08Jun 2017


  • Ain Chock Faculty of Sciences, Biology department, Casablanca, Morocco.
  • National Institute of Fischeries Research (INRH), Casablanca, Morocco.
  • Ben Msik Faculty of Sciences, Casablanca, Morocco.
  • Lorraine University (UdL), Interdisciplinary Laboratory of Continental Environments (LIEC) - UMR 7360 CNRS, Metz, France.
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In this study, four biomarkers, Acetylcholinesterase (AChE), Glutathione-s-transferase (GST), Metallothioneines (MT) and Malondialdehyde (MDA) were measured, during spring 2013, in indigenous mussels Mytilus galloprovincialis from five sites of Moroccan Atlantic center coast, subjected to the impact of anthropogenic activities. The results show a general stress in the studied area, with three groups of stations. The first one includes mussels from station S1 with low MDA and MT activities. The second encompasses the most polluted stations (S4 and S5) with high MT and MDA activities as well as low AChE and high GST activities. Lastly, mussels from the least polluted stations (S2 and S3) characterized by moderate MDA and MT levels, low GST and high AChE activities. The results indicate that the biochemical alterations observed in the mussel digestive gland could be used as suitable biomarkers for evaluating environmental quality of the media based on the biological assessing methods and can provide early warning information on the impact of contaminants on marine environment.

  1. Andrews, G.K., 2000. Regulation of metallothionein, gene expression by oxidative stress and metal ions. Biochem. Pharm. 59, 95-104.
  2. Barhoumi, B., Le Menach, K., Cl?randeau, C., Ben Ameur, W., Budzinski, H., Driss, M.R., Cachot, J., 2014. Assessment of pollution in the Bizerte lagoon (Tunisia) by the combined use of chemical and biochemical markers in mussels, Mytilus galloprovincialis. Mar. Pollut. Bull. 84, 379-390.
  3. Benbrahim, S., Chafik, A., Chfiri, R., Bouthir, F.Z., Siefeddine, M., Makaoui, A., 2006. Etude des facteurs influen?ant la r?partition g?ographique et temporelle de la contamination des c?tes atlantiques marocaines par les m?taux lourds: cas du mercure, du plomb et du cadmium. Mar. Life. 16, 37-47.
  4. Binelli, A., Ricciardi, F., Provini, A., 2006. New evidences for old biomarkers: effects of several xenobiotics on EROD and AChE activities in Zebra mussel (Dreissena polymorpha). Chemosphere 62, 510-519.
  5. Bolognesi, C., Frenzilli, G., Lasagna, C., Perrone, E., Roggieri, P., 2004. Genotoxicity biomarkers in Mytilus galloprovincialis: wild versus caged mussels. Mut. Res. 552, 153-162.
  6. Bouthir F.Z, Chafik, A., Benbrahim, S., Souabi, S., Mardhy, H.,? Messoudi, A., 2004.Qualit? physico-chimique des eaux c?ti?res du littoral de la Wilaya du grand Casablanca (oc?an Atlantique marocain) utilisant la moule Mytilus galloprovincialis comme indicateur de la contamination m?tallique Mar. Life, 14, 59-70.
  7. Bradford, M., 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein?dye blinding. Anal. Biochem. 72, 248-254.
  8. Brooks, S., Harman, C., Zaldibar, B., Izagirre, U., Glette, T., Marigomez, I., 2011. Integrated biomarker assessment of the effects exerted by treated produced water from an onshore natural gas processing plant in the North Sea on the mussel Mytilus edulis. Mar. Pollut. Bull. 62, 327-339.
  9. Canesi, L., Viarengo, A., Leonzio, C., Filippelli, M., Gallo, G., 1999. Heavy metals and glutathione metabolism in mussel tissues. Aquat. Toxicol. 46, 67-76.
  10. Capela, R., Raimundo, J., Santos, MM., Caetano, M., Micaelo, C., Vale, C., Guimaraes, L., Reis-Henriques, M.A., 2016. The use of Biomarkers as integrative tools for transitional water bodies monitoring in the Water Framework Directive Context- A holistic approach in Minho river transitional waters. Sci. Tot. Envir. 539, 85-86.
  11. Chafik, A., Cheggour, M., Cossa, D., Sifeddine, S.B.M., 2001. Quality of Moroccan Atlantic coastal waters: water monitoring and mussel watching. Aquat. Living Resour. 14, 239-249.
  12. Charouf, L. 1986. Les probl?mes d?ensablement des ports Marocains sur la fa?ade atlantique : Leur impact s?dimentologique sur le littoral. Ph. D. thesis, Paris-Sud Univ., Orsay, France, 312 p.
  13. Cheggour, M., Langston, W.J., Chafik, A., Texier, H., Idrissi, H., Boumezzough, A., 1999. Phosphate industry discharges and their impact on metal contamination and intertidal macrobenthos: Jorf Lasfar and Safi coastlines (morocco). Toxicol. Environ. Chem.70, 159-179.
  14. Cossu-Leguille,C., Vasseur,P., 2013. Aquatic biomarkers, in F?rard,J.F.,Blaise,C. (Eds), Encyclopedia of Aquatic Ecotoxicology, vol. 1, Springer, Dordrecht, Netherlands, pp. 49-66.
  15. De Luca-Abbott, S.B., Richardson, B.J., McClellan, K.E., Zheng, G.J., Martin, M., Lam, P.K.S., 2005. Field validation of antioxidant enzyme biomarkers in mussels (Perna viridis) and clams (Ruditapes philippinarum) transplanted in Hong Kong coastal waters. Mar. Pollut. Bull. 51, 694-707.
  16. Dellali, M., Gnassia Barelli, M., Romeo, M., Aissa, P., 2001. The use of acetylcholinesterase activity in Ruditapes decussatus and Mytilus galloprovincialis in the biomonitoring of Bizerta lagoon. Comp. Biochem. Phys. C 130, 227-235.
  17. Ellman, G.L., Courtney, K.D., Andreas, V., Featherstone, R.M., 1961. A new and rapid colorimetric determination of AChE activity. Biochem. Pharmacol. 7, 88-95.
  18. Fernandez, B., Campillo, A., Martinez-Gomez, C., Benedicto, J., 2010. Antioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomarkers of environmental stress along the Spanish Mediterranean coast. Aquat. Toxicol. 99, 186-197.
  19. Fulton, MH., Key, PB. 2001. Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ. Toxicol. Chem. 20, 37-45.
  20. Galgani, F., Bocquen?, G., 1989. A method for routine detection of organophosphates and carbamates in sea water. Environ. Technol. Lett. 10, 311-322.
  21. Galloway, T.S., Brown, R.J., Browne, M.A., Dissanayake, A., Lowe, D., Depledge, M.H., 2004. A multibiomarker approach to environmental assessment. Environ. Sci. Technol. 38, 1723-1731.
  22. G?ret, F., Jouan, A., Turpin, V., Bebianno, M.J., Cosson, R.P., 2002. Note. Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalves mollusks: the oyster (Crassostrea gigas) and the mussel (Mytilus edulis). Aquat. Living Resour. 15, 61-66.
  23. Guilhermino, L., Barros, B., Silva, M.C., Soares, A.M.V.M., 1998. Should the use of inhibition of cholinesterases as a specific biomarker for organophosphate and carbamate pesticides be questioned? Biomarkers 3, 157-163.
  24. Habig, W.H., Pabst, M.J., Jakobi, W.B., 1974. Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J. Biol. 249, 7130-7139.
  25. Hagger, J.A., Galloway, T.S., Oehlmann, J., Jobling, S., Depledge, M.H., 2006. Is there a causal association between genotoxicity and the imposex effects? Environ. Health Perspect. 114, 20-26.
  26. Hamza-Chaffai, A., 2014. Usefulness of Bioindicators and Biomarkers in Pollution Biomonitoring. Int. J. Biotechnol. Wellness Ind. 3, 19-26.
  27. He, X., Nie, X., Wang, Z., Cheng, Z., Li, K., Li, G., Wong, M.H., Liang, X., Tsui, M.T.K., 2011. Assessment of typical pollutants in waterborne by combining active biomonitoring and integrated biomarkers response. Chemosphere 84, 1422-1431.
  28. ICES, 2008. Report of the Fourth ICES/OSPAR Workshop on Integrated Monitoring of Contaminants and their Effects in Coastal and Open Sea Areas (WKIMON IV), 5? 7 February 2008. ICES, Copenhagen, Denmark. ICES CM 2008/ACOM: 49, 71.
  29. Jayed, M., Chafik, A., Benbrahim, S., Vale, C., Bakkas, S., Pereira, P., Ferreira, M., 2010. Polychlorinated biphenyls and chlorinated pesticides in the mussel Mytilus galloprovincialis sampled along the Moroccan Atlantic Coast. Journal of Oceanography and Marine science 1, 93-98.
  30. Jeng, M.C., Jeng, W.L., Hung, T.C., Yeh, C.Y., Tseng, R.J., Meng, P.J., Han, B.C., 2000. Mussel Watch: a review of Cu and other metals in various marine organisms in Taiwan, 1991-98. Environ. Poll. 110, 207-215.
  31. Kaimoussi, A., Chafik, A., Cheggour, A., Mouzdahir, A., Bakkas, S., 2000. Variations saisonni?res des concentrations en m?taux (Cd, Cu, Zn, Fe et Mn) chez la moule Mytilus galloprovincialis du littoral de la r?gion d?Eljadida (Maroc) Mar. Life 10, 77-85.
  32. Khessiba, A., Hoarau, P., Gnassia-Barelli, M., Aissa, P., Rom?o, M., 2001. Biochemical response of the mussel Mytilus galloprovincialis from Bizerta (Tunisia) to chemical pollutant exposure. Archives of Environ. Contam. Toxicol. 40, 222-229.
  33. Knight, J.A., Pieper, R.K., McClellan, L., 1988. Specificity of the thiobarbituric acid reaction: its use in studies of lipid peroxidation. Clin. Chem. 34, 2433-2438.
  34. Labrot, F., Ribera, D., Saint Denis, M., Narbonne, J.F., 1996. In vitro and in vivo studies of potential biomarkers of lead and uranium contamination: lipid peroxidation, acetylcholinesterase, catalase and glutathione peroxidase activities in three non mammalian species. Biomarkers 1, 21-28.
  35. Langston, W.J., Bebianno, M.J., Burt, G.R., 1998. Metal Handling strategies in molluscs. In: Langston, W.J., Bebianno, M.J. (Eds.), Metal metabolism in aquatic environments. Chapman Hall, London, 8, 219-284.
  36. Lehtonen, K.K., Leini?, S., Schneider, R., Leivuori, M., 2006. Biomarkers of pollution effects in the bivalves Mytilus edulis and Macoma balthica collected from the southern coast of Finland (Baltic Sea). Mar. Ecol. Prog. 322, 155-168.
  37. Livingstone, D.R., 1993. Biotechnology and pollution monitoring: use of molecular biomarkers in the aquatic environment. J. Chem. Technol. Biot. 57, 195-211.
  38. Livingstone, D.R., Donkin, P., Walker, C.H., 1992. Pollutants in marine ecosystems: an overview. In: Walker, C., Livingstone, D.R. (Eds.), Persistent Pollutants in Marine Ecosystems, SETAC Special Publications Series. Pergamon Press, 235-263.
  39. Maanan, M., 2007. Biomonitoring of heavy metals using Mytilus galloprovincialis in Safi coastal waters. Morocco. Environ. Toxicol. 22, 525-531.
  40. Maanan, M., 2008. Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environ. Pollut. 153, 176-83.
  41. Marnett, L.J., 1999. Lipid peroxidation ? DNA damage by malondialdehyde. Mut. Res. 424, 83-95.
  42. McCarthy, J.F., Shugart, L.R., 1990. Biological markers of environmental contamination. In: McCarthy, J.F., Shugart, L.R. (Eds.), Biomarkers of Environmental Contamination. Lewis Publisher, Boca Raton, FL, 3-16.
  43. Mora, P., Michel, X., Narbonne, J.-F., 1999. Cholinesterase activity as potential biomarker in two bivalves. Environ. Toxicol. Pharmacol. 7, 253-260.
  44. Moreira, , Guilhermino,? L., 2005. The use of Mytilus galloprovincialis, acetylcholinesterase and glutathione S-transferases activities as biomarkers of environmental contamination along the northwest Portuguese coast. Environ. Monit. Assess. 105, 309-325.
  45. Moustaid, K.,? Nasser, B., Baudrimont, I., Anane, R., El Idrissi, M., Bouzidi, A., 2005. ?valuation compar?e de la toxicit? des moules (Mytilus galloprovincialis) de deux sites du littoral atlantique marocain sur des souris. C. R. Biol. 328, 281-289.
  46. Narbonne, J.F, Daubeze, M., Cl?randeau, C. Garrigues, P., 1999. Scale of classifacation based on biochemical markers in mussels?: application to pollution monitoring in European coasts. Biomarkers 4, 415-424.
  47. Office Ch?rifien des Phosphates, Annual Report, Maroc. http://www.ocpgroup.ma/finance/rapports-publies/rapport-annuel, 2012.OSPAR, 2000. Quality Status Report: Region IV ? Bay of Biscay and Iberian Coast. OSPAR Commission, London.
  48. Parolini, M., Pedriali, A., Riva, C., Binelli, A., 2013. Sub-lethal effects caused by cocaine metabolite benzoylecgonine to the freshwater mussel Dreissena polymorpha. Sci. Tot. Envir. 444, 43-50.
  49. Pellerin-Massicotte, J., 1997. Influence of elevated temperature and air exposure on MDA levels and catalase activities in digestive glands of the blue mussel (Mytilus edulis L.). J. Rech. Oc?anogr. 22, 91?98.
  50. Pfeifer, S., Schiedek, D., Dippner, J.W., 2005. Effect of temperature and salinity on acetylcholinesterase activity, a common pollution biomarker, in Mytilus sp. from the south-western Baltic Sea. J. Exp. Mar. Biol. Ecol. 10, 41-47.
  51. Schiedek, D., Broeg, K., Barsiene, J., Lehtonen, K.K, Gercken, J., Pfeifer, S., Vuontisjarvi, H., Vuorinen, P.J., Dedonyte, V.,Koehler, A., Balk, L., Schneider, R., 2006. Biomarker responses as indication of contaminant effects in blue mussel (Mytilus edulis) and female eelpout (Zoarces viviparus) from the southwestern Baltic Sea. Mar. Poll. Bull. 53, 387-405.
  52. Serafim, A., Lopes, B., Company, R., Cravo, A., Gomes, T., Sousa, V., Bebianno, M.J., 2011. A multi-biomarker approach in cross-transplanted mussels Mytilus galloprovincialis. Ecotoxicology 20, 1959-1974.
  53. Stohs, S.J., Bagachi, D., Hassoun, E., Bgachi, M., 2000. Oxidative mechanism in the toxicity of chromium and cadmium ions. J. Environ. Pathol. Toxicol. Oncol. 19, 201-213 .
  54. Sunderman, F.W, Marzouk, A., Hopper, S.M., Zaharia, O., Reid, M.C., 1985. Increased lipid peroxidation in tissues of nickel chloride-treated rats. Ann. Clin. Lab. Sci. 15, 229-236.
  55. Thornalley, P., Va??k, M., 1985. Possible role for metallothionein in protection against radiation induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. BBA-Protein Structure and Molecular Enzymology 827, 36-44.
  56. Tim-Tim, ALS., Morgado, F., Moreira, S., Rangel, R., Nogueira, AJA., Soares, AMM., 2009. Cholinesterase and glutathione S-transferase activities of three mollusc species from the NW Portuguese coast in relation to the ?Prestige? oil spill. Chemosphere 77, 1465-1475.
  57. Torres, M.A., Testa, C.P., Gaspari, C., Masutti, M.B., Panitz, C.M.N., Curi-Pedrosa, R., Almeida, E.A., Di Mascio, P., Wilhelm Filho, D., 2002. Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island. Brazil. Mar. Poll. Bull. 44, 923-932.
  58. Viarengo, A., Burlando, B., Ceratto, N., Panfili, I., 2000. Antioxidant role of metallothioneins: a comparative overview. Cell. Mol. Biol. 46, 407-417.
  59. Viarengo, A., Canesi, L., 1991. Mussels as biological indicators of pollution. Aquaculture 94, 225-243.
  60. Viarengo, A., Canesi, L., Pertica, M., Poli, G., Moore, M.N., Orunesu, M., 1990. Heavy metal effects on lipid peroxidation in the tissues of Mytilus galloprovincialis Lam. Comp. Biochem. Physiol. 97C, 37-42.
  61. 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. Mar. Environ. Res. 44, 69-84.
  62. Vidal-Linan, L., Bellas, J., Campillo, J.A., Beiras, R., 2010. Integrated use of antioxidant enzymes in mussels, Mytilus galloprovincialis, for monitoring pollution in highly productive coastal areas of Galicia (NW Spain). Chemosphere 78, 265-272.
  63. Won, S., Novillo, A., Custodia, N., Rie, M.T., Fitzgerald, K., Osada, M., Callard, A.P., 2005. The freshwater mussel (Elliptio complanata) as a sentinel species: vitellogenin and steroid receptors. Integr. Comp. Biol. 45, 72-80.

[M. Zbiry, B. Elhaimeur, M. Bouhallaoui, S. Talba, M. Bekkali, J. F. F?rard and A. Benhra. (2017); SPATIAL VARIATION OF BIOMARKERS IN MUSSELS MYTILUS GALLOPROVINCIALIS FROM THE MOROCCAN ATLANTIC CENTER COAST. Int. J. of Adv. Res. 5 (6). 6-17] (ISSN 2320-5407). www.journalijar.com

Mariama Zbiry


Article DOI: 10.21474/IJAR01/4375       DOI URL: http://dx.doi.org/10.21474/IJAR01/4375

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