Resistance to contaminants in North American fish populations

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 552, Issue 1-2, 2004, Pages 73-100

  Wirgin, Isaac ^a   Waldman, John R ^b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Hudson River Foundation   (United States)

Author keywords

Aryl hydrocarbon receptor pathway; Evolutionary cost; Genetic adaptation; Physiological acclimation; Resistance

Indexed keywords

AROMATIC HYDROCARBON; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A; LEAD; MERCURY; MESSENGER RNA; POLYCHLORINATED BIPHENYL; POLYCHLORINATED DIBENZODIOXIN; POLYCHLORINATED DIBENZOFURAN; POLYCYCLIC AROMATIC HYDROCARBON; ZINC;

ACCLIMATIZATION; BIOLOGICAL TRAIT; CHEMICAL TERATOGENESIS; CHRONIC TOXICITY; CYPRINODONTIFORMES; DEVELOPMENTAL STAGE; DNA BINDING; EMBRYOTOXICITY; ENVIRONMENTAL EXPOSURE; EPIGENETICS; ESTUARY; EVOLUTIONARY ADAPTATION; FISH; GENETIC DIFFERENCE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HALOGENATION; HERITABILITY; LETHALITY; NONHUMAN; NORTH AMERICA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; REVIEW; TOXICITY TESTING; WATER CONTAMINATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; DRUG RESISTANCE; FISHES; FRESH WATER; NORTH AMERICA; WATER POLLUTANTS, CHEMICAL;

FUNDULUS; FUNDULUS HETEROCLITUS; MICROGADUS; MICROGADUS TOMCOD; VERTEBRATA;

EID: 3843111448     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2004.06.005     Document Type: Review

References (93)

1. Wirgin I., Waldman J.R. Altered gene expression and genetic damage in North American fish populations. Mutat. Res. 399:1998a;193-219
2. Klerks P.L., Leberg P.L., Lance R.F., McMillin D.J., Means J.C. Lack of development of pollutant-resistance or genetic differentiation of darter gobies (Gobionellus boleosoma) inhabiting a produced-water discharge site. Mar. Environ. Res. 44:1997;377-395
3. A.J. Shaw, The evolution of heavy metal tolerance in plants: adaptations, limits, and costs, in: V.E. Forbes (Ed.), Genetics and Ecolotoxicology, Taylor and Francis, Philadelphia, PA, 1999, pp. 9-30.
4. J.A. McKenzie, Ecological and Evolutionary Aspects of Insecticide Resistance, R.G. Landes Company, Austin, TX, 1996.
5. Klerks P.L., Levinton J.S. Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol. Bull. 176:1989;135-141
6. Klerks P.L., Batholomew P.R. Cadmium accumulation and detoxification in a Cd-resistant population of the oligochaete Limnodrilus hoffmeisteri. Aquat. Toxicol. 19:1991;97-112
7. Y.-Z. Gu, J.B. Hogenesch, C.A. Bradfield, The PAS SUPERFAMILY: sensors of environmental and development signals, Annu. Rev. Pharmacol. Toxicol. (2000) 519-561.
8. Ma Q. Induction of CYP1A1. The AhR/DRE paradigm: Transcription receptor regulation, and expanding biological roles. Curr. Drug Metab. 2:2001;149-164
9. Mimura J., Emma M., Sogawa K., Fujii-Kuriyama Y. Identification of a novel mechanism of regulation of Ah (dioxin) receptor function. Genes Dev. 13:1999;20-25
10. Hahn M.E., Karchner S.I., Shapiro M.A., Perera S.A. Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc. Natl. Acad. Sci. U.S.A. 94:1997;13743-13748
11. Hansson M.C., Wittzell H., Persson K., Von Schantz T. Unprecedented genomic diversity of AhR1 and AhR2 genes in Atlantic salmon (Salmo salar L.). Aquat. Toxicol. 68:2004;219-232
12. S.M. Cormier, R.N. Racine, Histopathology of Atlantic tomcod: a possible monitor of xenobiotics in northeast tidal rivers and estuaries, in: J.F. McCarthy, L.R. Shugart (Eds.), Biomarkers of Environmental Contamination, Lewis Publishers, Boca Raton, FL, 1990, pp. 59-71.
13. Dey W.P., Peck T.H., Smith C.E., Kreamer G.-L. Epizoology of hepatic neoplasia in Atlantic tomcod (Microgadus tomcod) from the Hudson River estuary. Can. J. Fish Aquat. Sci. 50:1993;1897-1907
14. Wirgin I.I., Grunwald C., Courtenay S., Kreamer G.-L., Reichert W.L., Stein J.E. A biomarker approach to assessing xenobiotic exposure in Atlantic tomcod from the North American Atlantic coast. Environ. Health Perspect. 102:1994;764-770
15. Wirgin I.I., Currie D.C., Garte S.J. Activation of the K-ras oncogene in liver tumors of Hudson River tomcod. Carcinogenesis. 10:1989;2311-2315
16. Roy N.K., Kreamer G.-L., Konkle B., Grunwald C., Wirgin I. Characterization and prevalence of a polymorphism in the 3′ untranslated region of cytochrome P4501A1 in cancer-prone Atlantic tomcod. Arch. Biochem. Biophys. 322:1995;204-213
17. Wirgin I.I., D'Amore M., Grunwald C., Goldman A., Garte S.J. Genetic diversity at the c-abl oncogene locus and in mitochondrial DNA between populations of cancer-prone Atlantic tomcod. Biochem. Genet. 28:1990;459-475
18. Courtenay S.C., Grunwald C.M., Kreamer G.-L., Fairchild W.L., Arsenault J.T., Ikonomou M., Wirgin I.I. A comparison of the dose and time response of CYP1A1 mRNA induction in chemically treated Atlantic tomcod from two populations. Aquat. Toxicol. 47:1999;43-69
19. Ikonomou M., Fernandez M., Courtenay S.C., Wirgin I.I. Comparison of congener patterns and total PCBs and PCDD/Fs in young-of-the-year and adult Atlantic tomcod Microgadus tomcod from multiple locations in the Hudson River estuary. Environ. Sci. Technol. 38:2004;976-983
20. Yuan Z., Wirgin M., Courtenay S., Ikonomou M., Wirgin I. Is hepatic cytochrome P4501A1 expression predictive of dioxins, furans, and PCB burdens in Atlantic tomcod from the Hudson River estuary? Aquat. Toxicol. 54:2001;217-230
21. Roy N.K., Courtenay S., Yuan Z., Ikonomou M., Wirgin I. An evaluation of the etiology of reduced CYP1A1 messenger RNA expression in the Atlantic tomcod from the Hudson River, New York, USA, using reverse transcriptase polymerase chain reaction analysis. Environ. Toxicol. Chem. 20:2001;1022-1030
22. Cantrell S.M., Joy-Schlezinger J., Stegeman J.J., Tillit D.E., Hannink M. Correlation of 2,3,7,8-tetrachlorodibenzo-p-dioxin induced apoptotic cell death in the embryonic vasculature with embryotoxicity. Toxicol. Appl. Pharmacol. 148:1998;24-34
23. J.J. Stegeman, M.E. Hahn, Biochemistry and molecular biology of monoxygenases: current perspectives on forms, functions, and regulation of cytochrome P450 in aquatic species, in: D.C. Malins, G.K. Ostrander (Eds.), Aquatic Toxicology: Molecular, Biochemical, and Cellular Perspectives, Lewis Publishers, Boca Raton, FL, 1994, pp. 87-206.
24. Van den Berg M., et al. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for human and wildlife. Environ. Health Perspect. 106:1998;775-792
25. Roy N.K., Courtenay S., Maxwell G., Yuan Z., Chamber R.C., Wirgin I. Cytochrome P4501A1 is induced by PCB 77 and benzo[a]pyrene treatment but not by exposure to the Hudson River environment in Atlantic tomcod (Microgadus tomcod) post-yolk sac larvae. Biomarkers. 7:2002;162-173
26. Wirgin I.I., Kreamer G.-L., Grunwald C., Squibb K., Garte S.J., Courtenay S. Effects of prior exposure history on cytochrome P450IA mRNA induction by PCB congener 77 in Atlantic tomcod. Mar. Environ. Res. 34:1992;103-108
27. Z. Yuan, Resistance of cytochrome P4501A1 mRNA to induction by halogenated aryl hydrocarbons in Hudson River Atlantic tomcod - its prevalence and mechanistic basis, Doctoral dissertation, Department of Environmental Medicine, New York University School of Medicine, Tuxedo, New York, 2003.
28. Courtenay S., Williams P.J., Grunwald C., Ong T.-L., Konkle B., Wirgin I.I. An assessment of within group variation in CYP1A1 mRNA inducibility in Atlantic tomcod. Environ. Health Perspect. 102(Suppl. 12):1994;85-90
29. Elonen G.E., Spehar R.L., Holcombe G.W., Johnson R.D., Fernandez J.D., Erickson R.J., Tietge J.E., Cook P.M. Comparative toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to seven freshwater fish species during early life-stage development. Environ. Toxicol. Chem. 17:1998;472-483
30. Walker M.K., Spitsbergen J.M., Olsen J.R., Peterson R.E. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) toxicity during early life stage development of lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 48:1991;875-883
31. Walker M.K., Cook P.M., Batterman A.R., Butterworth B.C., Berini C., Libal J.J., Hufnagle L.C., Peterson R.E. Translocation of 2,3,7,8- tetrachlorodibenzo-p-dioxin from adult female lake trout (Salvelinus namaycush) to oocytes: effects on early life stage development and sac fry survival. Can. J. Fish. Aquat. Sci. 51:1994;1410-1419
32. Sorrentino C., Roy N.K., Chambers R.C., Courtenay S.C., Wirgin I. B[a]P-DNA binding in early life-stages of Atlantic tomcod: population differences and chromium modulation. Mar. Environ. Res. 53:2004;383-388
33. Maier A., Dalton T.P., Puga A. Disruption of dioxin-inducible Phase I and Phase II gene expression patterns by cadmium, chromium, and arsenic. Mol. Carcinog. 28:2000;225-235
34. Risso-de Favernay C., Lafaurie M., Girard J.-P., Rahmani R. Effects of heavy metals and 3-methylcholanthrene on expression and induction of CYP1A1 and metallothionein levels in trout (Oncorhynchus mykiss) hepatocyte cultures. Environ. Toxicol. Chem. 9:2000;2239-2248
35. Dew C.B. The nonrandom size distribution and size-selective transport of age-0 Atlantic tomcod (Microgadus tomcod) in the lower Hudson River estuary. Can. J. Fish. Aquat. Sci. 52:1995;2353-2366
36. Roy N.K., Konkle B., Wirgin I. Evaluation of cytochrome P4501A1 regulatory elements in cancer-prone Atlantic tomcod. Pharmacogenetics. 6:1996;273-277
37. Roy N.K., Wirgin I. Characterization of the aromatic hydrocarbon receptor gene and its expression in Atlantic tomcod. Arch. Biochem. Biophys. 344:1997;373-386
38. N.K. Roy, J. Duffy, M. Zarzecka, I.I. Wirgin, Comparison of AHR, ARNT, and AHRR expression in chemically-treated and environmentally-exposed Atlantic tomcod from two populations, Abstract #725. SETAC 23rd Annual Meeting in North America, Salt Lake City, Utah, 2002.
39. Lotrich V.A. Summer home range and movements of Fundulus heteroclitus (Pisces: Cyprinodonidae) in a tidal creek. Ecology. 56:1975;191-198
40. Fritz E.S., Meredith W.H., Lotrich V.A. Fall and winter movements of and activity level of the mummichog, Fundulus heteroclitus, in a tidal creek. Chesapeake Sci. 16:1975;211-214
41. Brown B.L., Chapman R.W. Gene flow and mitochondrial DNA variation in the killifish Fundulus heteroclitus. Evolution. 45:1991;1147-1161
42. Powers D.A., Schulte P.M. Evolutionary adaptations of gene structure and expression in natural populations in relation to a changing environment: a multidisciplinary approach to address the million-year saga of a small fish. J. Exp. Zool. 282:1998;71-94
43. Prince R., Cooper K.R. Comparisons of the effects of 2,3,7,8- tetrachlordibenzo-p-dioxin on chemically impacted and nonimpacted subpopulations of Fundulus heteroclitus. I. TCDD toxicity. Environ. Toxicol. Chem.14:1995;579-588
44. Prince R., Cooper K.R. Comparisons of the effects of 2,3,7,8- tetrachlorodibenzo-p-dioxin on chemically impacted and nonimpacted subpopulations of Fundulus heteroclitus. II. Metabolic considerations. Environ. Toxicol. Chem. 14:1995;589-596
45. Henry T.A., Spitsbergen J.M., Hornung M.W., Abnet C.C., Peterson R.E. Early life-stage toxicity of 2,3,7,8-tetrachlorodibezo-p-dioxin in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 142:1997;56-86
46. Elskus A.A., Monosson E., McElroy A.E., Stegeman J.J., Woltering D.S. Altered CYP1A expression in Fundulus heteroclitus adults and larvae: a sign of pollutant resistance. Aquat. Toxicol. 45:1999;99-113
47. X. Arzuaga, S. Karchner, W. Powell, M. Hahn, A. Elskus, Sequence analysis and comparison of the CYP1A promoter region from AHR ligand resistant and responsive killifish (Fundulus heteroclitus) populations, 23rd Annual Meeting of Society of Environmental Toxicology and Chemistry, Salt Lake City, Utah, 16-20 November 2002.
48. Arzuaga X., Calcano W., Elskus A. The DNA de-methylating agent 5-azacytidine does not restore CYP1A induction in PCB resistant Newark Bay killifish (Fundulus heteroclitus). Mar. Environ. Res. 58:2004;517-520
49. Vogelbein W.K., Fournie J.W., Van Veld P.A., Huggett R.J. Hepatic neoplasms in the mummichog Fundulus heteroclitus from a creosote-contaminated site. Cancer Res. 50:1990;5978-5986
50. Vogelbein W.K., Fournie J.W. Ultrastruture of normal and neoplastic exocrine pancreas in the mummichog, Fundulus heteroclitus from a creosote contaminated site. Toxicol. Pathol. 22:1994;248-260
51. Van Veld P., Westbrook D. Evidence for depression of cytochrome P4501A in a population of chemically resistant mummichog (Fundulus heteroclitus). Environ. Sci. 3/4:1995;221-234
52. Owenby D.R., Newman M.C., Mulvey M., Vogelbein W.K., Unger M.A., Arzayus L.F. Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environ. Toxicol. Chem. 21:2002;1897-1902
53. Meyer J.N., Nacci D.E., Di Giulio R.T. Cytochrome P4501A in killifish (Fundulus heteroclitus): heritability of altered expression and relationship to survival in contaminated sediments. Toxicol. Sci. 68:2002;69-81
54. Meyer J., Di Giulio R. Patterns of heritability of decreased EROD activity and resistance to PCB 126-induced teratogenesis in laboratory-reared offspring of killifish (Fundulus heteroclitus) from a creosote-contaminated site in the Elizabeth River, VA, USA. Mar. Environ. Res. 54:2002;1-6
55. J.N. Meyer, A.R. Timme, R.A. Waterland, W.H. Powell, S.I. Karchner, M.E. Hahn, R.T. Di Giulio, Analysis of CpG methylation in the promoter region of the CYP1A gene in Fundulus heteroclitus from creosote-contaminated and reference sites, Pollutant Responses in Marine Organisms, Tampa, FL, May 2003, PRIMO 12, p. 81.
56. Oleksiak M.F., Kolell K.J., Crawford D.L. Utility of natural populations for microarray analyses: isolation of genes necessary for functional genomic studies. Mar. Biotechnol. S203:2001;203-211
57. Mulvey M., Newman M.C., Vogelbein W., Unger M.A. Genetic structure of Fundulus heteroclitus from PAH-contaminated and neighboring sites in the Elizabeth and York Rivers. Aquat. Toxicol. 61:2002;195-209
58. Mulvey M., Newman M.C., Vogelbein W.K., Unger M.A., Owenby D.R. Genetic structure and mtDNA diversity of Fundulus heteroclitus populations from polycyclic aromatic hydrocarbon-contaminated sites. Environ. Toxicol. Chem. 22:2003;671-677
59. Bergelson J., Purrington C.B. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:1996;536-558
60. Meyer J.N., Di Giulio R.T. Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol. Appl. 13:2003;490-503
61. Armknecht S.L., Kattari S.L., Van Veld P.A. An elevated glutathione S-transferase in creosote-resistant mummichog (Fundulus heteroclitus). Aquat. Toxicol. 41:1998;1-16
62. Van Veld P.A., Ko U., Vogelbein W.K., Westbrook W.K. Glutathione S-transferase in intestine, liver and hepatic lesions of mummichog (Fundulus heteroclitus) from a creosote-contaminated environment. Fish Physiol. Biochem. 9:1991;369-376
63. Cooper P.S. Altered expression of the xenobiotic P-gylcoprotein in liver and liver tumours of mummichog Fundulus heteroclitus from a creosote- contaminated environment. Biomarkers. 4:1999;48-58
64. Hahn M.E. Mechanisms of innate and acquired resistance to dioxin-like compounds. Rev. Toxicol. Series B: Environ. Toxicol. 2:1998;395-443
65. Meyer J.N., Wassenberg D.A., Karchner S.I., Hahn M.E., Di Giulio R.T. Expression and inducibility of aryl hydrocarbon receptor pathway genes in wild-caught killifish (Fundulus heteroclitus) with different contaminant-exposure histories. Environ. Toxicol. Chem. 22:2003;2337-2343
66. Meyer J.N., Smith J.D., Winston G.W., Di Giulio R.T. Antioxidant defenses in killifish (Fundulus heteroclitus) exposed to contaminated sediments and model prooxidants: short-term and heritable responses. Aquat. Toxicol. 65:2003;377-395
67. Pruell R.J., Norwood C.B., Bowen R.D., Boothman W.S., Rogerson P.F., Hackett M., Butterworth B.C. Geochemical study of sediment contamination in New Bedford Harbor, Massachusetts. Mar. Environ. Res. 29:1990;77-101
68. Long E., MacDonald D., Smith S., Calder F. Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ. Manage. 19:1995;81-97
69. Nacci D., Coiro L., Champlin D., Jayaraman S., McKinney R., Gleason T.R., Munns W.R. Jr., Specker J.L., Cooper K.R. Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar. Biol. 134:1999;9-17
70. S. Bello, Characterization of resistance to halogenated aromatic hydrocarbons in a population of Fundulus heteroclitus from a marine Superfund site. Ph.D. Thesis. Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, Woods Hole, MA, USA, 1999.
71. Nacci D.E., Kohan M., Pelleier M., George E. Effects of benzo[a]pyrene exposure on a fish population resistant to the toxic effects of dioxin-like compounds. Aquat. Toxicol. 57:2002;203-215
72. Bello S.M., Franks D.G., Stegeman J.J., Hahn M.E. Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine Superfund site: in vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes. Toxicol. Sci. 60:2001;77-91
73. Nacci D.E., Champlin D., Coiro L., McKinney R., Jayarman S. Predicting the occurrence of genetic adaptation to dioxin-like compounds in populations of the estuarine fish Fundulus heteroclitus. Environ. Toxicol. Chem. 21:2002;1525-1532
74. Cohen S. Strong positive selection and habitat-specific amino acid substitution patterns in Mhc from an estuarine fish under intense pollution stress. Mol. Biol. E. 19:2002;1870-1880
75. S.A. Roark, D. Nacci, L. Corio, D. Champlin, S.I. Guttman, Population genetic structure of a non-migratory estuarine fish Fundulus heteroclitus across a strong gradient of PCB contamination, Environ. Toxicol. Chem., in press.
76. Powell W.H., Bright R., Bello S., Hahn M.E. Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish Fundulus heteroclitus. Toxicol. Sci. 57:2000;229-239
77. Tanguay R.L., Abnet C.C., Heideman W., Peterson R.E. Cloning characterization of the zebrafish (Danio rerio) aryl hydrocarbon receptor. Biochim. Biophys. Acta (Gene Struct. Express.). 1444:1999;35-48
78. Abnet C.C., Tanguay R.L., Hahn M.E., Heideman W., Peterson R.E. Two forms of aryl hydrocarbon receptor type 2 in rainbow trout (Oncorhynchus mykiss): evidence for differential expression and enhancer specificity. J. Biol. Chem. 274:1999;15159-15166
79. Hahn M.E., Karchner S.I., Franks D.G., Merson R.R. Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish (Fundulus heteroclitus). Pharmacogenetics. 14:2004;1-13
80. Karchner S.I., Franks D.G., Powell W.H., Hahn M.E. Regulatory interactions among three members of the vertebrate aryl hydrocarbon receptor family: AHR repressor, AHR1, and AHR2. J. Biol. Chem. 277:2002;6949-6959
81. Black D.E., Gutjahr-Goebell R., Pruell R.J., Bergen B., Mills L., McElroy A.E. Reproduction and polychlorinated biphenyls in Fundulus heteroclitus (Linnaeus) from New Bedford Harbor, Massachusetts, USA. Environ. Toxicol. Chem. 17:1998;1405-1414
82. J.S. Weis, N. Mugue, P. Weis, Mercury tolerance, population effects, and population genetics in the mummichog, Fundulus heteroclitus, in: V.E. Forbes (Ed.), Genetics and Ecotoxicology, Taylor & Francis, Philadelphia, 1999, pp. 31-54.
83. Khan A.T., Weis J.S. Bioaccumulation of heavy metals in two populations of mummichog (Fundulus heteroclitus). Bull. Environ. Contam. Toxicol. 51:1993;1-5
84. Weis J.S., Weis P. A rapid change in methylmercury tolerance in a population of killifish, Fundulus heteroclitus, from a golf course pond. Mar. Environ. Res. 13:1984;231-245
85. J.S. Weis, P. Weis, M. Renna, S. Vajdya, Search for a physiological component of methylmercury tolerance in the mummichog, Fundulus heteroclitus, in: F.J. Vernberg, F.P. Thurberg, A. Calabrese, W.B. Vernberg (Eds.), Marine Pollution and Physiology: Recent Advances, University of South Carolina Press, Columbia, 1985, pp. 309-326.
86. Bush C.P., Weis J.S. Effects of salinity on fertilization success in two populations of Fundulus heteroclitus. Biol. Bull. 164:1983;406-417
87. Weis P., Weis J.S. Methylmercury inhibition of fin regeneration in fishes and its interaction with salinity and cadmium. Estuarine Coast. Mar. Sci. 6:1978;327-334
88. Klerks P.L., Lentz S.A. Resistance to lead and zinc in the western mosquitofish Gambusia affinis inhabiting contaminated Bayou Trepagnier. Ecotoxicology. 7:1998;11-17
89. McLaren J.B., Peck T.H., Dey W.P., Gardinier M. Biology of Atlantic tomcod in the Hudson River estuary. Am. Fish. Soc. Mono. 4:1988;102-112
90. Abraham, B. Jun, Species Profiles: Life Histories and Environmental Requirements of Coastal Fishes and Invertebrates: Mummichog and Striped Killifish. Biol. Rep. 82 (1985) 1-14.
91. P.L. Klerks, The influence of contamination complexity on adaptation to environmental contaminants, in: V.E. Forbes (Ed.), Genetics and Ecotoxicology, Taylor and Francis, Philadelphia, PA, 1999, pp. 103-121.
92. E.A. Carlson, N.K. Roy, M. Marzinke, I. Wirgin, Identification of novel genes associated with natural resistance to PCB-induced early life-stage toxicity in Atlantic tomcod populations. Abstract #89. SETAC 24th Annual Meeting in North America, Austin, TX, 2003.
93. M. Hansson, Evolution and ecology of AhR genes in Atlantic salmon (Salmo salar L.), Ph.D. Thesis, Lund University, 2004.