Antioxidant Defenses and Trace Metal Bioaccumulation Capacity of Cymbula nigra (Gastropoda: Patellidae)

  • G. A. Rivera-IngrahamEmail author
  • G. Malanga
  • S. Puntarulo
  • A. F. Pérez
  • A. Ruiz-Tabares
  • M. Maestre
  • R. González-Aranda
  • F. Espinosa
  • J. C. García-Gómez


The present study deals with the effect of trace metals on the endangered limpet Cymbula nigra. The Bay of Algeciras (Strait of Gibraltar) was used as the study site. Important industrial activity takes place in the area, including frequent oil spills. However, it is home to important populations of C. nigra. The objective of this work was to determine if these animals were being affected at a subcellular level by the pollutants present in their environment and to analyze the trace metal concentrations in the animal’s soft tissues. To determine the effects of water quality on the antioxidant activity and concentrations through field experimentation, a total of six sites were selected in Algeciras Bay, three located in the inner areas (environmentally degraded sites with higher levels of pollutants) and three in the outermost areas of the Bay. Stress associated to reactive oxygen species formation was assessed on digestive glands and gills as the enzymatic antioxidant activity of catalase (CAT), superoxide dismutase (SOD), and glutathione S-transferase (GST) and as the concentrations of lipid-soluble (α-tocopherol and β-carotene) and the water-soluble antioxidants (reduced and oxidized glutathione (GSH and GSSG)). Gills and digestive glands of those animals located in the inner areas of Algeciras Bay showed higher CAT activity values than those located in the outer areas. As a general pattern, we observed higher antioxidant activities and concentrations in digestive glands that in gills, suggesting the possibility that pollutants are mainly being incorporated by limpets through the food. As a general rule, larger animals showed greater concentrations of these compounds. Iron, zinc, and manganese, in this order, were present in the tissues at the highest concentrations. Chromium and manganese were found in significantly higher concentrations in those animals collected from the inner areas of the Bay. Through the present study, we provide the first data regarding the antioxidant defense levels and metal accumulation capacity of this species, and we reinforce the idea that this endangered species may be, in fact, relatively tolerant to degraded environments.


Cymbula Trace metals Limpet ROS Strait of Gibraltar Subcellular stress 



The authors would like to thank Jorge Francisco Marín Lora for his help in the sampling process. Thanks also go to an anonymous referee for his/her comments on the original manuscript and to the Servicio de Microanálisis del Centro de Investigación, Tecnología e Innovación de la Universidad de Sevilla staff for conducting the trace metal quantification. The study was funded by SP Funds from the University of Buenos Aires, from CONICET, and by the Spanish Ministry of Education through a grant awarded to G.A. Rivera-Ingraham (AP-2006-04220).


  1. Aebi, H. (1984). Catalase in vitro. Methods in Enzymology, 105, 121–126.CrossRefGoogle Scholar
  2. Alves de Almeida, E., Dias Bainy, A. C., Melo Loureiro, A. P., Martinez, G. R., Miyamoto, S., Onuki, J., et al. (2007). Oxidative stress in Perna perna and other bivalves as indicators of environmental stress in the Brazilian marine environment: antioxidants, lipid peroxidation and DNA damage. Comparative Biochemistry and Physiology, Part A, 146(4), 588–600.CrossRefGoogle Scholar
  3. Ansaldo, M., Najle, R., & Luquet, C. M. (2005). Oxidative stress generated by diesel seawater contamination in the digestive gland of the Antarctic limpet Nacella concinna. Marine Environmental Research, 59(4), 381–390.CrossRefGoogle Scholar
  4. Boening, D. W. (1999). An evaluation of bivalves as biomonitors of heavy metals pollution in marine waters. Environmental Monitoring and Assessment, 55, 459–470.CrossRefGoogle Scholar
  5. Boyden, C. R., & Zeldis, J. R. (1979). Preliminary observations using an attached microphonic sensor to study feeding behaviour of an intertidal limpet. Estuarine coastal and marine science, 9(6), 759–769.CrossRefGoogle Scholar
  6. Brown, R. J., Galloway, T. S., Lowe, D., Browne, M. A., Dissanayake, A., Jones, M. B., et al. (2004). Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquatic Toxicology, 66(3), 267–278.CrossRefGoogle Scholar
  7. Bryan, G. W. (1968). Concentrations of zinc and copper in the tissues of decapod crustaceans. Journal of the Marine Biological Association of the United Kingdom, 48, 303–321.CrossRefGoogle Scholar
  8. Bryan, G. W., Langston, W. J., Hummerstone, L. G., & Burt, G. R. (1985). A guide to the assessment of heavy-metal contamination using biological indicators. Plymouth: Occasional Publication of the Journal of the Marine Biological Association of the United Kingdom 4.Google Scholar
  9. Cadenas, E., & Sies, H. (1985). Oxidative stress: excited oxygen species and enzyme activity. Advances in Enzyme Regulation, 23, 217–237.CrossRefGoogle Scholar
  10. Cajaraville, M. P., Bebianno, M. J., Blasco, J., Porte, C., Sarasquete, C., & Viarengo, A. (2000). The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Science of the Total Environment, 247(2–3), 295–311.CrossRefGoogle Scholar
  11. Carballo, J. L., Naranjo, S. A., & García-Gómez, J. C. (1996). Use of marine sponges as stress indicators in marine ecosystems at Algeciras Bay (southern Iberian Peninsula). Marine Ecology Progress Series, 135, 109–122.CrossRefGoogle Scholar
  12. Casas, S., González, J. L., Andral, B., & Cossa, D. (2008). Relation between metal concentration in water and metal content of marine mussels (Mytilus galloprovincialis): impact of physiology. Environmental Toxicology and Chemistry, 27(7), 1543–1552.CrossRefGoogle Scholar
  13. Catsiki, V. A., Bei, F., & Nicolaidou, A. (1994). Size dependent metal concentrations in two marine gastropod species. Netherlands Journal of Aquatic Ecology, 28(2), 157–165.CrossRefGoogle Scholar
  14. Cavaletto, M., Ghezzi, A., Burlando, B., Evangelisti, V., Ceratto, N., & Viarengo, A. (2002). Effect of hydrogen peroxide on antioxidant enzymes and metallothionein level in the digestive glan of Mytilus galloprovincialis. Comparative Chemistry and Physiology C, 131(4), 447–455.Google Scholar
  15. Conradi, M., & López-González, P. J. (1999). The benthic gammaridea (Crustacea, Amphipoda) fauna of Algeciras Bay (Strait of Gibraltar): distributional ecology and some biogeographical considerations. Helgoland Marine Research, 53(1), 2–8.CrossRefGoogle Scholar
  16. Conradi, M., López-González, P. J., & García-Gómez, J. C. (1997). The amphipod community as a bioindicador in Algeciras Bay (Southern Iberian Peninsula) based on a spatio-temporal distribution. Marine Ecology, 18, 97–111.CrossRefGoogle Scholar
  17. Cravo, A., & Bebianno, M. J. (2005). Bioaccumulation of metals in the soft tissue of Patella aspera: application of metal/shell weight indices. Estuarine, Coastal and Shelf Science, 65(3), 571–586.CrossRefGoogle Scholar
  18. Della Santina, P., & Naylor, E. (1993). Endogenous rhythms in the homing behaviour of the limpet Patella vulgata Linnaeus. Journal of Molluscan Studies, 59, 87–91.Google Scholar
  19. Denton, G. R. W., & Burdon-Jones, C. (1981). Influence of temperature and salinity on the uptake, distribution and depuration of mercury, cadmium and lead by the black-lip oyster Saccostrea echinata. Marine Biology, 64, 317–326.Google Scholar
  20. Depledge, M. H., & Rainbow, P. S. (1990). Models of regulation and accumulation of trace metals in marine invertebrates. Comparative Biochemistry and Physiology, Part C, 97(1), 1–7.CrossRefGoogle Scholar
  21. Depledge, M. H., Weeks, J. M., & Bjerregaard, P. (1994). Heavy metals. In P. Calow (Ed.), Handbook of ecotoxicology (Vol. 2, pp. 79–105). Oxford: Blackwell.Google Scholar
  22. Desai, I. (1984). Vitamin E analysis methods for animal tissues. Methods in Enzymology, 105, 138–146.CrossRefGoogle Scholar
  23. Di Giulio, R. T., Washburn, P. C., Wenning, R. J., Winston, G. W., & Jewell, C. S. (1989). Biochemical responses in aquatic animal: a review of determinants of oxidative stress. Environmental Toxicology and Chemistry, 8(12), 1103–1123.CrossRefGoogle Scholar
  24. Douhri, H., & Sayah, F. (2009). The use of enzymatic biomarkers in two marine invertebrates Nereis diversicolor and Patella vulgata for the biomonitoring of Tangier’s bay (Morocco). Ecotoxicology and Environmental Safety, 72(2), 394–399.CrossRefGoogle Scholar
  25. Doyotte, A., Cossu, C., Jacquin, M., Babut, M., & Vasseur, P. (1997). Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or fiel exposure in the gills and the digestive glands of the freshwater bivalve Unio tumidis. Aquatic Toxicology, 39(2), 93–110.CrossRefGoogle Scholar
  26. Dwivedi, S., Tripathi, R. D., Rai, U. N., Srivastava, S., Mishra, S., Shukla, M. K., et al. (2006). Dominance of algae in ganga water polluter through fly-ash leaching: metal bioaccumulation potential of selected algal species. Bulletin of Environmental Contamination and Toxicology, 77, 427–436.CrossRefGoogle Scholar
  27. Eaton, D. L., & Bammler, T. K. (1999). Concise review of the glutathione S-transferases and their significance to toxicology. Toxicological Sciences, 49, 156–164.CrossRefGoogle Scholar
  28. Espinosa, F., Guerra-García, J. M., & García-Gómez, J. C. (2007). Sewage pollution and extinction risk: an endangered limpet as bioindicator? Biodiversity and Conservation, 16, 377–397.CrossRefGoogle Scholar
  29. Espinosa, F., Nakano, T., Guerra-García, J. M., & García-Gómez, J. C. (2011). Population genetic structure of the endangered limpet Cymbula nigra in a temperate Northern hemisphere region: influence of paleoclimatic events? Marine Ecology, 32(1), 1–5.CrossRefGoogle Scholar
  30. Farombi, E. O., Adelowo, O. A., & Ajimoko, Y. R. (2007). Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. International Journal of Environmental Research and Public Health, 4(2), 158–165.CrossRefGoogle Scholar
  31. Feldstein, T., Kashman, Y., Abelson, A., Fishelson, L., Mokady, O., Bresler, V., et al. (2003). Marine molluscs in environmental monitoring. III. Trace metals and organic pollutants in animal tissue and sediments. Helgoland Marine Research, 57, 212–219.CrossRefGoogle Scholar
  32. Fenton, H. J. H. (1894). Oxidation of tartaric acid in presence of iron. Journal of the Chemical Society, 65, 899–910.CrossRefGoogle Scholar
  33. Fernández, B., Campillo, J. A., Martínez-Gómez, C., & Benedicto, J. (2010). Antioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomarkers of environmental stress along the Spanish Mediterranean coast. Aquatic Toxicology, 99(2), 186–197.CrossRefGoogle Scholar
  34. Flohe, L., & Otting, F. (1984). Superoxide dismutase assays. Methods in Enzymology, 105, 93–104.CrossRefGoogle Scholar
  35. Frazier, J. M., George, S. S., Overnell, J., Coombs, T. L., & Kagi, J. (1985). Characterization of two molecular weight classes of cadmium binding proteins from the mussel, Mytilus edulis (L.). Comparative Biochemistry and Physiology, Part C, 80(2), 257–262.CrossRefGoogle Scholar
  36. Frenkiel, L. (1975). Contribution a l'étude des cycles de reproduction des Patellidae en Algérie. Pubblicacione de la Stazzione Zoologica di Napoli, 39, 153–189.Google Scholar
  37. Guerra-García, J. M., Maestre, M., González, A. R., & García-Gómez, J. C. (2006). Assessing a quick monitoring method using rocky intertidal communities as bioindicador: a multivariate approach in Algeciras Bay. Environmental Monitoring and Assessment, 116, 345–361.CrossRefGoogle Scholar
  38. Guerra-García, J. M., Ruiz-Tabares, A., Baeza-Rojano, E., Cabezas, M. P., Díaz-Pavón, J. J., Pacios, I., et al. (2010). Trace metals in Caprella (Crustacea: Amphipoda). A new tool for monitoring pollution in coastal areas? Biological Indicators, 10(3), 734–743.CrossRefGoogle Scholar
  39. Haber, F., & Weiss, J. (1932). Über die katalyse des hydroperoxydes. Naturwissenschaften, 20(51), 948–950.CrossRefGoogle Scholar
  40. Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130–7139.Google Scholar
  41. Hansen, J. A., Welsh, P. G., Lipton, J., & Suedkamp, M. J. (2002). The effects of long-term cadmium exposure on the growth and survival of juvenile bull trout (Salvelinus confluentus). Aquatic Toxicology, 58(3–4), 165–174. doi: 10.1016/S0166-445X(01)00233-8.CrossRefGoogle Scholar
  42. Harada, H., Kurauchi, M., Hayashi, R., & Eki, T. (2007). Shortened lifespan of nematode Caenorhabditis elegans after prolonged exposure to heavy metals and detergents. Ecotoxicology and Environmental Safety, 66(3), 378–383. doi: 10.1016/j.ecoenv.2006.02.017.CrossRefGoogle Scholar
  43. Hayashi, M., Ueda, T., Uyeno, K., Wada, K., Kinae, N., Saotome, K., et al. (1998). Development of genotoxicity assay systems that use aquatic organisms. Mutation Research / Fundamental and Molecular Mechanisms of Mutagenesis, 399, 125–133.CrossRefGoogle Scholar
  44. Hutcheson, M. S. (1974). The effect of temperature and salinity on cadmium uptake by the blue crab, Callinectes sapidus. Chesapeake Science, 15(4), 237–241.CrossRefGoogle Scholar
  45. Karr, J. R., & Dudley, D. R. (1981). Ecological perspective on water quality goals. Environmental Management, 5(1), 55–68.CrossRefGoogle Scholar
  46. Koufopanou, V., Reid, D. G., Ridgway, S. A., & Thomas, R. H. (1999). A molecular phylogeny of the patellid limpet (Gastropoda: Patellidae) and its implications for the origin of their antitropical distribution. Molecular Phylogenetics and Evolution, 11(1), 138–156.CrossRefGoogle Scholar
  47. Krantzberg, G. (1989). Metal accumulation by chironomid larvae: the effects of age and body weight on metal body burdens. Hydrobiologia, 188–189, 497–506.CrossRefGoogle Scholar
  48. Lance, E., Neffling, M. R., Gérard, C., Meriluoto, J., & Bormans, M. (2010). Accumulation of free and covalently bound microcystins in tissues of Lymnaea stagnalis (Gastropoda) following toxic cyanobacteria or dissolved microcystic-LR exposure. Environmental Pollution, 158(3), 674–680.CrossRefGoogle Scholar
  49. Langston, W. J., Bebianno, M. J., & Burt, G. R. (1998). Metal handling strategies in molluscs. In W. J. Langston & M. J. Bebianno (Eds.), Metal metabolism in aquatic environments (pp. 219–283). London: Chapman and Hall.Google Scholar
  50. Lares, M. L., & Orians, K. J. (1997). Natural Cd and Pb variations in Mytilus californianus during the upwelling season. Science of the Total Environment, 197(1–3), 177–195.CrossRefGoogle Scholar
  51. Leaver, M. J., & George, S. G. (1998). A piscine glutathione S-transferase which efficiently conjugates the end-products of lipid peroxidation. Marine Environmental Research, 46(1–5), 71–74. doi: 10.1016/S0141-1136(97)00071-8.CrossRefGoogle Scholar
  52. Lionetto, M. G., Caricato, R., Giordano, M. E., Pascariello, M. F., Marinosci, L., & Schettino, T. (2003). Integrated use of biomarkers (acetylcholinesterase and antioxidant enzymes activities) in Mytilus galloprovincialis and Mullus barbatus in an Italian coastal marine area. Marine Pollution Bulletin, 46(3), 324–330.CrossRefGoogle Scholar
  53. Livingstone, D. R. (2001). Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42(8), 656–666.CrossRefGoogle Scholar
  54. Livingstone, D. R., Förlin, L., & George, S. G. (1994). Molecular biomarkers and toxic consequences of impacts by organic pollution in aquatic organisms. In D. W. Sutcliffe (Ed.), Water quality and stress indicators in marine and freshwater systems: linking levels of organization (pp. 154–171). Ambleside, United Kingdom: Freshwater Biological Association.Google Scholar
  55. Lowry, O. M., Rosenbrough, N. J., Farr, O. L., & Randall, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193, 265–275.Google Scholar
  56. Malanga, G., Estevez, M. S., Calvo, J., Abele, D., & Puntarulo, S. (2007). The effect of seasonality on oxidative metabolism in Nacella (Patinigera) magellanica. Comparative Biochemistry and Physiology, Part A, 146(4), 551–558.CrossRefGoogle Scholar
  57. Manna, G. K., & Sadhukhan, A. (1986). Use of cells of gill and kidney of tilapia fish in micronucleus test (MNT). Current Science, 55, 498–501.Google Scholar
  58. McCord, J. M., & Fridovich, I. (1969). Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry, 244, 6049–6055.Google Scholar
  59. Miller, E. R., III, & Pondick, J. S. (1984). Heavy metal levels in Nucella lapillus (Gastropoda: Prosobranchia) from sites with normal and penis-bearing females from New England. Bulletin of Environmental Contamination and Toxicology, 33, 612–620.CrossRefGoogle Scholar
  60. Morales-Caselles, C., Kalman, J., Riba, I., & Del Valls, T. A. (2007). Comparing sediment quality in Spanish littoral areas affected by acute (Prestige, 2002) and chronic (Bay of Algeciras) oil spills. Environmental Pollution, 146(1), 233–240.CrossRefGoogle Scholar
  61. Morillo, J., & Usero, J. (2008). Trace metal bioavailability in the waters of two different habitats in Spain: Huelva estuary and Algeciras Bay. Ecotoxicology and Environmental Safety, 71(3), 851–859.CrossRefGoogle Scholar
  62. Nakhlé, K. F., Cossa, D., Khalaf, G., & Beliaeff, B. (2006). Brachidontes variabilis and Patella sp. as quantitative biological indicators for cadmium, lead and mercury in the Lebanese coastal waters. Environmental Pollution, 142(1), 73–82.CrossRefGoogle Scholar
  63. Navrot, J., Amiel, A. J., & Kronfeld, J. (1974). Patella vulgata: a biological monitor of coastal metal pollution—a preliminary study. Environmental Pollution, 7(4), 303–308.CrossRefGoogle Scholar
  64. Nias, D. J., McKillup, S. C., & Edyvane, K. S. (1993). Imposex in Lepsiella vinosa from Southern Australia. Marine Pollution Bulletin, 26(7), 380–384. doi: 10.1016/0025-326X(93)90185-M.CrossRefGoogle Scholar
  65. Niyogi, S., Biswas, S., Sarker, S., & Datta, A. G. (2001). Antioxidant enzymes in brackishwater oyster, Saccostrea cucullata as potential biomarkers of polyaromatic hydrocarbon pollution in Hooghly Estuary (India): seasonality and its consequences. The Science of the Total Environment, 281, 237–246.CrossRefGoogle Scholar
  66. Orren, M. J., Eagle, G. A., Hennig, H. F.-K. O., & Green, A. (1980). Variations in trace metal content of the mussel Choromytilus meridionalis (Kr.) with season and sex. Marine Pollution Bulletin, 11(9), 253–257.CrossRefGoogle Scholar
  67. Peterson, R. C. J. (1986). Population and guild analysis for interpretation of heavy metal pollution in streams. In J. Cairns Jr. (Ed.), Community Toxicity Testing (Special Technical Publications, Vol. 920, pp. 180–198). Philadelphia: American Society for Testing and Materials.CrossRefGoogle Scholar
  68. Phillips, D. J. H. (1976). The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead and copper. I. Effects of environmental variables on uptake of metals. Marine Biology, 38, 59–69.CrossRefGoogle Scholar
  69. Phillips, D. J. H. (1977). The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environments—a review. Environmental Pollution, 13(4), 281–317.CrossRefGoogle Scholar
  70. Rainbow, P. S. (1997). Trace metal accumulation in marine invertebrates: marine biology or marine chemistry? Journal of the Marine Biological Association of the United Kingdom, 77(1), 195–210.CrossRefGoogle Scholar
  71. Regoli, F., & Principato, G. (1995). Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquatic Toxicology, 31(2), 143–164. doi: 10.1016/0166-445X(94)00064-W.CrossRefGoogle Scholar
  72. Regoli, F., Gorbi, S., Frenzilli, G., Nigro, M., Corsi, I., Focardi, S., et al. (2002). Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. Marine Environmental Research, 54(3–5), 419–423.CrossRefGoogle Scholar
  73. Regoli, F., Nigro, M., Chiantore, M., & Winston, G. W. (2002). Seasonal variations of susceptibility to oxidative stress in Adamussium colbecki, a key bioindicator species for the Antarctic marine environment. The Science of the Total Environment, 289(1–3), 205–211.CrossRefGoogle Scholar
  74. Renault, L., & Moueza, M. (1971). Contribution à l'étude de Patella safiana Lamarck. Haliotis, 1, 19–20.Google Scholar
  75. Ridgway, S. A., Reid, D. G., Taylor, J. D., Branch, G. M., & Hodgson, A. N. (1998). A cladistic phylogeny of the family Patellidae (Mollusca: Gastropoda). Philosophical Transactions of the Royal Society B: biological sciences, 353, 1645–1671.CrossRefGoogle Scholar
  76. Rivera-Ingraham, G. A. (2010). Biología de la conservación de especies de patélidos en el umbral Atlántico-Mediterráneo. Sevilla, Spain: Tesis Doctoral. Universidad de Sevilla.Google Scholar
  77. Rivera-Ingraham, G. A., Espinosa, F., & García-Gómez, J. C. (2011). Ecological considerations and niche differentiation between juvenile and adult black limpets (Cymbula nigra). Journal of the Marine Biological Association of the United Kingdom, 91(1), 191–198.CrossRefGoogle Scholar
  78. Rodríguez-Ariza, A., Toribio, F., & López-Barea, J. (1994). Rapid determination of glutathione status in fish liver using high-performance liquid chromotography and electrochemical detection. Journal of Chromatography B: Biomedical Sciences and Applications, 656(2), 311–318.CrossRefGoogle Scholar
  79. Sánchez-Moyano, E. (1996). Variación espacio-temporal en la composición de las comunidades animales asociadas a macroalgas como respuestas a cambios en el medio. Implicaciones en la caracterización ambiental de las áreas costeras. Sevilla, Spain: University of Sevilla.Google Scholar
  80. Sá-Pinto, A., Branco, M., Harris, D. J., & Alexandrino, P. (2005). Phylogeny and phylogeography of the genus Patella based on mitocondrial DNA sequence data. Journal of Experimental Marine Biology and Ecology, 325(1), 95–110.CrossRefGoogle Scholar
  81. Sies, H. (1991). Oxidative stress: from basic research to clinical application. The American Journal of Medicine, 91(3), S31–S38.CrossRefGoogle Scholar
  82. Stegeman, J. J., Brouwner, M., Giulio, R. T. D., Förlin, L., Fowler, B. A., Sanders, B. M., et al. (1992). Molecular responses to environmental contamination: enzyme and protein systems as indicators of chemical exposure and effect. In R. J. Huggett, R. A. Kimerle, P. M. Mehrle Jr., & H. L. Bergman (Eds.), Biomarkers, biochemical, physiological, and histological markers of anthropogenic stress (pp. 253–336). United States of America: Lewis Publishers.Google Scholar
  83. Valavanidis, A., Vlahogianni, T., Dassenakis, M., & Scoullos, M. (2006). Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety, 64(2), 178–189.CrossRefGoogle Scholar
  84. Vasconcelos, V. M. (1995). Uptake and depuration of the heptapeptide toxin microcystin-LR in Mytilus galloprovincialis. Aquatic Toxicology, 32(2–3), 227–237.CrossRefGoogle Scholar
  85. Vasconcelos, V. M., Oliveira, S., & Teles, F. O. (2001). Impact of a toxic and a non-toxic strain of Microcystis aeruginosa on the crayfish Procambarus clarkia. Toxicon, 39, 1461–1470.CrossRefGoogle Scholar
  86. Viarengo, A. (1989). Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. CRC Review of Aquatic Sciences, 1, 295–317.Google Scholar
  87. Vlahogianni, T., Dassenakis, M., Scoullos, M. J., & Valavanidis, A. (2007). Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from Saronikos Gulf of Greece. Marine Pollution Bulletin, 54(9), 1361–1371.CrossRefGoogle Scholar
  88. Vosyliene, M. Z., Kazlauskiene, N., & Svecevičius, G. (2003). Effect of a heavy metal model mixture on biological parameters of rainbow trout Oncorhynchus mykiss. Environmental Science and Pollution Research, 10(2), 103–107.CrossRefGoogle Scholar
  89. Weihe, E., Kriews, M., & Abele, D. (2010). Differences in heavy metal concentrations and in the response of the antioxidant system to hypoxia and air exposure in the Antarctic limpet Nacella concinna. Marine Environmental Research, 69(3), 127–135.CrossRefGoogle Scholar
  90. Winston, G. W., & Di Giulio, R. T. (1991). Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology, 19(2), 137–161.CrossRefGoogle Scholar
  91. Yoshinaga, M., Ueki, T., & Michibata, H. (2007). Metal binding ability of glutathione transferases conserved between two animal species, the vanadium-rich ascidian Ascidia sydneiensis and the schistosome Schistosoma japonicum. Biochimica et biophysica acta, 1770(9), 1413–1418.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • G. A. Rivera-Ingraham
    • 1
    • 2
    Email author
  • G. Malanga
    • 3
  • S. Puntarulo
    • 3
  • A. F. Pérez
    • 4
  • A. Ruiz-Tabares
    • 1
  • M. Maestre
    • 1
  • R. González-Aranda
    • 1
  • F. Espinosa
    • 1
  • J. C. García-Gómez
    • 1
  1. 1.Laboratorio de Biología Marina, Departamento de Fisiología y ZoologíaUniversidad de SevillaSevillaSpain
  2. 2.Functional EcologyAlfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany
  3. 3.Fisicoquímica-IBIMOL Facultad de Farmacia y BioquímicaUniversidad de Buenos AiresBuenos AiresArgentina
  4. 4.Laboratorio de Ecología de Bentos Marino, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations