Skip to main content
Log in

Mechanisms of Endocrine Disruption with Particular Reference to Occurrence in Avian Wildlife: A Review

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

This review examines the evidence for endocrine disruption in birds. It reviews in vitro and in vivo laboratory based evidence for endocrine disruption by (1) agonism or antagonism of gonadal steroid hormones, (2) altering the activity of cytochrome P450 enzymes, (3) altering thyroid hormone function, (4) affecting intrinsic neuroendocrine control mechanisms and (5) activation of the stress response. It also discusses the evidence for the existence of such effects in free-living birds. In vitro studies demonstrate that mechanisms for potential endocrine disruption exist, but in vivo studies suggest that such mechanisms are insufficient to overwhelm endogenous homeostatic control. There are only two phenomena in wild birds where endocrine disruption has been cited as a possible cause: eggshell thinning and supernormal clutches. Evidence suggests that neither of these is caused by endocrine disruption. Despite three decades of concern, there is no evidence that avian wildlife has suffered endocrine disruption.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allen-Rowlands, C.F., Castracane, V.D., Hamilton, M.G. and Seifter, J. 1981. Effect of polybrominated biphenyls PBB on the pituitary-thyroid axis of the rat. Proceedings of the Society for Experimental Biology and Medicine 166, 506-14.

    Google Scholar 

  • Beestra, J.B., Vanengelen, J.G.M., Karels, P., Van der Hoek, H.J., Dejong, M., Docter, R., Krenning, E.P., Hennemann, G., Brouwer, A. and Visser, T.J. 1991. Thyroxine and 3,39,5-triiodothyronine are glucuronidated in rat liver by different uridine diphosphate glucuronyltransferases. Endocrinology 128, 741-6.

    Google Scholar 

  • Bitman, J., Cecil, H.C., Harris, S.J. and Fries, G.F. 1968. Estrogenic activity of o,p9-DDT in the mammalian uterus and avian oviduct. Science 162, 371-2.

    Google Scholar 

  • 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. Environmental Toxicology and Chemistry 14, 99-115.

    Google Scholar 

  • Brouwer, A., Blaner, W.S., Kukler, A. and Van den Berg, K.J. 1988. Study on the mechanism of interference of 3,4,39,49-tetrachlorobiphenyl with the plasma retinol-binding proteins in rodents. Chemico-Biological Interactions 68, 203-17.

    Google Scholar 

  • Brouwer, A., Klassonwehler, E., Bokdam, M., Morse, D.C. and Traag, W.A. 1990a. Competitive-inhibition of thyroxine binding to transthyretin by monohydroxy metabolites of 3,4,39,49-tetrachlorobiphenyl. Chemosphere 20, 1257-62.

    Google Scholar 

  • Brouwer, A., Murk, A.J. and Koeman, J.H. 1990b. Biochemical and physiological approaches in ecotoxicology. Functional Ecology 4, 275-81.

    Google Scholar 

  • Chang, L., Munro, S.L.A., Richardson, S.J. and Schreiber, G. 1999. Evolution of thyroid hormone binding by transthyretins in birds and mammals. European Journal of Biochemistry 259, 534-42.

    Google Scholar 

  • Colburn, T., Dumanoski, D. and Myers, J.P. 1996. Our Stolen Future. Boston: Little, Brown & Co.

    Google Scholar 

  • Conover, M.R. 1984. Occurrence of supernormal clutches in the Laridae. Wilson Bulletin 96, 249-67.

    Google Scholar 

  • Conover, M.R. and Hunt, G.L.J. 1984a. Experimental evidence that female-female pairs in gulls result from a shortage of breeding males. Condor 86, 472-6.

    Google Scholar 

  • Conover, M.R. and Hunt, G.L.J. 1984b. Female-female pairing and sex ratios in gulls: an historical perspective. Wilson Bulletin 96, 619-25.

    Google Scholar 

  • Cooke, A.S. 1973. Shell thinning in avian eggs by environmental pollutants. Environmental Pollution 4, 85-152.

    Google Scholar 

  • Cooke, A.S. 1975. Pesticides and eggshell formation. Symposium of the Zoological Society, London 35, 339-61.

    Google Scholar 

  • Davison, T.F., Flack, I.H. and Butler, E.J. 1978. The binding of thyroxine and triiodothyronine to plasma proteins in the chicken at the physiological pH. Research in Veterinary Science 25, 280-3.

    Google Scholar 

  • Dawson, A. 1994. Pesticide Interaction, pp. 47. Report to the Department of the Environment.

  • Dawson, A. 1998. Natural and anthropogenic environmental oestrogens: the scientific basis for risk assessment. Comparative reproductive physiology of non-mammalian species. Pure and Applied Chemistry 70, 1657-69.

    Google Scholar 

  • Dawson, A. and Pottinger, T.G. 1999. Non-Reproductive Effects of Endocrine Disrupting Chemicals, pp. 89. Report to the Department of the Environment, Transport and the Regions.

  • Elbrecht, A. and Smith, R. 1992. Aromatase enzyme activity and sex determination in chickens. Science 255, 467-70.

    Google Scholar 

  • Etches, R.J. and Kigami, K. 1997. Genotypic and phenotypic sex reversal. In S. Harvey and R.J. Etches ed Perspectives in Avian Endocrinology, pp. 57-67. Bristol: Journal of Endocrinology Ltd.

    Google Scholar 

  • Fowles, J.R., Fairbrother, A., Baechersteppan, L. and Kerkvliet, N.I. 1994. Immunological and endocrine effects of the flame-retardant pentabromodiphenyl ether de-71 in c57blr6j mice. Toxicology 86, 49-61.

    Google Scholar 

  • Fowles, J.R., Fairbrother, A., Trust, K.A. and Kerkvliet, N.I. 1997. Effects of Aroclor 1254 on the thyroid gland, immune function, and hepatic cytochrome P450 activity in mallards. Environmental Research 75, 119-29.

    Google Scholar 

  • Fox, G.A. and Boersma, D. 1983. Characteristics of supernormal ring-billed gull clutches and their attending adults. Wilson Bulletin 95, 552-9.

    Google Scholar 

  • French, J.B., Nisbet, I.T.C. and Schwabl, H. 2000. Does maternal polychlorinated biphenyl exposure affect steroid deposition into eggs of common terns Sterna hirundo ? In VII International Symposium on Avian Endocrinology, Varanasi, India, January 2000, Abstract 14.08.

  • French, J.B., Ottinger, M.A., Rattner, B.A. and Henry, P. 2000. Reproductive and developmental effects of polychlorinated biphenyls on American kestrels: endocrine disruption? In VII International Symposium on Avian Endocrinology, Varanasi, India, January 2000, Abstract 14.02.

  • Fry, D.M. and Toone, C.K. 1981. DDT-induced feminization of gull embryos. Science 213, 922-4.

    Google Scholar 

  • Gould, J.C., Cooper, K.R. and Scanes, C.G. 1997. Effects of polychlorinated biphenyl mixtures and three specific congeners on growth and circulating growth-related hormones. General and Comparative Endocrinology 106, 221-30.

    Google Scholar 

  • Hill, R.N., Erdreich, L.S., Paynter, O.E., Roberts, P.A., Rosenthal, S.L. and Wilkinson, C.F. 1989. Thyroid follicular cell carcinogenesis. Fundamental and Applied Toxicology 12, 629-97.

    Google Scholar 

  • Hoffman, D.J., Melancon, M.J., Klein, P.N., Eisemann, J.D. and Spann, J.W. 1998. Comparative developmental toxicity of planar polychlorinated biphenyl congeners in chickens, American kestrels, and common terns. Environmental Toxicology and Chemistry 17, 747-57.

    Google Scholar 

  • Hunt, G.L.J. and Hunt, M.W. 1977. Female-female pairing in Western gulls Larus occidentalis in southern California. Science 196, 1466-7.

    Google Scholar 

  • Janz, D.M. and Bellward, G.D. 1996a. In ovo 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure in three avian species. 2. Effects on estrogen receptor and plasma sex steroid hormones during the perinatal period. Toxicology and Applied Pharmacology 139, 292-300.

    Google Scholar 

  • Janz, D.M. and Bellward, G.D. 1996b. In ovo 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure in three avian species. 1. Effects on thyroid hormones and growth during the perinatal period. Toxicology and Applied Pharmacology 139, 281-291.

    Google Scholar 

  • Janz, D.M. and Bellward, G.D. 1997. Effects of acute 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on plasma thyroid and sex steroid hormone concentrations and estrogen receptor levels in adult great blue herons. Environmental Toxicology and Chemistry 16, 985-9.

    Google Scholar 

  • Jefferies, D.J. 1969. Induction of apparent hyperthyroidism in birds fed DDT. Nature London 222, 578-9.

    Google Scholar 

  • Jefferies, D.J. and French, M.C. 1969. Avian thyroid: effect of p,p9-DDT on size and activity. Science 166, 1278-80.

    Google Scholar 

  • Jefferies, D.J. and French, M.F. 1971. Hyper-and hypothyroidism in pigeons fed DDT: an explanation for the 'thin eggshell' phenomenon. Environmental Pollution 1, 235-42.

    Google Scholar 

  • Jefferies, D.J. and French, M.F. 1972. Changes in the pigeon thyroid by p,p9-DDE and dieldrin. Journal of Wildlife Management 36, 24-30.

    Google Scholar 

  • Jefferies, D.J. and Parslow, J.L.F. 1972. Effect of one polychlorinated biphenyl on size and activity of the gull thy Dawson 68 roid. Bulletin of Environmental Contamination and Toxicology 8, 306-10.

    Google Scholar 

  • Jefferies, D.J. and Parslow, J.L.F. 1976. Thyroid changes in PCB-dosed guillemots and their indication of one of the mechanisms of actions of these materials. Environmental Pollution 10, 293-311.

    Google Scholar 

  • Kühn, E.R. 1990. Hormonal control of peripheral monodeiodination in vertebrates. In A. Epple, C.G. Scanes and M.H. Stetson eds Progress in Comparative Endocrinology, pp. 421-426. New York: Wiley-Liss.

    Google Scholar 

  • Kühn, E.R., Mol, K. and Darras, V.M. 1995. Peripheral deiodination of thyroid hormones. Netherlands Journal of Zoology 45, 135-9.

    Google Scholar 

  • Lans, M.C., Klassonwehler, E., Willemsen, M., Meussen, E., Safe, S. and Brouwer, A. 1993. Structure-dependent, competitive interaction of hydroxy-polychlorobiphenyls, hydroxy-dibenzo-p-dioxins and hydroxy-dibenzofurans with human transthyretin. Chemico-Biological Interactions 88, 7-21.

    Google Scholar 

  • Lincer, J.L. and Peakall, D.B. 1970. Metabolic effects of polychlorinated biphenyls in the American kestrel. Nature London 228, 783-4.

    Google Scholar 

  • Lundholm, C.E. 1997. DDE-induced eggshell thinning in birds: effects of p,p9-DDE on the calcium and prostaglandin metabolism of the eggshell gland. Comparative Biochemistry and Physiology C?Pharmacology Toxicology & Endocrinology 118, 113-28.

    Google Scholar 

  • McArthur, M.L.B., Fox, G.A., Peakall, D.B. and Philogene, B.J.R. 1983. Ecological significance of behavioral and hormonal abnormalities in breeding ring doves fed an organochlorine chemical mixture. Archives of Environmental Contamination and Toxicology 12, 343-53.

    Google Scholar 

  • McNabb, F.M.A. and Freeman, T.B. 1990. Comparative studies of thyroid hormone deiodinase systems. In A. Epple, C.G. Scanes and M.H. Stetson, Progress in Comparative Endocrinology, pp. 433-8. New York: Wiley-Liss.

    Google Scholar 

  • McNabb, F.M.A. and Hughes, T.E. 1983. The role of serum binding proteins in determining free thyroid hormone concentrations during development in quail. Endocrinology 113, 957-63.

    Google Scholar 

  • Morse, D.C., Groen, D., Veerman, M., Van Amerongen, C.J., Koëter, H.B.W.M., Van Prooije, A.E.S., Visser, T.J., Koeman, J.H. and Brouwer, A. 1993. Interference of polychlorinated-biphenyls in hepatic and brain thyroidhormone metabolism in fetal and neonatal rats. Toxicology and Applied Pharmacology 122, 27-33.

    Google Scholar 

  • Morse, D.C., Koeter, H.B.W.M., Van Prooijen, A.E.S. and Brouwer, A. 1992. Interference of polychlorinated-biphenyls in thyroid-hormone metabolism-possible neurotoxic consequences in fetal and neonatal rats. Chemosphere 25, 165-8.

    Google Scholar 

  • Morse, D.C., Seegal, R.F., Borsch, K.O. and Brouwer, A. 1996. Long-term alterations in regional brain serotonin metabolism following maternal polychlorinated biphenyl exposure in the rat. Neurotoxicology Little Rock 17, 631-8.

    Google Scholar 

  • Murk, A.J., Bosveld, A.T.C., Vandenberg, M. and Brouwer, A. 1994. Effects of polyhalogenated aromatic hydrocarbons PHAHs on biochemical parameters in chicks of the common tern Sterna hirundo. Aquatic Toxicology 30, 91-115.

    Google Scholar 

  • Newton, I. and Wyllie, I. 1992. Recovery of a sparrowhawk population in relation to declining pesticide contamination. Journal of Applied Ecology 29, 436-84.

    Google Scholar 

  • Newton, I., Wyllie, I. and Asher, A. 1992. Long-term trends in organochlorine and mercury residues in some predatory birds in Britain. Environmental Pollution 79, 143-51.

    Google Scholar 

  • Norris, D.O. 1997. Vertebrate endocrinology, p. 634. San Diego: Academic Press.

    Google Scholar 

  • Nowicki, H.C. and Norman, A.W. 1972. Enhanced hepatic metabolism of testosterone, 4-androstene-3,17-dione and estradiol 17b in chickens pretreated with DDT or PCB. Steroids 19, 85-99.

    Google Scholar 

  • Peakall, D.B. 1967. Pesticide-induced enzyme breakdown of steroids in birds. Nature London 216, 505-7.

    Google Scholar 

  • Ratcliffe, D.A. 1967. Decrease in eggshell weight in certain birds of prey. Nature London 215, 208-10.

    Google Scholar 

  • Rattner, B.A. 1982. Diagnosis of anticholinesterase poisoning in birds: effects of environmental temperature and underfeeding on cholinesterase activity. Environmental Toxicology and Chemistry 1, 329-35.

    Google Scholar 

  • Rattner, B.A., Clarke, R.N. and Ottinger, M.A. 1986. Depression of plasma luteinizing hormone concentration in quail by the anticholinesterase insecticide parathion. Comparative Biochemistry and Physiology 83C, 451-3.

    Google Scholar 

  • Richie, P.J. and Peterle, T.J. 1979. Effect of DDE on circulating luteinizing hormone levels in ring doves during courtship and nesting. Bulletin of Environmental Contamination and Toxicology 23, 220-6.

    Google Scholar 

  • Risebrough, R.E., Rieche, P., Peakall, D.B., Herman, S.G. and Kirven, M.N. 1968. Polychlorinated biphenyls in the global ecosystem. Nature London 220, 1098-1102.

    Google Scholar 

  • Sanderson, J.T., Janz, D.M., Bellward, G.D. and Giesy, J.P. 1997. Effects of embryonic and adult exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on hepatic microsomal testosterone hydroxylase activities in great blue herons Ardea herodias. Environmental Toxicology and Chemistry 16, 1304-10.

    Google Scholar 

  • Sauer, P.J.J., Huisman, M., Koopman-Esseboom, C., Morse, D.C., Smits-Van Prooije, A.E., Van De Berg, K.J., Tuinstra, L.G.M.T., Van Der Paauw, C.G., Boersma, E.R., Weisglas-Kuperus, N., Lammers, J.H.C.M., Kulig, B.M.and Brouwer, A. 1994. Effects of polychlorinated biphenyls PCBs and dioxins on growth and development. Human & Experimental Toxicology 13, 900-6.

    Google Scholar 

  • Schreiber, G., Prapunpoj, P., Chang, L., Richardson, S.J., Aldred, A.R. and Munro, S.L. 1998. Evolution of thyroid hormone distribution. Clinical and Experimental Pharmacology and Physiology 25, 728-32.

    Google Scholar 

  • Schuur, A.G., Boekhorst, F.M., Brouwer, A. and Visser, T.J. 1997. Extrathyroidal effects of 2,3,7,8-tetrachlorodibenzop-dioxin on thyroid hormone turnover in male Sprague-Dawley rats. Endocrinology 138, 3727-34.

    Google Scholar 

  • Van Birgelen, A.P.J.M., Fase, K.M., Van Der Kolk, J., Poiger, H., Brouwer, A., Seinen, W. and Van Den Berg, M. 1996. Synergistic effect of 2,29,4,49,5,59-hexachlorobiphenyl and 2,3,7,8-tetrachlorodibenzo-p-dioxin on hepatic porphyrin levels in the rat. Environmental Health Perspectives 104, 550-7.

    Google Scholar 

  • Van Birgelen, A.P.J.M., Smit, E.A., Kampen, I.M., Groeneveld, C.N., Fase, K.M., Van Der Kolk, J., Poiger, H., Van Den Berg, M., Koeman, J.H. and Brouwer, A. 1995a. Endocrine Disruption in Birds 69 Subchronic effects of 2,3,7,8-TCDD or PCBs on thyroid hormone metabolism: use in risk assessment. European Journal of Pharmacology Environmental Toxicology and Pharmacology Section 5, 77-85.

    Google Scholar 

  • Van Birgelen, A.P.J.M., Van der Kolk, J., Fase, K.M., Bol, I., Poiger, H., Brouwer, A. and Van den Berg, M. 1995b. Subchronic dose-response study of 2,3,7,8-tetrachlorodibenzo-p-dioxin in female Sprague-Dawley rats. Toxicology and Applied Pharmacology 132, 1-13.

    Google Scholar 

  • Van den Berg, K.J., Van Raaji, J.A.G.M., Bragt, P.C. and Notten, W.R.F. 1991. Interactions of halogenated industrial chemicals with transthyretin and effects on thyroid hormone levels in vivo. Archives of Toxicology 65, 15-9.

    Google Scholar 

  • Van den Berg, M., Craane, B.L.H.J., Sinnige, T., Van Mourik, S., Dirksen, S., Boudewijn, T., Vav der Gaag, M., Lutke-Schipholt, I.J., Spenkelink, B. and Brouwer, A. 1994. Biochemical and toxic effects of polychlorinated biphenyls PCBs, dibenzo-p-dioxins PCCDs and dibenzofurans PCDFs in the cormorant Phalacrocarax carbo after in ovo exposure. Environmental Toxicology and Chemistry 13, 803-16.

    Google Scholar 

  • Van den Berg, M., Craane, L.H.J., Van Mourik, S. and Brouwer, A. 1995. The possible impact of chlorinated dioxins PCDDS, dibenzofurans PCDFS and biphenyls PCBS on the reproduction of the Cormorant Phalacrocorax carbo: an ecotoxicological approach. Ardea 83, 299-313.

    Google Scholar 

  • Wingfield, J.C., Newman, A.L., Hunt, G.L.J. and Farner, D.S. 1982. Endocrine aspects of female-female pairing in the Western gull, Larus occidentalis wymani. Animal Behavior 30, 9-22.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dawson, A. Mechanisms of Endocrine Disruption with Particular Reference to Occurrence in Avian Wildlife: A Review. Ecotoxicology 9, 59–69 (2000). https://doi.org/10.1023/A:1008964128501

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1008964128501

Navigation