Interspecies differences in biochemical, histopathological, and population responses in four wild fish species exposed to ethynylestradiol added to a whole lake

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 66, Issue 11, 2009, Pages 1920-1935

  Palace, V P ^a   Evans, R E ^a   Wautier, K G ^a   Mills, K H ^a   Blanchfield, P J ^a   Park, B J ^a   Baron, C L ^a   Kidd, K A ^b  

^a FRESHWATER INSTITUTE   (Canada)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CYPRINID; ESTROGENIC COMPOUND; HABITAT SELECTION; HISTOPATHOLOGY; INTERSPECIFIC VARIATION; LAKE POLLUTION; POLLUTION EFFECT; POLLUTION EXPOSURE; POPULATION DECLINE; SALMONID;

CATOSTOMUS COMMERSONI; CATOSTOMUS COMMERSONII; MARGARISCUS; MARGARISCUS MARGARITA; PIMEPHALES PROMELAS; SALMONIDAE; SALVELINUS NAMAYCUSH;

EID: 70350532000     PISSN: 0706652X     EISSN: None     Source Type: Journal    
DOI: 10.1139/F09-125     Document Type: Article

References (56)

1. Andersen, L., Holbech, H., Gessbo, A., Norrgren, L., and Petersen, G.I. 2003. Effects of exposure to 17a-ethinylestradiol during early development on sexual differentiation and induction of vitellogenin in zebrafish (Danio rerio). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 134: 365-374. doi:10.1016/S1532-0456(03)00006-1.
2. Chen, Y., and Harvey, H.H. 1995. Growth, abundance, and food supply of white sucker. Trans. Am. Fish. Soc. 124(2): 262-271. doi:10.1577/1548-8659(1995)124<0262:GAAFSO>2.3.CO;2.
3. Devlin, R.H., and Nagahama, Y. 2002. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture, 208(3-4): 191-364. doi:10.1016/S0044-8486(02)00057-1.
4. Elliot, M., Hemmingway, K.L., Krueger, D., Theil, R., and Arukwe, A. 2003. From the individual to the population and community responses to pollution. In Effects of pollution on fish. Edited by A.J. Lawrence and K.L. Hemmingway. Oxford University Press, Oxford, U.K. pp. 221-255.
5. Fee, E.J., Hecky, R.E., Kasian, S.E.M., and Cruikshank, D.R. 1996. Effects of lake size, water clarity and climatic variability on mixing depths in Canadian shield lakes. Limnol. Oceanogr. 41: 912-920.
6. Gagné, F., and Blaise, C. 1998. Estrogenic properties of municipal and industrial wastewaters evaluated with a rapid and sensitive chemoluminescent in situ hybridization assay (CISH) in rainbow trout hepatocytes. Aquat. Toxicol. 44(1-2): 83-91. doi:10.1016/ S0166-445X(98)00066-6.
7. Gimeno, S., Gerritsen, A., Bowmer, T., and Komen, H. 1996. Feminization of male carp. Nature, 384(6606): 221-222. doi:10.1038/384221a0. PMID:8918871.
8. Gimeno, S., Komen, H., Gerritsen, A.G.M., and Bowmer, T. 1998. Feminisation of young males of the common carp, Cyprinus carpio, exposed to 4-tert-penylphenol during sexual differentiation. Aquat. Toxicol. 43(2-3): 77-92. doi:10.1016/S0166-445X(98)00056-3.
9. Herwig, B.R., and Zimmer, K.D. 2007. Population ecology and prey consumption by fathead minnows in prairie wetlands: importance of detritus and larval fish. Ecol. Freshwat. Fish, 16(3): 282-294. doi:10.1111/j.1600-0633.2006.00220.x.
10. Hubert, W.A., and Rahel, F.J. 1989. Relations of physical habitat to abundance of four nongame fishes in high-plains streams: a test of habitat suitability index models. N. Am. J. Fish. Manag. 9(3): 332-340. doi:10.1577/1548-8675(1989)009<0332:ROPHTA>2. 3.CO;2.
11. Hutchinson, T.H., Ankley, G.T., Segner, H., and Tyler, C.R. 2006. Screening and testing for endocrine disruption in fish-biomarkers as "signposts," not "traffic lights," in risk assessment. Environ. Health Perspect. 114(Suppl. 1): 106-114. doi:10.1289/ehp.8062. PMID:16818255.
12. Jobling, S., and Tyler, C.R. 2003. Endocrine disruption in wild freshwater fish. Pure Appl. Chem. 75(11-12): 2219-2234. doi:10.1351/pac200375112219.
13. Jobling, S., Nolan, M., Tyler, C.R., Brighty, G., and Sumpter, J.P. 1998. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 32(17): 2498-2506. doi:10.1021/es9710870.
14. Kidd, K.A., Blanchfield, P.J., Mills, K.H., Palace, V.P., Evans, R.E., Lazorchak, J.M., and Flick, R.W. 2007. Collapse of a fish population after exposure to a synthetic estrogen. Proc. Natl. Acad. Sci. U.S.A. 104(21): 8897-8901. doi:10.1073/pnas.0609568104. PMID:17517636.
15. Lai, K.M., Scrimshaw, M.D., and Lester, J.N. 2002. The effects of natural and synthetic steroid estrogens in relation to their environmental occurrence. Crit. Rev. Toxicol. 32(2): 113-132. doi:10.1080/20024091064192. PMID:11951992.
16. Länge, R., Hutchinson, T.H., Croudace, C.P., Siegmund, F., Schweinfurth, H., Hampe, P., Panter, G.H., and Sumpter, J.P. 2001. Effects of the synthetic oestrogen 17a-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ. Contam. Toxicol. 20: 1216-1227.
17. Larsson, D.G.J., Adolfsson-Erici, M., Parkkonen, J., Pettersson, M., Berg, A.H., Olsson, P.-E., and Forlin, L. 1999. Ethinyloestradiol - an undesired fish contraceptive? Aquat. Toxicol. 45(2-3): 91-97. doi:10.1016/S0166-445X(98)00112-X.
18. Lavado, R., Thibaut, R., Raldu ́a, D., Martín, R., and Porte, C. 2004. First evidence of endocrine disruption in feral carp from the Ebro River. Toxicol. Appl. Pharmacol. 196(2): 247-257. doi:10.1016/j.taap.2003.12.012. PMID:15081271.
19. Mac, M.J. 1985. Effects of ration size on preferred temperature of lake charr Salvelinus namaycush. Environ. Biol. Fishes, 14(2-3): 227-231. doi:10.1007/BF00000830.
20. MacKay, M.E., Raelson, J., and Lazier, C.B. 1996. Up-regulation of estrogen receptor mRNA and estrogen receptor activity by estradiol in liver of rainbow trout and other teleostean fish. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 115: 201-209.
21. Magnuson, J.J., Crowder, L.B., and Medvick, P.A. 1979. Temperature as an ecological resource. Am. Zool. 19: 331-343.
22. Magnuson, J.J., Meisner, J.D., and Hill, D.K. 1990. Potential changes in the thermal habitat of great lakes fish after global climate warming. Trans. Am. Fish. Soc. 119(2): 254-264. doi:10. 1577/1548-8659(1990)119<0254:PCITTH>2.3.CO;2.
23. Martin, N.V., and Olver, C.H. 1980. The lake charr, Salvelinus namaycush. In Salmonid fishes of the genus Salvelinus. Edited by E.K. Balon. Dr. W. Junk bv Publishers, The Hague, The Netherlands. pp. 205-277.
24. Mills, K.H., Chalanchuk, S.M., Mohr, L.C., and Davies, I.J. 1987. Responses of fish populations in Lake 223 to 8 years of experimental acidification. Can. J. Fish. Aquat. Sci. 44(Suppl. 1): 114-125. doi:10.1139/f87-287.
25. Nash, J.P., Kime, D.E., Van der Ven, L.T.M., Wester, P.W., Brion, F., Maack, G., Stahlschmidt-Allner, P., and Tyler, C.R. 2004. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Perspect. 112(17): 1725-1733. PMID:15579420.
26. Orn, S., Holbech, H., Madsen, T.H., Norrgren, L., and Petersen, G.I. 2003. Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. Aquat. Toxicol. 65(4): 397-411. PMID:14568354.
27. Pakdel, F., Féon, S., Le Gac, F., Le Menn, F., and Valotaire, Y. 1991. In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout. Mol. Cell. Endocrinol. 75(3): 205-212. doi:10.1016/03037207(91)90162-L. PMID:2026276.
28. Palace, V.P., and Klaverkamp, J.F. 1993. Variation of hepatic enzymes in three species of freshwater fish from Precambrian shield lakes and the effect of cadmium exposure. Comp. Biochem. Physiol. C Comp. Pharmacol. Toxicol. 104: 147-153.
29. Palace, V.P., Evans, R.E., Wautier, K., Baron, C.L., Werner, J., Klaverkamp, J.F., Kidd, K.A., and Dick, T.A. 2001. Altered distribution of lipid-soluble antioxidant vitamins in juvenile sturgeon exposed to waterborne ethynylestradiol. Environ. Toxicol. Chem. 20(10): 2370-2376. doi:10.1897/1551-5028(2001)020<2370:ADOLSA>2.0.CO;2. PMID:11596772.
30. Palace, V.P., Evans, R.E., Wautier, K., Vandenbyllardt, L., Vandersteen, W., and Kidd, K. 2002. Induction of vitellogenin and histological effects in wild fathead minnows from a lake experimentally treated with the synthetic estrogen, ethynylestradiol. Water Qual. Res. J. Can. 37: 637-650.
31. Palace, V.P., Wautier, K.G., Evans, R.E., Blanchfield, P.J., Mills, K., Chalanchuk, S., Godard, D., McMaster, M.E., Tetrault, G., Peters, L.E., Vandenbyllaardt, L., and Kidd, K.A. 2006. Biochemical and histopathological effects in pearl dace (Margariscus margarita) chronically exposed to a synthetic estrogen in a whole lake experiment. Environ. Toxicol. Chem. 25: 1114-1125. doi:10.1897/04-557R1.1.
32. Papoulias, D.M., Chapman, D., and Tillitt, D.E. 2006. Reproductive condition and occurrence of intersex in bighead carp and silver carp in the Missouri River. Hydrobiologia, 571(1): 355-360. doi:10.1007/s10750-006-0260-7.
33. Park, B.J., and Kidd, K.A. 2005. Effects of the synthetic estrogen ethinylestradiol on early life stages of mink frogs and green frogs in the wild and in situ. Environ. Toxicol. Chem. 24(8): 2027-2036. doi:10.1897/04-227R.1. PMID:16152976.
34. Parrott, J.L., and Blunt, B.R. 2005. Life-cycle exposure of fathead minnows (Pimephales promelas) to an ethinylestradiol concentration below 1 ng/L reduces egg fertilization success and demasculinizes males. Environ. Toxicol. Chem. 20: 131-141.PMID:15793829.
35. Pawlowski, S., van Aerle, R., Tyler, C.R., and Braunbeck, T. 2004. Effects of 17a-ethinylestradiol in a fathead minnow (Pimephales promelas) gonadal recrudescence assay. Ecotoxicol. Environ. Saf. 57: 330-345. doi:10.1016/j.ecoenv.2003.07.019. PMID:15041256.
36. Piferrer, F. 2001. Endocrine sex control strategies for the feminization of teleost fish. Aquaculture, 197(1-4): 229-281. doi:10.1016/S0044-8486(01)00589-0.
37. Plumb, J.M., and Blanchfield, P.J. 2009. Performance of temperature and dissolved oxygen criteria to predict habitat use by lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 66: 2011-2023. doi:10.1139/F09-129.
38. Routledge, E.J., Sheahan, D., Desbrow, C., Brighty, G.C., Waldock, M., and Sumpter, J.P. 1998. Identification of estrogenic chemicals in STW effluent. II: In vivo responses in trout and roach. Environ. Sci. Technol. 32(11): 1559-1565. doi:10.1021/ es970796a.
39. Schindler, D.W., and Bayley, S.E. 1990. Fresh waters in cycle. In Planet under stress: the challenge of global change. Edited by C. Mungall and D.J. McLaren. Oxford University Press Canada, Don Mills, Ont. pp. 149-167.
40. Schmid, T., Gonzalez-Valero, J., Rufli, H., and Dietrich, D.R. 2002. Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). Toxicol. Lett. 131(1-2): 65-74. doi:10.1016/S0378-4274(02)00043-7.PMID:11988359.
41. Schultz, I.R., Orner, G., Merdink, J.L., and Skillman, A. 2001. Dose-response relationships and pharmacokinetics of vitellogenin in rainbow trout after intravascular administration of 17a-ethynylestradiol. Aquat. Toxicol. 51(3): 305-318. doi:10.1016/S0166-445X(00)00118-1.
42. Schultz, I.R., Skillman, A., Nicolas, J.M., Cyr, D.G., and Nagler, J.J. 2003. Short-term exposure to 17a-ethynylestradiol decreases the fertility of sexually maturing male rainbow trout (Oncorhynchus mykiss). Environ. Toxicol. Chem. 22(6): 1272-1280. doi:10.1897/1551-5028(2003)022<1272:STETED>2.0.CO;2. PMID:12785584.
43. Sellers, T.J., Parker, B.R., Schindler, D.W., and Tonn, W.M. 1998. Pelagic distribution of lake trout (Salvelinus namaycush) in small Canadian Shield lakes with respect to temperature, dissolved oxygen, and light. Can. J. Fish. Aquat. Sci. 55(1): 170-179. doi:10.1139/cjfas-55-1-170.
44. Snucins, E.J., and Gunn, J.M. 1995. Coping with a warm environment: behavioral thermoregulation by lake trout. Trans. Am. Fish. Soc. 124(1): 118-123. doi:10.1577/1548-8659(1995)124<0118:CWAWEB>2.3.CO;2.
45. Snyder, E.M., Snyder, S.A., Kelly, K.L., Gross, T.S., Villeneuve, D.L., Fitzgerald, S.D., Villalobos, S.A., and Giesy, J.P. 2004. Reproductive responses of common carp (Cyprinus carpio) exposed in cages to influent of the Las Vegas Wash in Lake Mead, Nevada, from late winter to early spring. Environ. Sci. Technol. 38(23): 6385-6395. doi:10.1021/es049690n. PMID:15597896.
46. Solé, M., Raldua, D., Piferrer, F., Barcelo, D., and Porte, C. 2003. Feminization of wild carp, Cyprinus carpio, in a polluted environment: plasma steroid hormones, gonadal morphology and xenobiotic metabolizing system. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 136: 145-156.
47. Sumpter, J.P., and Jobling, S. 1995. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 103(Suppl. 7): 173-178. doi:10.2307/3432529. PMID:8593867.
48. Tallman, R.F., and Gee, J.H. 1982. Intraspecific resource partitioning in a headwaters stream fish, the pearl dace Semotlius margarita (Cyrpinidae). Environ. Biol. Fishes, 7(3): 243-249. doi:10.1007/BF00002499.
49. Thorpe, K.L., Benstead, R., Hutchinson, T.H., and Tyler, C.R. 2007. Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas). Aquat. Toxicol. 85(3): 176-183. doi:10.1016/j.aquatox. 2007.08.012. PMID:17942165.
50. Tyler, C.R., van Aerle, R., Hutchinson, T.H., Maddix, S., and Trip, H. 1999. An in vivo testing system for endocrine disruptors in fish early life staghes using induction of vitellogenin. Environ. Toxicol. Chem. 18(2): 337-347. doi:10.1897/1551-5028(1999) 018<0337:AIVTSF>2.3.CO;2.
51. van Aerle, R., Nolan, T.M., Jobling, S., Christiansen, L.B., Sumpter, J.P., and Tyler, C.R. 2001. Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ. Toxicol. Chem. 20(12): 2841-2847. doi:10.1897/1551-5028(2001)020<2841:SDIASS>2. 0.CO;2. PMID:11764169.
52. Van den Belt, K., Verheyen, R., and Witters, H. 2003. Comparison of vitellogenin responses in zebrafish and rainbow trout following exposure to environmental estrogens. Ecotoxicol. Environ. Saf. 56(2): 271-281. doi:10.1016/S0147-6513(03)00004-6.PMID:12927559.
53. Weber, L.P., Hill, R.L., Jr., Janz, D.M., and Janz, D.M. 2003. Developmental estrogenic exposure in zebrafish (Danio rerio): II. Histological evaluation of gametogenesis and organ toxicity. Aquat. Toxicol. 63(4): 431-446. doi:10.1016/S0166-445X(02)00208-4. PMID:12758007.
54. Werner, J., Wautier, K., Evans, R.E., Baron, C.L., Kidd, K., and Palace, V.P. 2003. Waterborne ethynylestradiol induces vitellogenin and alters metallothionein expression in lake trout (Salvelinus namaycush). Aquat. Toxicol. 62(4): 321-328. doi:10.1016/ S0166-445X(02)00104-2.
55. Werner, J., Wautier, K., Mills, K., Chalanchuk, S., Kidd, K., and Palace, V.P. 2006. Reproductive fitness of lake trout (Salvelinus namaycush) exposed to environmentally relevant concentrations of the potent estrogen ethynylestradiol (EE2) in a whole lake exposure experiment. Sci. Mar. 70(Suppl. 2): 59-66.
56. Zillioux, E.J., Johnson, I.C., Kiparissis, Y., Metcalfe, C.D., Wheat, J.V., Ward, S.G., and Liu, H. 2001. The sheepshead minnow as an in vivo model for endocrine disruption in marine teleosts: a partial life-cycle test with 17alpha-ethynylestradiol. Environ. Toxicol. Chem. 20(9): 1968-1978. doi:10.1897/1551-5028(2001)020<1968:TSMAAI>2.0.CO;2. PMID:11521823.