148
Views
3
CrossRef citations to date
0
Altmetric
Eco/Toxicology

Gonadal histology and reproductive steroidogenesis in Lithobates pipiens exposed to atrazine

, &
Pages 583-600 | Received 30 Apr 2018, Accepted 01 Nov 2018, Published online: 09 Jan 2019

References

  • Allran, J. W., and W. H. Karasov. 2000. “Effects of Atrazine and Nitrate on Northern Leopard Frog (Rana pipiens) Larvae Exposed in the Laboratory from Posthatch through Metamorphosis.” Environmental Toxicology and Chemistry 19 (11): 2850.doi:10.1897/1551-5028(2000)019<2850:EOAANO >2.0.CO;2.
  • Bateman, K. S., G. D. Stentiford, and S. W. Feist. 2004. “A Ranking System for the Evaluation of Intersex Condition in European Flounder (Platichthys flesus).” Environmental Toxicology and Chemistry 23 (12): 2831–6. 10.1897/03-541.1.
  • Brodeur, J. C., A. Sassone, G. N. Hermida, and N. Codugnello. 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: 10–7. 10.1016/j.ecoenv.2013.01.019.
  • Brodeur, J. C., G. Svartz, C. S. Perez-Coll, D. J. Marino, and J. Herkovits. 2009. “Comparative Susceptibility to Atrazine of Three Developmental Stages of Rhinella arenarum and Influence on Metamorphosis: Non-Monotonous Acceleration of the Time to Climax and Delayed Tail Resorption.” Aquatic Toxicology 91 (2): 161–70. 10.1016/j.aquatox.2008.07.003.
  • Calvin, J. L., C. H. Slater, T. G. Bolduc, A. P. Laudano, and S. A. Sower. 1993. “Multiple Molecular Forms of Gonadotropin-Releasing Hormone in the Brain of an Elasmobranch: Evidence for Ir-Lamprey Gnrh.” Peptides 14 (4): 725–9. 10.1016/0196-9781(93)90104-O.
  • Carr, J. A., A. Gentles, E. E. Smith, W. L. Goleman, L. J. Urquidi, K. Thuett, R. J. Kendall, et al., and G. Van Der Kraak. 2003. “Response of Larval Xenopus laevis to Atrazine: Assessment of Growth, Metamorphosis, and Gonadal and Laryngeal Morphology.” Environmental Toxicology and Chemistry 22 (2): 396–405. 10.1897/1551-5028(2003)022<0396:ROLXLT >2.0.CO;2.
  • Chang, L. T., N. W. Yu, C. Y. Hsu, and H. W. Liu. 1996. “Gonadal Transformation in Male Rana catesbeiana Tadpoles Intraperitoneally Implanted with Estradiol Capsules.” General and Comparative Endocrinology 102 (3): 299–306. 10.1006/gcen.1996.0073.
  • Chardard, D., S. Kuntz, A. Chesnel, and S. Flament. 2003. “Effects of Androgens on Sex Differentiation of the Urodele pleurodeles waltl.” Journal of Experimental Zoology and Zoology 296 (1): 46–55. 10.1002/jez.a.10240.
  • Christensen, K. 1929. “Hermaphroditism in Rana pipiens.” The Anatomical Record 43 (4): 345–58. 10.1002/ar.1090430404.
  • Christensen, K. 1930. “Sex Differentiation and Development of Oviducts in Rana pipiens.” American Journal of Anatomy 45 (1): 159–87. 10.1002/aja.1000450107.
  • Coady, K., M. Murphy, D. Villeneuve, M. Hecker, P. Jones, J. Carr, K. Solomon, et al., and J. Giesy. 2004. “Effects of Atrazine on Metamorphosis, Growth, and Gonadal Development in the Green Frog (Rana clamitans).” Journal of Toxicology and Environmental Health, Part A 67 (12): 941–57. 10.1080/15287390490443722.
  • Coady, K. K., M. B. Murphy, D. L. Villeneuve, M. Hecker, P. D. Jones, J. A. Carr, K. R. Solomon, et al., and J. P. Giesy. 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 (2): 160–73. 10.1016/j.ecoenv.2004.10.010.
  • Conlon, J. M., F. Collin, Y.-C. Chiang, S. A. Sower, and H. Vaudry. 1993. “Two Molecular Forms of Gonadotropin-Releasing Hormone from the Brain of the Frog, Rana ridibunda: Purification, Characterization, and Distribution.” Endocrinology 132 (5): 2117–23. 10.1210/endo.132.5.8477660.
  • Cooper, R. L., J. M. Goldman, and T. E. Stoker. 1999. “Neuroendocrine and Reproductive Effects of Contemporary-Use Pesticides.” Toxicology and Industrial Health 15 (1): 26–36. 10.1177/074823379901500104.
  • Cooper, R. L., T. E. Stoker, L. Tyrey, J. M. Goldman, and W. K. McElroy. 2000. “Atrazine Disrupts the Hypothalamic Control of Pituitary-Ovarian Function.” Toxicological Sciences 53 (2): 297–307. 10.1093/toxsci/53.2.297.
  • Du Preez, L. H., N. Kunene, G. J. Everson, J. A. Carr, J. P. Giesy, T. S. Gross, A. J. Hosmer, et al., and G. J. Van Der Kraak. 2008. “Reproduction, Larval Growth, and Reproductive Development in African Clawed Frogs (Xenopus laevis) Exposed to Atrazine.” Chemosphere 71 (3): 546–52. 10.1016/j.chemosphere.2007.09.051.
  • Du Preez, L. H., N. Kunene, R. Hanner, J. P. Giesy, K. R. Solomon, A. Hosmer, and G. J. Van Der Kraak. 2009. “Population-Specific Incidence of Testicular Ovarian Follicles in Xenopus laevis from South Africa: A Potential Issue in Endocrine Testing.” Aquatic Toxicology 95 (1): 10. 10.1016/j.aquatox.2009.07.018.
  • EAI 2015. “Organics in Drinking Water.” Accessed 31 July. http://www.eai-labs.com/assets/docs/organics_in_water.pdf.
  • Fahien, C. M., and S. A. Sower. 1990. “Relationship between Brain Gonadotropin-Releasing Hormone and Final Reproductive Period of the Adult Male Sea Lamprey, Petromyson marinus.” General and Comparative Endocrinology 80 (3): 427–37. 10.1016/0016-6480(90)90192-O.
  • Falconi, R., D. Dalpiaz, and F. Zaccanti. 2004. “Ultrastructural Aspects of Gonadal Morphogenesis in Bufo Bufo (Amphibia anura) 1. Sex Differentiation.” Journal of Experimental Zoology Part Zoology 301 (5): 378–88. 10.1002/jez.a.20069.
  • Gore, A. C. 2001. “Environmental Toxicant Effects on Neuroendocrine Function.” Endocrine 14 (2): 235–46. 10.1385/ENDO:14:2:235.
  • Gosner, K. 1960. “A Simplified Table for Staging Anuran Embryos and Larvae with Notes on Identification.” Herpetologica 16: 183–90.
  • Guillette, L. J., Jr., D. A. Crain, M. P. Gunderson, S. A. E. Kools, M. R. Milnes, E. F. Orlando, A. A. Rooney, and A. R. Woodward. 2000. “Alligators and Endocrine Disrupting Contaminants: A Current Perspective.” American Zoologist 40 (3): 438–52.
  • Guillette, L. J., Jr., T. S. Gross, D. A. Gross, A. A. Rooney, and H. F. Percival. 1995. “Gonadal Steroidogenesis In Vitro from Juvenile Alligators Obtained from Contaminated or Control Lakes.” Environmental Health Perspectives Supplements 103 (S4): 31–6. 10.1289/ehp.95103s431.
  • Hayes, T., K. Haston, M. Tsui, A. Hoang, C. Haeffele, and A. Vonk. 2002. “Herbicides: Feminization of Male Frogs in the Wild.” Nature 419 (6910): 895–6.
  • Hayes, T., K. Haston, M. Tsui, A. Hoang, C. Haeffele, and A. Vonk. 2003. “Atrazine-Induced Hermaphroditism at 0.1 Ppb in American Leopard Frogs (Rana pipiens): Laboratory and Field Evidence.” Environmental Health Perspectives 111 (4): 568–75.
  • Hayes, T. B. 2004. “There is No Denying This: Defusing the Confusion about Atrazine.” Bioscience 54 (12): 1138–49. 10.1641/0006-3568(2004)054[1138:TINDTD.2.0.CO;2]
  • Hayes, T. B., A. Collins, M. Lee, M. Mendoza, N. Noriega, A. A. Stuart, and A. Vonk. 2002. “Hermaphroditic, Demasculinized Frogs after Exposure to the Herbicide Atrazine at Low Ecologically Relevant Doses.” Proceedings of the National Academy of Sciences 99 (8): 5476–80. 10.1073/pnas.082121499.
  • Hecker, M., J. P. Giesy, P. D. Jones, A. M. Jooste, J. A. Carr, K. R. Solomon, E. E. Smith, G. Van der Kraak, R. J. Kendall, and L. Du Preez. 2004. “Plasma Sex Steroid Concentrations and Gonadal Aromatase Activities in African Clawed Frogs (Xenopus laevis) from South Africa.” Environmental Toxicology and Chemistry 23 (8): 1996–2007. 10.1897/03-450.
  • Hecker, M., W. J. Kim, J.-W. Park, M. B. Murphy, D. Villeneuve, K. K. Coady, P. D. Jones, et al., and J. P. Giesy. 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 (4): 383–96. 10.1016/j.aquatox.2005.01.008.
  • Hogan, N. S., P. Duarte, M. G. Wade, D. R. Lean, and V. L. Trudeau. 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 (3): 515–23. 10.1016/j.ygcen.2008.03.011.
  • Hogan, N. S., D. R. Lean, and V. L. Trudeau. 2006. “Exposures to Estradiol, Ethinylestradiol and Octylphenol Affect Survival and Growth of Rana pipiens and Rana Sylvatica Tadpoles.” Journal of Toxicology and Environmental Health Part A 69 (16): 1555–69. 10.1080/15287390500470759.
  • Humphrey, R. R., R. Briggs, and G. Fankhauser. 1950. “Sex Differentiation in Triploid Rana pipiens Larvae and the Subsequent Reversal of Females to Males.” Journal of Experimental Zoology 115 (3): 399–427. 10.1002/jez.1401150302.
  • Jooste, A. M., L. H. Du Preez, J. A. Carr, J. P. Giesy, T. S. Gross, R. J. Kendall, E. E. Smith, G. L. Van der Kraak, and K. R. Solomon. 2005. “Gonadal Development of Larval Male Xenopus laevis Exposed to Atrazine in Outdoor Microcosms.” Environmental Science & Technology 39 (14): 5255–61. 10.1021/es048134q.
  • Kloas, W., I. Lutz, T. Springer, H. Krueger, J. Wolf, L. Holden, and A. Hosmer. 2009. “Does Atrazine Influence Larval Development and Sexual Differentiation in Xenopus laevis?” Toxicological Sciences 107 (2): 376–84. 10.1093/toxsci/kfn232.
  • Kohr, R. L., and P. A. Games. 1974. “Robustness of the Analysis of Variance, the Welch Procedure and a Box Procedure to Heterogeneous Variances.” Journal of Experimental Education 43 (1): 61–9. 10.1080/00220973.1974.10806305.
  • LaFiandra, E. M., K. J. Babbitt, and S. A. Sower. 2008. “Effects of Atrazine on Anuran Development are Altered by the Presence of a Nonlethal Predator.” Journal of Toxicology and Environmental Health Part A 71 (8): 505–11. 10.1080/15287390801907442.
  • Langlois, V. S., A. C. Carew, B. D. Pauli, M. G. Wade, G. M. Cooke, and V. L. Trudeau. 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 (4): 552–7. 10.1289/ehp.0901418.
  • Licht, P., B. R. McCreery, R. Barnes, and R. Pang. 1983. “Seasonal and Stress Related Changes in Plasma Gonadotropins, Sex Steroids, and Corticosterone in the Bullfrog, Rana catesbeiana.” General and Comparative Endocrinology 50 (1): 124–45. 10.1016/0016-6480(83)90249-6.
  • Mackenzie, C. A., M. Berrill, C. Metcalfe, and B. D. Pauli. 2003. “Gonadal Differentiation in Frogs Exposed to Estrogenic and Antiestrogenic Compounds.” Environmental Toxicology and Chemistry 22 (10): 2466–75. 10.1897/02-173.
  • Manochantr, S., P. Sretarugsa, C. Wanichanon, J. Chavadej, and P. Sobhon. 2003. “Classification of Spermatogenic Cells in Rana tigerina Based on Ultrastructure.” ScienceAsia 29: 241–54.
  • McDaniel, T. V., P. A. Martin, J. Struger, J. Sherry, C. H. Marvin, M. E. McMaster, S. Clarence, and G. Tetreault. 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 (4): 230–42. 10.1016/j.aquatox.2008.05.002.
  • Murphy, M., M. Hecker, K. Coady, A. Tompsett, E. Higley, P. Jones, L. Dupreez, K. Solomon, J. Carr, and E. Smith. 2006. “Plasma Steroid Hormone Concentrations, Aromatase Activities and Gsi in Ranid Frogs Collected from Agricultural and Non-Agricultural Sites in Michigan (USA).” Aquatic Toxicology 77 (2): 153–66. 10.1016/j.aquatox.2005.11.007.
  • Murphy, M. B., M. Hecker, K. K. Coady, A. R. Tompsett, P. D. Jones, L. H. Du Preez, G. J. Everson, et al., 2006. “Atrazine Concentrations, Gonadal Gross Morphology and Histology in Ranid Frogs Collected in Michigan Agricultural Areas.” Aquatic Toxicology 76 (3–4): 230–45. 10.1016/j.aquatox.2005.09.010.
  • Nolan, M., S. Jobling, G. Brighty, J. P. Sumpter, and C. R. Tyler. 2001. “A Histological Description of Intersexuality in the Roach.” Journal of Fish Biology 58 (1): 160–76. 10.1111/j.1095-8649.2001.tb00505.x.
  • Oka, T., O. Tooi, N. Mitsui, M. Miyahara, Y. Ohnishi, M. Takase, A. Kashiwagi, T. Shinkai, N. Santo, and T. Iguchi. 2008. “Effect of Atrazine on Metamorphosis and Sexual Differentiation in Xenopus laevis.” Aquatic Toxicology 87 (4): 215–26. 10.1016/j.aquatox.2008.02.009.
  • Oliveira, C. D., C. Zanetoni, and R. Zieri. 2002. “Morphological Observations on the Testes of Physalaemus cuvieri (Amphibia, Anura).” Revista Chilena de Anatomía 20 (3): 263–8.
  • Orton, F., J. A. Carr, and R. D. Handy. 2006. “Effects of Nitrate and Atrazine on Larval Development and Sexual Differentiation in the Northern Leopard Frog Rana pipiens.” Environmental Toxicology and Chemistry 25 (1): 65–71. 10.1897/05-136R.1.
  • Phuge, S. K., and N. P. Gramapurohit. 2015. “Sex Hormones Alter Sex Ratios in the Indian Skipper Frog, Euphlyctis Cyanophlyctis: Determining Sensitive Stages for Gonadal Sex Reversal.” General and Comparative Endocrinology 220: 70–7. 10.1016/j.ygcen.2014.04.030.
  • Piprek, R. P., A. Pecio, J. Z. Kubiak, and J. M. Szymura. 2012. “Differential Effects of Testosterone and 17beta-Estradiol on Gonadal Development in Five Anuran Species.” Reproduction 144 (2): 257–67. 10.1530/REP-12-0048.
  • Raucci, F., and M. M. Di Fiore. 2010. “The Maturation of Oocyte Follicular Epithelium of Podarcis S. sicula is Promoted by D-Aspartic Acid.” Journal of Histochemistry & Cytochemistry 58 (2): 157–71. 10.1369/jhc.2009.954636.
  • Reeder, A. L., G. L. Foley, D. K. Nichols, L. G. Hansen, B. Wikoff, S. Faeh, J. Eisold, et al., and V. R. Beasley. 1998. “Forms and Prevalence of Intersexuality and Effects of Environmental Contaminants on Sexuality in Cricket Frogs (Acris crepitans).” Environmental Health Perspectives 106 (5): 261–6. 10.1289/ehp.98106261.
  • Rohr, J. R., T. R. Raffel, N. T. Halstead, T. A. McMahon, S. A. Johnson, R. K. Boughton, and L. B. Martin. 2013. “Early-Life Exposure to a Herbicide Has Enduring Effects on Pathogen-Induced Mortality.” Proceedings of the Royal Society Part B: Biological Sciences 280 (1772): 20131502. 10.1098/rspb.2013.1502.
  • Saidapur, S. K., N. P. Gramapurohit, and B. A. Shanbhag, 2001. “Effect of Sex Steroids on Gonadal Differentiation and Sex Reversal in the Frog, Rana curtipes.” General and Comparative Endocrinology 124 (1): 115–23. 10.1006/gcen.2001.7699.
  • Smith, E. E., L. Du Preez, A. Gentles, K. Solomon, B. Tandler, J. Carr, G. Van Der Kraak, R. Kendall, J. Giesy, and T. S. Gross, 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 (1): 69–76. 10.1080/21564574.2005.9635519.
  • Solomon, K. R., D. B. Baker, R. P. Richards, K. R. Dixon, S. J. Klaine, T. W. La Point, R. J. Kendall, et al., 1996. “Ecological Risk Assessment of Atrazine in North American Surface Waters.” Environmental Toxicology and Chemistry 15 (1): 31–76. 10.1002/etc.5620150105.
  • Sower, S. A., W. W. Dickhoff, A. Gorbman, J. E. Rivier, and W. W. Vale, 1983. “Ovulatory and Steroid Responses in the Lamprey following Administration of Salmon Gonadotropin and Agonistic Analogues of Gnrh.” Canadian Journal of Zoology 61 (12): 2653–9. 10.1139/z83-349.
  • Sower, S. A., and C. B. Schreck, 1982. “Steroid and Thyroid Hormones during Sexual Maturation of Coho Salmon (Oncorhynchus kisutch) in Seawater or Fresh Water.” General and Comparative Endocrinology 47 (1): 42–53. 10.1016/0016-6480(82)90082-X.
  • Spolyarich, N., R. Hyne, S. Wilson, C. Palmer, and M. Byrne, 2010. “Growth, Development and Sex Ratios of Spotted Marsh Frog (Limnodynastes tasmaniensis) Larvae Exposed to Atrazine and a Herbicide Mixture.” Chemosphere 78 (7): 807–13. 10.1016/j.chemosphere.2009.11.048.
  • Spolyarich, N., R. V. Hyne, S. P. Wilson, C. G. Palmer, and M. Byrne, 2011. “Morphological Abnormalities in Frogs from a Rice-Growing Region in NSW, Australia, with Investigations into Pesticide Exposure.” Environmental Monitoring and Assessment 173 (1–4): 397–407. 10.1007/s10661-010-1395-6.
  • Sretarugsa, P., W. Weerachatyanukul, J. Chavadej, M. Kruatrachue, and P. Sobhon, 2001. “Classification of Developing Oocytes, Ovarian Development and Seasonal Variation in Rana tigerina.” ScienceAsia 27: 1–14.
  • Stoppa, E. G., S. A. Sower, C. N. Svendsen, and J. C. King, 1988. “Polygenic Expression of Gonadotropin-Releasing Hormone (GnRH) in Human?” Peptides 9: 419–23. 10.1016/0196-9781(88)90278-1.
  • Storrs-Mendez, S. I., and R. D. Semlitsch, 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 314 (1): 57–66. 10.1002/jez.b.21310.
  • Storrs-Mendez, S. I., and J. M. Kiesecker, 2004. “Survivorship Patterns of Larval Amphibians Exposed to Low Concentrations of Atrazine.” Environmental Health Perspectives 112 (10): 1054–7. 10.1289/ehp.6821.
  • Tabachnick, B. G., and L. S. Fidell. 1996. Using Multivariate Statistics. 3rd ed. New York: Harper Collins Publishers, Inc.
  • Tavera-Mendoza, L., S. Ruby, P. Brousseau, M. Fournier, D. Cyr, and D. Marcogliese, 2002a. “Response of the Amphibian Tadpole Xenopus laevis to Atrazine during Sexual Differentiation of the Ovary.” Environmental Toxicology and Chemistry 21 (6): 1264–7. 10.1897/1551-5028(2002)021<1264:ROTATX >2.0.CO;2.
  • Tavera-Mendoza, L., S. Ruby, P. Brousseau, M. Fournier, D. Cyr, and D. Marcogliese, 2002b. “Response of the Amphibian Tadpole Xenopus laevis to Atrazine during Sexual Differentiation of the Testis.” Environmental Toxicology and Chemistry 21 (3): 527–31. 10.1897/1551-5028(2002)021<0527:ROTATX >2.0.CO;2.
  • Tsai, P.-S., A. E. Kessler, J. T. Jones, and K. B. Wahr, 2005. “Alteration of the Hypothalamic-Pituitary-Gonadal Axis in Estrogen- and Androgen-Treated Adult Male Leopard Frog, Rana pipiens.” Reproductive Biology and Endocrinology 3 (1): 2.
  • Tsai, P.-S., Lunden, J. B., and J. T. Jones, 2003. “Effects of Steroid Hormones on Spermatogenesis and GnRH Release in Male Leopard Frogs, Rana pipiens.” General and Comparative Endocrinology 134 (3): 330–8. 10.1016/j.ygcen.2003.07.001.
  • Van Der Kraak, G. J., A. J. Hosmer, M. L. Hanson, W. Kloas, and K. R. Solomon, 2014. “Effects of Atrazine in Fish, Amphibians, and Reptiles: An Analysis Based on Quantitative Weight of Evidence.” Critical Reviews in Toxicology 44 (sup5): 1–66. 10.3109/10408444.2014.967836.
  • Villeneuve, D. L., M. Breen, D. C. Bencic, J. E. Cavallin, K. M. Jensen, E. A. Makynen, L. M. Thomas, L. C. Wehmas, R. B. Conolly, and G. T. Ankley, 2013. “Developing Predictive Approaches to Characterize Adaptive Responses of the Reproductive Endocrine Axis to Aromatase Inhibition: I. Data Generation in a Small Fish Model.” Toxicological Sciences 133 (2): 225–33. 10.1093/toxsci/kft068.
  • Villeneuve, D. L., N. D. Mueller, D. Martinovic, E. A. Makynen, M. D. Kahl, K. M. Jensen, E. J. Durhan, J. E. Cavallin, D. Bencic, and G. T. Ankley, 2009. “Direct Effects, Compensation, and Recovery in Female Fathead Minnows Exposed to a Model Aromatase Inhibitor.” Environmental Health Perspectives 117 (4): 624–31. 10.1289/ehp.11891.
  • Wallace, H., G. M. Badawy, and B. M. Wallace, 1999. “Amphibian Sex Determination and Sex Reversal.” Cellular and Molecular Life Sciences 55 (6-7): 901–9.
  • Wilson, K., and I. C. W. Hardy. 2002. “Statistical Analysis of Sex Ratios: An Introduction.” In Sex Ratios, edited by I. C. W. Hardy, 48–92. Cambridge: Cambridge University Press.
  • Witschi, E. 1929a. “Studies on Sex Differentiation and Sex Determination in Amphibians. I. Development and Sexual Differentiation of the Gonads of Rana sylvatica.” Journal of Experimental Zoology 52 (2): 235–65. 10.1002/jez.1400520202.
  • Witschi, E. 1929b. “Studies on Sex Differentiation and Sex Determination in Amphibians. II. Sex Reversal in Female Tadpoles of Rana sylvatica following the Application of High Temperature.” Journal of Experimental Zoology 52 (2): 267–91. 10.1002/jez.1400520203.
  • Wolf, J. C., D. R. Dietrich, U. Friederich, J. Caunter, and A. R. Brown, 2004. “Qualitative and Quantitative Histomorphological Assessment of Fathead Minnow Pimephales promelas Gonads as an Endpoint for Evaluating Endocrine-Active Compounds: A Pilot Methodology Study.” Toxicologic Pathology 32 (5): 600–12. 10.1080/01926230490515201.
  • Yu, K. L., C. S. Nahorniak, R. E. Peter, A. Corrigan, J. E. Rivier, and W. W. Vale, 1987. “Brain Distribution of Radioimmunoassayable Gonadotropin-Releasing Hormone in Female Goldfish: Seasonal Variation and Periovulatory Changes.” General and Comparative Endocrinology 67 (2): 234–46. 10.1016/0016-6480(87)90153-5.
  • Zar, J. H. 1996. Biostatistical Analysis. 3rd ed. New Jersey: Prentice-Hall, Inc.
  • Zaya, R. M., Z. Amini, A. S. Whitaker, S. L. Kohler, and C. F. Ide, 2011. “Atrazine Exposure Affects Growth, Body Condition and Liver Health in Xenopus laevis Tadpoles.” Aquatic Toxicology 104 (3-4): 243–53. 10.1016/j.aquatox.2011.04.021.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.