Bioaccumulation and Toxicity of Dissolved Heavy Metals from the Guadalquivir Estuary After the Aznalcóllar Mining Spill Using Ruditapes philippinarum

  • M. Laura Martín-Díaz
  • Julián Blasco
  • Marisa González de  Canales
  • Diego Sales
  • T. Ángel DelValls


The shore clam Ruditapes philippinarum was used as a biomonitoring organism to measure the potential impact that the mining spill in the Guadalquivir Estuary (SW, Spain) in 1998 may have exerted on local biota. Individuals were exposed to dissolved cadmium, copper, and zinc at concentrations found in local waters after the spill (3 μg · L−1 Cd, 15 μg · L−1 Cu, 700 μg · L−1 Zn) at two salinity values: 10 and 35. Residues of metals were measured in gill and digestive gland, together with metallothioneins in the digestive gland and histopathological lesions in gill, digestive gland, and gonad tissues over time. Heavy metals Zn and Cd associated with the mining spill, were bioaccumulated in clam tissues, associated with the activation of metallothioneins, and related to the histopathological lesions measured at all the clam tissues. The heavy metal Cu not related to the spill was not directly associated with effects measured. The bioaccumulation and adverse effects associated with Cd and Zn were significantly higher at low salinity (10) than at high salinity (35) values.


  1. Amiard, JC, Pineau, A, Boiteau, HL, Metayer, C, Amiard-Triquet, C 1987Application of atomic absorption spectrophotometry using Zeeman effect, to the determination of eight elements (Ag, Cd, Cr, Cu, Mn, Ni, Pb and Se) in biological materialsWater Res21663697Google Scholar
  2. Amiard, JC, Métayer, C, Baud, JP, Ribeyre, F 1991Influence de divers facteurs écologiques sur la bioaccumulation d’élements métaliques (Cd, Cu, Pb, Zn) chez de jeunes palourdes (Ruditapes philippinarum) au cours du prégrossissement en nourricerieRev Sciences l’eau4441452Google Scholar
  3. Blasco, J, Arias, AM, Sáenz, V 1999Heavy metals in organisms of the River Guadalquivir estuary: possible incidence of the Aznalcóllar disasterSci Total Environ242249259Google Scholar
  4. Bradford, MB 1976A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye bindingAnal Biochem72248254CrossRefPubMedGoogle Scholar
  5. Chong, K, Wang, W-X 2000Comparative studies on the biokinetics of Cd, Cr, and Zn in the green mussel Perna viridis and the Manila clam Ruditapes philippinarumEnviron Pollut115107121Google Scholar
  6. Clark, SL, Teh, SL, Hinton, DE 2000Tissue and cellular alterations in Asian clam (Potamocorbula amurensis) from San Francisco Bay: toxicological indicators of exposure and effect?Mar Environ Res50301305Google Scholar
  7. Cobelo-García, A, Prego, R, Nieto, O 2003Chemical speciation of dissolved lead in polluted environments. A case of study: the Pontevedra Ria (NW Spain)Cienc Mar29377388Google Scholar
  8. Comreys, AL 1973A first course in factor analysisAcademic PressNew YorkGoogle Scholar
  9. Cossa, D, Bourget, E, Piuze, J 1979Sexual maturation as a source of variation in the relationship between cadmium concentration and the body weight of the Mytilus edulisMar Pollut Bull10174178Google Scholar
  10. DelValls, TA, Blasco, J, Sarasquete, MC, Forja, JM, Gómez-Parra, A 1998Evaluation of heavy metal sediment toxicity in littoral ecosystems using juveniles of the fish Saprus aurataEcotox Environ Saf41157167Google Scholar
  11. DelValls, TA, Chapman, PM 1998Site-specific sediment quality values for the Gulf of Cádiz (Spain) and San Francisco Bay (USA), using the sediment quality triad and multivariate analysisCienc Mar243313336Google Scholar
  12. Engel, DW 1987Metal regulation and moulting in the blue crab, Callinectes sapidus: copper, zinc, and metallothioneinBiol Bull1726982Google Scholar
  13. Frane, J, Jenrich, R, Sampson, P 1985

    Factor Analysis

    Dixon, WJ eds. BMDP Statistical SoftwareUniversity of California PressBerkeley, California480500
    Google Scholar
  14. García-Luque, E, Sáenz, I, Riba, I, DelValls, TA, Forja, JM, Gómez-Parra, A 2003Heavy metals at the Guadalquivir estuaryCienc Mar29447456Google Scholar
  15. Gómez-Parra, A, Forja, JM, DelValls, TA, Sáenz, I, Riba, I 2000Early contamination by heavy metals of the Guadalquivir Estuary after Aznalcóllar mining spill (SW Spain)Mar Pollut Bull40121115–1123Google Scholar
  16. Gutierrez, M 1967Coloración histológica para ovarios de peces, crustáceos y moluscosInv Pesq31265271Google Scholar
  17. Lafontaine, Y, Gagné, F, Blaise, C, Costan, G, Gagnon, P, Chan, HM 2000Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St. Lawrence River (Canada)Aquat Toxicol505170Google Scholar
  18. Langston, WJ, Bebianno, MJ, Burt, GR 1998

    Metal handling strategies in molluscs

    Langston, WJBebiano, MJ eds. Metal metabolism in the aquatic environmentChapman and HallLondon, United Kingdom219272
    Google Scholar
  19. Lerch, K, Johnson, GF, Grushoff, P, Sternlieb, I 1985Canine hepatic lysosomal copper protein, identification as metallothioneinArch Biochem Physiol243108114Google Scholar
  20. Livingstone, DR 1993Biotechnology and pollution monitoring: use of molecular biomarkers in the aquatic environmentJ Chem Technol Biotechnol57195211Google Scholar
  21. Mantoura, RFC, Dickson, A, Rilery, JP 1978The complexation of metal with humic materials in natural watersEstuar Coast Mar Sci6387408Google Scholar
  22. Mouneyrac, C, Amiard, JC, Amiard-Triquet, C 1998Effect of natural factors (salinity and body weight) on cadmium, copper, zinc and metallothionein-like protein levels in resident populations of oysters (Crassostrea gigas) from a polluted estuaryMar Ecol Progr Ser162125135Google Scholar
  23. Olafson, RW, Olsson, PE 1987Electrochemical detection of metallothionein, zinc and copper levels during an annual reproductive cycle in Rainbow trout (Salmo gairdneri)Fish Physiol Biochem313947Google Scholar
  24. Phillips, DJH 1976The common mussel Mytilys edulis as an indicator of pollution by zinc, cadmium, lead and copper. Effects of environmental variables on the uptake of metalsMar Biol385969Google Scholar
  25. Rainbow, PS 1997Ecophysiology of trace metal uptake in crustaceansEstuar Coastal Shelf Sci44169175CrossRefGoogle Scholar
  26. Riba, I, García-Luque, E, Blasco, J, DelValls, TA 2003Bioavailability of heavy metals bound to estuarine sediments as a function of pH and salinity valuesChem Spec Bioav15101114Google Scholar
  27. Riba, I, González de Canales, M, Forja, JM, DelValls, TA 2004Sediment quality in the Guadalquivir estuary: sublethal effects associated with the Aznalcóllar mining spillMar Pollut Bull48153163Google Scholar
  28. Roesijadi, G 1992Metallothionein in metal regulation and toxicity in aquatic animalsRev Aquat Toxicol2281113Google Scholar
  29. Serafin, MA, Bebianno, MJ 2001Variation of metallothionein and metal concentrations in the digestive gland of the clam Ruditapes decussatus: sex and seasonal effectsEnviron Toxicol Chem20544552Google Scholar
  30. Sutherland, J, Major, CW 1981Internal heavy metal changes as a consequence of exposure of Mytilus edulis, the blue mussel, to elevated external copper (II) levelsComp Biochem Physiol68C6367Google Scholar
  31. Viarengo, A, Pertica, M, Canesi, L, Mazzucotelli, A, Orunesu, M, Bouquegneau, JM 1989Purification and biochemical characterization of a lysosomal copper-rich thionein-like protein involved in metal detoxification in the digestive glands of musselsComp Biochem Physiol93C389395Google Scholar
  32. Winge, D 1991

    Copper coordination in metallothionein

    Riordan, JFVallee, BL eds. Methods in enzymology, vol 205—metalobiochemistry, part B, metallothionein and related moleculesAcademic PressSan Diego, California
    Google Scholar
  33. Zamuda, CD, Wright, DA, Smucker, RA 1985The importance of dissolved organic compounds in the accumulation of copper by the American oyster, Crassostrea virginicaMar Environ Res16112Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • M. Laura Martín-Díaz
    • 1
  • Julián Blasco
    • 2
  • Marisa González de  Canales
    • 3
  • Diego Sales
    • 4
  • T. Ángel DelValls
    • 1
  1. 1.Departamento de Química FísicaFacultad de Cc. del Mar y AmbientalesCádizSpain
  2. 2.Instituto de Cc. Marinas de AndalucíaCádizSpain
  3. 3.Departamento de Biología Animal y FisiologíaFacultad de Cc. del Mar y AmbientalesCádizSpain
  4. 4.Dpto. Ingeniería Química, Tecnología de los Alimentos y Tecnología del Medio AmbienteFacultad de Cc. Del Mar y AmbientalesSpain

Personalised recommendations