Do hormone-modulating chemicals impact on reproduction and development of wild amphibians?

Biological Reviews

Volumn 90, Issue 4, 2015, Pages 1100-1117

  Orton, Frances ^a   Tyler, Charles R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Endocrine disrupting chemicals; Feminisation; Frogs; Intersex; Metamorphosis; Pesticides; Pollution; Reproduction

Indexed keywords

ENDOCRINE DISRUPTOR; WATER POLLUTANT;

AMPHIBIA; ANIMAL; FEMALE; MALE; METABOLISM; PHYSIOLOGY; REPRODUCTION; TOXICITY; WATER POLLUTANT;

AMPHIBIANS; ANIMALS; ENDOCRINE DISRUPTORS; FEMALE; MALE; REPRODUCTION; WATER POLLUTANTS, CHEMICAL;

EID: 84943387471     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12147     Document Type: Article

References (157)

1. Ahn, R. S., Han, S. J., Kim, S. C. & Kwon, H. B. (2007). Effects of butyltin compounds on follicular steroidogenesis in the bullfrog (Rana catesbeiana). Environmental Toxicology and Pharmacology 24, 149-154.
2. Beckmen, K. B., Blake, J. E., Ylitalo, G. M., Stott, J. L. & O'Hara, T. M. (2003). Organochlorine contaminant exposure and associations with hematological and humoral immune functional assays with dam age as a factor in free-ranging northern fur seal pups (Callorhinus ursinus). Marine Pollution Bulletin 46, 594-606.
3. Behrends, T., Urbatzka, R., Krackow, S., Elepfandt, A. & Kloas, W. (2010). Mate calling behavior of male South African clawed frogs (Xenopus laevis) is suppressed by the antiandrogenic endocrine disrupting compound flutamide. General and Comparative Endocrinology 168, 269-274.
4. Bernabò, I., Gallo, L., Sperone, E., Tripepi, S. & Brunelli, E. (2011). Survival, development, and gonadal differentiation in Rana dalmatina chronically exposed to chlorpyrifos. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 315A, 314-327.
5. Bosveld, A. T. C. & van den Berg, M. (2002). Reproductive failure and endocrine disruption by organohalogens in fish-eating birds. Toxicology 181-182, 155-159.
6. Boyd, S. K., Wissing, K. D., Heinsz, J. E. & Prins, G. S. (1999). Androgen receptors and sexual dimorphisms in the larynx of the bullfrog. General and Comparative Endocrinology 113, 59-68.
7. Brodeur, J. C., Sassone, A., Hermida, G. N. & Codugnello, N. (2013). Environmentally-relevant concentrations of atrazine induce non-monotonic acceleration of developmental rate and increased size at metamorphosis in Rhinella arenarum tadpoles. Ecotoxicology and Environmental Safety 92, 10-17.
8. Brody, J. G., Moysich, K. B., Humblet, O., Attfield, K. R., Beehler, G. P. & Rudel, R. A. (2007). Environmental pollutants and breast cancer. Cancer 109, 2667-2711.
9. Carlsson, G., Kulkarni, P., Larsson, P. & Norrgren, L. (2007). Distribution of BDE-99 and effects on metamorphosis of BDE-99 and -47 after oral exposure in Xenopus tropicalis. Aquatic Toxicology 84, 71-79.
10. Carr, J. A., Gentles, A., Smith, E. E., Goleman, W. L., Urquidi, L. J., Thuett, K., Kendall, R. J., Giesy, J. P., Gross, T. S., Solomon, K. R. & Van der Kraak, G. (2003a). Response of larval Xenopus laevis to atrazine: assessment of growth, metamorphosis, and gonadal and laryngeal morphology. Environmental Toxicology and Chemistry 22, 396-405.
11. Carr, J. A., Urquidi, L. J., Goleman, W. L., Hu, F., Smith, N. P., Theodorakis, C. W., Krest, S. & Linder, G. (2003b). Ammonium perchlorate disruption of thyroid function in natural amphibian populations: assessment and potential impact. In Multiple Stressor Effects in Relation to Declining Amphibian Populations, pp. 130-142. American Society for Testing and Materials, Bridgeport.
12. Carr, J. A. & Patiño, R. (2011). The hypothalamus-pituitary-thyroid axis in teleosts and amphibians: endocrine disruption and its consequences to natural populations. General and Comparative Endocrinology 170, 299-312.
13. Cheek, A. O., Ide, C. F., Bollinger, J. E., Rider, C. V. & McLachlan, J. A. (1999). Alteration of leopard frog (Rana pipiens) metamorphosis by the herbicide acetochlor. Archives of Environmental Contamination and Toxicology 37, 70-77.
14. Cheng, Y., Cui, Y., Chen, H.-M. & Xie, W.-P. (2011). Thyroid disruption effects of environmental level perfluorooctane sulfonates (PFOS) in Xenopus laevis. Ecotoxicology 20, 2069-2078.
15. Coady, K., Marino, T., Thomas, J., Sosinski, L., Neal, B. & Hammond, L. (2013). An evaluation of 2, 4-dichlorophenoxyacetic acid in the amphibian metamorphosis assay and the fish short-term reproduction assay. Ecotoxicology and Environmental Safety 90, 143-150.
16. Coady, K. K., Murphy, M. B., Villeneuve, D. L., Hecker, M., Jones, P. D., Carr, J. A., Solomon, K. R., Smith, E. E., Van der Kraak, G., Kendall, R. J. & Giesy, J. P. (2004). Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog (Rana clamitans). Journal of Toxicology and Environmental Health-Part A-Current Issues 67, 941-957.
17. Coady, K. K., Murphy, M. B., Villeneuve, D. L., Hecker, M., Jones, P. D., Carr, J. A., Solomon, K. R., Smith, E. E., Van Der Kraak, G., Kendall, R. J. & Giesy, J. P. (2005). Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, aromatase activity, and sex steroid concentrations in Xenopus laevis. Ecotoxicology and Environmental Safety 62, 160-173.
18. Corcoran, J., Winter, M. J. & Tyler, C. R. (2010). Pharmaceuticals in the aquatic environment: a critical review of the evidence for health effects in fish. Critical Reviews in Toxicology 40, 287-304.
19. Coyle, T. L. & Karasov, W. H. (2010). Chronic, dietary polybrominated diphenyl ether exposure affects survival, growth, and development of Rana pipiens tadpoles. Environmental Toxicology and Chemistry 29, 133-141.
20. Cushman, S. A. (2006). Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biological Conservation 128, 231-240.
21. Denver, R. J. (2009). Stress hormones mediate environment-genotype interactions during amphibian development. General and Comparative Endocrinology 164, 20-31.
22. Dittrich, R., Beckmann, M. W., Oppelt, P. G., Hoffmann, I., Lotz, L., Kuwert, T. & Mueller, A. (2011). Thyroid hormone receptors and reproduction. Journal of Reproductive Immunology 90, 58-66.
23. Duarte-Guterman, P., Langlois, V. S., Hodgkinson, K., Pauli, B. D., Cooke, G. M., Wade, M. G. & Trudeau, V. L. (2009). The aromatase inhibitor fadrozole and the 5-reductase inhibitor finasteride affect gonadal differentiation and gene expression in the frog Silurana tropicalis. Sexual Development 3, 333-341.
24. Du Preez, L. H., Kunene, N., Everson, G. J., Carr, J. A., Giesy, J. P., Gross, T. S., Hosmer, A. J., Kendall, R. J., Smith, E. E., Solomon, K. R. & Van Der Kraak, G. J. (2008). Reproduction, larval growth, and reproductive development in African clawed frogs (Xenopus laevis) exposed to atrazine. Chemosphere 71, 546-552.
25. Du Preez, L. H., Kunene, N., Hanner, R., Giesy, J. P., Solomon, K. R., Hosmer, A. & Van der Kraak, G. J. (2009). Population-specific incidence of testicular ovarian follicles in Xenopus laevis from South Africa: a potential issue in endocrine testing. Aquatic Toxicology 95, 10-16.
26. Egea-Serrano, A., Relyea, R. A., Tejedo, M. & Torralva, M. (2012). Understanding of the impact of chemicals on amphibians: a meta-analytic review. Ecology and Evolution 2, 1382-1397.
27. El Jamil, A., Magre, S., Mazabraud, A. & Penrad-Mobayed, M. (2008). Early aspects of gonadal sex differentiation in Xenopus tropicalis with reference to an antero-posterior gradient. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 309A, 127-137.
28. Emerson, S. B., Greig, A., Carroll, L. & Prins, G. S. (1999). Androgen receptors in two androgen-mediated, sexually dimorphic characters of frogs. General and Comparative Endocrinology 114, 173-180.
29. Epstein, M. S. & Blackburn, D. G. (1997). Histology and histochemistry of androgen-stimulated nuptial pads in the leopard frog, Rana pipiens, with notes on nuptial gland evolution. Canadian Journal of Zoology 75, 472-477.
30. Eubig, P. A., Aguiar, A. & Schantz, S. L. (2010). Lead and PCBs as risk factors for attention deficit/hyperactivity disorder. Environmental Health Perspectives 118, 1654-1667.
31. Fiorentino, M., Yamamoto, K., Tanaka, S., Pinelli, C., D'Aniello, B., Kikuyama, S. & Rastogi, R. K. (1999). Ontogenetic profile of FSH and LH in Rana esculenta. General and Comparative Endocrinology 116, 114-121.
32. Flament, S., Chardard, D., Chesnel, A. & Dumond, H. (2011). Sex determination and sexual differentiation in amphibians. In Hormones and Reproduction in Vertebrates (eds D. O. Norris and H. Lopez ), pp. 209-345. Academic Press Inc., London; Burlington; San Diego.
33. Foote, C. L. (1964). Intersexuality in amphibians. In Intersexuality in Vertebrates Including Man (eds C. N. Armstrong and A. J. Marshall ), pp. 233-272. Academic Press Inc., New York.
34. Giesy, J. P., Feyk, L. A., Jones, P. D., Kannan, K. & Sanderson, T. (2003). Review of the effects of endocrine-disrupting chemicals in birds. Pure and Applied Chemistry 75, 2287-2303.
35. Goleman, W. L., Carr, J. A. & Anderson, T. A. (2002). Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis. Environmental Toxicology and Chemistry 21, 590-597.
36. Gomez-Mestre, I., Kulkarni, S. & Buchholz, D. R. (2013). Mechanisms and consequences of developmental acceleration in tadpoles responding to pond drying. PLoS One 8, e84266.
37. Goto, Y., Kitamura, S., Kashiwagi, K., Oofusa, K., Tooi, O., Yoshizato, K., Sato, J., Ohta, S. & Kashiwagi, A. (2006). Suppression of amphibian metamorphosis by bisphenol A and related chemical substances. Journal of Health Science 52, 160-168.
38. Goulet, B. N. & Hontela, A. (2003). Toxicity of cadmium, endosulfan, and atrazine in adrenal steroidogenic cells of two amphibian species, Xenopus laevis and Rana catesbeiana. Environmental Toxicology and Chemistry 22, 2106-2113.
39. Gray, K. & Janssens, P. (1990). Gonadal hormones inhibit the induction of metamorphosis by thyroid hormones in Xenopus laevis tadpoles in vivo but not in vitro. General and Comparative Endocrinology 77, 202-211.
40. Guillette, L. J., Crain, D. A., Gunderson, M. P., Kools, S. A. E., Milnes, M. R., Orlando, E. F., Rooney, A. A. & Woodward, A. R. (2000). Alligators and endocrine disrupting contaminants: a current perspective. American Zoologist 40, 438-452.
41. Gutleb, A. C., Mossink, L., Schriks, M., van den Berg, H. J. H. & Murk, A. J. (2007). Delayed effects of environmentally relevant concentrations of 3, 3′, 4, 4′-tetrachlorobiphenyl (PCB-77) and non-polar sediment extracts detected in the prolonged-FETAX. Science of the Total Environment 381, 307-315.
42. Gyllenhammar, I., Holm, L., Eklund, R. & Berg, C. (2009). Reproductive toxicity in Xenopus tropicalis after developmental exposure to environmental concentrations of ethynylestradiol. Aquatic Toxicology 91, 171-178.
43. Hallinger, K. K., Zabransky, D. J., Kazmer, K. A. & Cristol, D. A. (2010). Birdsong differs between mercury-polluted and reference sites. The Auk 127, 156-161.
44. Harris, C. A., Hamilton, P. B., Runnalls, T. J., Vinciotti, V., Henshaw, A., Hodgson, D., Coe, T. S., Jobling, S., Tyler, C. R. & Sumpter, J. P. (2011). The consequences of feminization in breeding groups of wild fish. Environmental Health Perspectives 119, 306-311.
45. Hayes, T. B. (1997). Steroids as potential modulators of thyroid hormone activity in anuran metamorphosis. American Zoologist 37, 185-194.
46. Hayes, T. B. (1998). Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. Journal of Experimental Zoology 281, 373-399.
47. Hayes, T. B., Anderson, L. L., Beasley, V. R., de Solla, S. R., Iguchi, T., Ingraham, H., Kestemont, P., Kniewald, J., Kniewald, Z., Langlois, V. S., Luque, E. H., McCoy, K. A., Muñoz-de-Toro, M. N., Oka, T., Oliveira, C. A., Orton, F., Ruby, S., Suzawa, M., Tavera-Mendoza, L. E., Trudeau, V. L., Victor-Costa, A. B. & Willingham, E. (2011). Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes. The Journal of Steroid Biochemistry and Molecular Biology 127, 64-73.
48. Hayes, T. B., Case, P., Chui, S., Chung, D., Haeffele, C., Haston, K., Lee, M., Mai, V. P., Marjuoa, Y., Parker, J. & Tsui, M. (2006). Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environmental Health Perspectives 114, 40-50.
49. Hayes, T., Chan, R. & Licht, P. (1993). Interactions of temperature and steroids on larval growth, development, and metamorphosis in a toad (Bufo-Boreas). Journal of Experimental Zoology 266, 206-215.
50. Hayes, T. B., Collins, A., Lee, M., Mendoza, M., Noriega, N., Stuart, A. A. & Vonk, A. (2002). Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proceedings of the National Academy of Sciences of the United States of America 99, 5476-5480.
51. Hayes, T., Haston, K., Tsui, M., Hoang, A., Haeffele, C. & Vonk, A. (2003). Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environmental Health Perspectives 111, 568-575.
52. Hayes, T. B., Khoury, V., Narayan, A., Nazir, M., Park, A., Brown, T., Adame, L., Chan, E., Buchholz, D., Stueve, T. & Gallipeau, S. (2010). Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proceedings of the National Academy of Sciences of the United States of America 107, 4612-4617.
53. Hecker, M., Giesy, J. P., Jones, P. D., Jooste, A. M., Carr, J. A., Solomon, K. R., Smith, E. E., Van der Kraak, G., Kendall, R. J. & Du Preez, L. (2004). Plasma sex steroid concentrations and gonadal aromatase activities in African clawed frogs (Xenopus laevis) from South Africa. Environmental Toxicology and Chemistry 23, 1996-2007.
54. Hecker, M., Kim, W. J., Park, J. W., Murphy, M. B., Villeneuve, D., Coady, K. K., Jones, P. D., Solomon, K. R., Van Der Kraak, G., Carr, J. A., Smith, E. E., du Preez, L., Kendall, R. J. & Giesy, J. P. (2005). Plasma concentrations of estradiol and testosterone, gonadal aromatase activity and ultrastructure of the testis in Xenopus laevis exposed to estradiol or atrazine. Aquatic Toxicology 72, 383-396.
55. Hersikorn, B. D. & Smits, J. E. G. (2011). Compromised metamorphosis and thyroid hormone changes in wood frogs (Lithobates sylvaticus) raised on reclaimed wetlands on the Athabasca oil sands. Environmental Pollution 159, 596-601.
56. Hof, C., Araújo, M. B., Jetz, W. & Rahbek, C. (2011). Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480, 516-519.
57. Hoffmann, F. & Kloas, W. (2010). An environmentally relevant endocrine-disrupting antiandrogen, vinclozolin, affects calling behavior of male Xenopus laevis. Hormones and Behavior 58, 653-659.
58. Hogan, N. S., Duarte, P., Wade, M. G., Lean, D. R. S. & Trudeau, V. L. (2008). Estrogenic exposure affects metamorphosis and alters sex ratios in the northern leopard frog (Rana pipiens): identifying critically vulnerable periods of development. General and Comparative Endocrinology 156, 515-523.
59. Hopkins, W. A., Mendonca, M. T. & Congdon, J. D. (1997). Increased circulating levels of testosterone and corticosterone in southern toads, Bufo terrestris, exposed to coal combustion waste. General and Comparative Endocrinology 108, 237-246.
60. Howe, C. M., Berrill, M., Pauli, B. D., Helbing, C. C., Werry, K. & Veldhoen, N. (2004). Toxicity of glyphosate-based pesticides to four North American frog species. Environmental Toxicology and Chemistry 23, 1928-1938.
61. Hsu, C.-Y., Chang, L.-T., Ku, H.-H. & Lu, M.-H. (1985). In vitro estradiol synthesis and secretion by tadpole ovaries of different developmental stages. General and Comparative Endocrinology 57, 393-396.
62. Hu, F., Smith, E. E. & Carr, J. A. (2008). Effects of larval exposure to estradiol on spermatogenesis and in vitro gonadal steroid secretion in African clawed frogs, Xenopus laevis. General and Comparative Endocrinology 155, 190-200.
63. Huang, Y. W., Karasov, W. H., Patnode, K. A. & Jefcoate, C. R. (1999). Exposure of northern leopard frogs in the Green Bay ecosystem to polychlorinated biphenyls, polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans is measured by direct chemistry but not hepatic ethoxyresorufin-O-deethylase activity. Environmental Toxicology and Chemistry 18, 2123-2130.
64. Hyne, R. V., Spolyarich, N., Wilson, S. P., Patra, R. W., Byrne, M., Gordon, G., Sanchez-Bayo, F. & Palmer, C. G. (2009). Distribution of frogs in rice bays within an irrigated agricultural area: links to pesticide usage and farm practices. Environmental Toxicology and Chemistry 28, 1255-1265.
65. Iguchi, T. (2011). Amphibian development, growth and reproduction assay using Xenopus tropicalis and in vitro extrogen receptor transactivation assay. In ISAREN: 7th International Symposium on Amphibian and Reptilian Endocrinology and Neurobiology Frontiers in Endocrinology. Universtiy of Michigan, Ann Arbor.
66. Iwasawa, H. & Yamaguchi, K. (1984). Ultrastructural study of gonadal development in Xenopus laevis. Zoological Sciences 1, 591-600.
67. Jofre, M. B. & Karasov, W. H. (2008). Effect of mono-ortho and di-ortho substituted polychlorinated biphenyl (PCB) congeners on leopard frog survival and sexual development. Chemosphere 70, 1609-1619.
68. Jooste, A. M., Du Preez, L. H., Carr, J. A., Giesy, J. P., Gross, T. S., Kendall, R. J., Smith, E. E., Van der Kraak, G. L. & Solomon, K. R. (2005). Gonadal development of larval male Xenopus laevis exposed to atrazine in outdoor microcosms. Environmental Science and Technology 39, 5255-5261.
69. Karasov, W. H., Jung, R. E., Vanden Langenberg, S. & Bergeson, T. L. E. (2005). Field exposure of frog embryos and tadpoles along a pollution gradient in the Fox River and Green Bay ecosystem in Wisconsin, USA. Environmental Toxicology and Chemistry 24, 942-953.
70. Kidd, K. A., Blanchfield, P. J., Mills, K. H., Palace, V. P., Evans, R. E., Lazorchak, J. M. & Flick, R. W. (2007). Collapse of a fish population after exposure to a synthetic estrogen. Proceedings of the National Academy of Sciences of the United States of America 104, 8897-8901.
71. Kim, A. N., Ahn, R. S. & Kwon, H. B. (2006). Effects of azoles on the in vitro follicular steroidogenesis in amphibians. Integrative Biosciences 10, 203-209.
72. Kitamura, S., Kato, T., Iida, M., Jinno, N., Suzuki, T., Ohta, S., Fujimoto, N., Hanada, H., Kashiwagi, K. & Kashiwagi, A. (2005). Anti-thyroid hormonal activity of tetrabromobisphenol A, a flame retardant, and related compounds: affinity to the mammalian thyroid hormone receptor, and effect on tadpole metamorphosis. Life Sciences 76, 1589-1601.
73. Kloas, W., Lutz, I., Springer, T., Krueger, H., Wolf, J., Holden, L. & Hosmer, A. (2009). Does atrazine influence larval development and sexual differentiation in Xenopus laevis? Toxicological Sciences 107, 376-384.
74. Kojima, H., Katsura, E., Takeuchi, S., Niiyama, K. & Kobayashi, K. (2004). Screening for estrogen and androgen receptor activities in 200 pesticides by in vitro reporter gene assays using Chinese hamster ovary cells. Environmental Health Perspectives 112, 524-531.
75. Kvarnryd, M., Grabic, R., Brandt, I. & Berg, C. (2011). Early life progestin exposure causes arrested oocyte development, oviductal agenesis and sterility in adult Xenopus tropicalis frogs. Aquatic Toxicology 103, 18-24.
76. Lanctot, C., Robertson, C., Navarro-Martin, L., Edge, C., Melvin, S. D., Houlahan, J. & Trudeau, V. L. (2013). Effects of the glyphosate-based herbicide Roundup WeatherMax(R) on metamorphosis of wood frogs (Lithobates sylvaticus) in natural wetlands. Aquatic Toxicology 140-141, 48-57.
77. Langlois, V. S., Carew, A. C., Pauli, B. D., Wade, M. G., Cooke, G. M. & Trudeau, V. L. (2010). Low levels of the herbicide atrazine alter sex ratios and reduce metamorphic success in Rana pipiens tadpoles raised in outdoor mesocosms. Environmental Health Perspectives 118, 552-557.
78. Leary, C. J., Garcia, A. M. & Knapp, R. (2006). Elevated corticosterone levels elicit non-calling mating tactics in male toads independently of changes in circulating androgens. Hormones and Behavior 49, 425-432.
79. Lee, W., Kang, C.-W., Su, C.-K., Okubo, K. & Nagahama, Y. (2012). Screening estrogenic activity of environmental contaminants and water samples using a transgenic medaka embryo bioassay. Chemosphere 88, 945-952.
80. Lee, S. K. & Veeramachaneni, D. N. R. (2005). Subchronic exposure to low concentrations of di-n-butyl phthalate disrupts spermatogenesis in Xenopus laevis frogs. Toxicological Sciences 84, 394-407.
81. Levy, G., Lutz, I., Kruger, A. & Kloas, W. (2004). Bisphenol A induces feminization in Xenopus laevis tadpoles. Environmental Research 94, 102-111.
82. Liu, C., Deng, J., Yu, L., Ramesh, M. & Zhou, B. (2010). Endocrine disruption and reproductive impairment in zebrafish by exposure to 8:2 fluorotelomer alcohol. Aquatic Toxicology 96, 70-76.
83. Lou, Q.-Q., Zhang, Y.-F., Zhou, Z., Shi, Y.-L., Ge, Y.-N., Ren, D.-K., Xu, H.-M., Zhao, Y.-X., Wei, W.-J. & Qin, Z.-F. (2013). Effects of perfluorooctanesulfonate and perfluorobutanesulfonate on the growth and sexual development of Xenopus laevis. Ecotoxicology 22, 1133-1144.
84. MacKenzie, C. A., Berrill, M., Metcalfe, C. & Pauli, B. D. (2003). Gonadal differentiation in frogs exposed to estrogenic and anti-estrogenic compounds. Environmental Toxicology and Chemistry 22, 2466-2475.
85. Main, K. M., Skakkebæk, N. E., Virtanen, H. E. & Toppari, J. (2010). Genital anomalies in boys and the environment. Best Practice & Research Clinical Endocrinology & Metabolism 24, 279-289.
86. Mann, R. M., Hyne, R. V., Choung, C. B. & Wilson, S. P. (2009). Amphibians and agricultural chemicals: review of the risks in a complex environment. Environmental Pollution 157, 2903-2927.
87. Marlatt, V. L., Veldhoen, N., Lo, B. P., Bakker, D., Rehaume, V., Vallée, K., Haberl, M., Shang, D., van Aggelen, G. C., Skirrow, R. C., Elphick, J. R. & Helbing, C. C. (2013). Triclosan exposure alters postembryonic development in a Pacific tree frog (Pseudacris regilla) Amphibian Metamorphosis Assay (TREEMA). Aquatic Toxicology 126, 85-94.
88. McCoy, K. A., Bortnick, L. J., Campbell, C. M., Hamlin, H. J., Guillette, L. J. & St. Mary, C. M. (2008). Agriculture alters gonadal form and function in the toad Bufo marinus. Environmental Health Perspectives 116, 1526-1532.
89. McDaniel, T. V., Martin, P. A., Struger, J., Sherry, J., Marvin, C. H., McMaster, M. E., Clarence, S. & Tetreault, G. (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. Aquatic Toxicology 88, 230-242.
90. Mitsui, N., Tooi, O. & Kawahara, A. (2007). Vitellogenin-inducing activities of natural, synthetic, and environmental estrogens in primary cultured Xenopus laevis hepatocytes. Comparative Biochemistry and Physiology C: Toxicology & Pharmacology 146, 581-587.
91. Morrissey, C. A., Stanton, D. W. G., Pereira, M. G., Newton, J., Durance, I., Tyler, C. R. & Ormerod, S. J. (2013). Eurasian dipper eggs indicate elevated organohalogenated contaminants in urban rivers. Environmental Science and Technology 47, 8931-8939.
92. Mosconi, G., Di Rosa, I., Bucci, S., Morosi, L., Franzoni, M. F., Polzonetti-Magni, A. M. & Pascolini, R. (2005). Plasma sex steroid and thyroid hormones profile in male water frogs of the Rana esculenta complex from agricultural and pristine areas. General and Comparative Endocrinology 142, 318-324.
93. Murphy, M. B., Hecker, M., Coady, K. K., Tompsett, A. R., Jones, P. D., Du Preez, L. H., Everson, G. J., Solomon, K. R., Carr, J. A., Smith, E. E., Kendall, R. J., Van Der Kraak, G. & Giesy, J. P. (2006). Atrazine concentrations, gonadal gross morphology and histology in ranid frogs collected in Michigan agricultural areas. Aquatic Toxicology 76, 230-245.
94. Nakamura, M. (2010). The mechanism of sex determination in vertebrates-are sex steroids the key-factor? Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 313A, 381-398.
95. Newbold, R. R., Padilla-Banks, E., Jefferson, W. N. & Heindel, J. J. (2008). Effects of endocrine disruptors on obesity. International Journal of Andrology 31, 201-208.
96. Nomiyama, K., Nomura, Y., Takahashi, T., Uchiyama, Y., Arizono, K. & Shinohara, R. (2010). Hydroxylated polychlorinated biphenyls (OH-PCBs) induce vitellogenin through estrogenic activity in primary-cultured hepatocytes of the Xenopus laevis. Chemosphere 78, 800-806.
97. Norris, D. O. (2006). Vertebrate Endocrinology. Fourth Edition. Academic Press, London; Burlington; San Diego.
98. Oehlmann, J., Oetken, M. & Schulte-Oehlmann, U. (2008). A critical evaluation of the environmental risk assessment for plasticizers in the freshwater environment in Europe, with special emphasis on bisphenol A and endocrine disruption. Environmental Research 108, 140-149.
99. Oehlmann, J. & Schulte-Oehlmann, U. (2003). Endocrine disruption in invertebrates. Pure and Applied Chemistry 75, 2207-2218.
100. Ohtani, H., Miura, I. & Ichikawa, Y. (2000). Effects of dibutyl phthalate as an environmental endocrine disruptor on gonadal sex differentiation of genetic males of the frog Rana rugosa. Environmental Health Perspectives 108, 1189-1193.
101. Oka, T., Tooi, O., Mitsui, N., Miyahara, M., Ohnishi, Y., Takase, M., Kashiwagi, A., Shinkai, T., Santo, N. & Iguchi, T. (2008). Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis. Aquatic Toxicology 87, 215-226.
102. Oldfield, R. G. (2005). Genetic, abiotic and social influences on sex differentiation in cichlid fishes and the evolution of sequential hermaphroditism. Fish and Fisheries 6, 93-110.
103. Opitz, R., Braunbeck, T., Bogi, C., Pickford, D. B., Nentwig, G., Oehlmann, J., Tooi, O., Lutz, I. & Kloas, W. (2005). Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid system-disrupting activities of environmental compounds. Environmental Toxicology and Chemistry 24, 653-664.
104. Orton, F., Baynes, A., Clare, F., Duffus, A., Larroze, S., Scholze, M. & Garner, T. W. J. (2014). Body size, nuptial pad size and hormone levels: potential non-destructive biomarkers of reproductive health in wild toads (Bufo bufo). Ecotoxicology 20, 901-911.
105. Orton, F., Carr, J. A. & Handy, R. D. (2006). Effects of nitrate and atrazine on larval development and sexual differentiation in the northern leopard frog Rana pipiens. Environmental Toxicology and Chemistry 25, 65-71.
106. Orton, F., Lutz, I., Kloas, W. & Routledge, E. J. (2009). Endocrine disrupting effects of herbicides and pentachlorophenol: in vitro and in vivo evidence. Environmental Science and Technology 43, 2144-2150.
107. Orton, F. & Routledge, E. (2011). Agricultural intensity in ovo affects growth, metamorphic development and sexual differentiation in the common toad (Bufo bufo). Ecotoxicology 20, 901-911.
108. Papoulias, D. M., Schwarz, M. S. & Mena, L. (2013). Gonadal abnormalities in frogs (Lithobates spp.) collected from managed wetlands in an agricultural region of Nebraska, USA. Environmental Pollution 172, 1-8.
109. Park, B. J. & Kidd, K. (2005). Effects of the synthetic oestrogen ethinylestradiol on early life stages of mink frogs and green frogs in the wild and in situ. Environmental Toxicology and Chemistry 24, 2027-2036.
110. Pettersson, I., Arukwe, A., Lundstedt-Enkel, K., Mortensen, A. S. & Berg, C. (2006). Persistent sex-reversal and oviducal agenesis in adult Xenopus (Silurana) tropicalis frogs following larval exposure to the environmental pollutant ethynylestradiol. Aquatic Toxicology 79, 356-365.
111. Pickford, D. B., Hetheridge, M. J., Caunter, J. E., Hall, A. T. & Hutchinson, T. H. (2003). Assessing chronic toxicity of bisphenol A to larvae of the African clawed frog (Xenopus laevis) in a flow-through exposure system. Chemosphere 53, 223-235.
112. Pickford, D. B. & Morris, I. D. (1999). Effects of endocrine-disrupting contaminants on amphibian oogenesis: methoxychlor inhibits progesterone-induced maturation of Xenopus laevis oocytes in vitro. Environmental Health Perspectives 107, 285-292.
113. Pickford, D. B. & Morris, I. D. (2003). Inhibition of gonadotropin-induced oviposition and ovarian steroidogenesis in the African clawed frog (Xenopus laevis) by the pesticide methoxychlor. Aquatic Toxicology 62, 179-194.
114. Piprek, R. P., Pecio, A., Kubiak, J. Z. & Szymura, J. M. (2012). Differential effects of testosterone and 17β-estradiol on gonadal development in five anuran species. Reproduction 144, 257-267.
115. Ponse, K. (1949). La differenciation du sexe et l'intersexualite chez les vertebres. First Edition. Libraire de l'Universite, Lausanne.
116. Qin, Z. F., Qin, X. F., Yang, L., Han-Ting, L., Zhao, X. R. & Xu, X. B. (2007). Feminizing/demasculinizing effects of polychlorinated biphenyls on the secondary sexual development of Xenopus laevis. Aquatic Toxicology 84, 321-327.
117. Qin, X. F., Xia, X. J., Yang, Z. Z., Yan, S. S., Zhao, Y. X., Wei, R. G., Li, Y., Tian, M., Zhao, X. R., Qin, Z. F. & Xu, X. B. (2010). Thyroid disruption by technical decabromodiphenyl ether (DE-83R) at low concentrations in Xenopus laevis. Journal of Environmental Sciences (China) 22, 477-751.
118. Qin, Z. F., Zhou, J. M., Chu, S. G. & Xu, X. B. (2003). Effects of Chinese domestic polychlorinated biphenyls (PCBs) on gonadal differentiation in Xenopus laevis. Environmental Health Perspectives 111, 553-556.
119. Reeder, A. L., Foley, G. L., Nichols, D. K., Hansen, L. G., Wikoff, B., Faeh, S., Eisold, J., Wheeler, M. B., Warner, R., Murphy, J. E. & Beasley, V. R. (1998). Forms and prevalence of intersexuality and effects of environmental contaminants on sexuality in cricket frogs (Acris crepitans). Environmental Health Perspectives 106, 261-266.
120. Reeder, A. L., Ruiz, M. O., Pessier, A., Brown, L. E., Levengood, J. M., Phillips, C. A., Wheeler, M. B., Warner, R. E. & Beasley, V. R. (2005). Intersexuality and the cricket frog decline: historic and geographic trends. Environmental Health Perspectives 113, 261-265.
121. Reijnders, P. J. (1986). Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 324, 456-457.
122. Rohr, J. R. & McCoy, K. A. (2010). A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environmental Health Perspectives 118, 20-32.
123. Rose, C. S. (2005). Integrating ecology and developmental biology to explain the timing of frog metamorphosis. Trends in Ecology & Evolution 20, 129-135.
124. Routti, H., Arukwe, A., Jenssen, B. M., Letcher, R. J., Nyman, M., Bäckman, C. & Gabrielsen, G. W. (2010). Comparative endocrine disruptive effects of contaminants in ringed seals (Phoca hispida) from Svalbard and the Baltic Sea. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 152, 306-312.
125. Runnalls, T. J., Beresford, N., Losty, E., Scott, A. P. & Sumpter, J. P. (2013). Several synthetic progestins with different potencies adversely affect reproduction of fish. Environmental Science and Technology 47, 2077-2084.
126. Saka, M., Tada, N. & Kamata, Y. (2013). Application of an amphibian (Silurana tropicalis) metamorphosis assay to the testing of the chronic toxicity of three rice paddy herbicides: Simetryn, mefenacet, and thiobencarb. Ecotoxicology and Environmental Safety 92, 135-143.
127. Scheulhammer, A. M., Meyer, M. W., Sandheinrich, M. B. & Murray, M. W. (2007). Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36, 12-18.
128. Scholz, S. & Kluver, N. (2009). Effects of endocrine disrupters on sexual, gonadal development in fish. Sexual Development 3, 136-151.
129. Schwendiman, A. L. & Propper, C. R. (2012). A common environmental contaminant affects sexual behavior in the clawed frog, Xenopus tropicalis. Physiology and Behaviour 106, 520-526.
130. Searcy, B. T., Beckstrom-Sternberg, S. M., Beckstrom-Sternberg, J. S., Stafford, P., Schwendiman, A. L., Soto-Pena, J., Owen, M. C., Ramirez, C., Phillips, J., Veldhoen, N., Helbing, C. C. & Propper, C. R. (2012). Thyroid hormone-dependent development in Xenopus laevis: a sensitive screen of thyroid hormone signaling disruption by municipal wastewater treatment plant effluent. General and Comparative Endocrinology 176, 481-492.
131. Segner, H., Casanova-Nakayama, A., Kase, R. & Tyler, C. R. (2013). Impact of environmental estrogens on fish considering the diversity of estrogen signaling. General and Comparative Endocrinology 191, 190-201.
132. Shirey, E. A. L., Langerveld, A. J., Mihalko, D. & Ide, C. F. (2006). Polychlorinated biphenyl exposure delays metamorphosis and alters thyroid hormone system gene expression in developing Xenopus laevis. Environmental Research 102, 205-214.
133. Sitja-Bobadilla, A. (2009). Can Myxosporean parasites compromise fish and amphibian reproduction? Proceedings of the Royal Society B: Biological Sciences 276, 2861-2870.
134. Skelly, D., Bolden, S. & Dion, K. (2010). Intersex frogs concentrated in suburban and urban landscapes. EcoHealth 7, 374-379.
135. Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Hines, H. B. & Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125-134.
136. Smith, E. E., Du Preez, L. H., Gentles, A., Solomon, K. R., Tandler, B., Carr, J. A., Van der Kraak, G. L., Kendall, R. J., Giesy, J. P. & Gross, T. S. (2005). Assessment of laryngeal muscle and testicular cell types in Xenopus laevis (Anura Pipidae) inhabiting maize and non-maize growing areas of South Africa. African Journal of Herpetology 54, 69-76.
137. Sowers, A. D., Mills, M. A. & Klaine, S. J. (2009). The developmental effects of a municipal wastewater effluent on the northern leopard frog, Rana pipiens. Aquatic Toxicology 94, 145-152.
138. Spolyarich, N., Hyne, R., Wilson, S., Palmer, C. & Byrne, M. (2010). Growth, development and sex ratios of Spotted Marsh Frog (Limnodynastes tasmaniensis) larvae exposed to atrazine and a herbicide mixture. Chemosphere 78, 807-813.
139. Storrs-Mendez, S. I. & Semlitsch, R. D. (2010). Intersex gonads in frogs: understanding the time course of natural development and role of endocrine disruptors. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 314B, 57-66.
140. Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L. & Waller, R. W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783-1786.
141. Tata, J. R. (1996). Amphibian metamorphosis: an exquisite model for hormonal regulation of postembryonic development in vertebrates. Development, Growth & Differentiation 38, 223-231.
142. Tata, J. R. (1999). Amphibian metamorphosis as a model for studying the developmental actions of thyroid hormone. Biochimie 81, 359-366.
143. Tavera-Mendoza, L., Ruby, S., Brousseau, P., Fournier, M., Cyr, D. & Marcogliese, D. (2002a). Response of the amphibian tadpole Xenopus laevis to atrazine during sexual differentiation of the ovary. Environmental Toxicology and Chemistry 21, 1264-1267.
144. Tavera-Mendoza, L., Ruby, S., Brousseau, P., Fournier, M., Cyr, D. & Marcogliese, D. (2002b). Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the testis. Environmental Toxicology and Chemistry 21, 527-531.
145. Theodorakis, C. W., Rinchard, J., Carr, J. A., Park, J. W., McDaniel, L., Liu, F. J. & Wages, M. (2006). Thyroid endocrine disruption in stonerollers and cricket frogs from perchlorate-contaminated streams in east-central Texas. Ecotoxicology 15, 31-50.
146. Tobias, M., Marin, M. & Kelley, D. (1993). The roles of sex, innervation, and androgen in laryngeal muscle of Xenopus laevis. The Journal of Neuroscience 13, 324-333.
147. Van Schmidt, N. D., Cary, T. L., Ortiz-Santaliestra, M. E. & Karasov, W. H. (2012). Effects of chronic polybrominated diphenyl ether exposure on gonadal development in the northern leopard frog, Rana pipiens. Environmental Toxicology and Chemistry 31, 347-354.
148. Veldhoen, N., Boggs, A., Walzak, K. & Helbing, C. C. (2006a). Exposure to tetrabromobisphenol-A alters TH-associated gene expression and tadpole metamorphosis in the Pacific tree frog Pseudacris regilla. Aquatic Toxicology 78, 292-302.
149. Veldhoen, N., Skirrow, R. C., Osachoff, H., Wigmore, H., Clapson, D. J., Gunderson, M. P., Van Aggelen, G. & Helbing, C. C. (2006b). The bactericidal agent triclosan modulates thyroid hormone-associated gene expression and disrupts postembryonic anuran development. Aquatic Toxicology 80, 217-227.
150. Villalpando, I. & Merchant-Larios, H. (1990). Determination of the sensitive stages for the gonadal sex-reversal in Xenopus laevis tadpoles. International Journal of Developmental Biology 34, 281-285.
151. Wake, D. B. (2012). Facing extinction in real time. Science 335, 1052-1053.
152. WHO (2002). Global Assessment of the State-of-the-Science of Endocrine Disruptors, (eds T. Damstra, S. Barlow, A. Bergman, R. Kavlock, G. Van Der Kraak ) International Program on Chemical Safety, Geneva.
153. WHO (2012). State of the Science of Endocrine Disrupting Chemicals (eds A. Bergman, J. J. Heindel, S. Jobling, K. A. Kidd and R. T. Zoeller ), pp. 7-9. International Program on Chemical Safety, Geneva.
154. Williams, B. & Semlitsch, R. (2010). Larval responses of three midwestern anurans to chronic, low-dose exposures of four herbicides. Archives of Environmental Contamination and Toxicology 58, 819-827.
155. Witschi, E. (1930). Studies on sex differentiation and sex determination in amphibians. IV. The geographical distribution of the sex races of the European Grass frog (Rana temporaria, L.). A contribution to the problem of the evolution of sex. The Journal of Experimental Zoology 56, 149-165.
156. van Wyk, J. H., Pool, E. J. & Leslie, A. J. (2003). The effects of anti-androgenic and oestrogenic disrupting contaminants on breeding gland (nuptial pad) morphology, plasma testosterone levels, and plasma vitellogenin levels in male Xenopus laevis (African clawed frog). Archives of Environmental Contamination and Toxicology 44, 247-256.
157. Yoshimoto, S., Okada, E., Umemoto, H., Tamura, K., Uno, Y., Nishida-Umehara, C., Matsuda, Y., Takamatsu, N., Shiba, T. & Ito, M. (2008). A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proceedings of the National Academy of Sciences 105, 2469-2474.