Assessment of the health status of wild fish from the wheatley Harbour area of Concern, Ontario, Canada

Environmental Toxicology and Chemistry

Volumn 31, Issue 12, 2012, Pages 2798-2811

  Gilroy, Ève A M ^a   McMaster, Mark E ^a   Parrott, Joanne L ^a   Hewitt, L Mark ^a   Park, Bradley J ^b   Brown, Scott B ^a   Sherry, James P ^a  

^a ENVIRONMENT CANADA   (Canada)

^b FRESHWATER INSTITUTE   (Canada)

Author keywords

Areas of concern; Brown bullhead; Endocrine disruption; Goldfish; Polychlorinated biphenyls

Indexed keywords

ACTIVATION INDEX; AREAS OF CONCERNS; AROMATIC CONTAMINANTS; BROWN BULLHEAD; ENDOCRINE DISRUPTION; ENDOCRINE FUNCTIONS; EPITHELIAL CELLS; FISH POPULATIONS; GOLDFISH; HEALTH STATUS; HISTOLOGICAL EVALUATION; IN-VITRO; LAKE ERIE; ONTARIO , CANADA; OXYGENASES; PARTIALLY DEPLETED; PLASMA CONCENTRATION; PLASMA VITELLOGENIN; THYROID HORMONES; THYROID TISSUE;

FISH; FISHERIES; HEALTH; POLYCHLORINATED BIPHENYLS; PRINCIPAL COMPONENT ANALYSIS; SEPARATION; TISSUE; WAVE PLASMA INTERACTIONS;

GOLD;

11 OXOTESTOSTERONE; ESTRADIOL; OXYGENASE; TESTOSTERONE; THYROID HORMONE; THYROXINE; THYROXINE DEIODINASE; VITELLOGENIN;

ASSESSMENT METHOD; BIOCHEMICAL COMPOSITION; CELL ORGANELLE; COLLOID; CONCENTRATION (COMPOSITION); ENDOCRINE DISRUPTOR; ENZYME ACTIVITY; FISH; HEALTH STATUS; HISTOLOGY; HORMONE; PCB; WILD POPULATION;

AMEIURUS NEBULOSUS; ANDROGEN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANADA; CONTROLLED STUDY; ENDOCRINE FUNCTION; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; FISH; GOLDFISH; GONAD; HEALTH STATUS; HISTOLOGY; HORMONE SYNTHESIS; IN VITRO STUDY; MALE; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; STATISTICAL SIGNIFICANCE; TESTOSTERONE BLOOD LEVEL;

ANIMALS; ENVIRONMENTAL MONITORING; ESTRADIOL; FEMALE; GOLDFISH; GONADS; HEALTH STATUS; ICTALURIDAE; LAKES; MALE; ONTARIO; STRESS, PHYSIOLOGICAL; TESTOSTERONE; THYROXINE; VITELLOGENINS; WATER POLLUTANTS, CHEMICAL;

GREAT LAKES [NORTH AMERICA]; LAKE ERIE;

AMEIURUS NEBULOSUS; CARASSIUS AURATUS; COTTUS GOBIO;

EID: 84869880274     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.2021     Document Type: Article

References (76)

1. Environment Canada. 2003. Canada's RAP progress report 2003. Burlington, ON.
2. Bedard D, Petro S. 1995. Laboratory sediment bioassay report on Wheatley Harbour sediments 1992. PIBS 2479. Ontario Ministry of the Environment and Energy, Etobicoke, ON, Canada.
3. Dove A, Painter S, Williams D, Kraft J. 2003. Sediment quality and fish tissue contaminant investigations in Muddy Creek, 2002. ECB/EHD-OR/03-05/I. Environment Canada, Burlington, ON.
4. Sonstegard R, Leatherland JF. 1976. The epizootiology and pathogenesis of thyroid hyperplasia in coho salmon (Oncorhynchus kisutch) in Lake Ontario. Cancer Res 36:4467-4475.
5. Leatherland JF. 1998. Changes in thyroid hormone economy following consumption of environmentally contaminated Great Lakes fish. Toxicol Ind Health 14:41-57.
6. Otake T, Yoshinaga J, Enomoto T, Matsuda M, Wakimoto T, Ikegami M, Suzuki E, Naruse H, Yamanaka T, Shibuya N, Yasumizu T, Kato N. 2007. Thyroid hormone status of newborns in relation to in utero exposure to PCBs and hydroxylated PCB metabolites. Environ Res 105:240-246.
7. Sandala GM, Sonne-Hansen C, Dietz R, Muir DCG, Valters K, Bennett ER, Born EW, Letcher RJ. 2004. Hydroxylated and methyl sulfone PCB metabolites in adipose and whole blood of polar bear (Ursus maritimus) from East Greenland. Sci Total Environ 331:125-141.
8. Sandau CD, Ayotte P, Desailty E, Duffe J, Norstrom RJ. 2000. Analysis of hydroxylated metabolites of PCBs (OH-PCBs) and other chlorinated phenolic compounds in whole blood from Canadian Inuit. Environ Health Persp 108:611-616.
9. Turyk ME, Anderson HA, Persky VW. 2007. Relationships of thyroid hormones with polychlorinated biphenyls, dioxins, furans, and DDE in adults. Environ Health Perspect 115:1197-1203.
10. Brown SB, Adams BA, Cyr DG, Eales JG. 2004. Contaminant effects on the teleost fish thyroid. Environ Toxicol Chem 23:1680-1701.
11. Zhou T, John-Alder HB, Weis JS, Weis P. 2000. Endocrine disruption: Thyroid dysfunction in mummichogs (Fundulus heteroclitus) from a polluted habitat. Mar Environ Res 50:393-397.
12. Munkittrick KR, Barrett TJ, McMaster ME. 2010. Guidance for site-specifically assessing the health of fish populations with emphasis on Canada's Environmental Effects Monitoring Program. Water Qual Res J Canada 45:209-221.
13. Gilroy ÈAM, Muir DCG, McMaster ME, Darling C, Campbell LM, DeSolla SR, Parrott JL, Brown SB, Sherry JP. 2012. Polychlorinated biphenyls and their hydroxylated metabolites in wild fish from Wheatley Harbour Area of Concern, Ontario, Canada. Environ Toxicol Chem 31:2788-2797 (this issue).
14. Palmer MD. 1968. Some notes on small confined harbour pollution characteristics, Wheatley. Ontario Ministry of the Environment, Toronto, ON, Canada.
15. Environ International. 2007. Targeted ecological risk assessment for Muddy Creek, Wheatley Harbour, Lake Erie. Final Report. 21-18220A. Portland, ME, USA.
16. McMaster ME, Munkittrick KR, Luxon PL, Van Der Kraak GJ. 1994. Impact of low-level sampling stress on interpretation of physiological responses of white sucker exposed to effluent from a bleached kraft pulp mill. Ecotoxicol Environ Saf 27:251-264.
17. Smith SB, Donahue AP, Lipkin RJ, Blazer VS, Schmitt CJ, Goede RW. 2002. Illustrated field guide for assessing external and internal anomalies in fish. USGS/BRD/ITR-2002-2007. Reston, VA, USA.
18. McMaster ME, Munkittrick KR, Jardine JJ, Robinson RD, Van Der Kraak GJ. 1995. Protocol for measuring in vitro steroid production by fish gonadal tissue. Canadian Technical Report of Fisheries and Aquatic Sciences 1961. Department of Fisheries and Oceans, Burlington, ON, Canada.
19. McMaster ME, Munkittrick KR, Van Der Kraak GJ. 1992. Protocol for measuring circulating levels of gonadal sex steroids in fish. Canadian Technical Report of Fisheries and Aquatic Sciences 1836. Department of Fisheries and Oceans, Burlington, ON, Canada.
20. Parrott JL, Hewitt LM, Kovacs TG, MacLatchy DL, Martel PH, Paice M, Van Den Heuvel MR, Van Der Kraak GJ, McMaster ME. 2010. Responses in a fathead minnow (Pimephales promelas) lifecycle test and in wild white sucker (Catostomus commersoni) exposed to a Canadian bleached kraft mill effluent as part of Investigation of Cause Studies. Water Qual Res J Can 45:187-200.
21. Gallagher SR. 2002. One-dimensional SDS gel electrophoresis of proteins. Curr Protoc Cell Biol 37: 6.1.1-6.1.38.
22. Kavanagh RJ, Balch GC, Kiparissis Y, Niimi AJ, Sherry J, Tinson C, Metcalfe CD. 2004. Endocrine disruption and altered gonadal development in white perch (Morone americana) from the lower Great Lakes region. Environ Health Perspect 112:898-902.
23. McDaniel TV, Martin PA, Struger J, Sherry J, Marvin CH, McMaster ME. 2008. Potential endocrine disruption of sexual development in free ranging male northern leopard frogs (Rana pipiens) and green frogs (Rana clamitans) from areas of intensive row crop agriculture. Aquat Toxicol 88:230-242.
24. Al-Ansari AM, Saleem A, Kimpe LE, Sherry JP, McMaster ME, Trudeau VL, Blais JM. 2010. Bioaccumulation of the pharmaceutical 17α-ethinylestradiol in shorthead redhorse suckers (Moxostoma macrolepidotum) from the St. Clair River, Canada. Environ Pollut 158:2566-2571.
25. Dell'Angelica EC, Bonifacino JS. 2001. Staining proteins in gels, 1st ed. Curr Protoc Cell Biol May:6.6.1-6.6.14.
26. Dussault ÈB, Sherry JP, Lee H-B, Burnison BK, Bennie DT, Servos MR. 2005. In vivo estrogenicity of nonylphenol and its ethoxylates in the Canadian environment. Hum Ecol Risk Assess 11:353-364.
27. Marx A, Sherry J, Hansen P-D, Hock B. 2001. A new monoclonal antibody against vitellogenin from rainbow trout (Oncorhynchus mykiss). Chemosphere 44:393-399.
28. Osborne N, Sherry J, Rendell JL, Currie S. 2007. The role of hsp90 in 17α-ethynylestradiol-induced endocrine disruption in rainbow trout hepatocytes. Ecotoxicol Env Saf 68:13-19.
29. Brown SB, Evans RE, Vandenbyllardt L, Finnson KW, Palace VP, Kane AS, Yarechewski AY, Muir DCG. 2004. Altered thyroid status in lake trout (Salvelinus namaycush) exposed to co-planar 3, 3', 4, 4', 5-pentachlorobiphenyl. Aquat Toxicol 67:75-85.
30. Weibel ER. 1973. Stereological techniques for electron microscopic morphometry. In Hayat MA, ed, Principles and Techniques of Electron Microscopy: Biological Applications, Vol 3. Van Nostrand Reinhold, New York, NY, USA, pp 239-283.
31. Brown SB, Fisk AT, Brown M, Villella M, Muir DCG, Evans RE, Lockhart WL, Metner DA, Cooley HM. 2002. Dietary accumulation and biochemical responses of juvenile rainbow trout (Oncorhynchus mykiss) to 3, 3', 4, 4', 5-pentachlorobiphenyl (PCB 126). Aquat Toxicol 59:139-152.
32. Eales JG, Brown SB, Cyr DG, Adams BA, Finnson KR. 1999. Deiodination as an index of chemical disruption of thyroid hormone homeostasis and thyroidal status in fish. In Henshel DS, Black MC, Harrass MC, eds, Environmental Toxicology and Risk Assessment: Standardization of Biomarkers for Endocrine Disruption and Environmental Assessment: Eighth Volume. American Society for Testing and Materials, West Conshohocken, PA, USA, pp 136-164.
33. Brown SB, Eales JG. 1977. Measurement of L-thyroxine and 3, 5, 3'-triiodo-L-thyronine levels in fish plasma by radioimmunoassay. Can J Zool 55:293-299.
34. Bauer R. 1974. Use of alkaline Sephadex G-25 for extraction and measurement of serum thyroxine. Clin Chem 20:917-918.
35. Sweeting RM, Eales JG. 1992. HPLC analysis of in vitro hepatic deiodination products of thyroid hormones in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 85:367-375.
36. Hodson PV, Kloepper-Sams PJ, Munkittrick KR, Lockhart WL, Metner DA, Luxon L, 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. Department of Fisheries and Oceans, Burlington, ON, Canada.
37. Hewitt LM, Pryce AC, Parrott JL, Marlatt V, Wood C, Oakes K, Van Der Kraak GJ. 2003. Accumulation of ligands for aryl hydrocarbon and set steroid receptors in fish exposed to treated effluent from a bleached sulfite/groundwood pulp and paper mill. Environ Toxicol Chem 22:2890-2897.
38. Van Der Kraak GJ, Biddiscombe S. 1999. Polyunsaturated fatty acids modulate the properties of the sex steroid binding protein in goldfish. Fish Physiol Biochem 20:115-123.
39. Wells K, Van Der Kraak GJ. 2000. Differential binding of endogenous steroids and chemicals to androgen receptors in rainbow trout and goldfish. Environ Toxicol Chem 19:2059-2065.
40. Lowell RB, Ring B, Pastershank G, Walker S, Trudel L, Hedley K. 2005. National assessment of pulp and paper environmental effects monitoring data: Findings from cycles 1 through 3. Environment Canada, Burlington, ON.
41. Munkittrick KR, McMaster ME, Van Der Kraak GJ, Portt C, Gibbons A, Farwell A, Gray M. 2000. Development of Methods for Effects-Driven Cumulative Effects Assessment Using Fish Populations: Moose River Project. SETAC, Pensacola, FL, USA.
42. McMaster ME, Van Der Kraak GJ, Munkittrick KR. 1996. An epidemiological evaluation of the biochemical basis for steroid hormonal depressions in fish exposed to industrial wastes. J Great Lakes Res 22:153-171.
43. McMaster ME, Van Der Kraak GJ, Portt CB, Munkittrick KR, Sibley PK. 1991. Changes in hepatic mixed-function oxygenase (MFO) activity, plasma steroid levels and age at maturity of a white sucker (Catostomus commersoni) population exposed to bleached kraft pulp mill effluent. Aquat Toxicol 21:199-237.
44. McMaster ME, Van Der Kraak GJ, Munkittrick KR. 1995. Exposure to bleached kraft pulp mill effluent reduces the steroid biosynthetic capacity of white sucker ovarian follicles. Comp Biochem Physiol C 112:169-178.
45. Munkittrick KR, Portt CB, Van Der Kraak GJ, Smith IR, Rokosh D. 1991. Impact of bleached kraft mill effluent on population characteristics, liver MFO activity and serum steroid levels of a Lake Superior white sucker (Catostomus commersoni) population. Can J Fish Aquat Sci 48:1371-1380.
46. Munkittrick KR, McMaster ME, Portt CB, Van Der Kraak GJ, Smith IR, Dixon DG. 1992. Changes in maturity, plasma sex steroid levels, hepatic mixed-function oxygenase activity, and the presence of external lesions in lake whitefish (Coregonus clupeaformis) exposed to bleached kraft mill effluent. Can J Fish Aquat Sci 49:1560-1569.
47. Munkittrick KR, Van Der Kraak GJ, McMaster ME, Portt CB. 1992. Reproductive dysfunction and MFO activity in three species of fish exposed to bleached kraft mill effluent at Jackfish Bay, Lake Superior. Water Qual Res J Can 27:439-446.
48. Donaldson EM. 1990. Reproductive indices as measures of the effects of environmental stressors in fish. Am Fish S S 8:109-122.
49. Denslow ND, Chow MC, Kroll KJ, Green L. 1999. Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics. Ecotoxicology 8:385-398.
50. Sumpter JP, Jobling S. 1995. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect 103:173-178.
51. Thorpe KL, Benstead R, Hutchinson TH, Tyler CR. 2007. Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas). Aquat Toxicol 85:176-183.
52. Simmons DBD, Bols NC, Duncker BP, McMaster ME, Miller J, Sherry JP. 2012. Proteomic profiles of white sucker (Catostomus commersonii) sampled from within the Thunder Bay Area of Concern reveal up-regulation of proteins associated with tumor formation and exposure to environmental estrogens. Environ Sci Technol 46:1886-1894.
53. Marlatt VL, Lakoff J, Crump K, Maryniuk CJ, Watt J, Jewell L, Atkinson S, Blais JM, Sherry J, Moon TW, Trudeau VL. 2010. Sex- and tissue-specific effects of waterborne estrogen on estrogen receptor subtypes and E2-mediated gene expression in the reproductive axis of goldfish. Comp Biochem Physiol A 156:92-101.
54. Shi X, Zhang S, Pang Q. 2006. Vitellogenin is a novel player in defense reactions. Fish Shellfish Immun 20:769-772.
55. Li Z, Zhang S, Liu Q. 2008. Vitellogenin functions as a multivalent pattern recognition receptor with an opsonic activity. PLoS One 3:1-7.
56. Liu Q-H, Zhang S-C, Li Z-J, Gao C-R. 2009. Characterization of a pattern recognition molecule vitellogenin from carp (Cyprinus carpio). Immunology 214:257-267.
57. Chen TT, Sonstegard RA. 1984. Development of a rapid, sensitive and quantitative test for the assessment of the effects of xenobiotics on reproduction in fish. Mar Environ Res 14:429-430.
58. Zoeller RT, Tan SW, Tyl RW. 2007. General background on the hypothalamic-pituitary-thyroid (HPT) axis. Crit Rev Toxicol 37:11-53.
59. Carr JA, Patiño R. 2011. The hypothalamus-pituitary-thyroid axis in teleosts and amphibians: Endocrine disruption and its consequences to natural populations. Gen Comp Endocrinol 170:299-312.
60. Leatherland JF, Sonstegard RA. 1980. Seasonal changes in thyroid hyperplasia, serum thyroid hormone and lipid concentrations, and pituitary gland structure in Lake Ontario coho salmon, Oncorhynchus kisutch Walbaum and a comparison with coho salmon from Lakes Michigan and Erie. J Fish Biol 16:539-562.
61. Moccia RD, Leatherland JF, Sonstegard RA. 1981. Quantitative interlake comparison of thyroid pathology in Great Lakes Coho (Oncorhynchus kisutch) and Chinook (Oncorhynchus tschawytscha) salmon. Cancer Res 41:2200-2210.
62. Power DM, Llewellyn L, Faustino M, Nowell MA, Björnsson BT, Einarsdottir IE, Canario AVM, Sweeney GE. 2001. Thyroid hormones in growth and development of fish. Comp Biochem Physiol C 130:447-459.
63. Blanton ML, Specker JL. 2007. The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit Rev Toxicol 37:97-115.
64. Peter MCS. 2011. The role of thyroid hormones in stress response of fish. Gen Comp Endocrinol 172:198-210.
65. Zhou T, Rademacher DJ, Steinpreis RE, Weis JS. 1999. Neurotransmitter levels in two populations of larval Fundulus heteroclitus after methylmercury exposure. Comp Biochem Physiol C 124:287-294.
66. Brar NK, Waggoner C, Reyes JA, Kelley KM. 2010. Evidence for thyroid endocrine disruption in wild fish in San Francisco Bay, California, USA. Relationships to contaminant exposures. Aquat Toxicol 96:203-215.
67. LeRoy KD, Thomas P, Khan IA. 2006. Thyroid hormone status of Atlantic croaker exposed to Aroclor 1254 and selected PCB congeners. Comp Biochem Physiol C 144:263-271.
68. Coimbra AM, Reis-Henriques MA. 2007. Tilapia larvae aroclor 1254 exposure: Effects on gonads and circulating thyroid hormones during adulthood. Bull Environ Contam Toxicol 79:488-493.
69. Bergman Å, Brouwer A, Hagmar L, Sjödin A, Foster P, Skakkebæk N. 2001. Hydroxylated PCBs (OH-PCBs) as potential endocrine disrupters-Exposures and toxic effects. APMIS 109:S505.
70. Brouwer A, Morse DC, Lans MC, Schuur AG, Murk AJ, Klasson-Wehler E, Bergman Å, Visser TJ. 1998. Interactions of persistent environmental organohalogens with the thyroid hormone system: Mechanisms and possible consequences for animal and human health. Toxicol Ind Health 14:59-84.
71. Akutsu K, Hori S. 2004. Polybrominated diphenyl ether flame retardants in foodstuffs and human milk. J Food Hyg Soc Jpn 45:175-183.
72. Zhou T, Ross DG, DeVito MJ, Crofton KM. 2001. Effects of short-term in vivo exposure to polybrominated diphenyl ethers on thyroid hormones and hepatic enzyme activities in weanling rats. Toxicol Sci 61:76-82.
73. Parrott J, Chong-Kit R, Rokosh D. 1999. MFO induction in fish: A tool to measure environmental exposure. In Rao SS, ed, Impact Assessment of Hazardous Aquatic Contaminants: Concepts and Approaches. CRC, New York, NY, USA, pp 99-122.
74. Navas JM, Segner H. 2001. Estrogen-mediated suppression of cytochrome P4501A (CYP1A) expression in rainbow trout hepatocytes: role of estrogen receptor. Chem Biol Interact 138:285-298.
75. Elskus AA. 2004. Estradiol and estriol suppress CYP1A expression in rainbow trout hepatocytes. Mar Environ Res 58:463-467.
76. Pinkney AE, Harshbarger JC, May EB, Melancon MJ. 2004. Tumor prevalence and biomarkers of exposure in brown bullhead (Ameiurus nebulosus) from Back River, Furnace Creek, and Tuckahoe River, Maryland. Arch Environ Contam Toxicol 46:492-501.