Ocean Science Journal

, Volume 46, Issue 2, pp 85–94 | Cite as

Anthropogenic pollution stimulates oxidative stress in soft tissues of mussel Crenomytilus grayanus (Dunker1853)

  • Nina N. Belcheva
  • Maxim V. Zakhartsev
  • Nadezhda V. Dovzhenko
  • Avianna F. Zhukovskaya
  • Victor Ya. Kavun
  • Victor P. Chelomin


The digestive gland and gills of the mussel Crenomytilus grayanus extracted from three locations — (i) sampled from a clean and (ii) polluted site and (iii) transplanted from the nonpolluted to polluted site - were analysed for antioxidant enzymes (superoxide dismutase, catalase, glutathione reductase), total oxyradical scavenging capacity and levels of lipid peroxidation products (malondialdehyde, conjugated dienes and lipofuscin). Perturbation of redox status was found in both digestive gland and gill tissues of mussels living in the polluted area. As the activities of superoxide dismutase and catalase were 1.2–3 times higher, the total oxyradical scavenging capacity was lower by 20–35% and the levels of lipid peroxidation products were 2–7 times higher compared to mussels from the reference site. In transplanted mussels, the lipid peroxidation process in both tissues was significantly stimulated (the level of conjugated dienes was increased 1.7–2.5-fold; malondialdehyde and lipofuscin contents were increased 3.5–5-fold) and the total oxyradical scavenging capacity fell by 50–70%. In addition, the transplantation generally resulted in transient and variable responses of antioxidant enzymes for both tissues. Complex response-behaviour of the antioxidant enzymes strongly points to the necessity of employing a combined approach that takes into account activities of antioxidant enzymes and the total oxyradical scavenging capacity, as well as measurement of oxidative damage (e.g., lipid peroxidation) to evaluate the physiological health of molluscs.

Key words

antioxidant system oxidative stress heavy metal pollution molluscs 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Meth Enzymol 52:302–310CrossRefGoogle Scholar
  2. Chandran R, Sivakumar AA, Mohandass S, Aruchami M (2005) Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina fulica. Comp Biochem Physiol C 140:422–426Google Scholar
  3. Chelomin VP, Belcheva NN (1992) The effect of heavy metals on processes of lipid peroxidation in microsomal membranes from the hepatopancreas of bivalve mollusks Mizuhopecten yessoensis. Comp Biochem Physiol C 103:419–422CrossRefGoogle Scholar
  4. Chelomin VP, Zakhartsev MV, Kurilenko A, Belcheva NN (2005) An in vitro study of the effect of reactive oxygen species on subcellular distribution of deposited cadmium in digestive gland of mussel Crenomytilus grayanus. Aquat Toxicol 73:181–189CrossRefGoogle Scholar
  5. Company R, Serafim A, Bebiano MJ, Cosson R, Shillito B, Fiala-Medioni A (2004) Effect of cadmium and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 58:377–381CrossRefGoogle Scholar
  6. Cossu C, Doyotte A, Babut M, Exinger A, Vasseur P (2000) Antioxidant biomarkers in freshwater bivalves Unio tumidus in response to different contamination profiles of aquatic sediments. Ecotoxicol Environ Saf 45:106–121CrossRefGoogle Scholar
  7. De Almeida EA, Miyamot S, Bainy AC, de Medeiros MHG, Di Mascio P (2004) Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals. Mar Pollut Bull 49:386–392CrossRefGoogle Scholar
  8. Di Giulio RT, Washburn PC, Wenning RJ, Winston GW, Jewell CS (1989) Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environ Toxicol Chem 8:1103–1123CrossRefGoogle Scholar
  9. Dovzhenko NV, Kurilenko AV, Belcheva NN, Chelomin VP (2005) Cadmium-induced oxidative stress in the bivalve mollusk Modiolus modiolus. Russ J Mar Biol 31:309–313CrossRefGoogle Scholar
  10. Folch J, Lees M, Stanley J (1957) A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509Google Scholar
  11. Frenzilli G, Nigro M, Scarcelli V, Gorbi S, Regoli F (2001) DNA integrity and total oxyradical scavenging capacity in the Mediterranean mussel, Mytilus galloprovincialis: a field study in a highly eutrophicated coastal lagoon. Aquat Toxicol 53:19–32CrossRefGoogle Scholar
  12. George S (1982) Subcellular accumulation and detoxication of metals in aquatic animals. In: Vernberg WB, Calabrese A, Thurberg FP, Vernberg FJ (eds) Physiological Mechanisms of Marine Pollutant Toxicity, Academic Press, New York, pp 3–52Google Scholar
  13. Geret F, Serafim A, Barreira L, Bebianno MJ (2002) Response of antioxidant systems to copper in the gills of the clam Ruditapes decussatus. Mar Environ Res 54:413–417CrossRefGoogle Scholar
  14. Greenberg CS, Gaddock PR (1982) Rapid single-step membrane protein assay. Clin Chem 28:1725–1726Google Scholar
  15. Kavun V Ya, Shulkin VM (2005) Changes in the microelement composition in organs and tissues of the bivalve Crenomytilus grayanus acclimatized in a biotope with long-term heavy metal contamination. Russ J Mar Biol 31:109–114CrossRefGoogle Scholar
  16. Kovekovdova LT (1993) Tyazhelye metally v promyslovykh bespozvonochnykh zaliva Petra Velikogo v svyazi s usloviyami sushchestvovaniya (Heavy metals in fished invertebrates of Peter the Great Bay in connection with environment). Far Eastern Science Center, Vladivostok, pp 2–25 (In Russian)Google Scholar
  17. Livingston DP, Garcia-Martinez P, Winston GW (1989) Menadionstimulated oxyradical formation in digestive gland microsomes of the common mussel Mytilus edulis L. Aquat Toxicol 15:213–236CrossRefGoogle Scholar
  18. Livingston DP, Lips F, Martine PG, Pipe RK (1992) Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar Biol 112:265–276CrossRefGoogle Scholar
  19. Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666CrossRefGoogle Scholar
  20. Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev Med Vet-Toulouse 154:427–430Google Scholar
  21. Manduzio H, Monsinjon T, Rocher B, Leboulenger F, Galap C (2003) Characterization of an inducible isoform of the Cu/Zn superoxide dismutase in the blue mussel Mytilus edulis. Aquat Toxicol 64:73–83CrossRefGoogle Scholar
  22. Nasci C, Da Ros L, Campesan G, Van Vleet ES, Salizzato M, Sperni L, Pavoni B (1999) Clam transplantation and stressrelated biomarkers as useful tools for assessing water quality in coastal environments. Mar Pollut Bull 39:255–260CrossRefGoogle Scholar
  23. Olivier F, Ridd M, Klampp D (2002) The use of transplanted cultured tropical oysters (Saccosrea commercialis) to monitor Cd levels in North Queensland coastal waters (Australia). Mar Pollut Bull 44:1051–1062CrossRefGoogle Scholar
  24. Paoletti F, Aldinuccio D, Mocali A, Carparrini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase in tissue extracts. Anal Biochem 154:526–541CrossRefGoogle Scholar
  25. Perez E, Blasco J, Sole M (2004) Biomarker responses to pollution in two invertebrate species: Scrobicularia plana and Nereis diversicolor from the Cadiz bay (SW Spain). Mar Environ Res 58:275–279CrossRefGoogle Scholar
  26. Podgurskaya OV, Kavun V Ya (2005) Comparison of the subcellular distribution of heavy metals in organs of the bivalves Crenomytilus grayanus and Modiolus modiolus from a chronically polluted area. Russ J Mar Biol 31:435–442CrossRefGoogle Scholar
  27. Podorvanova NF, Ivashinnikova TS, Petrenko VS, Khomichuk LS (1989) Osnovnye cherty gidrokhimii zaligva Petra Velikogo, Yaponskoe more (The main hydrochemical features of Peter the Great Bay (the East Sea)). Far East Branch of the Russian Academy of Sciences, Vladivostok, pp 3–201 (In Russian)Google Scholar
  28. Regoli F (2000) Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. Aquat Toxicol 50:351–361CrossRefGoogle Scholar
  29. Regoli F, Gorbi S, Frenzilli G, Nigro M, Corsi I, Focardi S, Winston GW (2002) Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. Mar Environ Res 54:419–423CrossRefGoogle Scholar
  30. Regoli F, Hummel H, Amiard-Triquet C, Larroux C, Sukhotin A (1998a) Trace metals and variations of antioxidant enzymes in arctic bivalve populations. Arch Environ Contam Toxicol 35:594–601CrossRefGoogle Scholar
  31. Regoli F, Nigro M, Orlando E (1998b) Lysosomal and antioxidant responses to metals in the Antarctic scallop Adamussium colbecki. Aquat Toxicol 40:375–392CrossRefGoogle Scholar
  32. Regoli F, Principato G (1995) Glutathione, glutathione-depended and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquat Toxicol 31:143–164CrossRefGoogle Scholar
  33. Ribera D, Narbonne JF, Michel X, Livingstone DR, O’Hara X (1991) Responses of antioxidants and lipid peroxidation in mussels to oxidative damage exposure. Comp Biochem Physiol C 100:177–181CrossRefGoogle Scholar
  34. Romeo-Ruiz A, Amezcua O, Rodriguez-Ortega MJ, Munoz JL, Alhama J, Rodriguez-Ariza A, Gomez-Ariza JL, Lopez-Barea J (2002) Oxidative stress biomarkers in bivalves transplanted to the Guadalquivir estuary after Aznalcollar spill. Environ Toxicol Chem 22:92–100CrossRefGoogle Scholar
  35. Shen Y, Sangiah S (1995) Na+, K+-ATPase, glutathione, and hydroxyl free radicals in cadmium chloride-induced testicular toxicity in mice. Arch Environ Contam Toxicol 29:174–179CrossRefGoogle Scholar
  36. Shimasaki H, Hirai N, Ueta N (1988) Comparison of fluorescence characteristics of products of peroxidation of membrane phospholipids with those of products derived from reaction of malonaldehyde with glycine as a model of lipofuscin fluorescent substances. J Biochem 104:761–766Google Scholar
  37. Shulkin VM, Kavun V Ya, Presley BJ (2003) Metal concentrations in mussel Crenomytilus grayanus and Crassostrea gigas in relation to contamination of ambient sediments. Environ Int 29:493–502CrossRefGoogle Scholar
  38. Shulkin VM, Kavun V Ya, Tkalin AV, Presley B (2002) The influence of metal concentration in bottom sediments on metal accumulation by mytilids Crenomytilus grayanus and Modiolus kurilensis. Russ J Mar Biol 28:53–61CrossRefGoogle Scholar
  39. Simkiss K, Taylor M, Mason AZ (1982) Metal detoxification and bioaccumulation in molluscs. Mar Biol Lett 3:187–201Google Scholar
  40. Tkalin AV, Samsonov DP, Lishavkaya TS, Chernik GV (2000) New data on organochlorine distributions in the marine environment near Vladivostok. Mar Pollut Bull 40:879–881CrossRefGoogle Scholar
  41. Torres MA, Testa CP, Gaspari C, Masutti MB, Panitz CMN, Curi-Pedrosa R, De Almeida EA, Di Mascio P, Filho DW (2002) Oxidative stress in mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Mar Pollut Bull 44:923–932CrossRefGoogle Scholar
  42. Viarengo A (1989) Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. CRC Crit Rev Aquat Sci 1:295–317Google Scholar
  43. Viarengo A, Moore MN, Mancinelli G, Mazzucotelli A, Pipe RK, Farrar SV (1987) Metallothioneins and lysosomes in metal toxicity and accumulation in marine mussels: the effect of cadmium in the presence of phenanthrene. Mar Biol 94:251–257CrossRefGoogle Scholar
  44. Walker ST, Mantle D, Bythell JC, Thomason JC (2000) Oxidativestress: comparison of species specific and tissues specific effects in the marine bivalves Mytilus edulis (L.) and Dosinia lupinus (L.). Comp Biochem Physiol B 127:347–355CrossRefGoogle Scholar
  45. Wenning RJ, Di Giulio RT. Gallagher EP (1988) Oxidant-mediated biochemical effects of paraquat in the ribbed mussel, Geukensia demissa. Aquat Toxicol 12:157–170CrossRefGoogle Scholar
  46. Winston GW, Regoli F, Dugas AJ Jr, Fong JH, Blanchard KA (1998) A rapid gas chromatographic assay for determining oxyradical scavenging capacity of antioxidants and biological fluids. Free Rad Biol Med 24:480–493CrossRefGoogle Scholar

Copyright information

© Korea Ocean Research & Development Institute (KORDI) and the Korean Society of Oceanography (KSO) and Springer Netherlands 2011

Authors and Affiliations

  • Nina N. Belcheva
    • 1
  • Maxim V. Zakhartsev
    • 2
  • Nadezhda V. Dovzhenko
    • 1
  • Avianna F. Zhukovskaya
    • 1
  • Victor Ya. Kavun
    • 3
  • Victor P. Chelomin
    • 1
  1. 1.V.I. Il’ichev Pacific Oceanological Institute, Far Eastern BranchRussian Academy of SciencesVladivostokRussia
  2. 2.Institute of Pharmacy and Molecular Biotechnology (IPMB)University of HeidelbergHeidelbergGermany
  3. 3.A.V. Zhirmunsky Institute of Marine Biology, Far Eastern BranchRussian Academy of SciencesVladivostokRussia

Personalised recommendations