Linking behavioural alterations with biomarkers responses in the european seabass dicentrarchus labrax l. exposed to the organophosphate pesticide fenitrothion

Ecotoxicology

Volumn 19, Issue 8, 2010, Pages 1369-1381

  Almeida, Joana R ^a   Oliveira, Cristiana ^b   Gravato, Carlos ^b   Guilhermino, Lúcia ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

AChE activity; Biotransformation; Dicentrarchus labrax; Fenitrothion; Oxidative stress defences; Swimming velocity

Indexed keywords

ACETYLCHOLINESTERASE; BIOLOGICAL MARKER; CATALASE; CHOLINESTERASE; ETHOXYRESORUFIN DEETHYLASE; FENITROTHION; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; ISOCITRATE DEHYDROGENASE; LACTATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; CYTOCHROME P450 1A1; INSECTICIDE;

BEHAVIORAL RESPONSE; BIOACCUMULATION; BIOMARKER; BIOTRANSFORMATION; ENZYME ACTIVITY; FENITROTHION; FISH; INHIBITION; ORGANOPHOSPHATE; POLLUTION EFFECT; POLLUTION EXPOSURE; SURVIVAL; SWIMMING BEHAVIOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOTRANSFORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ECOTOXICOLOGY; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; EUROPEAN SEA BASS; LIPID PEROXIDATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SWIMMING; VELOCITY; ANIMAL; BASS; BRAIN; DRUG EFFECT; LIVER; METABOLISM;

DICENTRARCHUS LABRAX;

ACETYLCHOLINESTERASE; ANIMALS; BASS; BEHAVIOR, ANIMAL; BIOLOGICAL MARKERS; BRAIN; CYTOCHROME P-450 CYP1A1; FENITROTHION; INSECTICIDES; LIPID PEROXIDATION; LIVER; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE; SWIMMING;

EID: 79952279524     PISSN: 09639292     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10646-010-0523-y     Document Type: Article

References (97)

1. Amiard-Triquet C (2009) Behavioural disturbances: the missing link between sub-organismal and supra-organismal responses to stress? Prospects based on aquatic research. Hum Ecol Risk Assess 15:87-110
2. Baatrup E (2009) Measuring complex behaviour patterns in fish- effects of endocrine disruptors on the guppy reproductive behaviour. Hum Ecol Risk Assess 15:53-62
3. Ballesteros ML, Durando PE, Nores ML, Díaz MP, Bistoni MA, Wunderlin DA (2009) Endosulfan induces changes in spontaneous swimming activity and acetylcholinesterase activity of Jenynsia multidentata (Anablepidae, Cyprinodontiformes). Environ Pollut 157:1573-1580
4. Banni M, Jebali J, Guerbej H, Dondero F, Boussetta H, Viarengo A (2010) Mixture toxicity assessment of nickel and chlorpyrifos in the sea bass Dicentrarchus labrax. Arch Environ Contam Toxicol [Epub ahead of print]
5. Beauvais SL, Jones SB, Brewer SK, Little EE (2000) Physiological measures of neurotoxicity of diazinon and malathion to larval rainbow trout (Oncorhynchus mykiss) and their correlation with behavioural measures. Environ Toxicol Chem 19(7):1875-1880 (Pubitemid 30399747)
6. Beauvais SL, Jones SB, Parris JT, Brewer SK, Little EE (2001) Cholinergic and behavioral neurotoxicity of carbaryl and cadmium to larval rainbow trout (Oncorhynchus mykiss). Ecotoxicol Environ Saf 49:84-90 (Pubitemid 32473152)
7. Billiard SM, Bols NC, Hodson PV (2004) In vitro and in vivo comparisons of fish-specific CYP1A induction relative potency factors for selected polycyclic aromatic hydrocarbons. Ecotoxicol Environ Saf 59(3):292-299 (Pubitemid 39243970)
8. Bird RP, Draper AH (1984) Comparative studies on different methods of malondyhaldehyde determination. Methods Enzymol 90: 105-110
9. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
10. Brewer SK, Little EE, DeLonay AJ, Beauvais SL, Jones SB, Ellersieck MR (2001) Behavioural dysfunction correlate to altered physiology in rainbow trout (Oncorhynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Arch Environ Contam Toxicol 40:70-76 (Pubitemid 34240905)
11. Burke MD, Mayer RT (1974) Ethoxyresorufin: direct fluorimetric assay of a microsomal-O-deethylation which is preferentially inducible by 3-methylcholantrene. Drugs Metab Dispos 2: 583-588
12. Calò M, Bitto A, Lo Cascio P, Polito F, Lauriano ER, Minutoli L, Altavilla D, Squadrito F (2009) Cytochrome P450 (CYP1A) induction in sea bream (Sparus aurata) gills and liver following exposure to polychlorobiphenyls (PCBs). Vet Res Commun 33(1): 181-184
13. Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzymol 113:484-490 (Pubitemid 16195819)
14. Castro BB, Sobral O, Guilhermino L, Ribeiro R (2004) An in situ bioassay integrating individual and biochemical responses using small fish species. Ecotoxicology 13:667-681 (Pubitemid 40363053)
15. Clairborne A (1985) Catalase activity. In: Greenwald RA (ed) CRC handbook of methods in oxygen radical research. CRC Press, Boca Raton, pp 283-284
16. Cong NV, Phuong NT, Bayley M (2009) Effects of repeated exposure of diazinon on cholinesterase activity and growth in snakehead fish (Channa striata). Ecotoxicol Environ Saf 72:699-703
17. Damásio J, Guilhermino L, Soares AMVM, Riva MC, Barata C (2007) Biochemical mechanisms of resistance in Daphnia magna exposed to the insecticide fenitrothion. Chemosphere 70:74-82 (Pubitemid 350016241)
18. Dell'Omo G (2002) Behavioural ecotoxicology. Wiley, Chichester
19. Dezfuli BS, Simoni E, Giari L, Manera M (2006) Effects of experimental terbuthyllazine exposure on the cells of Dicentrarchus labrax (L.). Chemosphere 64:1684-1694 (Pubitemid 44067165)
20. Diamantino TC, Almeida E, Soares AMVM, Guilhermino L (2001) Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphia magna Straus. Bull Environ Contam Toxicol 57:979-985
21. Ecobichon D (2001) Toxic effects of pesticides. In: Klaasen CD, Amdur MO, Doull J (eds) Cassaret and Doull's toxicology: the basic science of poisons. McGraw-Hill, New York, pp 165-176
22. Elia AC, Galarini R, Taticchi MI, Dorr AJ, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162-167 (Pubitemid 36555400)
23. Ellis G, Goldberg DM (1971) An improved manual and semiautomatic assay for NADP-dependent isocitrate dehydrogenase activity, with a description of some kinetic properties of human liver and serum enzyme. Clin Biochem 2:175-185
24. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of aceylcholinesterase activity. Biochem Pharmacol 7:88-95
25. Escartin E, Porte C (1996) Bioaccumulation, metabolism and biochemical effects of the organophosphorous pesticide fenitrothion in Procambarus clarkii. Environ Toxicol Chem 15(6): 915-920 (Pubitemid 26174199)
26. Ferrari A, Venturino A, de D'Angelo AMP (2007) Effects of carbaryl and azinphosmethyl on juvenile rainbow trout (Oncorhynchus mykiss) detoxifying enzymes. Pest Biochem Physiol 88:134-142 (Pubitemid 46452720)
27. Ferreira M, Caetano M, Antunes P, Costa J et al (2010) Assessment of contaminants and biomarkers of exposure in wild and farmed seabass. Ecotoxicol Environ Saf 73:579-588
28. Flammarion P, Migeon B, Urios S, Morfin P, Garric J (1998) Effect of methidathion on the cytochrome P-450 1A in the cyprinid fish gudgeon (Gobio gobio). Aquat Toxicol 42(2):93-102 (Pubitemid 28273069)
29. Flohé L, Günzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114-121 (Pubitemid 14165378)
30. Flohé L, Ötting F (1984) Superoxide dismutase assays. Methods Enzymol 105:93-104 (Pubitemid 14165376)
31. Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25(1): 272-280 (Pubitemid 43031228)
32. Förlin L, Hylland K (2006) Hepatic cytochrome P4501A concentration and activity in Atlantic cod caged in two North Sea pollution gradients. In: Hylland K, Lang T, Vethaak AD (eds) Biological effects of contaminants in marine pelagic ecosystems. Society of Environmental Toxicology and Chemistry (SETAC), Pensacola
33. Frasco MF, Guilhermino L (2002) Effects of dimethoate and betanaphthoflavone on selected biomarkers of Poecilia reticulata. Fish Physiol Biochem 26:149-156 (Pubitemid 37168149)
34. Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorous insecticide exposure and effects. Environ Toxicol Chem 20(1):37-45 (Pubitemid 32061543)
35. Galloway TS (2006) Biomarkers in environmental and human health risk assessment. Mar Pollut Bull 53:606-613 (Pubitemid 44737863)
36. Galloway TS, Millward N, Browne MA, Depledge MH (2002) Rapid assessment of organophosphrous/carbamate exposure in the bivalve mollusc Mytilus edulis using combined esterase activities as biomarkers. Aquat Toxicol 61:169-180 (Pubitemid 35287179)
37. Galloway TS, Browne MA, Dissanayake A, Lowe D, Jones MB, Depledge MH (2004) A multibiomarker approach to environmental assessment. Environ Sci Technol 38:1723-1731 (Pubitemid 38364918)
38. Gravato C, Guilhermino L (2009) Effects of benzo(a)pyrene on seabass (Dicentrarchus labrax L.): biomarkers, growth and behaviour. Hum Ecol Risk Assess 15:121-137
39. Gravato C, Santos M (2003) Dicentrarchus labrax biotransformation and genotoxicity responses after exposure to a secondary treated industrial/urban effluent. Ecotoxicol Environ Saf 55(3):300-306 (Pubitemid 36683187)
40. Guilhermino L, Lopes MC, Carvallho AP, Soares AMVM (1996) Acetylcholinesterase activity in juveniles of Daphnia magna Straus. Bull Environ Contam Toxicol 57:979-985 (Pubitemid 26371220)
41. Guilhermino L, Barros P, Silva MC, Soares AMVM (1998) Should the use of inhibition of cholinesterases as a specific biomarker for organophosphate and carbamate pesticides be questioned? Biomarkers 3:157-163 (Pubitemid 28186604)
42. Guilhermino L, Lacerda MN, Nogueira A, Soares AMVM (2000) In vitro and in vivo inhibition of Daphnia magna acetylcholinesterase by surfactant agents: possible implications for contamination biomonitoring. Sci Total Environ 247:137-141 (Pubitemid 30145666)
43. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases, the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130-7139
44. Hagger JA, Jones MB, Lowe D, Paul Leonard DR, Owen R, Galloway TS (2008) Application of biomarkers for improving risk assessments of chemicals under the Water Framework Directive: a case study. Mar Pollut Bull 56:1111-1118
45. Hannam ML, Hagger JA, Jones MB, Galloway TS (2008) Characterisation of esterases as potential biomarkers of pesticide exposure in the lugworm Arenicola marina (Annelida: Polychaeta). Environ Pollut 152(2):342-350 (Pubitemid 351312319)
46. Hansson T, Schiedek D, Lehtonen KK, Pekka J et al (2006) Biochemical biomarkers in adult female perch (Perca fluviatilis) in a chronically polluted gradient in the Stockholm recipient (Sweden). Mar Pollut Bull 53(8):451-468 (Pubitemid 44425269)
47. Heath AG, Cech JJ, Bink L, Moberg P, Zinkl JG (1997) Physiological responses of fathead minnow larvae to rice pesticides. Ecotoxicol Environ Saf 37:280-288 (Pubitemid 27439149)
48. Hodson PV, Kloepper-Sams PJ, Munkittrick KR, Lockhart WL, Metner DA, Luxon PL, Smith IR, Gagnon MM, Servos M, Payne JF (1991) Protocols for measuring mixed function oxygenases of fish liver. Canadian Technical Report of Fisheries and Aquatic Sciences 1829
49. Jo SH, Son MK, Koh HJ, Lee SM et al (2001) Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP?-dependent isocitrate dehydrogenase. J Biol Chem 276(19):16168-16176
50. Kavitha P, Rao JV (2007) Oxidative stress and locomotory behaviour response as biomarkers for assessing recovery status of mosquito fish (Gambusia affinis) after lethal effect of an organophosphate pesticide, monocrotophos. Pesticide Biochem Physiol 87:182-188 (Pubitemid 44969924)
51. Kavitha P, Rao JV (2009) Sub-lethal effects of profenophos on tissuespecific antioxidant responses in a euryhyaline fish Oreochromis mossambicus. Ecotoxicol Environ Saf 72:1727-1733
52. Kennedy CJ, Farrell AP (2006) Effects of exposure to the watersoluble fraction of crude oil on the swimming performance and the metabolic and ionic recovery post-exercise in Pacific herring (Clupea pallasi). Environ Toxicol Chem 25:2715-2724 (Pubitemid 44898437)
53. Kienle C, Köhler HR, Filser J, Gerhardt A (2008) Effects of nickel chloride and oxygen depletion on behaviour and vitality of zebra fish Danio rerio (Hamilton, 1822) (Pisces, Cypriniformes) embryos and larvae. Environ Pollut 152:612-620 (Pubitemid 351444857)
54. Kitamura S, Kadota T, Yoshida M, Jinno N, Ohta S (2000) Wholebody metabolism of the organophosphorus pesticide, fenthion, in goldfish, Carassius auratus. Comp Biochem Physiol C 126(3): 259-266 (Pubitemid 30665524)
55. Labrot F, Ribeira D, Saint-Denis M, Narbonne JF (1996) In vitro and in vivo studies of potential biomarkers of lead and uranium contamination: lipid peroxidation, acetylcholinesterase, catalase and glutathione peroxidase activities in three non-mammalian species. Biomarkers 1:21-28 (Pubitemid 126710650)
56. Lee SM, Koh H-J, Park DL, Song BJ, Huh TL (2002) Cytosolic NADP?-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic Biol Med 32(11): 1185-1196 (Pubitemid 34603355)
57. Lemaire P, Berhaut J, Lemaire-Gony S, Lafaurie M (1992) Ultrastructural changes induced by benzo(a)pyrene in seabass (Dicentrarchus labrax) liver and intestine: importance of the intoxication route. Environ Res 57(1):59-72
58. Lemaire P, Fö rlin L, Livingstone DR (1996) Responses of hepatic biotransformation and antioxidant enzymes to CYP1A-inducers (3- methylcholantrene) in sea bass (Dicentrarchus labrax), dab (Limanda limanda) and rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 36:141-160 (Pubitemid 27014147)
59. Lemaire-Gony S, Lemaire P, Pulsford AL (1995) Effects of cadmium and benzo(a)pyrene on the immune system, gill ATPase and EROD activity of European seabass Dicentrarchus labrax. Aquat Toxicol 31(4):297-313
60. Levi PE, Hollingworth RM, Hodgson E (1988) Differences in oxidative dearylation and desulfuration of fenitrothion by cytochrome P-450 isozymes and in the subsequent inhibition of monooxygenase activity. Pest Biochem Physiol 32(3): 224-231 (Pubitemid 19025425)
61. Lima I, Moreira SM, Osten JR, Soares AMVM, Guilhermino L (2007) Biochemical responses of the marine mussel Mytilus galloprovincialis to petrochemical environmental contamination along the Northwestern coast of Portugal. Chemosphere 66: 1230-1242 (Pubitemid 44854097)
62. Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656-666 (Pubitemid 32717602)
63. Mcintosh AD, Hylland K, Gowland BTG, Davies IM (2006) Assessment of hepatic 7-ethoxiresorufin O-deethylase activity and CYP1A concentration in herring (Clupea harengus) and saithe (Pollachius virens) from two areas of the North Sea. In: Hylland K, Lang T, Vethaak AD (eds) Biological effects of contaminants in marine pelagic ecosystems. Society of Environmental Toxicology and Chemistry (SETAC), Pensacola
64. Miyamoto J, Takimoto Y, Mihara K (1979) Metabolism of organophosphorous insecticides in aquatic organisms, with special emphasis on fenitrothion. In: Kahn MAQ, Lech JJ, Menn JJ (eds) Pesticide and xenobiotic metabolism in aquatic species. ACS symposium series. American Society, Washington, DC, p 145
65. Moreira SM, Lima I, Ribeiro R et al (2006) Effects of estuarine sediment contamination on feeding and on key physiological functions of the polychaete Hediste diversicolor. Laboratory and in situ assays. Aquat Toxicol 78:186-201
66. Moyle PB, Cech JJ (2003) Fishes: an introduction to ichthyology, 5th edn. Prentice Hall, Upper Saddle River, pp 192-196
67. Novi S, Pretti C, Cognetti AM, Longo V, Marchetti S, Gervasi PG (1998) Biotransformation enzymes and their induction by ß-naphtoflavone in adult sea bass (Dicentrarchus labrax). Aquat Toxicol 41:63-81 (Pubitemid 28166164)
68. OECD (1992) OECD guidelines for the testing of chemicals. Test 203: fish, acute toxicity test
69. Ohkawa H (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351-358 (Pubitemid 9194347)
70. Oruç EO (2010) Oxidative stress, steroid hormone concentrations and acetylcholinesterase activity in Oreochromis niloticus exposed to chlorpyrifos. Pest Biochem Physiol 96:160-166
71. Payne JF, Mathieu A, Melvin W, Fancey LL (1996) Acetylcholinesterase, and old biomarker with a new future? Field trials in association with two urban rivers and a paper mill in Newfoundland. Mar Pollut Bull 32(2):225-231
72. Peakall DB, Thompson H, Baatrup E (2002) Relationship between behaviour and the biochemical/physiological biomarkers of exposure to environmental pollutants. In: Dell'Omo G (ed) Behavioural ecotoxicology. Wiley, Chichester, pp 187-208
73. Peña-Llopis S, Ferrando MD, Peña JB (2003) Fish tolerance to organophosphate-induced oxidative stress is dependent on the gluthathione metabolism and enhanced by N-acetylcisteine. Chemosphere 45:671-681
74. Pickett GD, Pawson MG (1994) Seabass: biology, exploitation and conservation. Fish and fisheries series 12. Chapman & Hall, London
75. Piner P, Sevgiler Y, Uner N (2007) In vivo effects of fenthion on oxidative processes by the modulation of glutathione metabolism in the brain of Oreochromis niloticus. Environ Toxicol 22(6): 605-612 (Pubitemid 350105972)
76. Rees CB, McCormick SD, Vanden Heuvel JP, Li W (2003) Quantitative PCR analysis of CYP1A induction in Atlantic salmon (Salmo salar). Aquat Toxicol 62(1):67-78 (Pubitemid 36159010)
77. Sancho E, Ferrando MD, Andreu E (1997) Response and recovery of brain acetylcholinesterase activity in the European eel, Anguilla anguilla, exposed to fenitrothion. Ecotoxicol Environ Saf 38:205-209 (Pubitemid 28082353)
78. Sancho E, Fernandez-Vega C, Villarroel MJ, Andreu-Moliner E, Ferrando MD (2009) Physiological effects of tricyclazole on zebrafish (Danio rerio) and post-exposure recovery. Comp Biochem Physiol C 150:25-32
79. Sandahl JF, Baldwin DH, Jenkins JJ et al (2005) Comparative thresholds for acetylcholinesterase inhibition and behavioural impairment in coho salmon exposed to chlorpyrifos. Environ Toxicol Chem 24:136-145 (Pubitemid 39658152)
80. Schlenk D (2005) Pesticide biotransformation in fish. Biochem Mol Biol Fish 6:171-190
81. Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369-392 (Pubitemid 38726150)
82. Solomon SS, De Fang F, Shao-nan L (2000) Hepatic glutathione S-transferase activity in mosquito fish (Gambusia affinis) and topmouth gudgeon (Pseudorasobora parva) exposed to fenitrothion. J Zhejiang Univ Sci 1(2):190-195
83. Stegeman JJ, Kloepper-Sams PJ (1987) Cytochrome P-450 enzymes and monooxygenase activity in aquatic animals. Environ Health Perspect 71:87-95 (Pubitemid 17115228)
84. Stegeman JJ, Schlezinger JJ, Craddock JE, Tillitt DE (2001) Cytochrome P450 1A expression in midwater fishes: potential effects of chemical contaminants in remote oceanic zones. Environ Sci Technol 35(1):54-62
85. Torres MA, Testa CP, Gáspari C et al (2002) Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island. Brazil Mar Pollut Bull 44:923-932 (Pubitemid 35291908)
86. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57-149 (Pubitemid 35441240)
87. Varò I, Navarro JC, Amat F, Guilhermino L (2003) Effect of dichlorvos on cholinesterase activity of the European seabass (Dicentrarchus labrax). Pesticide Biochem Physiol 75:61-72 (Pubitemid 36521978)
88. Vassault A (1983) Lactate dehydrogenase. In: Bergmeyer HV (ed) Methods in enzymatic analysis, vol 3. Verlag Chemie, Weinheim, pp 118-126
89. Vieira LR, Sousa A, Frasco MF, Lima I, Morgado F, Guilhermino L (2008) Acute effects of benzo[a]pyrene, anthracene and a fuel oil on biomarkers of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Sci Total Environ 395(2-3):87-100
90. Vieira LR, Gravato C, Soares AMVM, Morgado F, Guilhermino L (2009) Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 76:1416-1427
91. Walker CH, Hopkin SP, Sibly RM, Peakall DB (2001) Principles of ecotoxicology, 2nd edn. Taylor and Francis, London
92. Wallace WG, Estephan A (2004) Differential susceptibility of horizontal and vertical swimming activity to cadmium exposure in a gammaridean amphipod (Gammarus lawrencianus). Aquat Toxicol 69:289-297 (Pubitemid 38970054)
93. Weber DN, Dingel WM, Panos JJ et al (1997) Alterations in neurobehavioral responses in fishes exposed to lead and leadchelating agents. Am Zool 37:354-362
94. Weis JS, Smith G, Zhou T, Santiago-Bass C, Weis P (2001) Effects of contaminants on behaviour: biochemical mechanisms and ecological consequences. Bioscience 51(3):209-217 (Pubitemid 32449501)
95. Whyte JJ, Jung RE, Schmitt CJ, Tillitt DE (2000) Ethoxyresorufin- Odeethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev Toxicol 30:347-570 (Pubitemid 30636029)
96. Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137-161.
97. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Inc, Upper Saddle River.