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)

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 157, Issue 1, 2013, Pages 80-92

  Turja, Raisa ^a   Soirinsuo, Anna ^a   Budzinski, Hélène ^b   Devier, Marie Hélène ^b   Lehtonen, Kari K ^a  

^a FINNISH ENVIRONMENT INSTITUTE   (Finland)

^b INSTITUT DES SCIENCES MOLÉCULAIRES   (France)

Author keywords

Baltic Sea; Biomarkers; Chemical pollution; Low salinity; Mytilus trossulus; Oxidative stress

Indexed keywords

ACETYLCHOLINESTERASE; BIOLOGICAL MARKER; CATALASE; GLUTATHIONE TRANSFERASE; ORGANOTIN COMPOUND; POLYCHLORINATED BIPHENYL; POLYCYCLIC AROMATIC HYDROCARBON; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BALTIC SEA; BIOACCUMULATION; COASTAL WATERS; FEASIBILITY STUDY; FINLAND; LIPID PEROXIDATION; LYSOSOME MEMBRANE; MORPHOMETRICS; MUSSEL; MYTILUS; NONHUMAN; POLLUTION; PRIORITY JOURNAL; SALINITY; SEA POLLUTION; SOFT TISSUE; TISSUE GROWTH;

EID: 84870262488     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2012.09.006     Document Type: Article

References (93)

1. B. Antizar-Ladislao Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review Environ. Int. 34 2008 292 308 (Pubitemid 351232963)
2. A. Antsulevich, N. Maximovich, and I. Vuorinen Populations of the common mussel nearby the Island of Seili (Archipelago Sea, SW Finland) Boreal Environ. Res. 4 1999 367 375 (Pubitemid 129623394)
3. ATSDR Toxicological Profile for Polychlorinated biphenyls (PCBs) 2011 2000
4. J. Barsiene, K.K. Lehtonen, A. Koehler, K. Broeg, P.J. Vuorinen, T. Lang, J. Pempkowiak, J. Yvokien, V. Dedonyte, A. Rybakovas, R. Repecka, H. Vuontisjarvi, and J. Kopecka Biomarker responses in flounder (Platichthys flesus) and mussel (Mytilus edulis) in the Klaipeda-Butinge area (Baltic Sea) Mar. Pollut. Bull. 53 2006 422 436
5. P. Baumard, and H. Budzinski Internal standard quantification method and gas chromatograph mass spectrometer (GC-MS): a reliable tool for polycyclic aromatic hydrocarbon (PAH) quantification in natural matrices Analusis 25 1997 246 252 (Pubitemid 27440227)
6. P. Baumard, H. Budzinski, and P. Garrigues Analytical procedure for the analysis of PAHs in biological tissues by gas chromatography coupled to mass spectrometry: application to mussels Fresenius J. Anal. Chem. 359 1997 502 509 (Pubitemid 127713905)
7. P. Baumard, H. Budzinski, P. Garrigues, H. Dizer, and P.D. Hansen Polycyclic aromatic hydrocarbons in recent sediments and mussels (Mytilus edulis) from the Western Baltic Sea: occurrence, bioavailability and seasonal variations Mar. Environ. Res. 47 1999 17 47 (Pubitemid 28528671)
8. T. Baussant, S. Sanni, G. Jonsson, A. Skadsheim, and J.F. Borseth Bioaccumulation of polycyclic aromatic compounds: 1. Bioconcentration in two marine species and in semipermeable membrane devices during chronic exposure to dispersed crude oil Environ. Toxicol. Chem. 20 2001 1175 1184 (Pubitemid 32861470)
9. A.R. Beaumont, and M.D. Budd High mortality of the larvae of the common mussel at low concentrations of tributyltin Mar. Pollut. Bull. 15 1984 402 405
10. B. Beliaeff, and T. Burgeot Integrated biomarker response: a useful tool for ecological risk assessment Environ. Toxicol. Chem. 21 2002 1316 1322 (Pubitemid 34553287)
11. R. Bocchetti, D. Fattorini, B. Pisanelli, S. Macchia, L. Oliviero, F. Pilato, D. Pellegrini, and F. Regoli Contaminant accumulation and biomarker responses in caged mussels, Mytilus galloprovincialis, to evaluate bioavailability and toxicological effects of remobilized chemicals during dredging and disposal operations in harbour areas Aquat. Toxicol. 89 2008 257 266
12. G. Bocquene, and F. Galgani Biological effects of contaminants: cholinesterase inhibition by organophosphate and carbamate compounds ICES Tech. Mar. Sci. 22 1998 12
13. T. Borchardt Influence of food quantity on the kinetics of cadmium uptake and loss via food and seawater in Mytilus edulis Mar. Biol. 76 1983 67 76 (Pubitemid 14212326)
14. A. Box, A. Sureda, F. Galgani, A. Pons, and S. Deudero Assessment of environmental pollution at Balearic Islands applying oxidative stress biomarkers in the mussel Mytilus galloprovincialis Comp. Biochem. Physiol. C 146 2007 531 539 (Pubitemid 47500151)
15. M. Bradford 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
16. K. Broeg, and K.K. Lehtonen Indices for the assessment of environmental pollution of the Baltic Sea coasts: integrated assessment of a multi-biomarker approach Mar. Pollut. Bull. 53 2006 508 522 (Pubitemid 44397106)
17. H. Budzinski, M. Letellier, S. Thompson, K. LeMenach, and P. Garrigues Combined protocol for the analysis of polycyclic aromatic hydrocarbons (PAHs) and polychlorobiphenyls (PCBs) from sediments using focussed microwave assisted (FMW) extraction at atmospheric pressure Fresenius J. Anal. Chem. 367 2000 165 171
18. I. Carlberg, and B. Mannervik Purification and characterization of flavoenzyme glutathione reductase from rat liver J. Biol. Chem. 250 1975 5475 5480
19. C.C.C. Cheung, W.H.L. Siu, B. Richardson, S.B. De Luca-Abbott, and P.K.S. Lam Antioxidant responses to benzo[a]pyrene and Aroclor 1254 exposure in the green lipped mussel, Perna viridis Environ. Pollut. 128 2004 393 403 (Pubitemid 38064186)
20. A. Claiborne Catalase activity R.A. Greenwald, Handbook of Methods for Oxygen Radical Research 1985 CRC Press Boca Raton 283 284
21. G. Damiens, E. His, M. Gnassia-Barelli, F. Quiniou, and M. Romeo Evaluation of biomarkers in oyster larvae in natural and polluted conditions Comp. Biochem. Physiol. C 138 2004 121 128 (Pubitemid 39278357)
22. G. Damiens, M. Gnassia-Barelli, F. Loques, M. Romeo, and V. Salbert Integrated biomarker response index as a useful tool for environmental assessment evaluated using transplanted mussels Chemosphere 66 2007 574 583 (Pubitemid 44791413)
23. M.H. Devier, S. Augagneur, H. Budzinski, K. Le Menach, P. Mora, J.F. Narbonne, and P. Garrigues 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. 7 2005 224 240
24. S. Diez, M. Abalos, and J.M. Bayona Organotin contamination in sediments from the Western Mediterranean enclosures following 10 years of TBT regulation Water Res. 36 2002 905 918 (Pubitemid 34019239)
25. T.A. Dix, and J. Aikens Mechanisms and biological relevance of lipid peroxidation initiation Chem. Res. Toxicol. 6 1993 2 18 (Pubitemid 23040365)
26. J. Eggleton, and K.V. Thomas A review of factors affecting the release and bioavailability of contaminants during sediment disturbance events Environ. Int. 30 2004 973 980 (Pubitemid 38771994)
27. P.J. Fitzpatrick, J. OHalloran, D. Sheehan, and A.R. Walsh Assessment of a glutathione S-transferase and related proteins in the gill and digestive gland of Mytilus edulis (L), as potential organic pollution biomarkers Biomarkers 2 1997 51 56 (Pubitemid 127699884)
28. G. Frenzilli, R. Bocchetti, M. Pagliarecci, M. Nigro, F. Annarumma, V. Scarcelli, D. Fattorini, and F. Regoli Time-course evaluation of ROS-mediated toxicity in mussels, Mytilus galloprovincialis, during a field translocation experiment Mar. Environ. Res. 58 2004 609 613 (Pubitemid 38738935)
29. S. Gorbi, C. Lamberti, A. Notti, M. Benedetti, D. Fattorini, G. Moltedo, and F. Regoli An ecotoxicological protocol with caged mussels, Mytilus galloprovincialis, for monitoring the impact of an offshore platform in the Adriatic Sea Mar. Environ. Res. 65 2008 34 49 (Pubitemid 350138554)
30. B.T.G. Gowland, A.D. McIntosh, I.M. Davies, C.F. Moffat, and L. Webster Implications from a field study regarding the relationship between polycyclic aromatic hydrocarbons and glutathione S-transferase activity in mussels Mar. Environ. Res. 54 2002 231 235 (Pubitemid 35286430)
31. W.H. Habig, M.J. Pabst, and W.B. Jakoby Glutathione S-transferases - first enzymatic step in mercapturic acid formation J. Biol. Chem. 249 1974 7130 7139
32. J.A. Hagger, M.H. Depledge, and T.S. Galloway Toxicity of tributyltin in the marine mollusc Mytilus edulis Mar. Pollut. Bull. 51 2005 811 816 (Pubitemid 41608835)
33. B. Hamer, Z. Jaksic, D. Pavicic-Hamer, L. Peric, D. Medakovic, D. Ivankovic, J. Pavicic, C. Zilberberg, H.C. Schroeder, W.E.G. Mueller, N. Smodlaka, and R. Batel Effect of hypoosmotic stress by low salinity acclimation of Mediterranean mussels Mytilus galloprovincialis on biological parameters used for pollution assessment Aquat. Toxicol. 89 2008 137 151
34. HELCOM Hazardous substances of specific concern to the Baltic Sea - final report of the HAZARDOUS project Baltic Sea Environment Process Series 119 2009
35. HELCOM Hazardous substances in the Baltic Sea - an integrated thematic assessment of hazardous substances in the Baltic Sea Baltic Sea Environmental Process Series 120B 2010
36. P. Herve-Fernandez, F. Houlbreque, F. Boisson, S. Mulsow, J.L. Teyssie, F. Oberhaensli, S. Azemard, and R. Jeffree Cadmium bioaccumulation and retention kinetics in the Chilean blue mussel Mytilus chilensis: seawater and food exposure pathways Aquat. Toxicol. 99 2010 448 456
37. ICES Report of the Study Group on Integrated Monitoring of Contaminants and Biological Effects (SGIMC) 2011 14-18 March 2011, Copenhagen, Denmark
38. ICES Report of the Working Group on Biological Effects of Contaminants (WGBEC), 12-16 March 2012, Porto, Portugal 2012 ICES CM 2012/SSGHIE:04. 131 pp.
39. M. Kaloyianni, S. Dailianis, E. Chrisikopoulou, A. Zannou, S. Koutsogiannaki, D.H. Alamdari, G. Koliakos, and V.K. Dimitriadis Oxidative effects of inorganic and organic contaminants on haemolymph of mussels Comp. Biochem. Physiol. C 149 2009 631 639
40. N.S. Kim, W.J. Shim, U.H. Yim, S.Y. Ha, and P.S. Park Assessment of tributyltin contamination in a shipyard area using a mussel transplantation approach Mar. Pollut. Bull. 57 2008 883 888
41. J. Kopecka, K.K. Lehtonen, J. Barsiene, K. Broeg, P.J. Vuorinen, J. Gercken, and J. Pempkowiak Measurements of biomarker levels in flounder (Platichthys flesus) and blue mussel (Mytilus trossulus) from the Gulf of Gdansk (southern Baltic) Mar. Pollut. Bull. 53 2006 406 421 (Pubitemid 44397108)
42. K.K. Lehtonen, S. Leiniö, R. Schneider, and M. Leivuori 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 2006 155 168 (Pubitemid 44606077)
43. S. Leiniö, and K.K. Lehtonen Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea Comp. Biochem. Physiol. C 140 2005 408 421 (Pubitemid 40804362)
44. I. Lima, S.M. Moreira, J. Rendon-Von Osten, A.M.V.M. Soares, and L. Guilhermino Biochemical responses of the marine mussel Mytilus galloprovincialis to petrochemical environmental contamination along the North-western coast of Portugal Chemosphere 66 2007 1230 1242 (Pubitemid 44854097)
45. D.R. Livingstone Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms Mar. Pollut. Bull. 42 2001 656 666 (Pubitemid 32717602)
46. D.R. Livingstone, P.G. Martinez, X. Michel, J.F. Narbonne, S. Ohara, D. Ribera, and G.W. Winston Oxyradical production as a pollution mediated mechanism of toxicity in the common mussel, Mytilus edulis-L, and other mollusks Funct. Ecol. 4 1990 415 424
47. D.M. Lowe, and R.K. Pipe Contaminant induced lysosomal membrane damage in marine mussel digestive cells - an in vitro study Aquat. Toxicol. 30 1994 357 365 (Pubitemid 24356718)
48. H. Manduzio, T. Monsinjon, C. Galap, F. Leboulenger, and W. Rocher 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 (Pubitemid 39296974)
49. J.M. Mccord, and i Fridovic Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein) J. Biol. Chem. 244 1969 6049
50. J.P. Meador, and C.A. Rice Impaired growth in the polychaete Armandia brevis exposed to tributyltin in sediment Mar. Environ. Res. 51 2001 113 129
51. M.H. Medina, J.A. Correa, and C. Barata Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress Chemosphere 67 2007 2105 2114 (Pubitemid 46463929)
52. M.N. Moore, D. Lowe, and A. Köhler Biological effects of contaminants: measurement of lysosomal membrane stability Proceedings of the ICES Techniques in Marine Environmental Sciences 36 2004 The International Council for the Explorations of the Sea Copenhagen 31
53. M.N. Moore, M.H. Depledge, J.W. Readman, and D.R.P. Leonard An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management Mutat. Res. Fundam. Mol. Mech. Mutagen. 552 2004 247 268 (Pubitemid 39036831)
54. M. Nigro, A. Falleni, I. Del Barga, V. Scarcelli, P. Lucchesi, F. Regoli, and G. Frenzilli Cellular biomarkers for monitoring estuarine environments: transplanted versus native mussels Aquat. Toxicol. 77 2006 339 347
55. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358 (Pubitemid 9194347)
56. A. Orbea, and M.P. Cajaraville Peroxisome proliferation and antioxidant enzymes in transplanted mussels of four Basque estuaries with different levels of poly cyclic aromatic hydrocarbon and polychlorinated biphenyl pollution Environ. Toxicol. Chem. 25 2006 1616 1626 (Pubitemid 44681045)
57. OSPAR 2007/2008 CEMP Assessment: Trends and Concentrations of Selected Hazardous Substances in Sediments and Trends in TBT-specific Biological Effects 2008
58. D.J.H. Phillips The common mussel, Mytilus edulis, as an indicator of pollution by zinc, cadmium, lead and copper. I. Effects of environmental variables on uptake of metals Mar. Biol. 38 1976 59 69 (Pubitemid 8039643)
59. D.J.H. Phillips Common mussel Mytilus edulis as an indicator of trace metals in Scandinavian waters.1. Zinc and cadmium Mar. Biol. 43 1977 283 291 (Pubitemid 8284827)
60. D.J.H. Phillips Effects of salinity on net uptake of zinc by common mussel Mytilus edulis Mar. Biol. 41 1977 79 88 (Pubitemid 8108032)
61. D.J.H. Phillips Trace metals in the common Mussel, Mytilus edulis (L), and in the alga Fucus vesiculosus (L) from the region of the Sound (Oresund) Environ. Pollut. 18 1979 31 43 (Pubitemid 9076807)
62. A.L. Pikkarainen Polycyclic aromatic hydrocarbons in Baltic Sea bivalves Polycycl. Aromat. Compd. 24 2004 681 695
63. A. Pikkarainen Polychlorinated biphenyls and organochlorine pesticides in Baltic Sea sediments and bivalves Chemosphere 68 2007 17 24 (Pubitemid 46483621)
64. J. Potrykus, A. Albalat, J. Pempkowiak, and C. Porte Content and pattern of organic pollutants (PAHs, PCBs and DDT) in blue mussels (Mytilus trossulus) from the southern Baltic Sea Oceanologia 45 2003 337 355 (Pubitemid 36941842)
65. A. Power, and D. Sheehan Seasonal variation in the antioxidant defence systems of gill and digestive gland of the blue mussel Mytilus edulis Comp. Biochem. Physiol. C 114 1996 99 103 (Pubitemid 26253366)
66. A. Prevodnik, J. Gardestrom, K. Lilja, T. Elfwing, B. McDonagh, N. Petrovic, M. Tedengren, D. Sheehan, and T. Bollner Oxidative stress in response to xenobiotics in the blue mussel Mytilus edulis L.: evidence for variation along a natural Aquat. Toxicol. 82 2007 63 71 (Pubitemid 46441502)
67. S. Pytharopoulou, E. Sazakli, K. Grintzalis, C.D. Georgiou, M. Leotsinidis, and D.L. Kalpaxis Translational responses of Mytilus galloprovincialis to environmental pollution: integrating the responses to oxidative stress and other biomarker responses into a general stress index Aquat. Toxicol. 89 2008 18 27
68. J. Rank, K.K. Lehtonen, J. Strand, and M. Laursen DNA damage, acetylcholinesterase activity and lysosomal stability in native and transplanted mussels (Mytilus edulis) in areas close to coastal chemical dumping sites in Denmark Aquat. Toxicol. 84 2007 50 61 (Pubitemid 47088721)
69. F. Regoli, G. Frenzilli, R. Bocchetti, F. Annarumma, V. Scarcelli, D. Fattorini, and M. Nigro Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment Aquat. Toxicol. 68 2004 167 178 (Pubitemid 38622490)
70. M. Romeo, Y. Mourgaud, A. Geffard, M. Gnassia-Barelli, J.C. Amiard, and H. Budzinski Multimarker approach in transplanted mussels for evaluating water quality in Charentes, France, coast areas exposed to different anthropogenic conditions Environ. Toxicol. 18 2003 295 305 (Pubitemid 37258741)
71. J.M. Ruiz, R. Barreiro, L. Couceiro, and M. Quintela Decreased TBT pollution and changing bioaccumulation pattern in gastropods imply butyltin desorption from sediments Chemosphere 73 2008 1253 1257
72. D. Schiedek, K. Broeg, J. Barsiene, K.K. Lehtonen, J. Gercken, S. Pfeifer, H. Vuontisjarvi, P.J. Vuorinen, V. Dedonyte, A. Koehler, L. Balk, and R. Schneider Biomarker responses as indication of contaminant effects in blue mussel (Mytilus edulis) and female eelpout (Zoarces viviparus) from the southwestern Baltic Sea Mar. Pollut. Bull. 53 2006 387 405 (Pubitemid 44397102)
73. S.D. St-Jean, E. Pelletier, and S.C. Courtenay Hemocyte functions and bacterial clearance affected in vivo by TBT and DBT in the blue mussel Mytilus edulis Mar. Ecol. Prog. 236 2002 163 178 (Pubitemid 34780690)
74. S.D. St-Jean, E. Pelletier, and S.C. Courtenay Very low levels of waterborne butyltins modulate hemocyte function in the blue mussel Mytilus edulis Mar. Ecol. Prog. 236 2002 155 161 (Pubitemid 34780689)
75. J. Strand, and J.A. Jacobsen Imposex in two sublittoral neogastropods from the Kattegat and Skagerrak: the common whelk Buccinum undatum and the red whelk Neptunea antique Mar. Ecol. Prog. 244 2002 171 177 (Pubitemid 36035740)
76. J. Strand, J.A. Jacobsen, B. Pedersen, and Å. Granmo Butyltin compounds in sediment and molluscs from the shipping strait between Denmark and Sweden Environ. Pollut. 124 2003 7 15 (Pubitemid 36390299)
77. I. Sunila Reproduction of Mytilus edulis-L (Bivalvia) in a Brackish Water Area, the Gulf of Finland Ann. Zool. Fenn. 18 1981 121 128
78. P. Szefer, K. Frelek, K. Szefer, C.B. Lee, B.S. Kim, J. Warzocha, I. Zdrojewska, and T. Ciesielski Distribution and relationships of trace metals in soft tissue, byssus and shells of Mytilus edulis trossulus from the southern Baltic Environ. Pollut. 120 2002 423 444 (Pubitemid 36149733)
79. N. Tapie, H. Budzinski, and K. Le Menach Fast and efficient extraction methods for the analysis of polychlorinated biphenyls and polybrominated diphenyl ethers in biological matrices Anal. Bioanal. Chem. 391 2008 2169 2177
80. S. Thompson, and H. Budzinski Determination of polychlorinated biphenyls and chlorinated pesticides in environmental biological samples using focused microwave-assisted extraction Int. J. Environ. Anal. Chem. 76 2000 49 60 (Pubitemid 30172033)
81. S. Thompson, H. Budzinski, P. Garrigues, and J.F. Narbonne Comparison of PCB and DDT distribution between water-column and sediment-dwelling bivalves in Arcachon Bay France Mar. Pollut. Bull. 38 1999 655 662 (Pubitemid 29417901)
82. C. Tsangaris, K. Kormas, E. Strogyloudi, I. Hatzianestis, C. Neofitou, B. Andral, and F. Galgani Multiple biomarkers of pollution effects in caged mussels on the Greek coastline Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 151 2010 369 378
83. Turja, R.; Höher, N.; Snoeijs, P.; Kholodkevich, S.; Devier, M.-H.; Budzinski, H.; Lehtonen, K.K.; in preparation. A multibiomarker approach in caged Mytilus trossulus to assess two impacted coastal areas of the Baltic Sea.
84. R. Väinölä, and P. Strelkov Mytilus trossulus in Northern Europe Mar. Biol. 158 2011 817 833
85. A. Valavanidis, T. Vlahogianni, M. Dassenakis, and M. Scoullos Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants Ecotoxicol. Environ. Saf. 64 2006 178 189 (Pubitemid 43766114)
86. Porvoon Vesi Porvoon edustan merialueen yhteistarkkailu vuonna 2007 2007 In Finnish
87. A. Viarengo, and L. Canesi Mussels as biological indicators of pollution Aquaculture 94 1991 225 243
88. L. Vidal-Linan, J. Bellas, J.A. Campillo, and R. Beiras Integrated use of antioxidant enzymes in mussels, Mytilus galloprovincialis, for monitoring pollution in highly productive coastal areas of Galicia (NW Spain) Chemosphere 78 2010 265 272
89. T.H. Vlahogianni, and A. Valavanidis Heavy-metal effects on lipid peroxidation and antioxidant defence enzymes in mussels Mytilus galloprovincialis Chem. Ecol. 23 2007 361 371 (Pubitemid 47578103)
90. W.X. Wang, and R.C.K. Wong Combined effects of food quantity and quality on Cd, Cr, and Zn assimilation to the green mussel, Perna viridis J. Exp. Mar. Biol. Ecol. 290 2003 49 69 (Pubitemid 36551365)
91. M. Westerbom, M. Kilpi, and O. Mustonen Blue mussels, Mytilus edulis, at the edge of the range: population structure, growth and biomass along a salinity gradient in the north-eastern Baltic Sea Mar. Biol. 140 2002 991 999 (Pubitemid 36072709)
92. J. Widdows, and D.S. Page Effects of tributyltin and dibutyltin on the physiological energetics of the mussel, Mytilus edulis Mar. Environ. Res. 35 1993 233 249
93. J. Widdows, P. Donkin, F.J. Staff, P. Matthiessen, R.J. Law, Y.T. Allen, J.E. Thain, C.R. Allchin, and B.R. Jones 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 (Pubitemid 34119143)