Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): Laboratory and field evidence

Environmental Health Perspectives

Volumn 111, Issue 4, 2003, Pages 568-575

  Hayes, Tyrone ^a   Haston, Kelly ^a   Tsui, Mable ^a   Hoang, Anhthu ^a   Haeffele, Cathryn ^a   Vonk, Aaron ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amphibian; Atrazine; Endocrine disruption; Hermaphrodite

Indexed keywords

ATRAZINE; HERBICIDE; PESTICIDE;

AMPHIBIA; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; FROG; GONAD DEVELOPMENT; GONADAL DYSGENESIS; HERMAPHRODITISM; LABORATORY TEST; MALE; NONHUMAN; OBSERVATION; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; TESTIS CELL; UNITED STATES; VITELLOGENESIS; WATER ANALYSIS; WATER POLLUTION; XENOPUS LAEVIS;

AMPHIBIA; ANIMALIA; ANURA; PANTHERA PARDUS; RANA PIPIENS; VERTEBRATA; XENOPUS LAEVIS;

EID: 0038070176     PISSN: 00916765     EISSN: None     Source Type: Journal    
DOI: 10.1289/ehp.5932     Document Type: Article

References (34)

1. Akingbemi BT, Hardy MP. 2001. Oestrogenic and antiandrogenic chemicals in the environment: effects on male reproductive health. Ann Med 33:391-403.
2. Allran JW, Karasov WH. 2000. Effects of atrazine and nitrate on northern leopard frog (Rana pipiens) larvae exposed in the laboratory from posthatch through metamorphosis. Environ Toxicol Chem 19:2850-2855.
3. Battaglin WA, Goolsby DA. 1995. Spatial Data in Geographic Information System Format on Agricultural Chemical Use, Land Use, and Cropping Practices in the United States. U.S. Geological Survey Water-Resources Investigations Report 94-4176. Reston, VA:U.S. Geological Survey. Available: http://water.usgs.gov/pubs/wri/wri944176/ [accessed 19 February 2003].
4. Blaustein AR, Kiesecker JM. 2002. Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5(4):597-608.
5. Chen CW. 2001. Assessment of endocrine disruptors: approaches, issues, and uncertainties. Folia Histochem Cytobiol 39(suppl 2):20-23.
6. Conant RA. 1998. Field Guide to Reptiles and Amphibians: Eastern and Central North America. Boston:Houghton Mifflin.
7. Crain DA, Guillette LJ Jr, Rooney AA, Pickford DB. 1997. Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminants. Environ Health Perspect 105:528-533.
8. Gardner T. 2001. Declining amphibian populations: a global phenomenon in conservation biology. Anim Biodivers Conserv 24(2):25-44.
9. Goolsby DA, Pereira WE. 1995. Pesticides in the Mississippi River. In: Contaminants in the Mississippi River, 1987-92 (Meade RH, ed). U.S. Geological Survey Circular 1133. Reston, VA:U.S. Geological Survey, 87-102.
10. Hayes E. 1993. EPA's chemical information data base (Keith LH, ed). EPA Journal Jan/Feb/Mar:48.
11. Hayes TB. 1995. An histological examination of the effects of corticosterone in larvae of the western toad, Bufo boreas (Anura: Bufonidae), and the oriental fire-bellied toad, Bombina orientalis (Anura: Discoglossidae). J Morphol 226:297-307.
12. Hayes TB. 1998. Sex determination and primary sex differentiation in amphibians. J Exp Zool 281:373-399.
13. Hayes TB, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A. 2002. Feminization of male frogs in the wild. Nature 419:895-896.
14. Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, et al. 2002. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476-5480.
15. Holtfreter J. 1931. Uber die Aufzucht isolierter Teile des Amphibian Keimes II. Arch F Ent Mech 124:404-465.
16. Kiesecker JM. 2002. Synergism between trematode infection and pesticide exposure: a link to amphibian deformities in nature. Proc Natl Acad Sci USA. 99:9900-9904.
17. Kimbrough RA, Litke DW. 1995. Pesticides in Surface Water in Agricultural and Urban Areas of the South Platte River Basin from Denver, Colorado to North Platte, Nebraska, 1993-94. Water-Resources Investigations Report 97-4230. Denver, CO:U.S. Geological Survey.
18. McClaren A. 1995. Germ cells and germ cell sex. Philos Trans R Soc Lond B Biol Sci 350:229-233.
19. Nakatsuji N, Chuma S. 2001. Differentiation of mouse primordial germ cells into female or males germ cells. J Dev Biol 45:541-548.
20. Reeder AL, Foley GL, Nichols DK, Hansen LG, Wikoff B, Faeh S, et al. 1998. Forms and prevalence of intersexuality and effects of environmental contaminants on sexuality in cricket frogs (Acris crepitans). Environ Health Perspect 106:261-266.
21. Richards CM, Nace GW. 1978. Gynogenetic and hormonal sex reversal used in tests of the XX-XY hypothesis of sex determination in Rana pipiens. Growth 42:319-331.
22. Sanderson JT, Letcher RJ, Heneweer M, Giesy JP, van den Berg M. 2001. Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environ Health Perspect 109:1027-1031.
23. Sanderson JT, Seinen W, Giesy JP, van den Berg M. 2000. 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol Sci 54:121-127.
24. Solomon K, Keith R, David B, Baker R, Richards P, Dixon KR, et al. 1996. Ecological risk assessment of atrazine in North American surface waters. Environ Toxicol Chem 15:31-76.
25. Stebbins R. 1985. A Field Guide to Western Reptiles and Amphibians: Field Marks of all Species in Western North America, Including Baja California. Boston:Houghton Mifflin.
26. Tennant MK, Hill DS, Eldridge JC, Wetzel LT, Breckenridge CB, Stevens JT. 1994. Chloro-s-triazine antagonism of estrogen action: limited interaction with estrogen receptor binding. J Toxicol Environ Health 43:197-211.
27. Tevera-Mendoza L, Ruby S, Brousseau P, Fournier M, Cyr D, Marcogliese D. 2002. Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the testis. Environ Toxicol Chem 21:527-531.
28. Thiros SA. 2000. Quality of Shallow Ground Water in Areas of Recent Residential and Commercial Development in Salt Lake Valley, Utah 1999. U.S. Geological Survey Fact Sheet 106-00. Salt Lake City, UT:U.S. Geological Survey.
29. U.S. Environmental Protection Agency. 1994. Atrazine, simazine, and cyanizine. Notice of initiation of special review. Fed Reg 59:60412-60443.
30. U.S. EPA. Methods for Determination of Organic Compounds in Drinking Water-Supplement III. 1995. EPA/ 600/R-95-131. Washington, DC:U.S. Environmental Protection Agency.
31. U.S. EPA. Methods for the Determination of Organic Compounds in Drinking Water. EPA-600/4-88/039. Cincinnati, OH:U.S. Environmental Protection Agency.
32. Wake DB. 1991. Declining amphibian populations. Science 253:860.
33. Witschi E. 1929. Rudimentary hermaphroditism and Y chromosome in Rana temporaria. J Exp Zool 54:157-223.
34. Witschi E. 1957. The inductor theory of sex differentiation. J Fac Sci Hokkaido Univ Ser VI 13:428-439.