A multibiomarker approach to the assessment of pollution impacts in two Baltic Sea coastal areas in Sweden using caged mussels (Mytilus trossulus)

Science of the Total Environment

Volumn 473-474, Issue , 2014, Pages 398-409

  Turja, R ^a   Hoher N ^b   Snoeijs, P ^c   Barsiene J ^d   Butrimaviciene L ^d   Kuznetsova, T ^e   Kholodkevich, S V ^e,f   Devier, M H ^g   Budzinski, H ^g   Lehtonen, K K ^a  

^a FINNISH INSTITUTE OF MARINE RESEARCH   (Finland)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d Institute of Ecology   (Lithuania)

^e RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^f ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^g UNIVERSITÉ BORDEAUX 1   (France)

Author keywords

Baltic Sea; Biomarkers; Contamination; Mussel caging; Mytilus trossulus

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; BIOMARKERS; COASTAL ZONES; CONTAMINATION; HEART; POLYCYCLIC AROMATIC HYDROCARBONS; PRINCIPAL COMPONENT ANALYSIS;

BALTIC SEA; BIOTRANSFORMATION ACTIVITY; INTEGRATED BIOMARKER RESPONSE; LYSOSOMAL MEMBRANE STABILITIES; MULTI-BIOMARKER APPROACHES; MUSSEL CAGING; MYTILUS TROSSULUS; ORGANOCHLORINE PESTICIDES;

MOLLUSCS;

GLUTATHIONE TRANSFERASE; ORGANOCHLORINE DERIVATIVE; ORGANOTIN COMPOUND; PESTICIDE; POLYCYCLIC AROMATIC HYDROCARBON; THIAMINE; TRACE METAL;

ANTIOXIDANT; BIOMARKER; BIOTRANSFORMATION; COASTAL ZONE; ENZYME ACTIVITY; MARINE POLLUTION; MOLLUSC; ORGANOTIN COMPOUND; PAH; PESTICIDE; POLLUTION EFFECT; PRINCIPAL COMPONENT ANALYSIS; TRACE ELEMENT;

ARTICLE; BALTIC SEA; BIOENERGY; BIOTRANSFORMATION; CYTOTOXICITY; DRUG TISSUE LEVEL; ENVIRONMENTAL IMPACT; ENZYME ACTIVITY; GENOTOXICITY; HEART RATE; LYSOSOME MEMBRANE; MUSSEL; MYTILUS; MYTILUS TROSSULUS; NEUROTOXICITY; NONHUMAN; PHAGOCYTOSIS; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; SEASHORE; SWEDEN; WATER POLLUTION;

ATLANTIC OCEAN; BALTIC SEA; BOTHNIAN SEA; GULF OF BOTHNIA;

LONCHOCARPUS GLAUCIFOLIUS; MYTILUS EDULIS; MYTILUS TROSSULUS;

BALTIC SEA; BIOMARKERS; CONTAMINATION; MUSSEL CAGING; MYTILUS TROSSULUS;

ACETYLCHOLINESTERASE; ANIMALS; BIOLOGICAL MARKERS; CATALASE; ENVIRONMENTAL MONITORING; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HYDROCARBONS, CHLORINATED; LIPID PEROXIDATION; MYTILUS; ORGANOTIN COMPOUNDS; POLYCYCLIC HYDROCARBONS, AROMATIC; SUPEROXIDE DISMUTASE; SWEDEN; WATER POLLUTANTS, CHEMICAL;

EID: 84891366337     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2013.12.038     Document Type: Article

References (101)

1. Balk L., Hagerroth P., Akerman G., Hanson M., Tjarnlund U., Hansson T., et al. Wild birds of declining European species are dying from a thiamine deficiency syndrome. Proc Natl Acad Sci U S A 2009, 106:12001-12006.
2. Bamber S.D., Depledge M.H. Evaluation of changes in the adaptive physiology of shore crabs (Carcinus maenas) as an indicator of pollution in estuarine environments. Mar Biol 1997, 129:667-672.
3. Banni M., Negri A., Dagnino A., Jebali J., Ameur S., Boussetta H. Acute effects of benzo[a]pyrene on digestive gland enzymatic biomarkers and DNA damage on mussel Mytilus galloprovincialis. Ecotoxicol Environ Saf 2010, 73:842-848.
4. Baršienė J., Lazutka J., Syvokiene J., Dedonyte V., Rybakovas A., Bagdonas E., et al. Analysis of micronuclei in blue mussels and fish from the Baltic and North Seas. Environ Toxicol 2004, 19:365-371.
5. Baršienė J., Schiedek D., Rybakovas A., Syvokiene J., Kopecka J., Forlin L. Cytogenetic and cytotoxic effects in gill cells of the blue mussel Mytilus spp. from different zones of the Baltic Sea. Mar Pollut Bull 2006, 53:469-478.
6. Baumard P., Budzinski H., Garrigues P. Analytical procedure for the analysis of PAHs in biological tissues by gas chromatography coupled to mass spectrometry: application to mussels. Fresenius J Anal Chem 1997, 359:502-509.
7. Beliaeff B., Burgeot T. Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 2002, 21:1316-1322.
8. Bettendorff L., Wins P. Thiamin diphosphate in biological chemistry: new aspects of thiamin metabolism, especially triphosphate derivatives acting other than as cofactors. FEBS J 2009, 276:2917-2925.
9. Bocquene G., Galgani F. Biological effects of contaminants: cholinesterase inhibition by organophosphate and carbamate compounds. ICES Tech Mar Environ Sci 1998, 22:12.
10. Box A., Sureda A., Galgani F., Pons A., Deudero S. Assessment of environmental pollution at Balearic Islands applying oxidative stress biomarkers in the mussel Mytilus galloprovincialis. Comp Biochem Physiol C Toxicol Pharmacol 2007, 146:531-539.
11. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
12. Broeg K., Lehtonen K.K. Indices for the assessment of environmental pollution of the Baltic Sea coasts: Integrated assessment of a multi-biomarker approach. Mar Pollut Bull 2006, 53:508-522.
13. Brooks S., Harman C., Zaldibar B., Izagirre U., Glette T., Marigomez I. 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 2011, 62:327-339.
14. Brown S.B., Honeyfield D.C., Vandenbyllaardt L. Thiamine analysis in fish tissues. Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea 1998, 21:73-81.
15. Cajaraville M.P., Olabarrieta I., Marigomez I. In vitro activities in mussel hemocytes as biomarkers of environmental quality: a case study in the Abra Estuary (Biscay Bay). Ecotoxicol Environ Saf 1996, 35:253-260.
16. Carlberg I., Mannervik B. Purification and characterization of flavoenzyme glutathione reductase from rat liver. J Biol Chem 1975, 250:5475-5480.
17. Claiborne A. Catalase activity. Handbook of methods for oxygen radical research 1985, 283-284. CRC Press, Boca Raton. R.A. Greenwald (Ed.).
18. Curtis T.M., Williamson R., Depledge M.H. Simultaneous, long-term monitoring of valve and cardiac activity in the blue mussel Mytilus edulis exposed to copper. Mar Biol 2000, 136:837-846.
19. Damiens G., Gnassia-Barelli M., Loques F., Romeo M., Salbert V. Integrated biomarker response index as a useful tool for environmental assessment evaluated using transplanted mussels. Chemosphere 2007, 66:574-583.
20. Davies I.M., Vethaak A.D. Integrated marine environmental monitoring of chemicals and their effects. ICES Cooperative Research Report No. 315 2012, [277 pp.].
21. De Coen W.M., Janssen C.R. The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Environ Toxicol Chem 2003, 22:1632-1641.
22. Depeint F., Bruce W.R., Shangari N., Mehta R., O'Brien P.J. Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem Biol Interact 2006, 163:94-112.
23. Depledge M.H., Andersen B.B. A computer-aided physiological monitoring-system for continuous, long-term recording of cardiac activity in selected invertebrates. Comp Biochem Physiol A Physiol 1990, 96:473-477.
24. Devier M.H., Augagneur S., Budzinski H., Le Menach K., Mora P., Narbonne J.F., et al. One-year monitoring survey of organic compounds (PAHs, PCBs, TBT), heavy metals and biomarkers in blue mussels from the Arcachon Bay, France. J Environ Monit 2005, 7:224-240.
25. Erk M., Ivankovic D., Strizak Z. Cellular energy allocation in mussels (Mytilus galloprovincialis) from the stratified estuary as a physiological biomarker. Mar Pollut Bull 2011, 62:1124-1129.
26. Fernandez B., Campillo J.A., Martinez-Gomez C., Benedicto J. Antioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomarkers of environmental stress along the Spanish Mediterranean coast. Aquat Toxicol 2010, 99:186-197.
27. Fernandez B., Antonio Campillo J., Martinez-Gomez C., Benedicto J. Micronuclei and other nuclear abnormalities in mussels (Mytilus galloprovincialis) as biomarkers of cyto-genotoxic pollution in Mediterranean waters. Environ Mol Mutagen 2011, 52:479-491.
28. Galloway T.S., Depledge M.H. Immunotoxicity in invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 2001, 10:5-23.
29. Gibson G., Barclay L., Blass J. The role of the cholinergic system in thiamin deficiency. Ann N Y Acad Sci 1982, 378:382-403.
30. Giron-Perez M. Relationships between innate immunity in bivalve molluscs and environmental pollution. Invertebr Surviv J 2010, 7:149-156.
31. Gliszczynska-Swiglo A. Antioxidant activity of water soluble vitamins in the TEAC (trolox equivalent antioxidant capacity) and the FRAP (ferric reducing antioxidant power) assays. Food Chem 2006, 96:131-136.
32. Gnaiger E. Heat dissipation and energetic efficiency in animal anoxibiosis -economy contra power. J Exp Zool 1983, 228:471-490.
33. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases -first enzymatic step in mercapturic acid formation. J Biol Chem 1974, 249:7130-7139.
34. Hagger J.A., Jones M.B., Lowe D., Leonard D.R.P., Owen R., Galloway T.S. Application of biomarkers for improving risk assessments of chemicals under the Water Framework Directive: a case study. Mar Pollut Bull 2008, 56:1111-1118.
35. Hall L.W., Anderson R.D. The influence of salinity on the toxicity of various classes of chemicals to aquatic biota. Crit Rev Toxicol 1995, 25:281-346.
36. HELCOM Baltic Sea Action Plan HELCOM Ministerial Meeting, Krakow, Poland, 15 November 2007 [Last accessed 10th of August 2013]. http://www.helcom.fi/BSAP/ActionPlan/en_GB/ActionPlan/.
37. HELCOM Hazardous substances in the Baltic Sea An integrated thematic assessment of hazardous substances in the Baltic Sea. Baltic Sea Environmental Process Series 2010, 120B.
38. HELCOM Hazardous substances of specific concern to the Baltic Sea Final report of the HAZARDOUS project. Baltic Sea Environment Process Series 2009, 119.
39. Höher N., Köhler A., Strand J., Broeg K. Effects of various pollutant mixtures on immune responses of the blue mussel (Mytilus edulis) collected at a salinity gradient in Danish coastal waters. Mar Environ Res 2012, 75:35-44.
40. Johannesson K., Andre C. Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 2006, 15:2013-2029.
41. Johannesson K., Smolarz K., Grahn M., Andre C. The future of Baltic Sea populations: local extinction or evolutionary rescue?. Ambio 2011, 40:179-190.
42. John S., Kale M., Rathore N., Bhatnagar D. Protective effect of vitamin E in dimethoate and malathion induced oxidative stress in rat erythrocytes. J Nutr Biochem 2001, 12:500-504.
43. Karlsson M., Malmaeus M., Baresel C., Sivard Å., Ericsson T., Grahn O. Kostnadseffectivitet i åtgärder mot övergödning i Östersjön - Fallstudie Gävle fjärdar. IVL Rapport B2078 2012.
44. Kautsky N. Growth and size structure in a Baltic Mytilus edulis population. Mar Biol 1982, 68:117-133.
45. Kholodkevich S.V., Ivanov A.V., Kurakin A.S., Kornienko E.L., Fedotov V.P. Real time biomonitoring of surface water toxicity level at water supply stations. J Environ Bioindic 2008, 3:23-34.
46. Kholodkevich S.V., Kuznetsova T.V., Trusevich V.V., Kurakin A.S., Ivanov A.V. Peculiarities of valve movement and of cardiac activity of the bivalve mollusc Mytilus galloprovincialis at various stress actions. J Evol Biochem Physiol 2009, 45:524-526.
47. Kholodkevich S.V., Kuznetsova T.V., Lehtonen K.K., Kurakin A.S. Experiences on ecological status assessment of the Gulf of Bothnia different sites based on cardiac activity biomarkers of caged mussels (Mytilus edulis). ICES Annual Science Conference 2011, 19-23 September, Gdansk, Poland 2011, http://www.ices.dk/products/CMdocs/CM-2011/R/R2011.pdf.12p.
48. Koivisto M.E., Westerbom M. Habitat structure and complexity as determinants of biodiversity in blue mussel beds on sublittoral rocky shores. Mar Biol 2010, 157:1463-1474.
49. Kube S., Gerber A., Jansen J.M., Schiedek D. Patterns of organic osmolytes in two marine bivalves, Macoma balthica, and Mytilus spp., along their European distribution. Mar Biol 2006, 149:1387-1396.
50. Kuznetsova T.V., Sladkova G.V., Kholodkevich S.V. Evaluation of functional state of crayfish Pontastacus leptodactylus in normal and toxic environment by characteristics of their cardiac activity and hemolymph biochemical parameters. J Evol Biochem Physiol 2010, 46:241-250.
51. Leiniö S., Lehtonen K.K. Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea. Comp Biochem Physiol C Toxicol Pharmacol 2005, 140:408-421.
52. Lima I., Moreira S.M., Rendon-Von Osten J., Soares A.M.V.M., Guilhermino L. Biochemical responses of the marine mussel Mytilus galloprovincialis to petrochemical environmental contamination along the North-western coast of Portugal. Chemosphere 2007, 66:1230-1242.
53. Livingstone D.R. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 2001, 42:656-666.
54. Lockwood B.L., Somero G.N. Transcriptomic responses to salinity stress in invasive and native blue mussels (genus Mytilus). Mol Ecol 2011, 20:517-529.
55. Lowe D.M., Pipe R.K. Contaminant induced lysosomal membrane damage in marine mussel digestive Cells -an in vitro study. Aquat Toxicol 1994, 30:357-365.
56. Lukienko P.I., Mel'nichenko N.G., Zverinskii I.V., Zabrodskaya S.V. Antioxidant properties of thiamine. Bull Exp Biol Med 2000, 130:874-876.
57. Mancinelli R., Ceccanti M., Guiducci M.S., Sasso G.F., Sebastiani G., Attilia M.L., et al. Simultaneous liquid chromatographic assessment of thiamine, thiamine monophosphate and thiamine diphosphate in human erythrocytes: a study on alcoholics. J Chromatogr B Analyt Technol Biomed Life Sci 2003, 789:355-363.
58. Marabini L., Calo R., Fucile S. Genotoxic effects of polychlorinated biphenyls (PCB 153, 138, 101, 118) in a fish cell line (RTG-2). Toxicol in Vitro 2011, 25:1045-1052.
59. Mccord J.M., Fridovich I. Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 1969, 244:6049.
60. Moore M.N., Depledge M.H., Readman J.W., Leonard D.R.P. An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res Fund Mol Mech Mutag 2004, 552:247-268.
61. Moore M.N., Allen J.I., McVeigh A. Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 2006, 61:278-304.
62. Moore M.N., Viarengo A., Donkin P., Hawkins A.J.S. Autophagic and lysosomal reactions to stress in the hepatopancreas of blue mussels. Aquat Toxicol 2007, 84:80-91.
63. Moreira S., Guilhermino L. The use of Mytilus galloprovincialis acetylcholinesterase and glutathione S-transferases activities as biomarkers of environmental contamination along the northwest Portuguese coast. Environ Monit Assess 2005, 105:309-325.
64. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem J 2009, 417:1-13.
65. Neufeld D.S., Wright S.H. Response of cell volume in Mytilus gill to acute salinity change. J Exp Biol 1996, 199:473-484.
66. Nigro M., Falleni A., Del Barga I., Scarcelli V., Lucchesi P., Regoli F., et al. Cellular biomarkers for monitoring estuarine environments: transplanted versus native mussels. Aquat Toxicol 2006, 77:339-347.
67. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979, 95:351-358.
68. Oruc E.O., Usta D. Evaluation of oxidative stress responses and neurotoxicity potential of diazinon in different tissues of Cyprinus carpio. Environ Toxicol Pharmacol 2007, 23:48-55.
69. Owens T.G., King F.D. Measurement of respiratory electron transport system activity in marine zooplankton. Mar Biol 1975, 30:27-36.
70. Perez D.G., Fontanetti C.S. Hemocitical responses to environmental stress in invertebrates: a review. Environ Monit Assess 2011, 177:437-447.
71. Pinto E., Pedersen M., Snoeijs P., Van Nieuwerburgh L., Colepicolo P. Simultaneous detection of thiamine and its phosphate esters from microalgae by HPLC. Biochem Biophys Res Commun 2002, 291:344-348.
72. Pipe R.K., Coles J.A. Environmental contaminants influencing immune function in marine bivalve mollusks. Fish Shellfish Immunol 1995, 5:581-595.
73. Prevodnik A., Lija K., Bollner T. Effects of copper and cadmium on protein expression in Baltic sea blue mussels (Mytilus edulis sp.). Mar Environ Res 2006, 62:S90-S91.
74. Raftopoulou E.K., Dimitriadis V.K. Assessment of the health status of mussels Mytilus galloprovincialis along Thermaikos Gulf (Northern Greece): an integrative biomarker approach using ecosystem health indices. Ecotoxicol Environ Saf 2010, 73:1580-1587.
75. Regoli F., Frenzilli G., Bocchetti R., Annarumma F., Scarcelli V., Fattorini D., et al. Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment. Aquat Toxicol 2004, 68:167-178.
76. Riginos C., Cunningham C.W. Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol 2005, 14:381-400.
77. Rola R.C., Monteiro MdC, da Silva Reis S.R., Sandrini J.Z. Molecular and biochemical biomarkers responses in the mussel Mytilus edulis collected from Southern Brazil coast. Mar Pollut Bull 2012, 64:766-771.
78. Romeo M., Hoarau P., Garello G., Gnassia-Barelli M., Girard J.P. Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environ Pollut 2003, 122:369-378.
79. Santos L.H.M.L.M., Araujo A.N., Fachini A., Pena A., Delerue-Matos C., Montenegro M.C.B.S.M. Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mater 2010, 175:45-49.
80. Serafim A., Lopes B., Company R., Cravo A., Gomes T., Sousa V., et al. A multi-biomarker approach in cross-transplanted mussels Mytilus galloprovincialis. Ecotoxicology 2011, 20:1959-1974.
81. Shagirtha K., Muthumani M., Prabu S.M. Melatonin abrogates cadmium induced oxidative stress related neurotoxicity in rats. Eur Rev Med Pharmacol Sci 2011, 15:1039-1050.
82. Sheehan D., Meade G., Foley V.M., Dowd C.A. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 2001, 360:1-16.
83. Shumway S.E., Gabbott P.A., Youngson A. Effect of fluctuating salinity on concentrations of free amino-acids and ninhydrin-positive substances in adductor muscles of 8 species of bivalve mollusks. J Exp Mar Biol Ecol 1977, 29:131-150.
84. Smolders R., Bervoets L., De Coen W., Blust R. Cellular energy allocation in zebra mussels exposed along a pollution gradient: linking cellular effects to higher levels of biological organization. Environ Pollut 2004, 129:99-112.
85. Sokolova I.M., Frederich M., Bagwe R., Lannig G., Sukhotin A.A. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 2012, 79:1-15.
86. Sternbeck J. Vilka kemiska ämnen har påträffats i hav och kust inom det nationella screeningprogrammet?. WSP Rapport 2009.
87. Stohs S.J., Bagchi D., Hassoun E., Bagchi M. Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 2001, 20:77-88.
88. Strange K. Cellular volume homeostasis. Adv Physiol Educ 2004, 28:155-159.
89. Tapie N., Budzinski H., Le Menach K. Fast and efficient extraction methods for the analysis of polychlorinated biphenyls and polybrominated diphenyl ethers in biological matrices. Anal Bioanal Chem 2008, 391:2169-2177.
90. Thompson S., Budzinski H. Determination of polychlorinated biphenyls and chlorinated pesticides in environmental biological samples using focused microwave-assisted extraction. Int J Environ Anal Chem 2000, 76:49-60.
91. Tim-Tim A.L.S., Morgado F., Moreira S., Rangel R., Nogueira A.J.A., Soares A.M.M., et al. Cholinesterase and glutathione S-transferase activities of three mollusc species from the NW Portuguese coast in relation to the 'Prestige' oil spill. Chemosphere 2009, 77:1465-1475.
92. Tsangaris C., Kormas K., Strogyloudi E., Hatzianestis I., Neofitou C., Andral B., et al. Multiple biomarkers of pollution effects in caged mussels on the Greek coastline. Comp Biochem Physiol C Toxicol Pharmacol 2010, 151:369-378.
93. Turja R., Soirinsuo A., Budzinski H., Devier M.H., Lehtonen K.K. Biomarker responses and accumulation of hazardous substances in mussels (Mytilus trossulus) transplanted along a pollution gradient close to an oil terminal in the Gulf of Finland (Baltic Sea). Comp Biochem Physiol C Toxicol Pharmacol 2013, 157:80-92.
94. Turrens J.F. Mitochondrial formation of reactive oxygen species. J Physiol Lond 2003, 552:335-344.
95. Väinölä R., Hvilsom M.M. Genetic divergence and a hybrid zone between Baltic and North Sea Mytilus populations (Mytilidae: Mollusca). Biol. J. Linn. Soc. 1991, 43:127-148.
96. Väinölä R., Strelkov P. Mytilus trossulus in Northern Europe. Mar Biol 2011, 158:817-833.
97. Verslycke T., Janssen C.R. Effects of a changing abiotic environment on the energy metabolism in the estuarine mysid shrimp Neomysis integer (Crustacea: Mysidacea). J Exp Mar Biol Ecol 2002, 279:61-72.
98. Vidal-Linan L., Bellas J., Campillo J.A., Beiras R. Integrated use of antioxidant enzymes in mussels, Mytilus galloprovincialis, for monitoring pollution in highly productive coastal areas of Galicia (NW Spain). Chemosphere 2010, 78:265-272.
99. Wang W.-X., Rainbow P.S. Influence of metal exposure history on trace metal uptake and accumulation by marine invertebrates. Ecotoxicol Environ Saf 2005, 61:145-159.
100. Woldegiorgis A., Green J., Remberger M., Kaj L., Brorström-Lundén E. Results from the Swedish screening 2006 -sub report 4: Pharmaceuticals. IVL Report B1751 2007.
101. Yancey P.H. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 2005, 208:2819-2830.