Gonadal feminization and halogenated environmental contaminants in common terns (Sterna hirundo): Evidence that ovotestes in male embryos do not persist to the prefledgling stage

Ecotoxicology

Volumn 12, Issue 1-4, 2003, Pages 125-140

  Hart, Constance A ^a,d   Nisbet, Ian C T ^b   Kennedy, Sean W ^c   Hahn, Mark E ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b ICT Nisbet and Company   (United States)

^c CARLETON UNIVERSITY   (Canada)

^d Pest Management Regulatory Agency   (Canada)

Author keywords

Birds; Endocrine disruption; Feminization; Gonads; Ovotestes; PCBs

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; POLYCHLORINATED BIPHENYL DERIVATIVE; POLYCHLORINATED DIBENZODIOXIN; POLYCHLORINATED DIBENZOFURAN;

EMBRYO; PCB; POLLUTION EFFECT; SEABIRD;

ANIMAL TISSUE; ARTICLE; BIRD; EGG; EMBRYO; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL IMPACT ASSESSMENT; FEMALE; FEMINIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; REPRODUCTIVE TOXICITY; SEXUAL MATURATION;

ANIMALS; ANIMALS, NEWBORN; BIRDS; EMBRYONIC DEVELOPMENT; ENDOCRINE SYSTEM; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTANTS; FEMALE; HERMAPHRODITISM; MALE; OVARY; POLYCHLORINATED BIPHENYLS; TESTIS;

UNITED STATES;

ANIMALIA; AVES; HIRUNDO; IBIS; LARIDAE; STERNA; STERNA DOUGALLII; STERNA HIRUNDO;

EID: 0242584989     PISSN: 09639292     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1022505424074     Document Type: Article

References (77)

1. Ankley, G.T., Niemi, G.J., Lodge, K.B., Harris, H.J., Beaver, D.L., Tillitt, D.E., Schwartz, T.R., Giesy, J.P., Jones, P.D. and Hagley, C. (1993). Uptake of planar polychlorinated biphenyls and 2,3,7,8-substituted polychlorinated dibenzofurans and dibenzo-p-dioxins by birds nesting in the lower Fox River and Green Bay, Wisconsin, USA. Arch. Environ. Contam. Toxicol. 24, 332-44.
2. Ballschmiter, K. and Zell, M. (1980). Analysis of polychlorinated biphenyls (PCB) by glass capillary gas chromatography. Fresnius Z. Anal. Chem. 302. 20-31.
3. Barron, M.G., Galbraith, H. and Peltman, D. (1995). Comparative reproductive and developmental toxicology of PCBs in birds. Comp. Biochem. Physiol. 112C, 1-14.
4. Becker, P.H., Schuhmann, S. and Koepff, C. (1993). Hatching failure in common terns (Sterna hirundo) in relation to environmental chemicals. Environ. Poll. 79, 207-13.
5. Becker, P.H., Thyen, S., Mickstein, S., Sommer, U. and Schmieder, K.R. (1998). Monitoring pollutants in coastal bird eggs in the Wadden Sea. Final report of the Pilot Study 1996-1997. Wadden Sea Ecosystem No. 8. Wilhelmshaven, Germany: Common Wadden Sea Secretariat.
6. Berg, C., Halldin, K. and Brunstrom, B. (2001). Effects of bisphenol A and tetrabromobisphenol A on sex organ development in quail and chicken embryos. Environ. Toxicol. Chem. 20, 2836-40.
7. Berg, C., Halldin, K., Brunstrom, B. and Brandt, I. (1998). Methods for studying xenoestrogenic effects in birds. Toxicol. Lett. 103, 671-6.
8. Berg, C., Halldin, K., Fridolfsson, A.K., Brandt, I. and Brunstrom, B. (1999). The avian egg as a test system for endocrine disrupters: effects of diethylstilbestrol and ethynylestradiol on sex organ development. Sci. Tot. Environ. 233, 57-66.
9. Boss, W.R. and Witschi, E. (1947). The permanent effects of early stilbestrol injections on the sex organs of the herring gull (Larus argentatus). J. Exper. Zool. 105, 61-77.
10. Bosveld, A.T.C., Gradener, J., Murk, A.J., Brouwer, A., Van Kampen, M., Evers, E.H.G. and Van den Berg, M. (1995). Effects of PCDDs. PCDFs and PCBs in common tern (Sterna hirundo) breeding in estuarine and coastal colonies in the Netherlands and Belgium. Environ. Toxicol. Chem. 14, 99-115.
11. Bosveld, A.T.C., Nieboer, R., de Bont, A., Mennen, J., Murk, A.J., Feyk, L.A., Giesy, J.P. and van den Berg, M. (2000). Biochemical and developmental effects of dietary exposure to polychlorinated biphenyls 126 and 153 in common tern chicks (Sterna hirundo). Environ. Toxicol. Chem. 19, 719-30.
12. Bosveld, A.T.C. and Van den Berg, M. (1994). Effects of polychlorinated biphenyls, dibenzo-p-dioxins, and dibenzofurans on fish-eating birds. Environ. Rev. 2, 147-66.
13. Brunstrom, B. (1988). Sensitivity of embryos from duck, goose, herring gull, and various chicken breeds to 3,3′4,4′-tetrachlorobiphenyl. Poultry Sci. 67, 52-7.
14. Brunstrom, B., Axelsson, J. and Halldin, K. (2003). Effects of endocrine modulators on sex differentiation in birds. Ecotoxicology 12(1-4), 125-40.
15. Custer, T.W., Custer, C.M. and Stromborg, K.L. (1997). Distribution of organochlorine contaminants in double-crested cormorant eggs and sibling embryos. Environ. Toxicol. Chem. 16, 1646-9.
16. Custer, T.W., Nisbet, I.C.T. and Krynitsky, A.J. (1983). Organochlorine residues and shell characteristics of roseate tern eggs, 1981. J. Field Ornithol. 54, 394-400.
17. Custer, T.W., Pendleton, G. and Ohlendorf, H.M (1990). Within -and among - clutch variation of organochlorine residues in eggs of black-crowned night-herons. Environ. Monitor. Assess. 15, 83-9.
18. Dawson, A. (2000). Mechanisms of endocrine disruption with particular reference to occurrence in avian wildlife: a review. Ecotoxicology 9, 59-69.
19. Domm, L.V. (1939). Intersexuality in adult Brown Leghorn males as a result of estrogenic treatment during early embryonic life. Proc. Soc. Exptl. Biol. Med. 42, 766-8.
20. Domm, L.V. (1940). The effects of embryonic injection of estrogens on sexual characters of brown leghorn hens. Anat. Record 78(Suppl.), 145.
21. Domm, L.V. and Davis, D.E. (1941). The sexual behavior of intersexual domestic fowl. Anat. Record 81(Suppl.), 61.
22. French, J.B. Jr., Nisbet, I.C.T. and Schwabl, H. (2001). Maternal steroids and contaminants in common tern eggs: a mechanism of endocrine disruption? Comp. Biochem. Physiol. 128C, 91-8.
23. Fry, D.M. (1995). Reproductive effects in birds exposed to pesticides and industrial chemicals. Environ. Health Persp. 103(Suppl.), 165-71.
24. Fry, D.M., Toon, C.K., Speich, S.M. and Peard, R.J. (1987). Sex ratio skew and breeding patterns of gulls: demographic and toxicological considerations. Stud. Avian Biol. 10, 26-43.
25. Fry, D.M. and Toone, C.K. (1981). DDT-induced feminization of gull embryos. Science 213, 922-4.
26. Gaarenstroom, J.H. (1939). Action of sex hormones on the development of the Mullerian duct of the chick embryo. J. Exper. Zool. 82, 31-46.
27. Giesy, J.P., Ludvig, J.P. and Tillitt, D.E. (1994). Deformities in birds of the Great Lakes Region: Assigning causality. Environ. Sci. Technol. 28, 128-35.
28. Gilbertson, M., Kubiak, T., Ludwig, J. and Fox, G. (1991). Great Lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish-eating birds: similarity to chick-edema disease. J. Toxicol. Environ. Health 33, 455-520.
29. Haffen, K., Scheib, D., Guichard, A. and Cedard, L. (1975). Prolonged sexual bipotentiality of the embryonic quail testes and relation with sex steroid biosynthesis. Gen. Comp. Endocrinol. 26, 70-8.
30. Hart, C.A. (1998). Feminization in Common Terns (Sterna hirundo): Relationship to Persistent Organic Contaminants. Ph.D. Thesis, Woods Hole Oceanographic Institution/Massachusetts Institute of Technology.
31. Hart, C.A., Hahn, M.E., Nisbet, I.C.T., Moore, M.J., Kennedy, S.W. and Fry, D.M. (1998). Feminization in common terns (Sterna hirundo): relationship to dioxin equivalents and estrogenic compounds. Mar. Environ. Res. 46, 174-5.
32. Hoffman, D.J., Melancon, M.J., Klein, P.N., Eisemann, J.D. and Spann, J.W. (1998). Comparative developmental toxicity of planar polychlorinated biphenyls congeners in chickens, American kestrels and common terns. Environ. Toxicol. Chem. 17, 747-57.
33. Hoffman, D.J., Rice, C.P. and Kubiak, T.J. (1996). PCBs and dioxins in birds. In W.N. Beyer, G.H. Heinz and A.W. Redmon-Norwood (eds) Environmental Contaminants in Wildlife. pp. 165-207. Boca Raton: CRC/Lewis Publishers.
34. Hunt, G.L. and Hunt, M.W. (1977). Female-female pairing in Western gulls (Larus occidentalis) in southern California. Science 196, 1466-77.
35. Hunt, G.L., Wingfield, J.C., Newman, A. and Farner, D.S. (1980). Sex ratio of Western gulls on Santa Barbara Island, California. Auk 97, 473-9.
36. Karchner, S.I., Kennedy, S.W., Trudeau, S. and Hahn, M.E. (2000). Towards a molecular understanding of species differences in dioxin sensitivity: initial characterization of Ah receptor cDNAs in birds and an amphibian. Mar. Environ. Res. 50, 51-6.
37. Kennedy, S.W., Jones, S.P. and Bastien, L.J. (1995). Efficient analysis of cytochrome P4501A catalytic activity, porphyrins, and total proteins in chicken embryo hepatocyte cultures with a fluorescence plate reader. Anal. Biochem. 226, 362-70.
38. Kennedy, S.W., Lorenzen, A., James, C.A. and Collins, B.T. (1993). Ethoxyresorufin-O-deethylase and porphyrin analysis in chicken embryo hepatocyte cultures with a fluorescence multi-well plate reader. Anal. Biochem. 211, 102-12.
39. Kennedy, S.W., Lorenzen, A., Jones, S.P., Hahn, M.E. and Stegeman, J.J. (1996a). Cytochrome P4501A induction in avian hepatocyte cultures: a promising approach for predicting the sensitivity of avian species to toxic effects of halogenated aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 141, 214-30.
40. Kennedy, S.W., Lorenzen, A. and Norstrom, R.J. (1996b). Chicken embryo hepatocyte bioassay for measuring cytochrome P4501A-based 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalent concentrations in environmental samples. Environ. Sci. Technol. 30, 706-15.
41. Kozelka, A.W. and Gallagher, T.F. (1934). Effect of male hormone extracts, theelin and theelol on the chick embryo. Proc. Soc. Exptl. Biol. Med. 31, 1143-4.
42. Kubiak, T.J., Harris, H.J., Smith, L.M., Schwartz, T.R., Stalling, R.L., Trick, J.K., Sileo, L., Docherty, D.E. and Erdman, T.C. (1989). Microcontaminants and reproductive impairment of the Forster's tern on Green Bay, Lake Michigan -1983. Arch. Environ. Contam. Toxicol. 18, 706-27.
43. Lahr, E.L. and Riddle, O. (1945). Intersexuality in male embryos of pigeons. Anat. Record 92, 425-31.
44. Lake, J.L., McKinney, R., Lake, C.A., Osterman, F.A. and Heltshe, J. (1995). Comparisons of patterns of polychlorinated biphenyl congeners in water, sediment, and indigenous organisms from New Bedford harbor, Massachusetts. Arch. Environ. Contam. Toxicol. 29, 207-20.
45. Laulanie, M. (1886). Sur le mode d'evolution et la valeur de l'epithelium germinatif dans le testicule embryonnaire du poulet. Comptes Rendus et Memoires de la Societe de Biologie 38, 87-9.
46. Lewis, L.B. (1946). A study of some effects of sex hormones upon the embryonic reproductive system of the white pekin duck. Physiol. Zool. 19, 282-329.
47. Lorenzen, A., Shutt, L. and Kennedy, S.W. (1997). Sensitivity of common tern (Sterna hirundo) embryo hepatocyte cultures to CYP1A induction and porphyrin accumulation by halogenated aromatic hydrocarbons and common tern egg extracts. Arch. Environ. Contam. Toxicol. 32, 126-34.
48. Murk, A.J., Boudewijn, T.J., Menninger, P.L., Bosveld, A.T.C., Rossaert, G., Ysebaert, T., Meire, P. and Dirksen, S. (1996). Effects of polyhalogenated aromatic hydrocarbons and related contaminants on common tern reproduction: integration of biological, biochemical, and chemical data. Arch. Environ. Contam. Toxicol. 31, 128-40.
49. Nisbet, I.C.T. (1982). Eggshell characteristics and organochlorine residues in common terns. Colonial Waterbirds 5, 139-43.
50. Nisbet, I.C.T. (2002). Common tern Sterna hirundo (No. 618). In A. Poole and F. Gill (eds) The Birds of North America. Philadelphia PA: The Academy of Natural Sciences.
51. Nisbet, I.C.T., Fry, D.M., Hatch, J.J. and Lynn, B. (1996). Feminization of male common tern embryos is not correlated with exposure to specific PCB congeners. Bull. Environ. Contam. Toxicol. 57, 895-901.
52. Nisbet, I.C.T. and Hatch, J.J. (1999). Consequences of a female-biased sex-ratio in a socially monogamous bird: female-female pairs in the roseate tern Sterna dougallii. Ibis 141, 307-20.
53. Nisbet, I.C.T. and Reynolds, L.M. (1984). Organochlorine residues in common terns and associated estuarine organisms, Massachusetts, USA, 1971-81. Mar. Environ. Res. 11, 33-66.
54. Norstrom, R.J., Simon, M. and Muir, D.C.G. (1990). Polychlorinated dibenzo-p-dioxins and dibenzofurans in marine mammals in the Canadian north. Environ. Poll. 66, 1-19.
55. Norstrom, R.J., Simon, M. and Mulvihill, M.J. (1986). A gel-permeation/column chromatography cleanup method for the determination of CDDs in animal tissue. Int. J. Environ. Anal. Chem. 23, 267-87.
56. Peakall, D.B. (1967). Pesticide-induced enzymatic breakdown of steroids in birds. Nature 216, 505-6.
57. Peakall, D.B. (1969). Effect of DDT on calcium uptake and vitamin D metabolism in birds. Nature 224, 1219-20.
58. Peakall, D.B. (1970). p,p′-DDT: effect on calcium metabolism and concentration of estradiol in the blood. Science 168, 592-94.
59. Peakall, D.B. (1996). Disrupted patterns of behavior in natural populations as an index of ecotoxicity. Environ. Health Persp. 104(Suppl. 2), 331-5.
60. Peakall, D.B. and Fox, G.A. (1987). Toxicological investigations of pollutant-related effects in Great Lakes gulls. Environ. Health Persp. 71, 187-93.
61. Pincus, G. and Erickson, A.E. (1962). Sex modifications in hens' eggs following immersion in diethylstilbestrol solutions. Endocrinology 71, 24-30.
62. Pruell, R.J., Norwood, C.B., Bowen, R.D., Boothman, W.S., Rogerson, P.F., Hackett, M. and Butterworth, B.C. (1990). Geochemical study of sediment contamination in New Bedford Harbor, Massachusetts. Mar. Environ. Res. 29, 77-102.
63. Riddle, O. and Dunham, H.H. (1942). Transformation of males to intersexes by estrogen passed from blood of ring doves to their ovarian eggs. Endocrinology 30, 959-68.
64. Risebrough, R.W. (1999). "Endocrine disruption" and the "wildlife connection". Hum. Ecol. Risk Assess. 5, 869-83.
65. Romanoff, A.L. (1960). The Avian Embryo: Structural and Functional Development. New York: Macmillan.
66. Sabo, T.J., Kesseli, R., Halverson, J.L., Nisbet, I.C.T. and Hatch, J.J. (1994). PCR-based method for sexing roseate terns (Sterna dougallii). The Auk 111, 1023-7.
67. Scheib, D. (1983). Effects and role of estrogens in avian gonadal differentiation. Differentiation 23, S87-92.
68. Snedecor, J.G. (1949). A study of some effects of sex hormones on the embryonic reproductive system and comb of the white leghorn chick. J. Exper. Zool. 110, 205-46.
69. Stanley, A.J. (1937). Sexual dimorphism in North American hawks. J. Morphol. 61, 321-39.
70. Swift, C.H. (1916). Origin of the sex-cords and definitive spermatagonia in the male chick. Am. J. Anat. 20, 375-410.
71. Taber, E. (1964). Intersexuality in birds. In C.N. Armstrong and A.J. Marshall (eds) Intersexuality in Vertebrates Including Man, pp. 285-310. London: Academic Press.
72. Tillitt, D.E., Ankley, G.T., Giesy, J.P., Ludwig, J.P., Kurita-Matsuba, H., Weseloh, D.V., Ross, P.S., Bishop, C.A., Sileo, L., Stromborg, K.L., Larson, J. and Kubiak, T.J. (1992). Polychlorinated biphenyl residues and egg mortality in double-crested cormorants from the Great Lakes. Environ. Toxicol. Chem. 11, 1281-8.
73. Walker, M.K. and Catron, T.F. (2000). Characterization of cardiotoxicity induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related chemicals during early chick embryo development. Toxicol. Appl. Pharmacol. 167, 210-21.
74. Weaver, G. (1984). PCB contamination in and around New Bedford, Mass. Environ. Sci. Technol. 18, 22A-7A.
75. Weseloh, D.V.C., Hamr, P., Bishop, C.A. and Norstrom, R.J. (1995). Organochlorine contaminant levels in waterbird species from Hamilton harbour, Lake Ontario: an IJC area of concern. J. Gt. Lakes Res. 21, 121-37.
76. Willier, B.H., Gallagher, T.F. and Koch, F.C. (1937). The modification of sex development in the chick embryo by male and female sex hormones. Physiol. Zool. 10, 101-22.
77. Won, H.T. (1992). Analytical Manual. Department of Environment, Canadian Wildlife Service, Wildlife Toxicology and Surveys Branch 100 Gamelin Boulevard, Hull Quebec, K1A 0H3.