Skip to main content

Heavy metal bioaccumulation and metallothionein content in tissues of the sea bream Sparus aurata from three different fish farming systems

Abstract

The distribution and potential bioaccumulation of dietary and waterborne cadmium and lead in tissues of sea bream (Sparus aurata), a major aquaculture species, was studied in relation to three different fish farming systems. Metallothionein levels in fish tissues were also evaluated. Results demonstrate that metal concentrations in various tissues significantly vary among fish culture systems. Different tissues show different capacity for accumulating heavy metals. The content of both cadmium and lead is not strictly correlated with that of metallothionein. Indeed, the marked accumulation of both metals in liver, as well as the high lead content found in gills and kidney, are not accompanied by a concomitant accumulation of metallothioneins in these tissues. No correlation is present between heavy metals and metallothionein content in muscle tissue. The results also demonstrate that cadmium accumulates mainly via dietary food, whereas lead accumulation is not of food origin. Noteworthy is that the concentration of the two metals found in muscle in all instances is lower than the limits established by European Union legislation for fish destined for human consumption.

This is a preview of subscription content, access via your institution.

References

  1. Alasalvar, C., Taylor, K. D., & Shahidi, F. (2002). Comparative quality assessment of cultured and wild sea bream (Sparus aurata) stored in ice. Journal of Agricultural and Food Chemistry, 50(7), 2039–2045. doi:10.1021/jf010769a.

    Article  CAS  Google Scholar 

  2. Alvarado, N. E., Quesada, I., Hylland, K., Marigómez, I., & Soto, M. (2006). Quantitative changes in metallothionein expression in target cell-types in the gills of turbot (Scophthalmus maximus) exposed to Cd, Cu, Zn and after a depuration treatment. Aquatic Toxicology (Amsterdam, Netherlands), 77(1), 64–77. doi:10.1016/j.aquatox.2005.10.017.

    CAS  Google Scholar 

  3. Amérand, A., Vettier, A., Sébert, P., & Moisan, C. (2006). A comparative study of reactive oxygen species in red muscle: Pressure effects. Undersea & Hyperbaric Medicine, 33(3), 161–167.

    Google Scholar 

  4. Atif, F., Kaur, M., Ansari, R. A., & Raisuddin, S. (2008). Channa punctata brain metallothionein is a potent scavenger of superoxide radicals and prevents hydroxyl radical-induced in vitro DNA damage. Journal of Biochemical and Molecular Toxicology, 22(3), 202–208. doi:10.1002/jbt.20230.

    Article  CAS  Google Scholar 

  5. Bardach, J. E., Ryther, J. H., & Mc Larney, W. O. (1972). Aquaculture: The farming and husbandry of freshwater and marine organisms. In Culture of the common carp and culture of the Chinese carp (pp. 29–120). New York: Wiley.

    Google Scholar 

  6. Berntssen, M. H., Aspholm, O. O., Hylland, K., Wendelaar Bonga, S. E., & Lundebye, A. K. (2001). Tissue metallothionein, apoptosis and cell proliferation responses in Atlantic salmon (Salmo salar L.) parr fed elevated dietary cadmium. Comparative Biochemistry and Physiology C Toxicology and Pharmacology, 128(3), 299–310.

    Article  CAS  Google Scholar 

  7. Bondou, A., & Ribeire, F. (1989). Fish as “biological model” for experimental study in ecotoxicology. In A. Bondou & F. Ribeire (Eds.), Aquatic ecotoxicology. Fundamental concepts and methodologies (pp. 127–162). Boca Raton: CRC.

    Google Scholar 

  8. Canli, M., & Atli, G. (2003). The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environmental Pollution, 121(1), 129–136. doi:10.1016/S0269-7491(02)00194-X.

    Article  CAS  Google Scholar 

  9. Carginale, V., Scudiero, R., Capasso, C., Capasso, A., Kille, P., di Prisco, G., et al. (1998). Cadmium-induced differential accumulation of metallothionein isoforms in the Antarctic icefish, which exhibits no basal metallothionein protein but high endogenous mRNA levels. The Biochemical Journal, 332(2), 475–481.

    CAS  Google Scholar 

  10. Chesman, B. S., O’hara, S., Burt, G. R., & Langston, W. J. (2007). Hepatic metallothionein and total oxyradical scavenging capacity in Atlantic cod Gadus morhua caged in open sea contamination gradients. Aquatic Toxicology (Amsterdam, Netherlands), 84(3), 310–320. doi:10.1016/j.aquatox.2007.06.008.

    CAS  Google Scholar 

  11. Chowdhury, M. J., Baldisserotto, B., & Wood, C. M. (2005). Tissue-specific cadmium and metallothionein levels in rainbow trout chronically acclimated to waterborne or dietary cadmium. Archives of Environmental Contamination and Toxicology, 48, 381–390. doi:10.1007/s00244-004-0068-2.

    Article  CAS  Google Scholar 

  12. Ciardullo, S., Aureli, F., Coni, E., Guandalini, E., Iosi, F., Raggi, A., et al. (2008). Bioaccumulation potential of dietary arsenic, cadmium, lead, mercury, and selenium in organs and tissues of rainbow trout (Oncorhyncus mykiss) as a function of fish growth. Journal of Agricultural and Food Chemistry, 56(7), 2442–2451. doi:10.1021/jf703572t.

    Article  CAS  Google Scholar 

  13. Conte, F. S. (2004). Stress and welfare of cultured fish. Applied Animal Behaviour Science, 86, 205–233.

    Google Scholar 

  14. Coyle, P., Philcox, J. C., Carey, L. C., & Rofe, A. M. (2002). Metallothionein: The multipurpose protein. Cellular and Molecular Life Sciences, 59(4), 627–647. doi:10.1007/s00018-002-8454-2.

    Article  CAS  Google Scholar 

  15. Eastwood, S., & Couture, P. (2002). Seasonal variations in condition and heavy metals concentration of yellow perch (Perca flavescens) from a metal contaminated environment. Aquatic Toxicology (Amsterdam, Netherlands), 58, 43–56. doi:10.1016/S0166-445X(01)00218-1.

    CAS  Google Scholar 

  16. Ellman, G. L. (1958). A colorimetric method for determining low concentrations of mercaptans. Archives of Biochemistry and Biophysics, 74(2), 443–450. doi:10.1016/0003-9861(58)90014-6.

    Article  CAS  Google Scholar 

  17. Eroglu, K., Atli, G., & Canli, M. (2005). Effects of metal (Cd, Cu, Zn) interactions on the profiles of metallothionein-like proteins in the Nile fish Oreochromis niloticus. Bulletin of Environmental Contamination and Toxicology, 75(2), 390–399. doi:10.1007/s00128-005-0766-0.

    Article  CAS  Google Scholar 

  18. Fernandes, D., Bebianno, M. J., & Porte, C. (2008). Hepatic levels of metal and metallothioneins in two commercial fish species of the Northern Iberian shelf. The Science of the Total Environment, 391(1), 159–167. doi:10.1016/j.scitotenv.2007.10.057.

    Article  CAS  Google Scholar 

  19. Filipovic, V. M., & Biserka, R. (2007). Metal exposure assessment in native fish, Mullus barbatus L., from the Eastern Adriatic Sea. Toxicology Letters, 168, 292–301. doi:10.1016/j.toxlet.2006.10.026.

    Article  Google Scholar 

  20. George, S. G., & Olssen, P.-E. (1994). Metallothioneins as indicators of trace metal pollution. In K. J. M. Kramer (Ed.), Biological monitoring of coastal waters and estuaries (pp. 151–178). Boca Raton: CRC.

    Google Scholar 

  21. Ghoshal, K., & Jacob, S. T. (2001). Regulation of metallothionein gene expression. Progress in Nucleic Acid Research and Molecular Biology, 66, 357–384. doi:10.1016/S0079-6603(00)66034-8.

    Article  CAS  Google Scholar 

  22. Goyer, R. A. (1996). Toxic effects of metals. In C. D. Klaassen (Ed.), Casarett and Doull’s toxicology (5th ed., pp. 691–736). New York: McGraw-Hill.

    Google Scholar 

  23. Harrison, S. E., & Klaverkamp, J. F. (1989). Uptake, elimination and tissue distribution of dietary and aqueous cadmium by rainbow trout (Salmo gairdneri Richardson) and lake whitefish (Coregonus clupeaformis Mithill). Environmental Toxicology and Chemistry, 8, 87–97. doi:10.1897/1552-8618(1989)8[87:UEATDO]2.0.CO;2.

    CAS  Google Scholar 

  24. Ikebuchi, H., Teshima, R., Suzuki, K., Terao, T., & Yamane, Y. (1986). Simultaneous induction of Pb-metallothionein-like protein and Zn-thionein in the liver of rats given lead acetate. The Biochemical Journal, 233, 541–546.

    CAS  Google Scholar 

  25. Langston, W. J. (1990). Toxic effects of metals and the incidence of metal pollution in marine ecosystems. In R. W. Furness, & P. S. Rainbow (Eds.), Heavy metals in the marine environment (pp. 101–122). Boca Raton: CRC.

    Google Scholar 

  26. Langston, W. J., Chesman, B. S., Burt, G. R., Pope, N. D., & McEvoy, J. (2002). Metallothionein in liver of eels Anguilla anguilla from the Thames Estuary: An indicator of environmental quality? Marine Environmental Research, 53(3), 263–293. doi:10.1016/S0141-1136(01)00113-1.

    Article  CAS  Google Scholar 

  27. Linde, A. R., Sanchez-Galan, S., & Garcia-Vazquez, E. (2004). Heavy metal contamination of European eel (Anguilla anguilla) and brown trout (Salmo trutta) caught in wild ecosystems in Spain. Journal of Food Protection, 467(10), 2332–2336.

    Google Scholar 

  28. Loganathan, P., Hedley, M. J., & Grace, N. D. (2008). Pasture soils contaminated with fertilizer-derived cadmium and fluorine: Livestock effects. Reviews of Environmental Contamination and Toxicology, 192, 29–66. doi:10.1007/978-0-387-71724-1_2.

    Article  CAS  Google Scholar 

  29. Mariottini, M., Corsi, I., & Focardi, S. (2006). PCB levels in European eel (Anguilla anguilla) from two coastal lagoons of the Mediterranean. Environmental Monitoring and Assessment, 117(1–3), 519–528. doi:10.1007/s10661-006-2767-9.

    Article  CAS  Google Scholar 

  30. McKee, M. J., Kromrey, G. B., May, T. W., & Orazio, C. E. (2008). Contaminant levels in rainbow trout, Oncorhynchus mykiss, and their diets from Missouri coldwater hatcheries. Bulletin of Environmental Contamination and Toxicology, 80, 450–454. doi:10.1007/s00128-008-9374-0.

    Article  CAS  Google Scholar 

  31. Minghetti, M., Leaver, M. J., Carpenè, E., George, S. G. (2008). Copper transporter 1, metallothionein and glutathione reductase genes are differentially expressed in tissues of sea bream (Sparus aurata) after exposure to dietary or waterborne copper. Comparative Biochemistry and Physiology C Toxicology and Pharmacology, 147(4), 450–459.

    Article  CAS  Google Scholar 

  32. Moltedo, O., Verde, C., Capasso, A., Parisi, E., Remondelli, P., Bonatti, S., et al. (2000). Zinc transport and metallothionein secretion in the intestinal human cell line Caco-2. The Journal of Biological Chemistry, 275, 31819–31825. doi:10.1074/jbc.M002907200.

    Article  CAS  Google Scholar 

  33. Nesto, N., Romano, S., Moschino, V., Mauri, M., & Da Ros, L. (2007). Bioaccumulation and biomarker responses of trace metals and micro-organic pollutants in mussels and fish from the Lagoon of Venice, Italy. Marine Pollution Bulletin, 55(10–12), 469–484. doi:10.1016/j.marpolbul.2007.09.009.

    Article  CAS  Google Scholar 

  34. Riggio, M., Trinchella, F., Filosa, S., Parisi, E., & Scudiero, R. (2003a). Accumulation of zinc, copper, and metallothionein mRNA in lizard ovary proceeds without a concomitant increase in metallothionein content. Molecular Reproduction and Development, 66(4), 374–382. doi:10.1002/mrd.10365.

    Article  CAS  Google Scholar 

  35. Riggio, M., Filosa, S., Parisi, E., & Scudiero, R. (2003b). Changes in zinc, copper and metallothionein contents during oocyte growth and early development of the teleost Danio rerio (zebrafish). Comparative Biochemistry and Physiology C Toxicology and Pharmacology, 135(2), 191–196.

    Article  Google Scholar 

  36. Rojas, E., Herrera, L. A., Poirier, L. A., & Ostrosky-Wegman, P. (1999). Are metals dietary carcinogens? Mutation Research, 443(1–2), 157–181.

    CAS  Google Scholar 

  37. Sarkar, A., Ray, D., Shrivastava, A. N., & Sarker, S. (2006). Molecular biomarkers: Their significance and application in marine pollution monitoring. Ecotoxicology (London, England), 15(4), 333–340. doi:10.1007/s10646-006-0069-1.

    CAS  Google Scholar 

  38. Serrano, R., Barreda, M., & Blanes, M. A. (2008). Investigating the presence of organochlorine pesticides and polychlorinated biphenyls in wild and farmed gilthead sea bream (Sparus aurata) from the Western Mediterranean sea. Marine Pollution Bulletin, 56(5), 963–972. doi:10.1016/j.marpolbul.2008.01.014.

    Article  CAS  Google Scholar 

  39. Trinchella, F., Riggio, M., Filosa, S., Volpe, M. G., Parisi, E., & Scudiero, R. (2006). Cadmium distribution and metallothionein expression in lizard tissues following acute and chronic cadmium intoxication. Comparative Biochemistry and Physiology C Toxicology and Pharmacology, 144(3), 272–278.

    Article  Google Scholar 

  40. Ureña, R., Peri, S., del Ramo, J., & Torreblanca, A. (2007). Metal and metallothionein content in tissues from wild and farmed Anguilla anguilla at commercial size. Environment International, 33, 532–539. doi:10.1016/j.envint.2006.10.007.

    Article  Google Scholar 

  41. Usero, J., Izquierdo, C., Morillo, J., & Gracia, I. (2004). Heavy metals in fish (Solea vulgaris, Anguilla anguilla and Liza aurata) from salt marshes on the southern Atlantic coast of Spain. Environment International, 29(7), 949–956. doi:10.1016/S0160-4120(03)00061-8.

    Article  CAS  Google Scholar 

  42. Viarengo, A., Ponzano, E., Dondero, F., & Fabbri, R. (1997). A simple spectrophotometric method for metallothionein evaluation in marine organisms: An application to Mediterranean and Antarctic molluscs. Marine Environmental Research, 44, 69–84. doi:10.1016/S0141-1136(96)00103-1.

    Article  CAS  Google Scholar 

  43. Ysart, G., Miller, P., Croasdale, M., Crews, H., Robb, P., Baxter, M., et al. (2000). 1997 UK Total Diet Study—Dietary exposures to aluminium, arsenic, cadmium, chromium, copper, lead, mercury, nickel, selenium, tin and zinc. Food Additives and Contaminants, 17(9), 775–786. doi:10.1080/026520300415327.

    Article  CAS  Google Scholar 

  44. Yudkovski, Y., Rogowska-Wrzesinska, A., Yankelevich, I., Shefer, E., Herut, B., & Tom, M. (2008). Quantitative immunochemical evaluation of fish metallothionein upon exposure to cadmium. Marine Environmental Research, 65(5), 427–436. doi:10.1016/j.marenvres.2008.02.001.

    Article  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rosaria Scudiero.

Additional information

This work is devoted to Dr. Elio Parisi, the Only Teacher and Second Father to us. Unforgettable.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cretì, P., Trinchella, F. & Scudiero, R. Heavy metal bioaccumulation and metallothionein content in tissues of the sea bream Sparus aurata from three different fish farming systems. Environ Monit Assess 165, 321–329 (2010). https://doi.org/10.1007/s10661-009-0948-z

Download citation

Keywords

  • Cadmium
  • Lead
  • Tissue distribution
  • Metallothionein
  • Aquaculture
  • Sea bream