Effect of hypoosmotic stress by low salinity acclimation of Mediterranean mussels Mytilus galloprovincialis on biological parameters used for pollution assessment

Aquatic Toxicology

Volumn 89, Issue 3, 2008, Pages 137-151

  Hamer, Bojan ^a,c   Jakšić, Željko ^a   Pavičić Hamer, Dijana ^a   Perić, Lorena ^a   Medaković, Davorin ^a   Ivanković, Dušica ^a   Pavičić, Jasenka ^a   Zilberberg, Carla ^b,c   Schröder, Heinz C ^c   Müller, Werner E G ^c   Smodlaka, Nenad ^a   Batel, Renato ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Biomarkers; Environmental condition variations; Hypoosmotic stress; Mytilus galloprovincialis; Salinity; Temperature

Indexed keywords

DNA; METALLOTHIONEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; SEA WATER;

ACCLIMATION; ASSESSMENT METHOD; BIOCHEMISTRY; BIOMARKER; BIVALVE; CONCENTRATION (COMPOSITION); ENVIRONMENTAL CHANGE; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESS; MARICULTURE; MARINE POLLUTION; OSMOSIS; SALINITY; SEAWATER; SURVIVAL; TESTING METHOD;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA DETERMINATION; ENVIRONMENTAL FACTOR; ENZYME ACTIVATION; HYPOOSMOTIC STRESS; MARICULTURE; MUSSEL; MYTILUS GALLOPROVINCIALIS; NONHUMAN; OXYGEN CONSUMPTION; POLLUTION MONITORING; PRIORITY JOURNAL; SALINITY; SEA POLLUTION; SEASONAL VARIATION; STATISTICAL SIGNIFICANCE; SUMMER; SURVIVAL; WATER TEMPERATURE; WINTER;

ANIMALS; DNA DAMAGE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENVIRONMENTAL MONITORING; FLUOROMETRY; GILLS; METALLOTHIONEIN; MUSCLE PROTEINS; MYTILUS; OSMOTIC PRESSURE; OXYGEN CONSUMPTION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PRINCIPAL COMPONENT ANALYSIS; SALINITY; SEASONS; SEAWATER;

MYTILUS GALLOPROVINCIALIS;

EID: 50149104396     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2008.06.015     Document Type: Article

References (121)

1. Almada-Villela P.C. The effects of reduced salinity on the shell growth of small Mytilus edulis. J. Mar. Biol. 64 (1984) 171-182
2. Anestis A., Lazou A., Portner H.O., and Michaelidis B. Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R911-R921
3. Apraiz I., Mi J., and Cristobal S. Identification of proteomic signatures of exposure to marine pollutants in mussels (Mytilus edulis). Mol. Cell. Proteomics 5 (2006) 1274-1285
4. Atkinson D.E. In: Vogel H.J. (Ed). Metabolic Regulation (1971), Academic Press, New York 1-21
5. Babarro J.M.F., and de Zwaan A. Influence of abiotic factors on bacterial proliferation and anoxic survival of the sea mussel Mytilus edulis L. J. Exp. Mar. Biol. Ecol. 273 (2002) 33-49
6. Batel R., Jakšić Z., Bihari N., Hamer B., Fafand{combining short stroke overlay}el M., Chauvin C., Schröder H., Müller W.E.G., and Zahn R.K. A microplate assay for DNA damage determination (Fast Micromethod) in cell suspensions and solid tissues. Anal. Biochem. 270 (1999) 195-200
7. Bayne B.L. Measuring the effects of pollution at the cellular and organism level. In: Kullemberg G. (Ed). The Role of the Oceans as a Waste Disposal Option (1986), Riedel, New York, NY 617-634
8. Berger V.J., and Kharazova A.D. Mechanisms of salinity adaptations in marine molluscs. Hydrobiologia 355 (1997) 115-126
9. Bierkens J.G.E.A. Applications and pitfalls of stress-proteins in biomonitoring. Toxicology 153 (2000) 61-72
10. Bierkens J., de Perre W.V., and Maes J. Effect of different environmental variables on the synthesis of HSP70 in Raphidocelis subcapitata. Comp. Biochem. Physiol. C 120 (1998) 29-34
11. Bihari N., Hamer B., Jakšić Z., Fafand{combining short stroke overlay}el M., Mičić M., and Batel R. Application of alkaline elution, Fast Micromethod and flow cytometry in detection of marine contamination. Cell. Mol. Biol. 48 (2002) 373-377
12. Bihari N., Fafand{combining short stroke overlay}el M., Hamer B., and Kralj-Bilen B. PAH content, toxicity and genotoxicity of coastal marine sediments from the Rovinj area, Northern Adriatic, Croatia. Sci. Total Environ. 366 (2006) 602-611
13. Bihari N., Fafandel M., and Piškur V. Polycyclic aromatic hydrocarbons and ecotoxicological characterization of seawater, sediment, and mussel Mytilus galloprovincialis from the Gulf of Rijeka, the Adriatic Sea, Croatia. Arch. Environ. Cont. Toxicol. 52 (2007) 379-387
14. Bocchetti R., and Regoli F. Seasonal variability of oxidative biomarkers, lysosomal parameters, metallothioneins and peroxisomal enzymes in the Mediterranean mussel Mytilus galloprovincialis from Adriatic Sea. Chemosphere 65 (2006) 913-921
15. Bodin N., Burgeot T., Stansiere J.Y., Bocquene G., Menard D., Minier C., Boutet I., Amat A., Cherel Y., and Budzinski H. Seasonal variations of battery of biomarkers and physiological indices for the mussel Mytilus galloprovincialis transplanted into the northwest Mediterranean Sea. Comp. Biochem. Physiol. C 138 (2004) 411-427
16. Bøhle B. Effects of adaptation to reduced salinity on filtration activity and growth of mussels (Mytilus edulis L.). J. Exp. Mar. Biol. Ecol. 10 (1972) 41-47
17. Böhm M., Schröder H.C., Müller I.M., Müller W.E.G., and Gamulin V. The mitogen-activated protein kinase p38 pathway is conserved in metazoans: cloning and activation of p38 of the SAPK2 subfamily from the sponge Suberites domuncula. Biol. Cell 92 (2000) 95-104
18. Böhm M., Hentschel U., Friedrich A., Fieseler L., Steffen R., Gamulin V., Müller I., and Müller W. Molecular response of the sponge Suberites domuncula to bacterial infection. Mar. Biol. 139 (2001) 1037-1045
19. Bonneris E., Perceval O., Masson S., Hare L., and Campbell P.G.C. Subcellular partitioning of Cd, Cu and Zn in tissues of indigenous unionid bivalves living along a metal exposure gradient and links to metal-induced effects. Environ. Pollut. 135 (2005) 195-208
20. Borković S.S., Šaponjić J.S., Pavlović S.Z., Blagojević D.P., Milošević S.M., Kovačević T.B., Radojčić R.M., Spasić M.B., Žikić R.V., and Saičić Z.S. The activity of antioxidant defence enzymes in the mussel Mytilus galloprovincialis from the Adriatic Sea. Comp. Biochem. Physiol. C 141 (2005) 366-374
21. + channels. Neuron 41 (2004) 351-365
22. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
23. Buhagiar A., and Abel P.D. Development of a computer program for analysing toxicity test results-the "Toxicologist" system. In: Abel P.D., and Axiak V. (Eds). Ecotoxicology and the Marine Environment (1990), Ellis Horwood, Chichester, UK
24. Cajaraville M.P., Bebianno M.J., Blasco J., Porte C., Sarasquete C., and Viarengo A. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci. Total Environ. 247 (2000) 295-311
25. Canesi L., Betti M., Ciacci C., Scarpato A., Citterio B., Pruzzo C., and Gallo G. Signaling pathways involved in the physiological response of mussel hemocytes to bacterial challenge: the role of stress-activated p38 MAP kinases. Dev. Comp. Immunol. 26 (2002) 325-334
26. Chelomin V.P., Zakhartsev M.V., Kurilenko A.V., and Belcheva N.N. An in vitro study of the effect of reactive oxygen species on subcellular distribution of deposited cadmium in digestive gland of mussel Crenomytilus grayanus. Aquat. Toxicol. 73 (2005) 181-189
27. 2-induced cytotoxicity. Toxicol. Appl. Pharmacol. 205 (2004) 225-236
28. Conway de Macario E., and Macario A.J.L. Stressors, stress, and survival: overview. Frontiers Biosci. 5 (2000) 780-786. http://www.bioscience.org/2000/v5/d/macario/fulltext.htm (Available from: http://www.bioscience.org/2000/v5/d/macario/fulltext.htm)
29. Cornet M. Effects of seawater salinity fluctuations on primary tissue culture from the mussel Mytilus galloprovincialis. Potential application to detection of seawater genotoxicity. Toxicol. In Vitro 20 (2006) 1500-1505
30. Cosa G., Facsaneanu K.-S., McLean J.R.N., McNamee J.P., and Scaiano J.C. Photophysical properties of fluorescent DNA-dyes bound to single- and double-stranded DNA in aqueous buffered solution. Photochem. Photobiol. 73 (2001) 585-599
31. Davenport J. The isolation response of mussels (Mytilus edulis L.) exposed to falling sea water concentration. J. Mar. Biol. Assoc. UK 59 (1979) 123-132
32. de Vooys C.G.N. Anaerobic metabolism in sublittoral living Mytilus galloprovincialis in the Mediterranean. IV. Role of amino acids in adaptation to low salinities during anaerobiosis and aerobiosis. Comp. Biochem. Physiol. A 100 (1991) 423-431
33. de Vooys C.G.N., and de Zwaan A. The rate of oxygen consumption and ammonia excretion by Mytilus edulis after various periods of exposure to air. Comp. Biochem. Physiol. 60 (1978) 343-347
34. de Zwaan A., and Eertman R.H.M. Anoxic or aerial survival of bivalves and other euryoxyc invertebrates as a useful response to environmental stress-a comprehensive review. Comp. Biochem. Physiol. C 113 (1996) 299-312
35. Dixon D.R., Pruski A.M., Dixon L.R.J., and Jha A.N. Marine invertebrate eco-genotoxicology: a methodological overview. Mutagenesis 17 (2002) 495-507
36. Dolcetti L., and Venier P. Susceptibility to genetic damage and cell types in Mediterranean mussels. Mar. Environ. Res. 54 (2002) 487-491
37. Domouhtsidou G.P., Dailianis S., Kaloyianni M., and Dimitriadis V.K. Lysosomal membrane stability and metallothionein content in Mytilus galloprovincialis (L.), as biomarkers: combination with trace metal concentrations. Mar. Pollut. Bull. 48 (2004) 572-586
38. Dondero F., Piacentini L., Banni M., Rebelo M., Burlando B., and Viarengo A. Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345 (2005) 259-270
39. Dragun Z., Erk M., Raspor B., Ivanković D., and Pavičić J. Metal and metallothionein level in the heat-treated cytosol of gills of transplanted mussels Mytilus galloprovincialis Lmk. Environ. Int. 30 (2004) 1019-1025
40. Eertman R.H.M., Wagenvoort A.J., Hummel H., and Smaal A.C. Survival in air" of the blue mussel Mytilus edulis L. as a sensitive response to pollution-induced environmental stress. J. Exp. Mar. Biol. Ecol. 170 (1993) 179-195
41. Fader S.C., Yu Z., and Spotila J.R. Seasonal variation in heat shock proteins (HSP70) in stream fish under natural conditions. J. Therm. Biol. 19 (1994) 335-341
42. Gabrieldes, G. (Ed.), 1997. The MED POL Biomonitoring Program Concerning the Effects of Pollutants on Marine Organisms Along the Mediterranean Coasts. UNEP (OCA)/MED WG. 132/3. Athens.
43. Gaitanaki C.I., Kefaloyianni E., Marmari A., and Beis I. Various stressors rapidly activate the p38-MAPK signalling pathway in Mytilus galloprovincialis (Lam.). Mol. Cell. Biol. Biochem. 260 (2004) 119-127
44. Geffard A., Amird-Triquet C., and Amiard J.-C. Do seasonal changes affect metallothionein induction by metals in mussels, Mytilus edulis?. Ecotoxicol. Environ. Saf. 61 (2005) 209-220
45. Goldberg E.D. The Mussel Watch-a first step in global marine monitoring. Mar. Pollut. Bull. 6 (1975) 111
46. Gomez-Mendikute A., Elizondo M., Venier P., and Cajaraville M.P. Characterization of mussel gill cells in vivo and in vitro. Cell Tissue Res. 321 (2005) 131-140
47. Gorbi S., Lamberti C.V., Notti A., Benedetti M., Fattorini D., Moltedo G., and Regoli F. An ecotoxicological protocol with caged mussels, Mytilus galloprovincialis, for monitoting the impact of an offshore platform in the Adriatic sea. Mar. Environ. Res. 65 (2008) 34-49
48. Gosling E.M. The Mussel Mytilus: Ecology, Physiology, Genetics and Culture. Developments Aquatic Culture and Fishers' Science vol. 25 (1992), Elsevier Press, Amsterdam/London/New York/Tokyo
49. Guerlet E., Ledy K., Meyer A., and Giamberini L. Towards a validation of a cellular biomarker suite in native and transplanted zebra mussels: a 2-year integrative field study of seasonal and pollution-induced variations. Aquat. Toxicol. 81 (2007) 377-388
50. Hamer B., Pavičić-Hamer D., Müller W.E.G., and Batel R. Stress-70 proteins in marine mussel Mytilus galloprovincialis as biomarkers of environmental pollution: a field study. Environ. Int. 30 (2004) 873-882
51. Hamer B., Najdek M., Blažina M., Radić T., Reifferscheid G., Müller W.E.G., Zahn R.K., and Batel R. Genotoxic sub-lethal injuries, filamentous growth and culturability of Salmonella typhimurium TA1535/pSK1002. Fresenius Environ. Bull. 14 (2005) 625-633
52. Hamer B., Pavičić-Hamer D., Müller W.E.G., Zahn R.K., and Batel R. Detection of stress-70 proteins of mussel Mytilus galloprovincialis using 2D gel electrophoresis: a Proteomics approach. Fresenius Environ. Bull. 14 (2005) 605-611
53. Hellou J., and Law R.J. Stress on stress response of wild mussels, Mytilus edulis and Mytilus trossulus, as an indicator of ecosystem health. Environ. Pollut. 126 (2003) 407-416
54. Helmuth B.S.T., and Hofmann G.E. Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol. Bull. 201 (2001) 374-384
55. Hofmann G.E., Buckley B.A., Place S.P., and Zippay M.L. Molecular chaperones in ectothermic marine animals: biochemical function and gene expression. Integr. Comp. Biol. 42 (2002) 808-814
56. Hylland K. Biological effects in the management of chemicals in the marine environment. Mar. Pollut. Bull. 53 (2006) 614-619
57. ICES WGBEC, 1999. Report of the Working Group on Biological Effects of Contaminants. Influence of Fluctuating Salinity on Responses of Biomarkers to Contaminants. Available from: http://www.ices.dk.
58. Ivanković D., Pavičić J., Erk M., Filipović-Marijić V., and Raspor B. Evaluation of the Mytilus galloprovincialis Lam. digestive gland metallothionein as a biomarker in a long-term field study: seasonal and spatial variability. Mar. Pollut. Bull. 50 (2005) 1303-1313
59. Jakšić Z., and Batel R. DNA integrity determination in marine invertebrates by Fast Micromethod. Aquat. Toxicol. 65 (2003) 361-376
60. Jakšić Z., Batel R., Bihari N., Mičić M., and Zahn R.K. Adriatic coast as a microcosm for global genotoxic marine contamination-a long-term field study. Mar. Pollut. Bull. 50 (2005) 1314-1327
61. Joergensen C.B. Bivalve Filter Feeding: Hydrodynamics, Bioenergetics, Physiology and Ecology vol. 1 (1990), Olsen & Olsen, Fredensborg, Denmark
62. Kefaloyianni E., Gourgou E., Ferle V., Kotsakis E., Gaitanaki C., and Beis I. Acute thermal stress and various heavy metals induce tissue-specific pro- or anti-apoptic events via the p38-MAPK signal transduction pathway in Mytilus galloprovincialis (Lam.). J. Exp. Biol. 208 (2005) 4427-4436
63. Kurz D.J., Decary S., Hong Y., Trivier E., Akhmedov A., and Erusalimsky J.D. Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J. Cell Sci. 117 (2004) 2417-2426
64. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacterlophage T4. Nature 227 (1970) 680-685
65. Legras S., Mouneyrac C., Amiard J.C., Amiard-Triquet C., and Rainbow P.S. Changes in metallothionein concentrations in response to variation in natural factors (salinity, sex, weight) and metal contamination in crabs from a metal-rich estuary. J. Exp. Mar. Biol. Ecol. 246 (2000) 259-279
66. Lucu C., and Pavičić D. Role of seawater concentration and major ions in oxygen consumption rate of isolated gills of the shore crab Carcinus mediterraneus Csrn. Comp. Biochem. Physiol. A 112 (1995) 565-572
67. +-ATPase activity, unsaturated fatty acids and metallothioneins in gills of the shore crab Carcinus aestuarii after dilute seawater acclimation. Comp. Biochem. Physiol. A 149 (2008) 362-372
68. Luedeking A., and Koehler A. Regulation of expression of multixenobiotic resistance (MXR) genes by environmental factors in the blue mussel Mytilus edulis. Aquat. Toxicol. 69 (2004) 1-10
69. Lundebye A.-K., Langston W.J., and Depledge M.H. Stress proteins and condition index as biomarkers of tributyltin exposure and effect in mussels. Ecotoxicology 6 (1997) 127-136
70. MacDonald J.A., and Storey K.B. Identification of a 115 kDa MAP-kinase activated by freezing and anoxic stresses in the marine periwinkle, Littorina littorea. Arch. Biochem. Biophys. 450 (2006) 208-214
71. Manduzio H., Monsinjon T., Galap C., Leboulenger F., and Rocher B. Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat. Toxicol. 70 (2004) 83-93
72. Manduzio H., Rocher B., Durand F., Galap C., and Leboulenger F. The point about oxidative stress in molluscs. Invertebrate Survival J. 2 (2005) 91-104
73. Maret W. Oxidative metal release from metallothionein via zinc-thiol/disulfide interchange. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 237-241
74. Maret W. Zinc and sulfur: a critical biological partnership. Biochemistry 43 (2004) 3301-3309
75. Marigomez I., Orbea A., Olabarrieta I., Etxeberria M., and Cajaraville M.P. Structural changes in the digestive lysosomal system of sentinel mussels as biomarkers of environmental stress in Mussel-Watch programmes. Comp. Biochem. Physiol. C 113 (1996) 291-297
76. McCarthy J.F., and Shugart L.R. Biomarkers of Environmental Contamination (1990), Chelsea, Lewis pp. 205-216
77. Minier C., Borghi V., Moore M.N., and Porte C. Seasonal variation of MXR and stress proteins in the common mussel, Mytilus galloprovincialis. Aquat. Toxicol. 50 (2000) 167-176
78. Monserrat J.M., Martínez P.E., Geracitano L.A., Amado L.L., Martins C.M.G., Pinho G.L.L., Chaves I.S., Ferreira-Cravo M., Ventura-Lima J., and Bianchini A. Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp. Biochem. Physiol. C 146 (2007) 221-234
79. Moore M.N. Cellular responses to pollutants. Mar. Pollut. Bull. 16 (1985) 134-139
80. Mouneyrac C., Amiard-Triquet C., Amiard J.C., and Rainbow P.S. Comparison of metallothionein concentrations and tissue distribution of trace metals in crabs (Pachygrapsus marmoratus) from a metal-rich estuary, in and out of the reproductive season. Comp. Biochem. Physiol. C 129 (2001) 193-209
81. Narbonne J.F., Daubeze M., Clerandeau C., and Garrigues P. Scale of classification based on biochemical markers in mussels: application to pollution monitoring in European coasts. Biomarkers 4 (1999) 415-424
82. Neufeld D.S., and Wright S.H. Response of cell volume in Mytilus gill to acute salinity change. J. Exp. Biol. 199 (1996) 473-484
83. Neufeld G.J., Holiday C.W., and Pritchard J.B. Salinity adaptation of gill Na,K ATPase in the blue crab Callinectes sapidus. J. Exp. Zool. 211 (1980) 215-224
84. Nevo E. Evolution of genome-phenome diversity under environmental stress. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 6233-6240
85. Nicholson S. Ecocytological and toxicological responses to copper in Perna viridis (L.) (Bivalvia: Mytilidae) haemocyte lysosomal membranes. Chemosphere 45 (2001) 399-407
86. +-dependent ATPase activities in Tapes philippinarum and Mytilus galloprovincialis. Toxicol. In Vitro 20 (2006) 1145-1153
87. Parsons P.A. Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol. Rev. 80 (2005) 589-610
88. Parsons P.A. Energetic efficiency under stress underlies positive genetic correlations between longevity and other fitness traits in natural populations. Biogerontology 8 (2007) 55-61
89. Pavičić J., Škreblin M., Raspor B., Branica M., Tušek-Žnidarič M., Kregar I., and Stegnar P. Metal pollution assessment of the marine environment by determination of metal-binding proteins in Mytilus sp. Mar. Chem. 22 (1987) 235-248
90. Pavičić J., Raspor B., and Martinčić D. Quantitative determination of metallothionein-like proteins in mussels: methodological approach and field evaluation. Mar. Biol. 115 (1993) 435-444
91. Pavičić-Hamer D., and Hamer B. Chemical and ecotoxicological quality assessment of the Rovinj costal area, Northern Adriatic, Croatia. 38th CIESM Congress Proceedings, vol. 38 (2007) 302
92. Pérez-Cadahia B., Laffon B., Pasaro E., and Mendez J. Evaluation of PAH bioaccumulation and DNA damage in mussels (Mytilus galloprovincialis) exposed to spilled Prestige crude oil. Comp. Biochem. Physiol. C 138 (2004) 453-460
93. Petrović S., Ozretić B., Krajnović-Ozretić M., and Bobinac D. Lysosomal membrane stability and metallothioneins in digestive gland of mussels (Mytilus galloprovincialis Lam.) as biomarkers in a field study. Mar. Pollut. Bull. 42 (2001) 1373-1378
94. Petrović S., Semenčić L., Ozretić B., and Ozretić M. Seasonal variations of physiological and cellular biomarkers and their use in the biomonitoring of north Adriatic coastal waters (Croatia). Mar. Pollut. Bull. 49 (2004) 713-720
95. Pierce S.K. Invertebrate cell volume control mechanisms: a coordinated use of intracellular amino acids and inorganic ions as osmotic solute. Biol. Bull. 163 (1982) 405-419
96. Prevodnik A., Gardestrom J., Lilja K., Elfwing T., McDonagh B., Petrović N., Tedengren M., Sheehan D., and Bollner T. Oxidative stress in response to xenobiotics in the blue mussel Mytilus edulis L.: evidence for variation along a natural salinity gradient of the Baltic Sea. Aquat. Toxicol. 82 (2007) 63-71
97. Pytharopoulou S., Kouvela E.C., Sazakli E., Leotsinidis M., and Kalpaxis D.L. Evaluation of the global protein synthesis in Mytilus galloprovincialis in marine pollution monitoring: seasonal variability and correlations with other biomarkers. Aquat. Toxicol. 80 (2006) 33-41
98. Rainer S.F., Ivanovici A.M., and Wadley V.A. Effect of reduced salinity on adenylate energy charge in three estuarine molluscs. Mar. Biol. 54 (1979) 91-99
99. Rankin J.C., and Davenport J.A. Techniques in osmoregulatory research. Animal Osmoregulation (1981), Blackie & Son Ltd., Glasgow/London (Chapter 11, pp. 169-184)
100. Schröder H.C., Batel R., Hassanein H.M.A., Lauenroth S., Jenke H.-S., Simat T., Steinhart H., and Müller W.E.G. Correlation between the level of the potential biomarker, heat-shock protein, and the occurrence of DNA damage in the dab, Limanda limanda: a field study in the North Sea and the English Channel. Mar. Environ. Res. 49 (2000) 201-215
101. Schroth W., Ender A., and Schierwater B. Molecular biomarkers and adaptation to environmental stress in Moon Jelly (Aurelia spp.). Mar. Biotechnol. 7 (2005) 449-461
102. Serra R., Isani G., Tramontano G., and Carpene E. Seasonal dependance of cadmium accumulation and Cd-binding proteins in Mytilus galloprovincialis exposed to cadmium. Comp. Biochem. Physiol. C 123 (1999) 165-174
103. Sheehan D., and Power A. Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comp. Biochem. Physiol. C 123 (1999) 193-199
104. Shepard J.L., Olsson B., Tedengren M., and Bradley B.P. Protein expression signatures identified in Mytilus edulis exposed to PCBs, copper and salinity stress. Mar. Environ. Res. 50 (2000) 337-340
105. Supek F., Peharec P., Krsnik-Rasol M., and Šmuc T. Enhanced analytical power of SDS-PAGE using machine learning algorithms. Proteomics 8 (2008) 28-31
106. Thomas R.E., Harris P.M., and Rice S.D. Survival in air of Mytilus trossulus following long-term exposure to spilled Exxon Valdez crude oil in Prince Williams sound. Comp. Biochem. Physiol. C 122 (1999) 147-152
107. Tremblay R., and Pellerin-Massicotte J. Effect of the tidal cycle on lysosomal membrane stability in the digestive gland of Mya arenaria and Mytilus edulis L. Comp. Biochem. Physiol. A 117 (1997) 99-104
108. Tsuchiya M. Mass mortality in a population of the mussel M. edulis L. caused by high temperature on rocky shores. J. Exp. Mar. Biol. Ecol. 66 (1983) 101-111
109. Viarengo A., and Canesi L. Mussels as biological indicators of pollution. Aquaculture 94 (1991) 225-243
110. Viarengo A., and Nott J. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp. Biochem. Physiol. C 104 (1993) 355-372
111. Viarengo A., Mancinelli G., Orunesu M., Martino G., Faranda F., and Mazzucotelli A. Effects of sublethal copper concentrations, temperature, salinity and oxygen levels on calcium content and on cellular distribution of copper in the gills of Mytilus galloprovincialis Lam.: a multifactorial experiment. Mar. Environ. Res. 24 (1988) 227-231
112. Viarengo A., Canesi L., Pertica M., and Livingstone D.R. Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Comp. Biochem. Physiol. C 100 (1991) 187-190
113. Viarengo A., Canesi L., Pertica M., Mancinelli G., Accomando R., Smaal A.C., and Orunesu M. Stress on stress response: a simple monitoring tool in assessment of a general stress syndrome in mussels. Mar. Environ. Res. 39 (1995) 245-248
114. Viarengo A., Ponzano E., Dondero F., and Fabbri R. A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar. Environ. Res. 44 (1997) 69-84
115. Viarengo A., Burlando B., Dondero F., Marro A., and Fabbri R. Metallothionein as a tool in biomonitoring programmes. Biomarkers 4 (1999) 455-466
116. Viarengo A., Burlando B., Cavaletto M., Marchi B., Ponzano E., and Blasco J. Role of metallothionein against oxidative stress in the mussel Mytilus galloprovincialis. Am. J. Physiol. 277 (1999) 1612-1619
117. Vidal M.-L., Basseres A., and Narbonne J.-F. Seasonal variations of pollution biomarkers in two populations of Corbicula fluminea (Müller). Comp. Biochem. Physiol. C 131 (2002) 133-151
118. Widdows J. Physiological indices of stress in Mytilus edulis. J. Mar. Biol. Assoc. UK 58 (1978) 125-142
119. Widdows J., Bayne B.L., Livingstone D.R., Newell R.I.E., and Donkin P. Physiological and biochemical responses of bivalve molluscs to exposure to air. Comp. Biochem. Physiol. A 62 (1979) 301-308
120. Widdows J., Donkin P., Staff F.J., Matthiessen P., Law R.J., Allen Y.T., Thain J.E., Allchin C.R., and Jones B.R. Measurement of stress effects (scope for growth) and contaminant levels in mussels (Mytilus edulis) collected from the Irish Sea. Mar. Environ. Res. 53 (2002) 327-356
121. Zahn R.K., Zahn-Daimler G., Ax S., Reifferscheid G., Waldmann P., Fujisawa H., and Hosokawa M. DNA damage susceptibility and repair in correlation to calendric age and longevity. Mech. Ageing Dev. 119 (2000) 101-112