Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-13T02:59:28.723Z Has data issue: false hasContentIssue false
  • English
  • Français

Trace metal and biomarker levels in tissues ofArgopecten purpuratus in the north of Chile, and the potential use ofthis species as a bioindicator of metallic stress

Published online by Cambridge University Press:  05 September 2012

Manuel Zapata ,
Marianne Lang ,
Ricardo Riso ,
Dario Moraga  and
Carlos Riquelme
Manuel Zapata*
Affiliation:
Laboratoire des Sciences de l’Environnement Marin, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, UMR CNRS 6539, UBO/IRD/IFREMER. Place Nicolas Copernic, 29280 Plouzané, France Laboratorio de Ecología Microbiana, Universidad de Antofagasta 170 Antofagasta, y Centro de Investigación Científica y Tecnológica para la Minería CICITEM, Chile
Marianne Lang
Affiliation:
Laboratoire des Sciences de l’Environnement Marin, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, UMR CNRS 6539, UBO/IRD/IFREMER. Place Nicolas Copernic, 29280 Plouzané, France
Ricardo Riso
Affiliation:
Laboratoire des Sciences de l’Environnement Marin, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, UMR CNRS 6539, UBO/IRD/IFREMER. Place Nicolas Copernic, 29280 Plouzané, France
Dario Moraga
Affiliation:
Laboratoire des Sciences de l’Environnement Marin, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, UMR CNRS 6539, UBO/IRD/IFREMER. Place Nicolas Copernic, 29280 Plouzané, France
Carlos Riquelme
Affiliation:
Laboratorio de Ecología Microbiana, Universidad de Antofagasta 170 Antofagasta, y Centro de Investigación Científica y Tecnológica para la Minería CICITEM, Chile
*
a Corresponding author:mzarcos@gmail.com
Get access

Abstract

The capacity to bioaccumulate trace metals present in San Jorge Bay, Antofagasta, Chile,was determined in northern scallop, Argopecten purpuratus, to examine thevalue of this important commercially species as a bioindicator of heavy metal pollution inareas where it is cultured. Scallops were sampled in summer 2009 in four sites: threenatural populations (Coloso, Historic District and La Rinconada, marine reserve), and acommercial hatchery (Colorado). The concentrations of three heavy metals (copper, cadmiumand lead) were then determined through stripping chronopotentiometric methods, and thelevels of four biomarkers: three genes implicated in the stress and oxidative metabolism,i.e., glutathione peroxidase (GPx), glutathione s-transferase (GST) and heat shock protein70 (HSP70), and a protein marker in the digestive gland and gill, a metallothionein (MT).The Historic District, located in the downtown area of the city, showed the highest metalconcentration of all the sampled sites, as well as the highest levels of the fourbiomarkers. This can be largely attributed to the nearby international port area of thetown and high sea traffic flow, exacerbated by the prevailing winds.

Keywords

Trace metalsCopperCadmiumLeadGenetic markerMetallothioneinPollutionArgopecten purpuratusPacific Ocean
Type
Brief Report
Information
Aquatic Living Resources , Volume 25 , Issue 3 , July 2012 , pp. 259 - 267
Copyright
© EDP Sciences, IFREMER, IRD 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Avendaño M., Cantillánez M., 2008, Aspectos biológicos y poblacionales de Argopecten purpuratus en la reserva marina La Rinconada : contribución para su manejo. In : Lovatelli, Farias A., Uriarte E.I. (Eds.). Estado actual del cultivo y manejo de moluscos bivalvos y su proyección futura : factores que afectan su sustentabilidad en América Latina. Taller Técnico Regional de la FAO. 20–24 de agosto de 2007, Puerto Montt, Chile. FAO Actas de Pesca y Acuicultura. No. 12. Roma, FAO, pp. 249–266.
Becker, A., Soliman, K.F.A., 2009, The role of intracellular glutathione in inorganic mercury-induced toxicity in neuroblastoma cells. Neurochem. Res. 34, 1677–1684. CrossRefGoogle ScholarPubMed
Boutet, I., Tanguy, A., Auffret, M., Riso, R., Moraga, D., 2002, Immunochemical quantification of metallothioneins in marine molluscs : characterization of a metal exposure bioindicator. Environ. Toxicol. Chem. 21, 1009–1014. CrossRefGoogle ScholarPubMed
Boutet, I., Moraga, D., Marinovic, L., Obreque, J., Chavez-Crooker, P., 2008, Characterization of reproduction-specific genes in a marine bivalve mollusc : Influence of maturation stage and sex on mRNA expression. Gene. 407, 130–138. CrossRefGoogle Scholar
Brooks, R., Rumsby, M., 1965, The Biogeochemistry of trace element uptake by some New Zealand Bivalves. Limnol. Oceanogr. 10, 521–527. CrossRefGoogle Scholar
Bustamante, P., Luna-Acosta, L., Clemens, S., Cassi, R., Thomas-Guyon, H., Warnau, M., 2012, Bioaccumulation and metabolisation of 14C-pyrene by the Pacific oyster Crassostrea gigas exposed via seawater. Chemosphere 87, 938–944. CrossRefGoogle Scholar
Canesi, L., Viarengo, A., Leonzio, C., Filippelli, M., Gallo, G., 1999, Heavy metals and glutathione metabolism in mussel tissues. Aquat. Toxicol. 46, 67–76. CrossRefGoogle Scholar
Chandran, R., Sivakumar, A., Mohandass, S., Aruchami, M., 2005, Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod Achatina fulica. Comp. Biochem. Physiol. C. 140, 422–426. Google Scholar
David, E., Tanguy, A., Riso, R., Quiniou, L., Laroche, J., Moraga, D., 2012, Responses of Pacific oyster Crassostrea gigas populations to abiotic stress in environmentally contrasted estuaries along the Atlantic coast of France. Aquat. Toxicol. 109, 70–79. CrossRefGoogle Scholar
Dondero, F., Piacentini, L., Marsano, F., Rebelo, M., Vergani, L., Venier, P., Viarengo, A., 2006, Gene transcription profiling in pollutant exposed mussels (Mytilus spp.) using a new low-density oligonucleotide microarray. Gene 376, 24–36. CrossRefGoogle ScholarPubMed
Escribano, R., Hidalgo, P., 2001, Circulación inducida por el viento en Bahía de Antofagasta, norte de Chile (23° S). Rev. Biol. Mar. Oceanogr. 36, 43–60. CrossRefGoogle Scholar
Farrington, J.W., Tripp, B.W., 1993, International mussel watch. Oceanus 36, 62–64. Google Scholar
Feder, M.E., Hofmann, G.E., 1999, Heat-shock proteins, molecular chaperones, and the stress response : evolutionary and ecological physiology. Ann. Rev. Physiol. 61, 243–282. CrossRefGoogle ScholarPubMed
Ferreira-Cravo, M., Ventura-Lima, J., Sandrini, J.Z., Amado, L.L., Geracitano, L.A., Rebelo, M., Bianchini, A., Monserrat, J.M., 2009, Antioxidant responses in different body regions of the polychaeta Laeonereis acuta (Nereididae) exposed to copper. Ecotoxicol. Environ. Saf. 72, 388–393. CrossRefGoogle Scholar
Franzellitti, S., Fabbri, E., 2005, Differential HSP70 gene expression in the Mediterranean mussel exposed to various stressors. Biochem. Biophys. Res. Commun. 336, 1157–1163. CrossRefGoogle ScholarPubMed
Gorbi, S., Virno, C., Notti, A., Benedetti, M., Fattorini, D., Moltedo, G., Regoli, F., 2008, An ecotoxicological protocol with caged mussels, Mytilus galloprovincialis, for monitoring the impact of an offshore platform in the Adriatic sea. Mar. Environ. Res. 65, 34–49. CrossRefGoogle Scholar
Ivanina, A.V., Sokolova, I.M., Sukhotin, A.A., 2008, Oxidative stress and expression of chaperones in aging mollusks. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 150, 53e61. CrossRefGoogle ScholarPubMed
Ivanina, A.V., Taylor, C., Sokolova, I.M., 2009, Effects of elevated temperature and cadmium exposure on stress protein response in eastern oysters Crassostrea virginica (Gmelin). Aquat. Toxicol. 91, 245–254. CrossRefGoogle Scholar
Jadhav, S.H., Sarkar, S.N., Aggarwal, M., Tripathi, H.C., 2007, Induction of oxidative stress in erythrocytes of male rats subchronically exposed to a mixture of eight metals found as groundwater contaminants in different parts of India. Arch. Environ. Contam. Toxicol. 52, 145–151. CrossRefGoogle Scholar
Kägi, R., Schäffer, A., 1988, Biochemistry of metallothionein. Biochemistry 27, 8509–8515. CrossRefGoogle ScholarPubMed
Ketterer, B., Coles, B., Meyer, D.J., 1983, The role of glutathion in detoxification. Environ. Health Perspect. 49, 59–69. CrossRefGoogle Scholar
Kim, M.O., Phyllis, E.B., 1998, Oxidative stress in critical care : is antioxidant supplementation beneficial? J. Am. Diet. Assoc. 98, 1001–1008. Google Scholar
Legeay, A., Achard-Joris, M., Baudrimont, M., Massabuau, J.C., Bourdineaud, J.P., 2005, Impact of cadmium contamination and oxygenation levels on biochemical responses in the Asiatic clam Corbicula fluminea. Aquat. Toxicol. 74, 242–253. CrossRefGoogle Scholar
Livingstone, D., Lips, F., Garcia Martinez, P., Pipe, R., 1992, Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar. Biol. 122, 265–276. CrossRefGoogle Scholar
Livak, K., Schmittgen, T., 2001, Analysis of relative gene expression data using real time quantitative RPC and the 2−ΔΔCT method. Methods 25, 402–408. CrossRefGoogle Scholar
Machreki-Ajmia, M., Rebaib, T., Hamza-Chaffaia, A., 2011, Variation of metallothionein-like protein and metal concentrations during the reproductive cycle of the cockle Cerastoderma glaucum from an uncontaminated site : A 1-year study in the Gulf of Gabès area (Tunisia). Mar. Biol. Res. 7, 261–271. CrossRefGoogle Scholar
Mackay, E.A., Overnell, J., Dunbar, B., 1993, Complete amino acids sequences of five dimeric and four monomeric forms of metallothionein from the edible mussel Mytilus edulis. Eur. J. Biochem. 218, 183–194. CrossRefGoogle ScholarPubMed
Mao, H., Wang, D., Yang, W., 2012, The involvement of metallothionein in the development of aquatic invertebrate. Aquat. Toxicol. 110, 208–213. CrossRefGoogle ScholarPubMed
Maria, V.L., Santos, M.A., Bebianno, M.J., 2009, Biomarkers of damage and protection in Mytilus galloprovincialis cross transplanted in Ria Formosa Lagoon (Portugal). Ecotoxicology 18, 1018–1028. CrossRefGoogle Scholar
Marchand, J., Quiniou, L., Riso, R., Thebaut, M.-T., Laroche, L., 2004, Physiologial cost of tolerance in the European flouder Platichthys flesus, along the French Atlantic coast. Aquat. Toxicol. 70, 327–343. CrossRefGoogle Scholar
Moraga, D., Mdelgi-Lasram, E., Romdhane, M., El Abed, A., Boutet, I., Tanguy, A., Auffret, M., 2002, Genetic responses to metal contamination in two clams : Ruditapes decussatus and Ruditapes philippinarum. Mar. Environ. Res. 54, 521–525. CrossRefGoogle ScholarPubMed
Muñoz P., 2002, Evaluación de las vías de transporte de plomo total en un área costera de Chile a través de un balance geoquímico. Tesis Doctoral Oceanografía. Universidad de Concepción.
Navarro, A., Faria, M., Barata, C., Piña, B., 2011, Transcriptional response of stress genes to metal exposure in zebra mussel larvae and adults. Environ. Pollut. 159, 100–107. CrossRefGoogle ScholarPubMed
Nawrot, T., Plusquin, M., Hogervorst, J., Roels, H.A., Celis, H., Thijs, L., Vangronsveld, J., Van Hecke, E., Staessen, J.A., 2006, Environmental exposure to cadmium and risk of cancer : a prospective population-based study. Lancet Oncology 7, 119–126. CrossRefGoogle ScholarPubMed
Pan, K., Wang, W.-X., 2008a, Allometry of cadmium and zinc concentrations and bioaccumulation in the scallop Chlamys nobilis. Mar. Ecol. Prog. Ser. 365, 115–126. CrossRefGoogle Scholar
Pan, K., Wang, W.-X., 2008b, Validation of biokinetic model of metals in the scallop Chlamys nobilis in complex field environment. Environ. Sci. Technol. 42, 6285–6290. CrossRefGoogle Scholar
Phillips, D.J.H., 1976, The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead and copper. II. Relationship of metals in the mussel to those discharged by industry. Mar. Biol. 38, 59–69. Google Scholar
Pytharopoulou, S., Grintzalis, K., Sazakli, E., Leotsinidis, M., Georgiou, C., Kalpaxis, D., 2011, Translational responses and oxidative stress of mussels experimentally exposed to Hg, Cu and Cd : One pattern does not fit at all. Aquat. Toxicol. 105, 157–165. CrossRefGoogle Scholar
Quinn, B., Gagne, F., Weber, J., Blaise, C., 2005, Ecotoxicological effects of a semi-submerged municipal dump (Castle harbour, Bermuda) on the Calico scallop Argopecten gibbus. Mar. Pollut. Bull. 51, 534–544. CrossRefGoogle ScholarPubMed
Raspor, B., Dragun, Z., Erk, M., Ivankovic, D., Pavicic, J., 2004, Is the digestive gland of Mytilus galloprovincialis a tissue of choice for estimating cadmium exposure by means of metallothioneins? Sci. Total Environ. 333, 99–108. CrossRefGoogle Scholar
Riso, R., Le Corre, P., Chaumery, C., 1997a, Rapid and simultaneous analysis of trace metals (Cu, Pb and Cd) in seawater by potentiometric stripping analysis. Anal. Chim. Acta 351, 83–89. CrossRefGoogle Scholar
Riso, R., Monbet, P., Le Corre, P., 1997b, Measurement of copper in sea-water by constant current stripping analysis (CCSA) with a rotating gold disk electrode. The Analyst 122, 1593–1596. CrossRefGoogle Scholar
Rutllant, J., Fuenzalida, H., Torres, R., Figueroa, D., 1998, Interacción océano-atmósfera-tierra en la región de Antofagasta (Chile 23° S). Experimento Diclima. Rev. Chil. Hist. Nat. 71, 405-427. Google Scholar
Salamanca, M., Camaño, A., Jara, B., Rodríguez, T., 2000, Cu, Pb and Zn distribution in nearshore water en San Jorge Bay, Northern Chile. Gayana 64, 195–204. Google Scholar
Salamanca, M., Jara, B., Rodríguez, T., 2004, Niveles de Cu, Pb y Zn en agua y Perumytilus purpuratus en Bahía San Jorge, Norte de Chile. Gayana 68, 53–62. Google Scholar
Singh, S., Eapem, S., D’Souza, S.F., 2006, Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plants, Bacopa monnieri L. Chemosphere 62, 233–246. CrossRefGoogle Scholar
Solé, M., Porte, C., Barcelo, D., Albaigés, J., 2000, Bivalves residue analysis for the assessment of coastal pollution in the Ebro Delta (NW Mediterranean). Mar. Pollut. Bull. 40, 746–753. CrossRefGoogle Scholar
Song, L., Wu, L., Ni, D., Chang, Y., Xu, W., Xing, K., 2006, The cDNA cloning and mRNA expression of heat shock protein 70 gene in the haemocytes of bay scallop (Argopecten irradians, Lamarck 1819) responding to bacteria challenge and naphthalin stress. Fish Shellfish Immun. 21, 335–345. CrossRefGoogle ScholarPubMed
Tanguy, A., Boutet, I., Riso, R., Boudry, P., Auffret, M., Moraga, D., 2003, Metallothionein genes in the European flat oyster Ostrea edulis : a potential ecological tool for environmental monitoring? Mar. Ecol. Prog. Ser. 257, 87–97. CrossRefGoogle Scholar
Tanguy, A., Boutet, I., Laroche, J., Moraga, D., 2005, Molecular identification and expression study of differentially regulated genes in the Pacific oyster Crassostrea gigas in response to pesticide exposure. Fed. Eur. Biochem. Soc. J. 272, 390–403. Google ScholarPubMed
Tapia, J., Vargas-Chacoff, L., Bertrán, C., Carrasco., Torres, F., Pinto, R., Urzúa, S., Valderrama, A., Letelier, L., 2010, Study of the content of cadmium, chromium and lead in bivalves molluscs of the Pacific Ocean (Maule region, Chile). Food Chem. 121, 666–671. CrossRefGoogle Scholar
Valdés, J., Román, D., 2010, Distribution and temporal variation of trace metal enrichment in surface sediments of San Jorge Bay, Chile. Environ. Monit. Assess. 16, 185–197. CrossRefGoogle Scholar
Valdés, J., Román, D., Rivera, L., Ávila, J., Cortés, P., 2011, Metal contents in coastal waters of San Jorge Bay, Antofagasta, northern Chile : a base line for establishing seawater quality guidelines. Environ. Monit. Assess. 183, 231–242. CrossRefGoogle Scholar
Valko, M., Morris, H., Cronin, M.T.D., 2005, Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161–1208. CrossRefGoogle ScholarPubMed
Veldhoen, N., Lowe, C.J., Davis, C., Mazumder, A., Helbing, C.C., 2009, Gene expression profiling in the deep water horse mussel Modiolus modiolus (L.) located near a marine municipal wastewater outfall. Aquat. Toxicol. 93, 116–124. CrossRefGoogle Scholar
Veldhoen, N., Kobylarz, M., Lowe, C.J., Meloche, L., deBruyn, A.M.H., Helbing,, C.C., 2011, Relationship between mRNA biomarker candidates and location near a marine municipal wastewater outfall in the benthic indicator species Modiolus modiolus (L). Aquat. Toxicol. 105, 119–126. CrossRefGoogle Scholar
Venier, P., De Pitta, C., Pallavicini, A., Marsano, F., Varotto, L., Romualdi, C., Dondero, F., Viarengo, A., Lanfranchi, G., 2006, Development of mussel mRNA profiling : can gene expression trends reveal coastal water pollution? Mutat. Res. 602, 121–134. Google Scholar
Xie, L., Klerks, P.L., 2004, Metallothionein-like protein in the least killifish Heterandria formosa and its role in cadmium resistance. Environ. Toxicol. Chem. 23, 173–177. CrossRefGoogle ScholarPubMed
Yap, C.K., Ismael, A., Tan, S.G., 2004, Heavy metal (Cd, Cu, Pb, and Zn) concentrations in the green-lipped mussel Perna viridis (Linnaeus) collected from some wild and aquacultural sites in the west coast of Peninsular Malaysia. Food Chem. 84, 569–575. CrossRefGoogle Scholar
Zapata, M., Tanguy, A., David, E., Moraga, D., Riquelme, C., 2009, Transcriptomic response of Argopecten purpuratus post-larvae to copper exposure under experimental conditions. Gene 442, 121–131. CrossRefGoogle ScholarPubMed
Zhang, Y., Song, J., Yuan, H., Xu, Y., He, Z., Duan, L., 2010, Biomarker responses in the bivalve (Chlamys farreri) to exposure of the environmentally relevant concentrations of lead, mercury, copper. Environ. Toxicol. Pharmacol. 30, 19–25. CrossRefGoogle Scholar