Oxidative stress in the clam Ruditapes decussatus (Linnaeus, 1758) in relation to polycyclic aromatic hydrocarbon body burden

Environmental Toxicology

Volumn 22, Issue 2, 2007, Pages 203-221

  Barreira, Luísa A ^a   Mudge, Stephen M ^b   Bebianno, Maria J ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b BANGOR UNIVERSITY   (United Kingdom)

Author keywords

Antioxidant enzymes; Biomarkers; Clams; Molluscs; PAHs; Ria Formosa lagoon; Ruditapes decussatus

Indexed keywords

ADENOSINETRIPHOSPHATE; CLIMATE CHANGE; METABOLISM; OXIDATIVE STRESS; POLYCYCLIC AROMATIC HYDROCARBONS; TISSUE;

ANTIOXIDANT ENZYMES; MOLLUSCS; RIA FORMOSA LAGOONS; RUDITAPES DECUSSATUS;

ENZYME ACTIVITY;

ANTIOXIDANT; BIOLOGICAL MARKER; CATALASE; GLUTATHIONE PEROXIDASE; OXYGEN RADICAL; POLYCYCLIC AROMATIC HYDROCARBON; SUPEROXIDE DISMUTASE;

ANTIOXIDANT; BIOMARKER; BIVALVE; ECOTOXICOLOGY; ENZYME ACTIVITY; LAGOON; LIPID; OXIDATION; PAH; PEROXY RADICAL; POLLUTION EFFECT; SEASONAL VARIATION; SELENIUM; TOXICITY TEST; WATER POLLUTION;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BODY BURDEN; CLAM; ENVIRONMENTAL IMPACT ASSESSMENT; ENZYME ACTIVITY; EXOCRINE GLAND; INDICATOR ORGANISM; LIPID PEROXIDATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPRODUCTION; SEASONAL VARIATION; SPECIES HABITAT; WATER TEMPERATURE;

ANIMALS; BIOLOGICAL MARKERS; BIVALVIA; BODY BURDEN; CATALASE; CYTOSOL; ENVIRONMENTAL MONITORING; GASTROINTESTINAL TRACT; GLUTATHIONE PEROXIDASE; LIPID PEROXIDATION; MITOCHONDRIA; OXIDATIVE STRESS; POLYCYCLIC HYDROCARBONS, AROMATIC; PORTUGAL; SUPEROXIDE DISMUTASE; WATER POLLUTANTS, CHEMICAL;

EURASIA; EUROPE; FARO [PORTUGAL]; PORTUGAL; RIA FORMOSA; SOUTHERN EUROPE;

BIVALVIA; MOLLUSCA; VENERUPIS (RUDITAPES) DECUSSATUS;

EID: 34047190880     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.20257     Document Type: Article

References (76)

1. Akcha F, Izuel C, Venier P, Budzinski H, Burgeot T, Narbonne JF. 2000. Enzymatic biomarker measurement and study of DNA adduct formation in benzo[a]pyrene-contaminated musselsm, Mytilus galloprovincialis. Aquatic Toxicol 49:269-287.
2. Barata C, Varo I, Navarro JC, Arun S, Porte C. 2005. Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol 140:175-186.
3. Barreira LA, Mudge SM, Bebianno MJ. 2007. Polycyclic aromatic hydrocarbons in clams Ruditapes decussatus (Linnaeus, 1758). J Environ Monit 9 (DOI: 10.1039/b614919g).
4. Baumard P, Budzinski H, Garrigues P. 1998. Polycyclic aromatic hydrocarbons in sediments and mussels of the Western Mediterranean sea. Environ Toxicol Chem 17:765-776.
5. Bebianno MJ, Serafim MA. 2003. Variation of metal and metallothionein concentrations in a natural population of Ruditapes decussatus. Arch Environ Contam Toxicol 44:53-66.
6. Bebianno MJ, Géret F, Hoarau P, Serafim MA, Coelho MR, Gnassia-Barelli M, Roméo M. 2004. Biomarkers in Ruditapes decussatus: A potential bioindicator species. Biomarkers 9:305-330.
7. Beiras R, Albentosa M. 2004. Inhibition of embryo development of the commercial bivalves Ruditapes decussatus and Mytilus galloprovincialis by trace metals; implications for the implementation of seawater quality criteria. Aquaculture 230:205-213.
8. Binelli A, Provini A. 2003. POPs in edible clams from different Italian and European markets and possible human health risk. Mar Pollut Bull 46:879-886.
9. Bodin N, Burgeot T, Stanisière JY, Bocquené G, Menard D, Minier C, Boulet I, Amat A, Cherel Y, Budzinski H. 2004. Seasonal variations of a battery of biomarkers and physiological indices for the mussel Mytilus galloprovincialis transplanted into the northwest Mediterranean Sea. Comp Biochem Physiol 138:411-427.
10. Cajaraville MP, Bebianno MJ, 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. Sci Total Environ 247:295-311.
11. Cancio I, Ibabe A, Cajaraville MP. 1999. Seasonal variation of perosixomal enzyme activities and peroxisomal structure in mussels Mytilus galloprovincialis and its relationship with the lipid content. Comp Biochem Physiol 123:135-144.
12. Canova S, Degan P, Peters LD, Livingstone DR, Voltan R, Venier P. 1998. Tissue dose. DNA adducts, oxidative DNA damage and CYP1A-immunopositive proteins in mussels exposed to waterborne benzo[a]pyrene. Mutat Res 399:17-30.
13. Chaudière J, Ferrari-Iliou R. 1999. Intracellular antioxidants: From chemical to biochemical mechanisms. Food Chem Toxicol 37:949-962.
14. Cheung CCC, Zheng GJ, Li AMY, Richardson BJ, Lam PKS. 2001. Relantionships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels. Perna viridis. Aquatic Toxicol 52:189-203.
15. Chícharo L, Chícharo MA. 2001. Effects of environmental conditions on planktonic abundances, benthic recruitment and growth rates of the bivalve mollusc Ruditapes decussatus in a Portuguese coastal lagoon. Fisheries Res 53:235-250.
16. Coelho MR, Bebianno MJ, Lansgton WJ. 2002. Organotin levels in the Ria Formosa lagoon, Portugal. Appl Organomet Chem 16:384-390.
17. 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 45:106-121.
18. De Luca-Abbott SB, Richardson BJ, McClellan KE, Zheng GJ, Martin M, Lam PKS. 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.
19. Dellali M, Gnassia-Barelli M, Roméo M, Aissa P. 2001. The use of acetylcholinesterase activity in Ruditapes decussatus and Mytilus galloprovincialis in the biomonitoring of Bizerta lagoon. Comp Biochem Physiol 130:227-235.
20. den Besten PJ. 1998. Concepts for the implementation of biomarkers in environmental monitoring. Mar Environ Res 46:253-256.
21. Doyotte A, Cossu C, Jacquin M, Babut M, Vasseur P. 1997. Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquatic Toxicol 39:93-110.
22. Erdelmeier I, Gérard-Monnier D, Yadan JC, Chaudière J. 1998. Reactions of N-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Mechanistic aspects of the colorimetric assay of lipid peroxidation. Chem Res Toxicol 11:1184-1194.
23. Ferreira AM, Vale C. 1998. PCB accumulation and alterations of lipids in two length classes of the oyster Crassostrea angulata and of the clam Ruduapes decussatus. Mar Environ Res 45:259-268.
24. Fisher SW, Hwang H, Atanasoff M, Landrum PF. 1999. Lethal body residues for pentachlorophenol in zebra mussels (Dreissena polymorpha) under varying conditions of temperature and pH. Ecotoxicol Environ Saf 43:274-283.
25. French PW. 1998. The impact of coal production on the sediment record of the Sevem Estuary. Environ Pollut 103:37-43.
26. Gamble SC, Goldfarb PS, Porte C, Livingstone DR. 1995. Glutathione peroxidase and other antioxidant enzyme function in marine invertebrates (Mytilus edulis, Pacten maximus, Carcinus maenas and Asterias rubens). Mar Environ Res 39:191-195.
27. Geret F, Bebianno MJ. 2004. Does zinc produce reactive oxygen species in Ruditapes decussatus? Ecotoxicol Environ Saf 57:399-409.
28. Geret F, Serafim A, Barreira L, Bebianno MJ. 2002a. Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussatus. Biomarkers 7:242-256.
29. Geret F, Serafim A, Barreira L, Bebianno MJ. 2002b. Response of antioxidant systems to copper in the gills of the clam Ruditapes decussatus. Mar Environ Res 54:413-417.
30. Geret F, Serafim A, Bebianno MJ. 2003. Antioxidant enzyme activities, metallothioneins and lipid peroxidation as biomarkers in Ruditapes decussatus? Ecotoxicology 12:417-426.
31. Goldberg ED, Bertine KK. 2000. Beyond the mussel watch-New directions for monitoring marine pollution. Sci Total Environ 247:165-174.
32. Greenwald RA. 1985. Handbook of Methods for Oxygen Radical Research. Boca Raton, FL: CRC Press. 447 p.
33. Halliwell B. 1996. Antioxidants in human health and disease. Ann Rev Nutr 16:33-50.
34. Halliwell B, Gutteridge JMC. 1986. Oxygen free radicals and iron in relation to biology and medicine: Some problems and concepts. Arch Biochem Biophys 246:501-514.
35. Lawrence RA, Burk RF. 1976. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952-958.
36. Lemaire P, Matthews A, Förlin L, Livingstone DR. 1994. Stimulation of oxyradical production of hepatic microsomes of flounder (Platichthys flesus) and perch (Perca fluviatilis) by model and pollutant xenobiotics. Arch Environ Contam Toxicol 26:191-200.
37. Lesser MP. 2006. Oxidative stress in marine environments: Biochemistry and physiological ecology. Ann Rev Phys 68:6.1-6.26.
38. Lionetto MG, Caricato R, Giordano ME, Pascariello MF, Marinosi 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. Mar Pollut Bull 46:324-330.
39. Livingstone DR, Martinez PG, Winston GW. 1989. Menadione-stimulated oxyradical formation in digestive gland microsomes of the common mussel, Mytilus edulis L. Aquatic Toxicol 15:213-236.
40. Livingstone DR, Martinez PG, Michel X, Narbonne JF, O'Hara S, Ribera D, Winston GW. 1990. Oxyradical production as a pollution-mediated mechanism of toxicity in the common mussel, Mytilus edulis L., and other molluscs. Funct Ecol 4:415-424.
41. Livingstone DR, Lips F, Martinez PG, Pipe RK. 1992. Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar Biol 112:265-276.
42. Livingstone DR, Lemaire P, Matthews A, Peters LD, Porte C, Fitzpatrick PJ, Förlin L, Nasci C, Fossato V, Wootton N, Goldfarb P. 1995. Assessment of the impact of organic pollutants on goby (Zosterissor ophiocephalus) and mussel (Mytilus galloprovincialis) from the Venice Lagoon, Italy: Biochemical studies. Mar Environ Res 39:235-240.
43. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin Phenol reagent. J Biol Chem 193:265-275.
44. McCord JM, Fridovich I. 1969. Superoxide dismutase: An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049-6055.
45. Moore MN, Depledge MH, Readman JW, Leonard DRP. 2004. An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res 552:247-268.
46. Moraga D, Mdelgi-Lasram E, Romdhane MS, 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.
47. Nasci C, Ros L, Campesan G, Fossato VU. 1998. Assessment of the impact of chemical pollutants on mussel. Mytilus galloprovincialis, from the Venice Lagoon, Italy. Mar Environ Res 461:279-282.
48. Nasci C, Ros L, Campesan G, Vleet ES, Salizzato M, Sperni L, Pavoni B. 1999. Clam transplantation and stress-related biomarkers as useful tools for assessing water quality in coastal environments. Mar Pollut Bull 39:255-260.
49. Nasci C, Da Ros L, Nesto N, Sperni L, Passarini F, Pavoni B. 2000. Biochemical and histochemical responses to environmental contaminants in clams. Tapes philippinarum, transplanted to different polluted areas of Venice Lagoon, Italy. Mar Environ Res 50:425-430.
50. Newton A, Mudge SM. 2003. Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuarine, Coastal and Shelf Science. 57:73-85.
51. Ohnishi S, Kawanishi S. 2002. Double base lesions of DNA by a metabolite of carcinogenic benzo[a]pyrene. Biochem Biophys Res Commun 290:778-782.
52. Orbea A, Marigomez I, Fernandez C, Tarazona JV, Cancio I, Cajaraville MP. 1999. Structure of peroxisomes and activity of the marker enzyme catalase in digestive epithelial cells in relation to PAH content in mussels from two Basque estuaries (Bay of Biscay): Seasonal and site-specific. Arch Environ Contam Toxicol 36:158-166.
53. Orbea A, Fahimi HD, Cajaraville MP. 2000. Immunolocalization of four antioxidant enzymes in digestive glands of molluscs and crustaceans and fish liver. Histochem Cell Biol 114:393-404.
54. Orbea A, Ortiz-Zarragoitia M, Solé M, Porte C, Cajaraville MP. 2002. Antioxidant enzymes and peroxisome proliferation in relation to contaminant body burdens of PAHs and PCBs in bivalve molluscs, crabs and fish from the Urdaibai and Plentzia estuaries (Bay of Biscay). Aquatic Toxicol 58:75-98.
55. Porte C, Solé M, Albaigés J, Livingstone DR. 1991. Responses of mixed-function oxygenase and antioxidase system of Mytilus sp. to organic pollution. Comp Biochem Physiol 100:183-186.
56. Porte C, Biosca X, Solé M, Pastor D, Albaigés J. 1996. The Aegean Sea oil spill one year after: Petroleum hydrocarbons and biochemical responses in marine bivalves. Mar Environ Res 42:404-405.
57. Porte C, Morcillo Y, Solé M. 1998. Evaluation of a suite of biomarkers of exposure in clams transplanted to a tributyltin-polluted environment. Mar Environ Res 46:329-330.
58. Porte C, Biosca X, Pastor D, Solé M, Albaigés J. 2000. The Aegean sea oil spill. II. Temporal study of the hydrocarbons accumulation in bivalves. Environ Sci Technol 34:5067-5075.
59. Power A, Sheehan D. 1996. Seasonal variation in the antioxidant defence systems of gill and digestive gland of the blue mussel, Mytilus edulis. Comp Biochem Physiol 114C:99-103.
60. Regoli F, Nigro M, Orlando E. 1998. Lysosomal and antioxidant responses to metals in the Antarctic scallop Adamussium colbecki. Aquatic Toxicol 40:375-392.
61. Rodríguez-Ariza A, Rodríguez-Ortega MJ, Marenco JL, Amezcua O, Alhama J, López-Barea J. 2003. Uptake and clearance of PCB congeners in Chamaelea gallina: Response of oxidative stress biomarkers. Comp Biochem Physiol 134:57-67.
62. Roméo M, Gnassia-Barelli M. 1995. Metal distribution in different tissues and in subcellular fractions of the Mediterranean clam Ruditapes decussatus treated with cadmium, copper, or zinc. Comp Biochem Physiol 111:457-463.
63. Schneider K, Roller M, Kalberlah F, Schuhmacher-Wolz U. 2002. Cancer risk assessment for oral exposure to PAH mixtures. J Appl Toxicol 22:73-83.
64. Serafim MA, Bebianno MJ. 2001. Variation of metallothionein and metal concentrations in the digestive gland of the clam Ruditapes decussatus: Sex and seasonal effects. Environ Toxicol Chem 20:544-552.
65. Smaoui-Damak W, Hamza-Chaffai A, Bebianno MJ, Amiard JC. 2004. Variation of metallothioneins in gills of the clam Ruditapes decussatus from the Gulf of Gabès (Tunisia). Comp Biochem Physiol 139:181-188.
66. Sobral P, Widdows J. 1997. Effects of elevated temperatures on the scope for growth and resistance to air exposure of the clam Ruditapes decussatus (L.), from southern Portugal. Sci Mar 61:163-171.
67. Solé M. 2000. Effects of tributyltin on the MFO system of the clam Ruditapes decussata: A laboratory and field approach. Comp Biochem Physiol 125:93-101.
68. Solé M, Porte C, Albaigés J. 1994. Mixed function oxygenase system components and antioxidant enzymes in different marine bivalves: Its relation with contaminant body burdens. Aquatic Toxicol 30:271-283.
69. Solé M, Porte C, Albaigés J. 1995. Seasonal variations in the mixed-function oxygenase system components and antioxidant enzymes of the mussel Mytilus galloprovincialis. Environ Toxicol Chem 14:157-164.
70. Solé M, Porte C, Barceló D, Albaigés J. 2000. Bivalve residue analysis for the assessment of coastal pollution in the Ebro Delta (NW Mediterranean). Mar Pollut Bull 40:746-753.
71. Solé M, Porte C, Biosca X, Mitchelmore CL, Chipman JK, Livingstone DR, Albaigés J. 1996. Effects of the "Aegean Sea" oil spill on biotransformation enzymes, oxidative stress and dna-adducts in digestive gland of the mussel (Mytilus edulis L.). Comp Biochem Physiol 113C:257-265.
72. Urrutia MB, Ibarrola I, Iglesias JIP, Navarro E. 1999. Energetics of growth and reproduction in a high-tidal population of the clam Ruditapes decussatus from Urdaibai Estuary (Basque Country, N. Spain). J Sea Res 42:35-48.
73. Viarengo A, Canesi L, Pertica M, Livingstone DR. 1991. Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Comp Biochem Physiol 100C:187-190.
74. Vidal M-L, Bassères A, Narbonne J-F. 2002a. Influence of temperature, pH, oxygenation, water-type and substrate on biomarker responses in the freshwater clam Corbicula fluminea (Müller). Comp Biochem Physiol 132:93-104.
75. Vidal M-L, Bassères A, Narbonne J-F. 2002b. Seasonal variation of pollution biomarkers in two populations of Corbicula fluminea (Müller). Comp Biochem Physiol 131:133-151.
76. Wilhelm-Filho D, Tribess T, Gáspari C, Claudio FD, Torres MA, Magalhães ARM. 2001. Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture 203:149-158.