by the bull ray (mean, 1.582 mg/kg; range, 0.129–3.050 mg/kg d.w.) and the eagle ray (mean, 0.222 mg/kg; range, 0.070–0.467 mg/kg, d.w.). Only one specimen of the common stingray was analysed, with a mean value in the muscle of 1.596 mg/kg, d.w. Hg and MMHg contents in the bull ray were found to be positively correlated with species length and weight. The highest MMHg accumulation was found in muscle tissue. Hg and MMHg were also found in two embryos of a bull ray, indicating Hg transfer from the mother during pregnancy. The number of specimens and the size coverage of the bull rays allowed an assessment of Hg accumulation with age. It was shown that in bigger bull ray specimens, the high uptake of inorganic Hg in the liver and the slower MMHg increase in the muscle were most probably due to the demethylation of MMHg in the liver. The highest Hg and MMHg contents in all organs were found in the pelagic stingray, which first appeared in the northern Adriatic in 1999. High Hg and MMHg concentrations were also found in prey species such as the banded murex (Hexaplex trunculus), the principal prey of the eagle rays and bull rays, the anchovy (Engraulis encrasicholus) and the red bandfish (Cepola rubescens), which are preyed upon by the pelagic stingray, as well as in zooplankton and seawater. Based on previously published data, a tentative estimation of MMHg bioamagnification was established. The average increase in MMHg between seawater, including phytoplankton, and zooplankton in the Gulf was about 104, and MMHg in anchovy was about 50-fold higher than in zooplankton. The bioaccumulation of MMHg between seawater and small pelagic fish (anchovy) amounted to 106 and between water and the muscle of larger pelagic fish (pelagic stingray) to 107. The MMHg increase between surface sediment and benthic invertebrates (murex) and between benthic invertebrates and small benthic fish was 102. Ultimately, the trophic transfer resulted in a 103 accumulation of MMHg between water and muscle of larger benthic fish (bull ray, eagle ray, common stingray), suggesting lower bioaccumulation by benthic feeding species.

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References

  1. Andersen JL, Depledge MH (1997) A survey of total mercury and methylmercury in edible fish and invertebrates from Azorean waters. Mar Environ Res 44:331–350

    CAS  Article  Google Scholar 

  2. Andres S, Laporte J, Mason R (2002) Mercury accumulation and flux across the gills and the intestine of the blue crab (Callinectes sapidus). Aquat Toxicol 56:303–320

    CAS  Article  Google Scholar 

  3. André JM, Ribeyre F, Boudou A (1990) Mercury contamination levels and distribution in tissues and organs of delphinids (Stenella attennuata) from the Eastern Tropical Pacific, in relation to biological and ecological factors. Mar Environ Res 30:43–72

    Article  Google Scholar 

  4. Back RC, Watras CJ (1995) In: Porcella DB, Huckabee JW, Wheatley B (eds) Mercury as a global pollutant. Kluwer, Dordrecht, pp 931–938

    Google Scholar 

  5. Bernhard M (1988) Mercury in the Mediterranean, UNEP Report, 141 pp

  6. Boening D (2000) Eological effects, transport, and fate of mercury. A general review. Chemosphere 40:1335–1351

    CAS  Article  Google Scholar 

  7. Boudou A, Ribeyre F (1997) Mercury in the food web: accumulation and transfer mechanisms. Met Ions Biol Syst 34:289–319

    CAS  Google Scholar 

  8. Bratkič A, Ogrinc N, Kotnik J, Faganeli J, Žagar D, Yano S, Tada A (2013) Mercury speciation driven by seasonal changes in a contaminated estuarine environment. Environ Res 125:171–178

    Article  Google Scholar 

  9. Buzina R, Stegnar P, Buzina-Subotičanec K, Horvat M, Petrić I, Farley TMM (1995) Dietary mercury intake and human exposure in an Adriatic population. Sci Total Environ 170:199–208

    CAS  Article  Google Scholar 

  10. Capape C, Guelorget O, Vergne Y, Marques A, Quingnard JP (2006) Skates and rays (Chondrichthyes) from waters off Languedocian coast (southern France, northern Mediterranean): a historical survey and present status. Annales Ser Hist Nat 16:165–178

    Google Scholar 

  11. Cardellicchio N, Decataldo A, Di Leo A, Misiono A (2002) Accumulation and tissue distribution of mercury and selenium in striped dolphins (Stenella coeruleoalba) from the Mediterranean Sea (southern Italy). Environ Pollut 116:265–271

    CAS  Article  Google Scholar 

  12. Chen CY, Serrell N, Evers DC, Fleishmaa BJ, Lambert KF, Weiss J, Mason RP, Bank MS (2008a) Meeting report: methylmercury in marine ecosystems—from sources to seafood consumers. Environ Health Perspect 116:1706–1712

    CAS  Article  Google Scholar 

  13. Chen C, Amirabahman A, Fisher N, Harding G, Lamborg C, Nacci D, Taylor D (2008b) Methylmercury in marine ecosystems: spatial patterns and processes of production, bioaccumulation, and biomagnification. EcoHealth 5:399–408

    Article  Google Scholar 

  14. Chen CY, Driscoll CD, Lambert KF, Mason RP, Rardin LR, Serrell N, Sunderland EM (2013) Marine mercury fate: from sources to seafood consumers. Environ Res 119:1–2

    Article  Google Scholar 

  15. Choy CA, Popp BN, Kaneko JJ, Drazen JC (2009) The influence of depth on mercury levels in pelagic fishes and their prey. PNAS 106:13865–13869

    CAS  Article  Google Scholar 

  16. Covelli S, Faganeli J, Horvat M, Brambati A (2001) Mercury contamination of coastal sediments as the result of long-term cinnabar mining activity (Gulf of Trieste, northern Adriatic Sea). Appl Geochem 15:541–558

    Article  Google Scholar 

  17. Commission of the European Communities (2001). EU commission decision 466/2001/EC of March 8, 2001 setting maximum levels for certain contaminants in foodstuffs. G.U. EU-L 77/1 of 16/03/2001

  18. Cuvin-Aralar ML, Furness RW (1991) Mercury and selenium interaction: a review. Ecotoxicol Environ Safety 21:348–364

    CAS  Article  Google Scholar 

  19. Davenport S (1995) Mercury in blue sharks and deep water dogfish from around Tasmania. Austral Fish 54:20–22

    Google Scholar 

  20. Downs SG, Macleod CL, Lester JN (1998) Mercury in precipitation and its relations to bioaccumulation in fish: a literature review. Water Air Soil Pollut 108:149–187

    CAS  Article  Google Scholar 

  21. Dulčič J, Lipej L, Orlando Bonaca M, Jenko R, Grbec B, Guélorget O, Capapé C (2008) The bull ray, Pteromylaeus bovinus (Myliobatidae), in the northern Adriatic Sea. Cybium 32:119–123

    Google Scholar 

  22. Faganeli J, Horvat M, Covelli S, Fajon V, Logar M, Lipej L, Cermelj B (2003) Mercury and methylmercury in the Gulf of Trieste (northern Adriatic Sea). Sci Total Environ 304:315–326

    CAS  Article  Google Scholar 

  23. EFSA (2012) Scientific opinion on the risk for public health related to the presence of mercury and methylmercury in food. EFSA Journal 10(12):2985 (241 pp). doi:10.2903/j.efsa.2012.2985

    Google Scholar 

  24. Fitzgerald WF, Lamborg CH, Hammerschmidt CR (2007) Marine biogeochemical cycle of mercury. Chem Rev 107:641–662

    CAS  Article  Google Scholar 

  25. Hall BD, Bodaly RA, Fudge RJP, Rudd JWM, Rosenberg DM (1997) Food as the dominant pathway of methylmercury uptake by fish. Water Air Soil Pollut 100:13–24

    CAS  Google Scholar 

  26. Hammerschmidt CR, Fitzgerald WF (2006) Bioaccumulation and trophic transfer of methylmercury in Long Island Sound. Arch Environ Contam Toxicol 51:416–424

    CAS  Article  Google Scholar 

  27. Hansen JC, Gilman AP (2005) Exposure of Arctic populations to methylmercury from consumption of marine food: an updated risk–benefit assessment. Int J Circumpolar Health 64:121–136

    Article  Google Scholar 

  28. Hines ME, Horvat M, Faganeli J, Bonzongo J-C, Barkay T, Scott KJ, Bailey EA, Major EB, Warwick JJ (2000) Mercury biogeochemistry in the Idrija River, Slovenia, from above the mine into the Gulf of Trieste. Environ Res 83:129–139

    CAS  Article  Google Scholar 

  29. Hines ME, Faganeli J, Adatto I, Horvat M (2006) Microbial mercury transformations in marine, estuarine and freshwater sediment downstream of the Idrija mercury mine, Slovenia. Appl Geochem 21:1924–1939

    CAS  Article  Google Scholar 

  30. Horvat M, Byrne AR, May K (1990) A modified method for the determination of methylmercury by gas chromatography. Talanta 37:207–212

    CAS  Article  Google Scholar 

  31. Horvat M, Lupšina V, Pilhar B (1991) Determination of total mercury in coal fly ash by gold amalgamation cold vapour atomic absorption spectrometry. Anal Chim Acta 243:71–79

    CAS  Article  Google Scholar 

  32. Horvat M, Covelli S, Faganeli J, Logar M, Mandić V, Rajar R, Širca A, Žagar D (1999) Mercury in contaminated coastal environments: a case study: the Gulf of Trieste. Sci Total Environ 237(238):43–56

    Article  Google Scholar 

  33. Horvat M, Kontić B, Kotnik J, Ogrinc N, Jereb V, Fajon V, Logar M, Faganeli J, Rajar R, Širca A, Petkovšek G, Žagar D, Dizdarevic T (2003a) Remediation of mercury polluted sites due to mining activities. Crit Rev Anal Chem 33:291–296

    CAS  Article  Google Scholar 

  34. Horvat M, Kotnik J, Logar M, Fajon V, Zvonarić T, Pirrone N (2003b) Speciation of mercury in surface and deep-sea waters in the Mediterranean Sea. Atmos Environ 37:S93–S108

    CAS  Article  Google Scholar 

  35. Jardas I (1996) Jadranska ihtiofavna. Školska knjiga, Zagreb (in Croatian, English. summary)

  36. Joiris CR, Holsbeek L, Larroissi Moatemri N (1999) Total and methylmercury sardines Sardinela aurita and Sardina pilchardus from Tunisia. Mar Poll Bull 38:188–192

    Google Scholar 

  37. Kojadinović J, Potier M, Le Corre M, Cosson RP, Bustamante P (2007) Bioaccumulation of trace elements in pelagic fish from the western Indian Ocean. Environ Pollut 146:548–566

    Article  Google Scholar 

  38. Karagas MR, Choi AL, Oken E, Horvat M, Schoeny R, Kamai E, Cowell W, Grandjean G, Korrick S (2012) Evidence on the human health effects of low-level methylmercury exposure. Environ Health Perspect 120(6):799–806

    CAS  Article  Google Scholar 

  39. Kotnik J, Horvat M, Ogrinc N, Fajon V, Žagar D, Cossa D, Sprovieri F, Pirrone N (2013) Mercury and its species in the Adriatic Sea. Mar Chem (in review)

  40. Lipej L, Mavrič B, Paliska D, Capape C (2013) Feeding habits of the pelagic stingray Pteroplatytrygon violacea (Chondrichthyes: Dasyatidae) in the Adriatic Sea. J Mar Biol Assoc UK 93(2):285–290

    Article  Google Scholar 

  41. Malatt J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648

    Article  Google Scholar 

  42. Mavrič B, Jenko R, Makovec T, Lipej L (2004) On the occurrence of the pelagic stingray, Dasyatis violacea (Bonaparte, 1832), in the Gulf of Trieste (northern Adriatic). Annales Ser Hist Nat 14:181–186

    Google Scholar 

  43. Meyers G, Davidson PW, Cox C, Shamlaye CF, Cernichiari E, Clarkson TW (2000) Twenty-seven years of human neurotoxicity of methylmercury exposure. Environ Res 83:275–285

    Article  Google Scholar 

  44. Munthe J, Bodaly RA, Branfireun BA, Driscoll CT, Gilmour CC, Harris R, Horvat M, Lucotte M, Malm O (2007) Recovery of mercury-contaminated fisheries. Ambio 36(1):33–44

    CAS  Article  Google Scholar 

  45. National Academy of Science (2000) Toxicological effects of methylmercury. Washington, DC

  46. Nathanson MH, Mariwalla K, Ballatori N, Boyer J (1995) Effect of Hg2+ on cytosolic Ca2+ in isolated skate hepatocytes. Cell Calcium 18:429–439

    CAS  Article  Google Scholar 

  47. Oliviera Ribeiro CA, Belger L, Pelletier E, Rouleau C (2002) Histopathological evidence of inorganic mercury and methylmercury in arctic char (Salvelinus alpinus). Environ Res 90:217–225

    Article  Google Scholar 

  48. Olsvik P, Gundersen P, Andersen RA, Zachariassen KE (2001) Metal accumulation and metallothionein in brown trout, Salmo trutta, from two Norwegian rivers differently contaminated with Cd, Cu and Zn. Comp Biochem Physiol 128C:189–201

    CAS  Google Scholar 

  49. Ornaghi F, Ferrini S, Prati M, Giavini E (1993) The protective effects of N-acetyl-l-cysteine against methyl mercury embryotoxicity in mice. Fund Appl Toxicol 20:437–445

    CAS  Article  Google Scholar 

  50. Palmisano F, Cardelicchio N, Zambonin PG (1995) Speciation of mercury in dolphin liver: a two step mechanism for the demethylation accumulation process and role of selenium. Marine Environ Res 40:109–143

    CAS  Article  Google Scholar 

  51. Parizek J, Ostadalova I (1967) The protective effect of small amounts of selenite in sublimate intoxication. Experientia 23:142–143

    CAS  Article  Google Scholar 

  52. Pellegrini D, Barghigiani C (1989) Mercury in the Mediterranean. Mar Pollut Bull 20:59–63

    Article  Google Scholar 

  53. Peterson SA, Ralston NV, Whanger PD, Oldfield JE, Mosher WD (2009) Selenium and mercury interactions with emphasis on fish tissue. Environ Bioind 4:318–334

    CAS  Article  Google Scholar 

  54. Pethybridge H, Cossa D, Butler ECV (2010) Mercury in 16 demersal sharks from southeast Australia: biotic and abiotic sources of variation and consumer health implications. Marine Environ Res 69:18–26

    CAS  Article  Google Scholar 

  55. Régine MB, Gilles D, Yannick D, Alain B (2006) Mercury distribution in fish organs and food regimes: significant relationships from twelve species collected in French Guiana (Amazon Basin). Sci Total Environ 368:262–270

    Article  Google Scholar 

  56. Riisgard HU, Hansen S (1990) Biomagnification of mercury in a marine grazing food-chain: algal cells Phaeodactylum tricornutum, mussel Mytilus edulis and flounders Platichthys flesus studied by means of a stepwise reduction-CVAAS method. Mar Ecol Prog Series 62:259–270

    Article  Google Scholar 

  57. Storelli MM, Giacominelli-Stuffler R, Marcotrigiano GO (2002) Total and methylmercury residues in cartilaginous fish from Mediterranean Sea. Mar Pollut Bull 44:1354–1358

    CAS  Article  Google Scholar 

  58. Storelli MM, Giacominelli-Stuffler RA, Storelli A, Marcotrigiano GO (2003) Total mercury and methylmercury content in edible fish from the Mediterranean Sea. J Food Protect 66:300–303

    CAS  Google Scholar 

  59. Storelli MM, Storelli A, Giacominelli-Stuffler R, Marcotrigiano GO (2005) Mercury speciation in the muscle of two commercially important fish, hake (Merluccius merluccius) and striped mullet (Mullus barbatus) from the Mediterranean Sea: estimated weekly intake. Food Chem 89:295–300

    CAS  Article  Google Scholar 

  60. Ščančar J, Zuliani T, Turk T, Milačič R (2007) Organotin compounds and selected metals in the marine environment of northern Adriatic Sea. Environ Monit Assess 127:271–282

    Article  Google Scholar 

  61. Trombini C, Fabbri D, Lombardo M, Vassura I, Zavoli E, Horvat M (2003) Mercury and methylmercury contamination in surficial sediments and clams of a coastal lagoon (Pialassa Baiona, Ravenna, Italy). Cont Shelf Res 23:1821–1831

    Article  Google Scholar 

  62. Turk V, Mozetič P, Malej A (2007) Overview of eutrophication-related events and other irregular episodes in Slovenian Sea (Gulf of Trieste, Adriatic Sea). Annales 17:197–215

    Google Scholar 

  63. Tušek-Žnidarič M, Falnoga I, Skreblin M, Turk V (2006) Induction of metallothionein-like proteins by mercury and distribution of mercury and selenium in the cells of hepatopancreas and gill tissues in mussel Mytilus galloprovincialis. Biol Trace Element Res 111:121–135

    Article  Google Scholar 

  64. Walker TI (1976) Effects of species, sex, length, and locality on mercury content at school shark Mustelus antarcticus Guenther from southeastern Australian waters. Austral J Mar Freshwat Res 27:603–608

    CAS  Article  Google Scholar 

  65. Watras CJ, Bloom NS (1992) Mercury and methylmercury in individual zooplankton: implications for bioaccumulation. Limnol Oceanogr 37:1313–1318

    Article  Google Scholar 

  66. Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury. In: Hoffman DJ, Rattner BA, Burton GA, Cairns J (eds) Handbook of ecotoxicology (Chapter 16), 2nd edn. CRC, Boca Raton, pp 409–463

  67. Zalups RK, Lash LH (1996) Alterations in renal cellular glutathione metabolism after in vivo administration of a subtoxic dose of mercuric chloride. J Biochem Toxicol 11:1–9

    Article  Google Scholar 

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Acknowledgments

The work was supported by the Slovenian Agency for Research through the programme P1-0143 and the project J1-2136. Partially, the 7 FP EU ArcRisk also supported the work. Linguistic corrections and editing by Dr. A.R. Byrne are also acknowledged.

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Horvat, M., Degenek, N., Lipej, L. et al. Trophic transfer and accumulation of mercury in ray species in coastal waters affected by historic mercury mining (Gulf of Trieste, northern Adriatic Sea). Environ Sci Pollut Res 21, 4163–4176 (2014). https://doi.org/10.1007/s11356-013-2262-0

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Keywords

  • Mercury
  • Methylmercury
  • Fish
  • Rays
  • Bioaccumulation
  • Northern Adriatic