Widespread occurrence of intersex in black basses (Micropterus spp.) from U.S. rivers, 1995-2004

Aquatic Toxicology

Volumn 95, Issue 1, 2009, Pages 60-70

  Hinck, Jo Ellen ^a   Blazer, Vicki S ^b   Schmitt, Christopher J ^a   Papoulias, Diana M ^a   Tillitt, Donald E ^a  

^a Columbia Environmental Research Center ^*  (United States)

^b LEETOWN SCIENCE CENTER   (United States)

Author keywords

Endocrine disruption; Environment; Estrogenic; Fishes; Ovotestis

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHANE; 1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; MERCURY; NONACHLOR; POLYCHLORINATED BIPHENYL; SEX HORMONE; VITELLOGENIN;

CHEMICAL POLLUTANT; DDD; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; FISH; INTERSEX; PCB; RIVER BASIN;

AGE DETERMINATION; ANIMAL TISSUE; ARTICLE; BASS; CONTROLLED STUDY; ESTROGEN ACTIVITY; FEMALE; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HERMAPHRODITISM; MALE; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; RIVER; SEASONAL VARIATION; SEX DIFFERENTIATION; SPECIES DIFFERENCE; SPERMATOZOON MATURATION; UNITED STATES;

ANIMALS; BASS; DISORDERS OF SEX DEVELOPMENT; FEMALE; FISH DISEASES; MALE; OOCYTES; PREVALENCE; RIVERS; TESTIS; UNITED STATES; WATER POLLUTANTS, CHEMICAL;

NORTH AMERICA; UNITED STATES;

MICROPTERUS; MICROPTERUS DOLOMIEU; MICROPTERUS SALMOIDES; PISCES;

EID: 71749106475     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2009.08.001     Document Type: Article

References (71)

1. Anderson M.J., Cacela D., Beltman D., Teh S.J., Okihiro M.S., Hinton D.E., Denslow N., and Zelikoff J.T. Biochemical and toxicopathic biomarkers assessed in smallmouth bass recovered from a polychlorinated biphenyl-contaminated river. Biomarkers 8 (2003) 317-393
2. Allen Y., Mattheiessen P., Scott A.P., Haworth S., Feist S., and Thain J.E. The extent of oestrogenic contamination in the UK estuarine and marine environments-further surveys of flounder. Sci. Total Environ. 233 (1999) 5-20
3. Ankley G.T., Tillitt D.E., Giesy J.P., Jones P.D., and Verbrugge D.A. Bioassay derived 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents in PCB containing extracts from the flesh and eggs of Lake Michigan chinook salmon (Oncorhynchus tshawytscha) and possible implications for reproduction. Can. J. Fish. Aquat. Sci. 48 (1991) 1685-1690
4. Baldigo B.P., Sloan R.J., Smith S.B., Denslow N.D., Blazer V.S., and Gross T.S. Polychlorinated biphenyls, mercury, and potential endocrine disruption in fish from the Hudson River, New York, USA. Aquat. Sci. 68 (2006) 206-228
5. Bateman K.S., Stentiford G.D., and Feist S.W. A ranking system for the evaluation of intersex condition in European flounder (Platichthys flesus). Environ. Toxicol. Chem. 23 (2004) 2831-2836
6. Bjerregaard L.B., Korsgaard B., and Bjerregaard P. Intersex in wild roach (Rutilus rutilus) from a Danish sewage effluent-receiving streams. Ecotox. Environ. Saf. 64 (2006) 321-328
7. Blazer V.S. Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol. Biochem. 26 (2002) 85-101
8. Blazer V.A., Iwanowicz L.R., Iwanowicz D.D., Smith D.R., Young J.A., Hedrick J.D., Foster S.W., and Reeser S.J. Intersex (testicular oocytes) in smallmouth bass from the Potomac River and selected nearby drainages. J. Aquat. Animal Health 19 (2007) 242-253
9. Cooper R.L., and Kavlock R.J. Endocrine disruptors and reproductive development: a weight-of-evidence overview. J. Endocrin. 152 (1997) 159-166
10. Denslow N.D., Chow M.C., Kroll K.J., and Green L. Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics. Ecotoxicology 8 (1999) 385-398
11. Devlin R.H., and Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208 (2002) 191-364
12. Drevnick P.E., and Sandheinrich M.B. Effects of dietary methylmercury on reproductive endocrinology of fathead minnows. Environ. Sci. Technol. 37 (2003) 4390-4396
13. Garcia-Reyero N., Barber D.S., Gross T.S., Johnson K.G., Sepúlveda M.S., Szabo N.J., et al. Dietary exposure of largemouth bass to OCPs changes expression of genes important for reproduction. Aquat. Toxicol. 78 (2006) 358-369
14. Gercken J., and Sordyl H. Intersex in feral marine and freshwater fish from northeastern Germany. Mar. Environ. Res. 54 (2002) 651-655
15. Gillom R.J., Barbash J.E., Crawford C.G., Hamilton P.A., Martin J.D., Nakagaki N., Nowell L.H., Scott J.C., Stackelberg P.E., Thelin G.A., and Wolock D.M. The Quality of our Nation's Waters-Pesticides in the Nation's Streams and Ground Water 1992-2001 (2006), U.S. Geological Survey Circular 1291 p. 172
16. Gray M., Niimi A.J., and Metcalfe C.D. Factors affecting the development of testis-ova in medaka, Oryzias latipes, exposed to octylphenol. Environ. Toxicol. Chem. 18 (1999) 1835-1842
17. Hanselman T.A., Graetz D.A., and Wilkie A.C. Manure-borne estrogens as potential environmental contaminants: a review. Environ. Sci. Technol. 37 (2003) 5471-5478
18. Hecker M., Tyler C.R., Hoffmann M., Maddix S., and Karbe L. Plasma biomarkers in fish provide evidence for endocrine modulation in the Elbe River, Germany. Environ. Sci. Technol. 36 (2002) 2311-2321
19. Hecker M., Murphy M.B., Coady K.K., Villeneuve D.L., Jones P.D., Carr J.A., Solomon K.R., Smith E.E., van der Kraak G., Gross T., Du Preez L., Kendall R.J., and Giesy J.P. Terminology of gonadal anomalies in fish and amphibian resulting from chemical exposures. Rev. Environ. Contam. Toxicol. 187 (2006) 103-131
20. Hegrenes S.G. Masculinization of spawning channel catfish in the Red River of the North. Copeia 2 (1999) 491-494
21. Hinck J.E., Schmitt C.J., Blazer V.S., Denslow N.D., Bartish T.M., Anderson P.J., Coyle J.J., Dethloff G.M., and Tillitt D.E. Environmental contaminants and biomarker responses in fish from the Columbia River and its tributaries: spatial and temporal trends. Sci. Total Environ. 366 (2006) 549-578
22. Hinck J.E., Blazer V.S., Denslow N.D., Myers M.S., Gross T.S., and Tillitt D.E. Biomarkers of contaminant exposure in northern pike (Esox lucius) from the Yukon River Basin, Alaska. Arch. Environ. Contam. Toxicol. 52 (2007) 529-562
23. Hinck J.E., Blazer V.S., Denslow N.D., Echols K.R., Gross T.S., May T.W., Anderson P.J., Coyle J.J., and Tillitt D.E. Chemical contaminants, health indicators, and reproductive biomarker responses in fish from the Colorado River and its tributaries. Sci. Total Environ. 378 (2007) 376-402
24. Hinck J.E., Blazer V.S., Denslow N.D., Echols K.R., Gale R.W., Wieser C., May T.W., Ellersieck M.R., Coyle J.J., and Tillitt D.E. Chemical contaminants, health indicators, and reproductive biomarker responses in fish from rivers in the Southeastern U.S. Sci. Total Environ. 390 (2008) 538-557
25. Hinck J.E., Schmitt C.J., Ellersieck M.R., and Tillitt D.E. Relations between and among contaminant concentrations and biological endpoints in bass (Micropterus spp.) and common carp (Cyprinus carpio) in large U.S. rivers, 1995-2004. J. Environ. Monit. 10 (2008) 1499-1518
26. James M.F. Hermaphroditism in the largemouth bass. J. Morph. 79 (1946) 93-96
27. Jobling S., Nolan M., Tyler C.R., Brighty G., and Sumpter J.P. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 32 (1998) 2498-2506
28. Jobling S., Coey S., Whitmore J.G., Kime D.E., Van Look K.J.W., McAllister B.G., Beresford N., Henshaw A.C., Brighty G., Tyler C.R., and Sumpter J.P. Wild intersex roach (Rutilus rutilus) have reduced fertility. Bio. Reprod. 67 (2002) 515-524
29. Johnston P.M. The embryonic history of the germ cells of the largemouth black bass, Micropterus salmoides salmoides (Lacepede). J. Morphol. 88 (1951) 471-542
30. June F.C. Reproductive patterns in seventeen species of warmwater fishes in a Missouri River reservoir. Environ. Biol. Fish. 2 (1977) 285-296
31. Kime D.E. A strategy for assessing the effects of xenobiotics on fish reproduction. Sci. Total Environ. 225 (1999) 3-11
32. Koger C.S., Teh S.J., and Hinton D.E. Determining the sensitive stages of intersex induction in medaka (Oryzias latipes) exposed to 17 b-estradiol or testosterone. Mar. Environ. Res. 50 (2000) 201-206
33. Kolodiei E.P., and Sedlak D.L. Rangeland grazing as a source of steroid hormones to surface waters. Environ. Sci. Technol. 41 (2007) 3514-3520
34. Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., and Buxton H.T. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol. 36 (2002) 1202-1211
35. Körner O., Vermeirssen E.L.M., and Holm-Burkhardt P. Intersex in feral brown trout from Swiss midland rivers. J. Fish Biol. 67 (2005) 1734-1740
36. Krisfalusi M., and Nagler J.J. Induction of intersex in genotypic male rainbow trout (Oncorhynchus mykiss) embryos following immersion in estradiol-17b. Molecular Reprod. Develop. 56 (2000) 495-501
37. Lavado R., Thibaut R., Raldua D., Martin R., and Porte C. First evidence of endocrine disruption in feral carp from the Ebro River. Toxicol. Appl. Pharmacol. 196 (2004) 247-257
38. Liney K.E., Jobling S., Shears J.A., Simpson P., and Tyler C.R. Assessing the sensitivity of different life stages for sexual disruption in roach (Rutilus rutilus) exposed to effluents from wastewater treatment works. Environ. Health Perspect. 113 (2005) 1299-1307
39. Lorenzen A., and Kennedy S.W. A fluorescence-based protein assay for use with a microplate reader. Anal. Biochem. 214 (1993) 346-348
40. Luna L.G. Histopathological Methods and Color Atlas of Special Stains and Tissue Artifacts (1992), American Histolabs, Inc., Gaithersburg, MD
41. McDaniel T.V., Martin P.A., Struger J., Sherry J., Marvin C.H., McMaster M.E., Clarence S., and Tetreault G. Potential endocrine disruption of sexual development in free ranging male northern leopard frogs (Rana pipiens) and green frigs (Rana clamitans) from areas of intensive row crop agriculture. Aquat. Toxicol. 88 (2008) 230-242
42. Mills L.J., and Chichester C. Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations?. Sci. Total Environ. 343 (2005) 1-34
43. Minier C., Caltot G., Leboulanger R., and Hill E.M. An investigation of the incidence of intersex fish in Seine-Maritime and Sussex regions. Analusis 28 (2000) 801-806
44. Moser M., Whipple J., Sakanari J., and Reilly C. Protandrous hermaphroditism in striped bass from Coos Bay, Oregon. Trans. Am. Fish. Soc. 112 (1983) 567-569
45. Nash J.P., Kime D.E., Van der Van L.T.M., Wester P.W., Brion F., Maack G., Stahlschmidt-Allner P., and Tyler C.R. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Perspect. 112 (2004) 1725-1733
46. Nolan M., Jobling S., Brighty G., Sumpter J.P., and Tyler C.R. A histological description of intersexuality in the roach. J. Fish Biol. 58 (2001) 160-176
47. O'Farrell M.M., and Peirce R.E. The occurrence of a gynandromorphic migratory trout, Salmo trutta L. J. Fish Biol. 34 (1989) 327
48. Orlando E.E., Kolok A.S., Binzcik G.A., Gate J.L., Horton M.K., Lambright C.S., Gray Jr. L.E., Soto A.M., and Guillette Jr. J.L. Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow. Environ. Health Perspect. 112 (2004) 353-358
49. Orlando E.F., and Guillette Jr. J.L. Sexual dimorphic responses in wildlife exposed to endocrine disrupting compounds. Environ. Res. 104 (2007) 163-173
50. Piferrer F. Endocrine sex control strategies for the feminization of teleosts fish. Aquaculture 197 (2001) 229-281
51. Saville D.J. Multiple comparison procedures: the practical solution. Am. Statist. 44 (1990) 174-180
52. Schmid T., Gonzalez-Valero J., Rufli H., and Dietrich D.R. Determination of vitellogenin kinetics in male fathead minnows (Pimephales promelas). Tox. Lett. 131 (2002) 65-74
53. Schmitt, C.J., 2002. Biomonitoring of Environmental Status and Trends (BEST) Program: environmental contaminants and their effects on fish in the Mississippi River Basin. U.S. Geological Survey Biological Science Report USGS/BRD/BSR 2002-2004, Columbia, MO, 217p.
54. Schmitt C.J., Hinck J.E., Blazer V.S., Denslow N.D., Dethloff G.M., Bartish T.M., Coyle J.J., and Tillitt D.E. Environmental contaminants and biomarker responses in fish from the Rio Grande and its U.S. tributaries: spatial and temporal trends. Sci. Total Environ. 250 (2005) 161-193
55. Sikstrom C.B., Metner D.A., and Lockhart W.L. Hermaphroditism in a white sucker (Catostomus commersoni) from the Athabasca River, Alberta. Trans. Am. Fish. Soc. 104 (1975) 413
56. 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. 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 (2004) 6385-6395
57. Solé M., Raldua D., Pifferrer F., Barceló D., and Porte C. Feminization of wild carp, Cyprinus carpio, in a polluted environment: plasma steroid hormones, gonadal morphology and xenobiotic metabolizing system. Comp. Biochem. Physiol. C 136 (2003) 145-156
58. Stentiford G.D., Longshaw M., Lyons B.P., Jones G., Green M., and Feist S.W. Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar. Environ. Res. 55 (2003) 137-159
59. Stuber, R.J., Gebhart, G., Maughan, O.E., 1982. Habitat suitability index models: largemouth bass. U.S. Department of the Interior. FWS/OBS-82/10.16. 32 p.
60. Sumpter J.P. Endocrine disruption in the aquatic environment. In: Metzler M. (Ed). The Handbook of Environmental Chemistry, vol. 3 Part M Endocrine Disruptors, Part II (2002), Springer-Verlag, Berlin, Heidelberg 271-289
61. Sumpter J.P., and Jobling S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 103 S7 (1995) 173-178
62. Thorpe K.L., Benstead R., Hutchinson T.H., and Tyler C.R. Associations between altered vitellogenin concentrations and adverse health effects in fathead minnow (Pimephales promelas). Aquat. Toxicol. 85 (2007) 176-183
63. U.S. Geological Survey, 2003. NAWQA Pesticide National Synthesis Project, Sacramento, California, at URL http://ca.water.usgs.gov/pnsp/.
64. Vajda A.M., Barber L.B., Gray J.L., Lopez E.M., Woodling J.D., and Norris D.O. Reproductive disruption in fish downstream form an estrogenic wastewater effluent. Environ. Sci. Technol. 42 (2008) 3407-3414
65. van Aerle R., Nolan M., Jobling S., Christiansen L.B., Sumpter J.P., and Tyler C.R. Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ. Toxicol. Chem. 20 (2001) 2841-2847
66. Vethaak A.D., Lahr J., Kuiper R.V., Grinwis G.C.M., Rankouhi T.R., Giesy J.P., and Gerritsen A. Estrogenic effects in fish in The Netherlands: some preliminary results. Toxicol. 181-182 (2002) 147-150
67. Vine E., Shears J., van Aerle R., Tyler C.R., and Sumpter J.P. Endocrine (sexual) disruption is not a prominent feature in the pike (Esox lucius), a top predator, living in English waters. Environ. Toxicol. Chem. 24 (2005) 1436-1443
68. Whyte J.J., Jung R.E., Schmitt C.J., and Tillitt D.E. Ethoxyresorufin-O deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit. Rev. Toxicol. 30 (2000) 347-570
69. Whyte J.J., Schmitt C.J., and Tillitt D.E. The H4IIE cell bioassay as an indicator of dioxin-like chemicals in wildlife and the environment. Crit. Rev. Toxicol. 34 (2004) 1-83
70. Woodling J.D., Lopez E.M., Maldonado T.A., Norris D.O., and Vajda A.M. Intersex and other reproductive disruption of fish in wastewater effluent dominated Colorado streams. Comp. Biochem. Physiol. C 144 (2006) 10-15
71. Zillioux E.J., Johnson I.C., Kiparissis Y., Metcalfe C.D., Wheat J.V., Ward S.G., and Liu H. The sheepshead minnow as an in vivo model for endocrine disruption in marine teleosts: a partial life-cycle test with 17-ethynylestradiol. Environ. Toxicol. Chem. 20 (2001) 1968-1978