Investigating the Impact of Chronic Atrazine Exposure on Sexual Development in Zebrafish

Birth Defects Research Part B - Developmental and Reproductive Toxicology

Volumn 95, Issue 4, 2012, Pages 276-288

  Corvi, Margaret M ^a   Stanley, Kerri A ^a   Peterson, Tracy S ^a   Kent, Michael L ^a   Feist, Stephen W ^b   La Du, Jane K ^a   Volz, David C ^c   Hosmer, Alan J ^d   Tanguay, Robert L ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b CENTRE FOR ENVIRONMENT   (United Kingdom)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d SYNGENTA CROP PROTECTION   (United States)

Author keywords

atrazine; chronic exposure; sex differentiation; sexual development; zebrafish

Indexed keywords

ATRAZINE; ESTRADIOL;

ACUTE TOXICITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYSTITIS; EMBRYO; FEMALE; HISTOPATHOLOGY; LONG TERM EXPOSURE; MALE; NONHUMAN; OOCYTE; PERITONITIS; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; SPERMATID; SPERMATOCYTE; SPERMATOGONIUM; TOXICITY TESTING; WATER QUALITY; WILD TYPE; ZEBRA FISH;

ANIMALS; ATRAZINE; EMBRYO, NONMAMMALIAN; ENVIRONMENTAL EXPOSURE; FEMALE; GONADS; MALE; SEXUAL DEVELOPMENT; ZEBRAFISH;

EID: 84865113145     PISSN: 15429733     EISSN: 15429741     Source Type: Journal    
DOI: 10.1002/bdrb.21016     Document Type: Article

References (42)

1. Bringolf RB, Belden JB, Summerfelt RC. 2004. Effects of atrazine on fathead minnow in a short-term reproduction assay. Environ Toxicol Chem 23(4):1019-1025.
2. Coady KK, Murphy MB, Villeneuve DL, Hecker M, Jones PD, Carr JA, Solomon KR, Smith EE, Van Der Kraak G, Kendall RJ, Giesy JP. 2004. Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog (Rana clamitans). J Toxicol Environ Health A 67(12):941-957.
3. Dietrich DR, Krieger HO. 2008. Fish species of interest. Histological analysis of endocrine disruptive effects in small laboratory fish. Hoboken, NJ: John Wiley & Sons, Inc. p. 7-18.
4. Dionne E. 1992. Atrazine technical-chronic toxicity to the fathead minnow (Pimephales promelas) during a full life-cycle exposure. Wareham, MA: Springborn Laboratories, Inc; submitted by Ciba-Geigy Corp., Greensboro, NC. EPA MRID 425471-03.
5. Giddings JM, Anderson TA, Hall Jr LW, Hosmer AJ, Kendall RJ, Richards RP, Solomon KR, Williams WM. 2005. Atrazine in North American surface waters: a probabilistic aquatic ecological risk assessment. Pensacola, FL: Pensacola Society of Environmental Toxicology and Chemistry (SETAC). 432 p.
6. Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A. 2002a. Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs Rana pipiens: laboratory and field evidence. Environ Health Perspect 111(4):568-575.
7. Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, Vonk A. 2002b. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99(8):5476-5480.
8. Hayes TB, 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). Proc Natl Acad Sci USA 107(10):4612-4617.
9. 2-estradiol): support for the demasculinization/feminization hypothesis. Environ Health Perspect 114(S-1):134-141.
10. Huber W. 1993. Ecotoxicological relevance of atrazine in aquatic systems. Environ Toxicol Chem 12(10):1865-1881.
11. Kazeto Y, Place AR, Trant JM. 2004. Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat Toxicol 69(1):25-34.
12. Kent ML, Buchner C, Watral VG, Sanders JL, LaDu J, Peterson TS, Tanguay RL. 2011. Development and maintenance of a specific pathogen-free (SPF) zebrafish research facility for Pseudoloma neurophilia. Dis Aquat Org 95(1):73-79.
13. 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? Toxicol Sci 107(2):376-384.
14. LaFiandra EM, Babbitt KJ, Sower SA. 2008. Effects of atrazine on anuran development are altered by the presence of a nonlethal predator. J Toxicol Environ Health A 71(8):505-511.
15. Langlois VrS, Carew AC, Pauli BD, Wade MG, Cooke GM, Trudeau VL. 2009. Low levels of the herbicide atrazine alter sex ratios and reduce metamorphic success in Rana pipiens tadpoles raised in outdoor mesocosms. Environ Health Perspect 118(4):552-557.
16. Lawrence C, Ebersole J, Kesseli R. 2008. Rapid growth and out-crossing promote female development in zebrafish (Danio rerio). Environ Biol Fish 81(2):239-246.
17. Maack G, Segner H. 2003. Morphological development of the gonads in zebrafish. J Fish Biol 62(4):895-906.
18. Maack G, Segner H. 2004. Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp Biochem Physiol C: Toxicol Pharmacol 139(1-3):47-55.
19. Macek KJ, Buxton KS, Sauter S, Gnilka S, Dean JW. 1976. Chronic toxicity of atrazine to selected aquatic invertebrates and fishes. EPA MRID 000243-77. Duluth, MN: USEPA, Off. Res. Dev., Environ. Res. Lab. 49 p.
20. Murray KN, Bauer J, Tallen A, Matthews JL, Westerfield M, Varga ZM. (in press). Characterization and management of asymptomatic mycobacterium infections at the Zebrafish International Resource Center. Comp Med 2011;50:675-679.
21. Nadzialek S, Spanò L, Mandiki S, Kestemont P. 2008. High doses of atrazine do not disrupt activity and expression of aromatase in female gonads of juvenile goldfish (Carassius auratus L.). Ecotoxicology 17(6):464-470.
22. 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. Aquat Toxicol 87(4):215-226.
23. Orban L, Sreenivasan R, Olsson P-E. 2009. Long and winding roads: testis differentiation in zebrafish. Mol Cell Endocrinol 312(1-2):35-41.
24. Reimers MJ, Flockton AR, Tanguay RL. 2004. Ethanol- and acetaldehyde-mediated developmental toxicity in zebrafish. Neurotoxicol Teratol 26(6):769-781.
25. Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schäfers C, Vandenbergh GF, Watts M, Wenzel A. 2003. Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol Environ Safety 54(3):302-314.
26. Shang EH, Yu RM, Wu RS. 2006. Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio). Environ Sci Technol 40(9):3118-3122.
27. Solomon KR. 1996. Overview of recent developments in ecotoxicological risk assessment. Risk Analysis 16(5):627-633.
28. Solomon, RK, Carr, AJ, Preez DHL, Giesy, PJ, Kendall, JR, Smith, EE, Kraak VD. 2008. Effects of atrazine on fish, amphibians, and aquatic reptiles: a critical review. London: Informa Healthcare. 52 p.
29. Spanò L, Tyler CR, Aerle Rv, Devos P, Mandiki SNM, Silvestre F, Thomé J-P, Kestemont P. 2004. Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquat Toxicol 66(4):369-379.
30. Spiteri ID, Guillette LJ, Jr, Crain DA. 1999. The functional and structural observations of the neonatal reproductive system of alligators exposed in ovo to atrazine, 2, 4-D, or estradiol. Toxicol Ind Health 15(1-2):181-186.
31. 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(7):807-813.
32. Storrs SI, Semlitsch RD. 2008. Variation in somatic and ovarian development: predicting susceptibility of amphibians to estrogenic contaminants. Gen Comp Endocrinol 156(3):524-530.
33. Suzawa M, Ingraham HA. 2008. The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells. PLoS ONE 3(5):e2117.
34. Thelin GP, Stone WW. 2010. Method for estimating annual atrazine use for counties in the conterminous United States, 1992-2007. Reston, VA: U.S. Geological Survey Scientific Investigations Report.
35. Tillitt DE, Papoulias DM, Whyte JJ, Richter CA. 2010. Atrazine reduces reproduction in fathead minnow (Pimephales promelas). Aquat Toxicol 99(2):149-159.
36. USEPA. 1996. Ecological effects test guidelines-OPPTS 850.1400 Fish early life stage toxicity test. (EPA Document No. EPA 712-C-96-121).
37. USEPA. 2005. Draft final report on multi-chemical evaluation of the short-term reproduction assay with the fathead minnow. 169 p.
38. USEPA. 2007. White Paper on the potential for atrazine to affect amphibian gonadal development. Submitted to the FIFRA Scientific Advisory Panal (SAP) for Review and Comment.
39. USEPA. 2008. The potential for atrazine to affect amphibian gonadal development. FIFRA Scientific Advisory Panel Meeting SAP Minutes No 2007-08 October 9-11, 2007.
40. USEPA. 2011a. Atrazine background. Pesticides: topical & chemical fact sheets. Available at: http://www.epa.gov/pesticides/factsheets/atrazinebackground.htm.
41. USEPA. 2011b. Atrazine ecological monitering program data. Document ID: EPA-HQ-OPP-2003-0367-0205. Available at: http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2003-0367-0205.
42. Whipps CM, Matthews JL, Kent ML. 2008. Distribution and genetic characterization of Mycobacterium chelonae in laboratory zebrafish Danio rerio. 82:45-54.