Evaluation of neutral red retention assay, micronucleus test, acetylcholinesterase activity and a signal transduction molecule (cAMP) in tissues of Mytilus galloprovincialis (L.), in pollution monitoring

Marine Environmental Research

Volumn 56, Issue 4, 2003, Pages 443-470

  Dailianis, S ^a   Domouhtsidou, G P ^b   Raftopoulou, E ^b   Kaloyianni, M ^a   Dimitriadis, V K ^b  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Acetylcholinesterase; Biomonitoring; cAMP; Digestive gland; Gills; Haemolymph; Mantle gonad; Mussels; Neutral red; Northern Greece; Signal transduction molecule

Indexed keywords

ASSAYS; BIOMARKERS; CORRELATION METHODS; STRESSES; TISSUE;

MICRONUCLEUS TESTS;

POLLUTION;

ACETYLCHOLINESTERASE; BIOLOGICAL MARKER; CYCLIC AMP; NEUTRAL RED;

BIOMONITORING;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASSAY; BLOOD CELL; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; EVALUATION; EXOCRINE GLAND; GILL; GONAD; GREECE; HEMOLYMPH; MICRONUCLEUS TEST; MUSSEL; MYTILUS GALLOPROVINCIALIS; NONHUMAN; POLLUTION MONITORING; SIGNAL TRANSDUCTION; VALIDATION PROCESS; WATER POLLUTION;

MYTILUS GALLOPROVINCIALIS;

EID: 0038690222     PISSN: 01411136     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0141-1136(03)00005-9     Document Type: Article

References (108)

1. Adams S.M. Status and use of biological indicators for evaluating the effects of stress on fish. Am. Fish. Soc. Symp. 8:1990;1-8.
2. Albanis T.A., Danis T.G., Kourgia M.K. Trasportation of pesticides in estuaries of the Axios, Loudias and Aliakmon rivers (Thermaikos gulf), Greece. Science of the Total Environment. 156:1994;11-22.
3. Amiard J.C., Amiard-Triquet C., Berthert B., Metayer C. Contribution to the ecotoxicological study of cadmium, lead, copper and zinc in the mussel Mytilus edulis. Marine Biology. 9:1986;425-431.
4. Amiard-Triquet C., Altmann S., Amiard J.C.et al. Fate and effects of micropollutants in the Gironde estuary, France. a multidisciplinary approach Hydrobiologia. 373/374:1998;259-279.
5. Anagnostou C., Georgakopoulou-Gregoriadou E., Zenetos A., Kamberi E., Karageorgis A., Kontogiannis C., Pagou K., Panagiotidis P., Pancucci A., Siokou I., Symboura N., Chatjanestis I., Psyllidou-Giuranovits R. The state of the marine ecosystem of the bay and the Gulf of Thessaloniki - the reaction capacity of the ecosystem. Proceedings 5th Panellenic Symposium of Oceanography and Fishery. 1:1997;83-86.
6. Anagnostou C., Kamberi H., Karageorgis A. Horizontal and vertical distribution of heavy metals in sediments from Thermaikos Gulf. Rapp. Comm. Int. Mer. Medit. 35:1998;222.
7. Barron M.G., Woodburn K.B. Ecotoxicology and chlorpyrifos. Ware G.W. Reviews of environmental contamination and toxicology, 131. 1995;1-93 Springer-Verlag, New York.
8. Biondi C., Fabbri E., Ferretti M.E., Sonetti D., Bolognani Fantin A.M. Effects of lead exposure on cAMP and correlated enzymes in Viviparus ater (Mollusca gastropoda) neurons system. Comparative Biochemistry Physiology. 946:1989;327-333.
9. Bocquene G., Galgani F., Truquet P. Characterization and assay conditions for the use of AChE activity from several marine species in pollution monitoring. Marine Environmental Research. 30:1990;75-89.
10. Bolognesi C., Landini E., Roggieri P., Fabbri R., Viarengo A. Genotoxicity biomarkers in the assessment of heavy metal effects in mussels. experimental studies Environmental and Molecular Mutagenesis. 33(4):1999;287-292.
11. Boynton A.L., Whitfield J.F.(1983) Greengard P., Robison G.A. Advances in cyclic nucleotide research, 15. 1983;193 Raven Press, New York.
12. Bresler V., Bissinger V., Abelson A., Dizer H., Sturm A., Kratke R., Fishelson L., Hansen P.D. Marine molluscs and fish as biomarkers of pollution stress in littoral regions of the Red Sea, Mediterranean Sea and North Sea. Helgoland Marine Research. 53:1999;219-243.
13. Brunetti R., Majone F., Gola I., Beltrame C. The micronucleus test. examples and application to marine ecology Marine Ecology Progress Series. 44:1988;65-68.
14. Camus L., Grosvik B.E., Borseth J.F., Jones M.B., Depledge M.H. Stability of lysosomal and cell membranes in haemocytes of the common mussel (Mytilus edulis). effect of low temperatures Marine Environmental Research. 50:2000;325-329.
15. Camusso M., Balestrini R., Muriano F., Mariani M. Use of freshwater mussel Dreissena polymorpha to assess trace metal pollution in the lower river Po (Italy). Chemosphere. 29:1994;729-745.
16. Caprio J., Brand J.G., Teeter J.H., Valenticic T., Kalinoski D.L., Kohbara J., Kumazawa T., Wegert S. The taste system of the channel catfish. from biophysics to behaviour Trends in Neuroscience. 16(5):1993;192-197.
17. Catsiki V., Hatzianestis I., Strogyloudi E., Belou O., Gogou M., Rigas F. Distribution of metals and organic contaminants in mussels from Thermaikos Gulf. Proccedings of the 7th International Conference on Environmental Science and Technology. vol. A Syros island, Greece. September:2001;106-113.
18. Chen J.H., Bayne C.J. Hemocyte adhesion in the California mussel (Mytilus californianus). regulation by adenosine Biochimica et Biophysica Acta. 1268:1995;178-184.
19. Cossa D. A review of the use of Mytilus spp. as quantitative indicators of cadmium and mercury contamination in coastal waters. Oceanologica Acta. 12(4):1989;417-432.
20. Darzynkiewicz Z. Mammalian cell-cycle analysis. Fantes P., Brooks R. The cell cycle: a practical approach. 1993;45-68 Oxford University Press, Oxford.
21. Darzynkiewicz Z. Simultaneous analysis of cellular RNA and DNA content. Methods in Cell Biology. 41:1994;401-424.
22. Das R.K., Nanda N.K. Induction of micronuclei in peripheral erythrocytes of fish Heteropneustes fossilis by mitomycin C and paper mill effluent. Mutation Research. 175:1986;67-71.
23. Day K.E., Scott I.M. Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides. Aquatic Toxicology. 18:1990;101-114.
24. Dellali M., Gnassia-Barelli M., Romeo M., Aissa P. The use of acetylcholinesterase activity in Ruditapes decussatus and Mytilus galloprovincialis in the biomonitoring of Bizerta lagoon. Comparative Biochemistry and Phyciology. 130C:2001;227-235.
25. de Lemos C.T., Rodel P.M., Terra N.R., Erdtmann B. Evaluation of basal micronucleus frequency and hexavalent chromium effects in fish erythrocytes. Environmental Toxicology and Chemistry. 20(6):2001;1320-1324.
26. Devi M., Fingerman M. Inhibition of acetylcholinesterase activity in the central nervous system of the red Swamp crayfish, Procambarus clarkii, by mercury, cadmium and lead. Bulletin of Environmental Contamination and Toxicology. 55:1995;746-750.
27. Dierickx P.J., Van De Vijver I. Correlation of the neutral red uptake inhibition assay of cultured fathead minnow cells with fish lethality tests. Bulletin of Environmental Contamination and Toxicology. 46:1991;649-653.
28. Domouhtsidou G.P., Dimitriadis V.K. Lysosomal and lipid alterations in the digestive gland of mussels, Mytilus galloprovincialis (L.) as biomarkers of environmental stress. Environmental Pollution. 115:2001;123-137.
29. Edwards C.A., Fisher S.W. The use of cholinesterase measurements in assessing the impacts of pesticides on terrestrial and aquatic invertebrates. Mineau P. Cholinesterase-inhibiting insecticides. 1991;255-275 Elsevier, Amsterdam.
30. Eichhom G.L., Clarck P., Tarien E. The interaction of metal ions with polynucleotides and related compounds. Journal of Biological Chemistry. 244:1969;937-942.
31. Ellman G.L., Courtney K.O., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology. 7:1961;88-95.
32. Enrich M.J.D., Villaramin J.A., Martinez I.R., Ibarguren I. Measurement of adenosine 3′,5′-cyclic monophosphate and guanosine 3′,5′-cyclic monophosphate in mussel (Mytilus galloprovincialis Lmk.) by high-performance liquid chromatography with diode array detection. Analytical Biochemistry. 285(1):2002;105-112.
33. Escartin E., Porte C. The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environmental Toxicology and Chemistry. 16(10):1997;2090-2095.
34. Exton J.H. Hamet P., Sands H. Advances in cyclic nucleotide research, 12. 1980;319 Raven Press, New York.
35. Fernandez M., Cao J., Villamarin J.A. In vivo phosphorylation of phosphofructokinase from the Bivalve Mollusk Mytilus galloprovincialis. Archives of Biochemistry and Biophysics. 353(2):1998;251-256.
36. Fernley P.W., Moore M.N., Lowe D.M., Donkin P., Evans S. Impact of the Sea Empress oil spill on lysosomal stability in mussel blood cells. Marine Environmental Research. 50:2000;451-455.
37. Fishelson L. Eilat (Gulf of Aqaba) littoral. life on the red line of biodegradation Israel Journal of Zoology. 41:1995;3-55.
38. Fishelson L., Bresler V., Manelis R., Zuk-Rimon Z., Dotan A., Hornung H., Yawetz A. Toxicological aspects associated with the ecology of Donax trunculus (Bivalvia, Mollusca) in a polluted environment. Science of the Total Environment. 226:1999;121-131.
39. Galgani F., Bocquene G. A method for routine detection of organophosphates and carbamates in sea water. Environmental Technology Letters. 10:1988;311-322.
40. Hamza-Chaffai A., Romeo M., Gnassia-Barelli M., El Abed A. Effect of Copper and Lindane on Some Biomarkers Measured in the Clam Ruditapes decussates. Bulletin of Environmental Contamination and Toxicology. 61:1998;397-404.
41. Hatzianestis I., Sklivagou E., Georgakopoulou E. Organic contaminants in sediments and mussels from Thermaikos Gulf, Hellas. Toxicology and Environmental Chemistry. 74:2000;203-216.
42. Haugland R.P. Handbook of fluorescent probes and research chemicals. 6th ed. 1996;Molecular Probes, Eugene, Oregon.
43. Hauton C., Hawkins L.E., Hutchinson S. The use of the neutral red retention assay to examine the effects of temperature and salinity on haemocytes of the European flat oyster Ostrea edulis (L.). Comparative Biochemistry and Physiology B. 119:1998;619-623.
44. Herbert, A., & Hansen, P. D. (1998). Genotoxicity in fish embryos. In Microscale testing in aquatic toxicology (pp. 491-505). Boca Raton: CRC Press.
45. Heyer C.B., Kater S.B., Karlsson U.L. Neuromuscular systems in molluscs. American Zoologist. 13:1973;247-270.
46. Holland H.T., Coppage D.L., Butler P.A. Use of fish brain acetylcholinesterase to monitor pollution by organophosphorus pesticides. Bulletin of Environmental Contamination and Toxicology. 2:1967;156-162.
47. Kamarianos, A., Karamanlis, X., & Galoupi, E. (2002). Pollution of coastal areas of N. Greece by organochlorine pesticides and polychlorinated biphenyls (PCBs). In Proceedings of the 1st Environmental Conference of Macedonia, 1-4 March 2002, Thessaloniki (p. 116).
48. Kamarianos, A., & Kilikidis, S. (1997). Pollution monitoring of Thermaikos Gulf using organochloride pesticides and polychlorinated biphenyls (PCBs), (1991-1996). In Proceedings of the 5th Conference of Environmental Science and Technology (vol. B, pp. 326-333), Lesvos Island, Greece.
49. Kohler A., Deismemann H., Lauritzen B.M. Histological and cytochemical indices of toxic injury in the liver of dab Limanda limanda. Marine Ecology Progress Series. 91:1992;249-261.
50. Krishnakumar P.K., Casillas E., Varanasi U. Effect of environmental contamination on the health of Mytilus edulis from Puget Sound, Washington. cytochemical measures of lysosomal responses in the digestive cells using automatic image analysis Marine Ecology Progress Series. 106:1994;249-261.
51. Lafontaine deY., Gagne F., Blaise C., Costan G., Gagnon P., Chan H.M. Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquatic toxicology. 50:2000;51-71.
52. Lowe D.M., Fossato V.U., Depledge M.H. Contaminant-induced lysosomal membrane damage in blood cells of mussels Mytilus galloprovincialis from the Venice Lagoon. an in vitro study Marine Ecology Progress Series. 129:1995;189-196.
53. Lowe D.M., Moore M.N., Evans B.M. Contaminant impact on interactions of molecular probes with lysosomes in living hepatocytes from dab Limanda limanda. Marine Ecology Progress Series. 91:1992;135-140.
54. Lowe D.M., Pipe R.K. Contaminant induced lysosomal membrane damage in marine mussel digestive cells. an in vitro study Aquatic Toxicology. 30:1994;357-365.
55. Lowe D.M., Soverchia C., Moore M.N. Lysosomal membrane responses in the blood and digestive cells of mussels experimentally exposed to fluoranthene. Aquatic Toxicology. 33:1995;105-112.
56. MacDonald J.A., Storey K.B. Cyclic AMP-dependent protein kinase. role in anoxia and freezing tolerance of the marine periwinkle Littorina littorea Marine Biology. 133:1999;193-203.
57. Majone F., Brunetti R., Gola I., Levis A.G. Persistence of micronuclei in the marine mussel, Mytilus galloprovincialis, after treatment with mitomycin C. Mutation Research. 191:1987;157-161.
58. Majone F., Beltrame C., Brunetti R. Frequencies of micronuclei detected on Mytilus galloprovincialis by different staining techniques after treatment with zinc chloride. Mutation Research. 209:1988;131-134.
59. Marvin C.H., McCarry B.E., Bryant D.W. Determination and genotoxicity of polycyclic aromatic hydrocarbons isolated from Dreissena polymorpha (zebra mussels) sampled from Hamilton Harbour. Journal of Great Lakes Research. 20:1994;523-530.
60. Matozzo V., Ballarin L., Pampanin D.M., Marin M.G. Effects of copper and cadmium exposure on functional responses of hemocytes in the clam, Tapes philippinarum. Archives of Environmental Contamination and Toxicology. 41:2001;163-170.
61. Mendes J.J.A. The endocrine disrupters. a major medual challenge Food and Chemical Toxicology. 40(6):2002;781-788.
62. Mercer A.L., McGregor D.D. Neural regulation and pharmacology of the gut of Chione stutchburyi, a bivalve mollusc. Comparative Biochemistry and Physiology. 73C:1982;243-251.
63. Mersh J., Jeanjean H., Spor J.C., Pihan J.C. The freshwater mussel Dreissena polymorpha as a bioindicator for trace metals, organochlorines and radionuclides. Neumann D., Jenner H.A. The Zebra Mussel Dreissena polymorpha. Limnologie Aktuell, 4. 1992;227-244 Gustav Fisher, Stuttgart.
64. Mersh J., Beauvais M.N. The micronucleus assay in the zebra mussel, Dreissena polymorpha, to in situ monitor genotoxicity in freshwater environments. Mutation Research. 393:1997;141-149.
65. Mersh J., Beauvais M.N., Nagel P. Induction of micronuclei in haemocytes and gill cells of zebra mussels, Dreissena polymorpha, exposed to clastogens. Mutation Research. 371:1996;47-55.
66. Mersh J., Pihan J.C. Simultaneous assessment of environmental impact on condition and trace metal availability in zebra mussels Dreissena polymorpha transplanted into the Wiltz River, Luxembourg. Comparison with the aquatic moss Fontinalis antipyretica. Archives of Environmental Contamination and Toxicology. 25:1993;353-364.
67. Migliore L., Barale R., Belluomini D., Cognetti A.G., Loprieno N. Cytogenetic damage induced in human lymphocytes by adriamycin and vincristine. a comparison between micronucleus and chromosomal aberration assays Toxicology in Vitro I. 1987;247-254.
68. 3- and cAMP-induced responses in isolated olfactory receptor neurons from the channel catfish. Journal of Membrane Biology. 127:1992;173-183.
69. Moore M.N. Cellular responses to pollutants. Marine Pollution Bulletin. 16:1985;134-139.
70. Moulton C.A., Fleming W.J., Purnell C.E. Effects of two cholinesterase-inhibiting pesticides on freshwater mussels. Environmental Toxicology and Chemistry. 15:1996;131-137.
71. Najimi S., Bouhaimi S., Daubeze M., Zekhnini A., Pellerin J., Narbonne J.F., Moukrim A. Use of acetylcholinesterase in Perna perna and Mytilus galloprovincialis as a biomarker of pollution of Agadir marine bay (South Marocco). Bulletin of Environmental Contamination and Toxicology. 58:1997;901-912.
72. NCMR, Oceanography Institute (1997). Monitoring of the quality of the marine environment of the gulf of Thessaloniki through 1977. Final technical report, pp. 1-250 (In Greek).
73. Nepomuceno J.C., Ferrari I., Spano M.A., Centeno A.J. Detectioin of micronuclei in peripheral erythrocytes of Cyprinus carpio exposed to metallic mercury. Environmental of Molecular Mutegenesis. 30:1997;293-297.
74. Ozretic B., Krajinovic-Ozretic M. Esterase heterogeneity in mussels Mytilus galloprovincialis. effects of organophosphate and carbamate pesticides in vitro Comparative Biochemistry and Physiology. 103 C:1992;221-225.
75. Pareschi M.C., Ferretti M.E., Zeni C., Caligiuri A.S., Vignocchi B., Biondi C. Effect of exposure to linear alkylbenzene sulphonate on cAMP levels in Ictalurus sp. olfactory and gustatory tissues. Comparative Biochemistry and Physiology. 116C(1):1997;11-16.
76. Payne J.F., Mathieu A., Melvin W., Fancey L.L. Acetylcholinesterase, an old biomarker with a new future? Field trials in association with two urban rivers and paper mill in Newfoundland. Marine Pollution Bulletin. 32(2):1996;225-231.
77. Petrovic S., Ozretic B., Krajnovic-Ozretic M., Bobinac D. Lysosomal membrane stability and metallothioneins in digestive gland of mussels (Mytilus galloprovincialis Lam.) as biomarkers in a field study. Marine Pollution Bulletin. 42(12):2001;1373-1378.
78. Plaut M.et al. Hamet P., Sands H. Advances in cyclic nucleotide research, 12. 1980;161 Raven Press, New York.
79. Regoli F. Lysosomal responses as sensitive stress index in biomonitoring heavy metal pollution. Marine Ecology Progress Series. 84:1992;63-69.
80. Regoli F. Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean Mussel Mytilus galloprovincialis. Archives of Environmental Contamination and Toxicology. 34:1998;48-63.
81. Ringwood A.H., Deanna E.C., Hoguet J. Effects of natural and anthropogenic stressors on lysosomal destabilization in oysters Crassostrea virginica. Marine Ecology Progress Series. 166:1998;163-171.
82. Ringwood A.H., Hameedi M.J., Lee R.F., Brouwer M., Peters E.C., Scott G.I., Luoma S.N., Digiulio R.T. Bivalve biomarker workshop. overview and discussion summaries Biomarkers. 4:1999;391-399.
83. Roy S., Hanninen O. Biochemical monitoring of the aquatic environment: possibilities and limitations. Richardson M. Ecotoxicology monitoring. 1993;119-135 VCH-Verlag.
84. Scarpato R.L., Migliore G., Alfinito-Cognetti, Barale R. Induction of micronuclei in gill tissue of Mytilus galloprovincialis exposed to polluted marine waters. Marine Pollution Bulletin. 21:1990;74-80.
85. Schimd W. The micronucleus test for cytogenetic analysis. Hollaender A. Chemical mutagens: principles and methods for their detection (Vol. 4). 1976;31-53 Plenum Press, New York, NY.
86. Sorensen K., Brodbeck U. A sensitive protein assay method using micro-titer plates. Experientia. 42:1986;161-162.
87. Stien X., Percic P., Gnassia-Barelli M., Romeo M., Lafaurie M. Evaluation of biomarkers in caged fishes and mussels to assess the quality of waters in a bay of the NW Mediterranean Sea. Environmental Pollution. 99:1998;339-345.
88. Sutherland E.W., Robison G.A., Butcher R.W. Some aspects of the biological role of adenosine 3′, 5′-monophosphate (cyclic AMP). Circulation. 37:1968;279-306.
89. UNEP. (1993). Selected techniques for monitoring biological effects of pollutants in marine organisms. MAP Technical Reports Series No. 71, Athens.
90. UNEP. (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, Greece.
91. UNEP/RAMOGE. (1999). Manual on the biomarkers recommended for the MED POL biomonitoring programme. UNEP, Athens.
92. Van der Gaag M.A., Gauthier A., Noordsij Y.Levi., Wrisberg M.N. Methods to measure genotoxins in wastewater evaluation with in vivo and in vitro tests. Waters M.D.et al. Genetic toxicology of complex mixtures (Vol. 6). 1990;215-232 Plenum Press, New York.
93. Varela, V. M., Augspurger, T. (1996). Cholinesterase activity as a device for biomonitoring pesticide exposure in the freshwater mussel Elliptio complanata. Publication No. 95-4F23, US Fish and Wildlife Service, Southeast Region, Atlanta, GA.
94. Venier P., Maron S., Canova S. Detection of micronuclei in gill cells and haemocytes of mussels exposed to benzo[a]pyrene. Mutation Research. 390:1997;33-44.
95. Viarengo A., Marro A., Marchi B., Burlando B. Single and combined effects of heavy metal and hormones on lysosomes of haemolymph cells from the mussel Mytilus galloprovincialis. Marine Biology. 137:2000;907-912.
96. Viarengo A., Moore M.N., Mancinelli G., Mazzucotelli A., Pipe R.K., Farrar S.V. Metallothioneins and lysosomes in metal toxicity and accumulation in marine mussels. the effect of cadmium in the presence and absence of phenanthrene Marine Biology. 94:1987;251-257.
97. Viarengo A., Ponzano E., Dondero F., Fabbri R. A simple spectrophotometric method for MT evaluation in marine organisms. an application to Mediterranean and Antarctic molluscs Marine Environmental Research. 44:1997;69-84.
98. Voutsinou-Taliadouri, F., Hatzianestis, I., Georgakopoulou-Gregoriadou, E. (1998). Trace elements, pesticides and PCBs levels in sediments of a bay influenced by anthropogenic activities (Thermaikos bay, N.W Aegean Sea). In International Symposium on Marine Pollution (pp. 668-680). Extended synopses, Monaco.
99. Walker C.H., Thompson H.M. Phylogenetic distribution of cholinesterases and related esterases. Mineau P. Cholinesterase-inhibiting insecticides. 1991;1-17 Elsevier, Amsterdam.
100. Wedderburn J., McFadzen I., Sanger R.C., Beesley A., Heath C., Hornsby M., Lowe D. The field application of cellular and physiological biomarkers, in the mussel Mytilus edulis, in conjunction with early life stage bioassays and adult histopathology. Marine Pollution Bulletin. 40(3):2000;257-267.
101. Weiss C.M. Use of fish to detect organic insecticides in water. Journal WPCF. 37:1965;647-658.
102. Weiss C.M., Gakstatter J.H. Detection of pesticides in water by biochemical assay. Journal WPCF. 36:1964;240-252.
103. Williams A.K., Sova R.C. Acetylcholinesterase levels in brain of fish from polluted waters. Bulletin of Environmental Contamination and Toxicology. 1:1966;198-204.
104. Williams R.C., Metcalfe C.D. Development of an in vivo hepatic micronucleus assay with rainbow trout. Aquatic Toxicology. 23:1992;193-202.
105. Wogram J., Sturm A., Segner H., Liess M. Effects of parathion on acetylcholinesterase, butyrylcholinesterase, and carboxylesterase in three-spined stickleback (Gasterosteus aculeatus) following short-term exposure. Environmental Toxicology and Chemistry. 20(7):2001;1528-1531.
106. Wrisberg M.N., Bilbo C.M., Spliid H. Induction of micronuclei in haemocytes of Mytilus edulis and statistical analysis. Ecotoxicology and Environmental Safety. 23(2):1992;191-205.
107. Zahariadis, G., & Stratis, J. (1995). Heavy metals and nutrients. MED-POL program: monitoring in Thermaikos Gulf (annual report). Aristotle University of Thessaloniki, Greek Ministry of the Environment.
108. Zinckl J.G., Shea P.J., Nakamoto R.J., Callman J. Brain cholinesterase of rainbow trout poisoned by carbamyl. Bulletin of Environmental Contamination and Toxicology. 38:1987;29-35.