Impact of Long-Term Exposure to 17α-Ethinylestradiol in the Live-Bearing Fish Heterandria formosa

Abstract

17α-ethinylestradiol (EE2) is a potent synthetic estrogen that is routinely detected in aquatic ecosystems and exhibits estrogenic activity. Acute and chronic toxicity have been described for oviparous and ovoviviparous fish species; however, no information is available on the impacts of EE2 on viviparous, matrotrophic fish despite their ecological importance. The present study investigated the consequences of long-term EE2 exposure in the least killifish (Heterandria formosa). Effects on growth, time-to-sexual maturity, fecundity, and offspring survival were examined in an 8-month, life-cycle experiment. Starting as 0–6-day-old fish, least killifish were continuously exposed to EE2 at nominal concentrations of 0, 5, or 25 ng/L (measured concentrations averaged 0, 4.3, and 21.5 ng/L respectively). In the F0 generation, EE2-exposure did not affect survival but resulted in increased time-to-sexual maturity and a sex-dependent effect on size; female standard length was reduced while male standard length was increased. This caused the ordinarily larger females and smaller males to become more similar in size. Condition factor was reduced for both sexes. Fecundity was reduced by 50% and 75% at 5 and 25 ng/L EE2-exposure respectively. Continued EE2-exposure in the F1 generation resulted in significantly reduced survival. These results suggest that despite their matrotrophic development, these fish experience delayed development and reduced reproductive success from EE2-exposure and that effects appear to intensify in the second generation.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Data Availability

Data pertaining to this manuscript are available, upon request, from the lead author (LMJ).

References

  1. Abramoff M, Magalhaes P, Ram S (2004) Image processing with image. J Biophotonics 11:36–42

    Google Scholar 

  2. Al-Ansari A, Saleem A, Kimpe L, Sherry J, McMaster M, Trudeau V, Blais J (2010) Bioaccumulation of the pharmaceutical 17α-ethinylestradiol in shorthead redhorse suckers (Moxostoma macrolepidotum) from the St. Clair River, Canada. Environ Pollut 158:2566–2571

    CAS  Google Scholar 

  3. Balch G, Mackenzie C, Metcalfe C (2004) Alterations to gonadal development and reproductive success in Japanese medaka (Oryzias latipes) exposed to 17α-ethinylestradiol. Environ Toxicol Chem 23:782–791

    CAS  Google Scholar 

  4. Barel-Cohen K, Shore L, Shemesh M, Wenzel A, Mueller J, Kronfeld-Schor N (2006) Monitoring of natural and synthetic hormones in a polluted river. J Environ Manag 78:16–23

    CAS  Google Scholar 

  5. Belfroid A, Van der Horst A, Vethaak A, Schafer A, Rijs G, Wegener J, Cofino W (1999) Analysis and occurrence of estrogenic hormones and their glucuronides in surface water and waste water in The Netherlands. Sci Total Environ 225:101–108

    CAS  Google Scholar 

  6. Belk M, Lydeard C (1994) Effect of Gambusia holbrooki on a similar-sized, syntopic Poeciliid, Heterandria formosa: competitor or predator? Copeia 1994:296–302

    Google Scholar 

  7. Bergman Å, Heindel J, Jobling S, Kidd K, Zoeller R (2012) State-of-the-science of endocrine disrupting chemicals, 2012: an assessment of the state of the science of endocrine disruptors prepared by a group of experts for the United Nations Environment Programme and World Health Organization. Toxicol Lett 211:S3

    Google Scholar 

  8. Bhandari R, Saal F, Tillitt D (2015) Transgenerational effects from early developmental exposures to bisphenol A or 17α-ethinylestradiol in medaka, Oryzias latipes. Sci Rep. https://doi.org/10.1038/srep09303

    Article  Google Scholar 

  9. Bizarro C, Ros O, Vallejo A, Prieto A, Etxebarria N, Cajaraville M, Ortiz-Zarragoitia M (2014) Intersex condition and molecular markers of endocrine disruption in relation with burdens of emerging pollutants in thicklip grey mullets (Chelon labrosus) from Basque estuaries (South-East Bay of Biscay). Mar Environ Res 96:19–28

    CAS  Google Scholar 

  10. Blackwell B, Brown M, Willis D (2000) Relative weight (Wr) status and current use in Fisheries assessment and management. Rev Fish Sci 8:1–44

    Google Scholar 

  11. Buchberger W (2007) Novel analytical procedures for screening of drug residues in water, waste water, sediment and sludge. Anal Chim Acta 593:129–139

    CAS  Google Scholar 

  12. Cargouet M, Perdiz D, Mouatassim-Souali A, Tamisier-Karolak S, Levi Y (2004) Assessment of river contamination by estrogenic compounds in Paris area (France). Sci Total Environ 324:55–66

    CAS  Google Scholar 

  13. Chen C, When T, Wang G, Cheng H, Lin Y, Lien G (2010) High estrogen concentrations in receiving river discharg from a concentrated livestock feedlot. Sci Total Environ 408:3223–3230

    CAS  Google Scholar 

  14. Cheong R, Henrich S, Farr J, Travis J (1984) Variation in fecundity and its relationship to body size in a population of the least killifish, Heterandria formosa (Pisces: Poeciliidae). Copeia 3:720–726

    Google Scholar 

  15. Christiansen L, Winther-Nelsen M, Helweg C (2002) Feminization of fish: the effect of estrogenic compounds and their fate in sewage treatment plants and nature (Environmental Project No. 720-2002). Danish Environmental Protection Agency, København, Denmark

  16. Clouzot L, Marrot B, Doumenq P, Roce N (2008) 17 alpha-ethinylestradiol: an endocrine disrupter of great concern. Analytical methods and removal processes applied to water purification. A review. Environ Progr Sustain Energy 27:383–396

    CAS  Google Scholar 

  17. Constanz G (1989) Reproductive biology of the poeciliid fishes. In: Meffe GK, Snelson FF Jr (eds) Englewood Cliffs. Prentice Hall, NJ

    Google Scholar 

  18. Desbrow C, Routledge E, Brighty G, Sumpter J, Waldock M (1998) Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environ Sci Technol 32:1549–1557

    CAS  Google Scholar 

  19. Diaz-Cruz S, Barcelo’ D (2004) Occurrence and analysis of selected pharmaceuticals and metabolites as contaminants present in wastewaters, sludge and sediments. Handb Environ Chem 5:227–260

    CAS  Google Scholar 

  20. Duong C et al (2010) Estrogenic chemicals and estrogenicity in river waters of South Korea and seven Asian countries. Chemosphere 78:286–293

    CAS  Google Scholar 

  21. Dziewecyznski T, Hebert O (2013) The effects of short-term exposure to an endocrine disrupter on behavioural consistency in male juvenile and adult Siamese fishting fish. Arch Environ Contam Toxicol 64:316–326

    Google Scholar 

  22. Faulk C, Fuiman L, Thomas P (1999) Parental exposure to ortho, paradichlorodiphenyltrichloroethane impairs survival skills of Atlantic croaker (Micropogonias undulatus) larvae. Environ Toxicol Chem 18:254–262

    CAS  Google Scholar 

  23. Fonseca A, Cardoso M, Esteves V (2013) Determination of estrogens in raw and treated wastewater by high-performance liquid chromatograpy: ultraviolet detection. J Environ Anal Toxicol 4:203

    Google Scholar 

  24. Foran C, Peterson B, Benson W (2002) Transgenerational and developmental exposure of Japanese medaka (Oryzias latipes) to ethinylestradiol results in endocrine and reproductive differences in the response to ethinylestradiol as adults. J Toxicol Sci 68:389–402

    CAS  Google Scholar 

  25. Fraser E, Renton R (1940) Observation on the breeding and development of the viviparous fish Heterandria formosa. Q J Microsc Sci 81:479–520

    Google Scholar 

  26. Gadd J, Tremblay L, Northcott G (2010) Steroid estrogens, conjugated estrogens and estrogenic activity in farm dairy shed effluents. Environ Pollut 158:730–736

    CAS  Google Scholar 

  27. Gennotte V et al (2015) Brief exposure of embryos to steroids or aromatase inhibitor induces sex reversal in Nile tilapia (Oreochromis niloticus). J Exp Zool 323A:31–38

    Google Scholar 

  28. Gibson R, Smith M, Spary C, Tyler C, Hill A (2005) Mixtures of estrogenic contaminates in the bile of fish exposed to wastewater treatment works effluents. Environ Sci Technol 39:2461–2471

    CAS  Google Scholar 

  29. Hardman J, Limbird L, Molinoff P, Ruddon R, Goodman A (1996) Goodman and Gilman’s: the pharmacological basis of therapeutics. Toxicol Lett 86:1–55

    Google Scholar 

  30. Hemming J, Turner P, Brooks B, Waller W, LaPoint T (2002) Assessment of toxicity reduction in wastewater effluent flowing through a treatment wetland using Pimephales promelas, Ceriodaphnia dubia, and Vibrio fischeri. Arch Environ Contam Toxicol 42:9–16

    CAS  Google Scholar 

  31. Jackson L, Felgenhauer B, Klerks P (2018) Feminization, altered gonadal development, and liver damage in least killifish (Heterandria formosa) exposed to sublethal concentrations of 17α-ethinylestradiol. Ecotox Environ Safe 170:331–337

    Google Scholar 

  32. Johnson A (2010) Natural variations in flow are critical in determining concentrations fo point source contaminants in rivers; as estrogen example. Environ Sci Technol 44:7865–7870

    CAS  Google Scholar 

  33. Johnson A, Sumpter P (2014) Putting pharmaceuticals into the wider context of challenges to fish populations in rivers. Phil Trans R Soc B. https://doi.org/10.1098/rstb.2013.0581

    Article  Google Scholar 

  34. Jurgens M, Holthaus K, Johnson A, Smith J (2002) The potential for estradiol and ethynylestradiol degradation in English rivers. EnvironToxicol Chem 21:480–488

    CAS  Google Scholar 

  35. Kah O, Dufour S (2011) Conserved and divergent features of reproductive neuroendocrinology in teleost fishes. In: Norris D, Lopez K (eds) Hormones and reproduction of vertebrates. Academic Press, London, pp 15–42

    Google Scholar 

  36. Kidd K, Blanchfield P, Mills K, Palace V, Evans R, Lazorchak J, Flick R (2007) Collapse of a fish population after exposure to a synthetic estrogen. PNAS 104:8897–8901

    CAS  Google Scholar 

  37. Kitamura S, Ogata H, Takashima F (1994) Activities of F-type prostaglandins as releaser sex pheromones in cobitide loach. Misgurnus anguillicaudatus Comp Biochem Physiol A 107:161–169

    Google Scholar 

  38. Kolpin D, Furlong E, Meyer M, Thurman E, Zaugg S, Barber L, Buxton H (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: a national reconnaissance. Environ Sci Technol 36:1202–1211

    CAS  Google Scholar 

  39. Kostich M, Flick R, Martinson J (2013) Comparing predicted estrogen concentrations with measurements in U.S. waters. Environ Pollut 178:271–277

    CAS  Google Scholar 

  40. Kristensen T, Baatrup E, Bayley M (2005) 17α-ethinylestradiol reduces the competitive reproductive fitness of the male guppy (Poecilia reticulate). Biol Reprod 72:150–156

    CAS  Google Scholar 

  41. Kunz P, Kienle C, Carere M, Homazava N, Kase R (2015) In vitro bioassays to screen for endocrine active pharmaceuticals in surface and waste waters. JPBA 106:107–115

    CAS  Google Scholar 

  42. Lange R et al (2001) Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ Toxicol Chem 20:1216–1227

    CAS  Google Scholar 

  43. Lange A, Paull G, Hamilton P, Iguchi T, Tyler C (2011) Implications of persistent exposure to treated wastewater effluent for breeding in wild roach (Rutilus rutilus) populations. Environ Sci Technol 45:1673–1679

    CAS  Google Scholar 

  44. Langer R (2009) Efficacy, safety, and tolerability of low-dose hormone therapy in managing menopausal symptoms. J Am Board Fam Med 22:563–573

    Google Scholar 

  45. Larsson D, Adolfsson-Erici M, Parkkonen J, Petterson M, Berg A, Olsson P, Forlin L (1999) Ethynylestradiol: an undesired fish contraceptive. Aquat Toxicol 454:91–97

    Google Scholar 

  46. Lavelle C, Sorensen P (2011) Behavioral responses of adult male and female fathead minnows to a model estrogenic effluent and its effects on exposure regime and reproductive success. Aquat Toxicol 101:521–528

    CAS  Google Scholar 

  47. Lazorchak J, McCormick F, Henry T, Herlihy A (2003) Contamination of fish in streams of the Mid-Atlantic Region: an approach to regional indicator selection and wildlife assessment. Environ Toxicol Chem 22:545–553

    CAS  Google Scholar 

  48. Lei B, Huang S, Zhou Y, Wang D, Wang Z (2009) Levels of six estrogens in water and sediment from three rivers in Tianjin area, China. Chemosphere 76:36–42

    CAS  Google Scholar 

  49. Liu J, Wang R, Huang B, Lin C, Zhou J, Pan X (2012a) Biological effects and bioaccumulation of steroidal and phenolic endocrine disrupting chemicals in high-back crucian carp exposed to wastewater treatment plant effluents. Environ Pollut 162:325–331

    CAS  Google Scholar 

  50. Liu S, Ying G, Zhou L, Zhang R, Chen Z, Lai H (2012b) Steroids in typical swine farm and their release into the environment. Water Res 45:3754–3768

    Google Scholar 

  51. Martin S, Hitch A, Purcell K, Klerks P, Leberg P (2009) Life history variation along a salinity gradient in coastal marshes. Aquat Biol 8:15–28

    Google Scholar 

  52. Montgomery T, Brown A, Gendelman H, Ota M, Clottfelter E (2012) Exposure to 17α-ethinylestradiol decreases motility and ATP in sperm of male fighting fish Betta splendens. Environ Toxicol 29:243–252

    Google Scholar 

  53. Nash J, Van der Ven L, Brion F, Maack G, Stahlschmidt-Allner P, Tyler C (2004) Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect 112:1725–1733

    CAS  Google Scholar 

  54. Nehemia A, Maganira J, Rumisha C (2012) Length-weight relationship and condition factor of talapia species grown in marine and fresh water ponds. Agric Biol J North Am 3:117–124

    Google Scholar 

  55. Nelson E, Do H, Lewis R, Carr S (2011) Diurnal variability of pharmaceutical, personal care product, estrogen and alkylphenol concentrations in effluent from a tertiary wastewater treatment facility. Environ Sci Technol 45:1228–1234

    CAS  Google Scholar 

  56. Pojana G, Gomiero A, Jonkers N, Marcomini A (2007) Natural and synthetic endocrine disrupting compounds (EDCs) in water, sediment and biota of a coastal lagoon. Environ Int 33:929–936

    CAS  Google Scholar 

  57. Reznick D, Callahan H, Llauredo R (1996) Maternal effects on offspring quality in poeciliid fishes. Am Zool 36:147–156

    Google Scholar 

  58. Rolland R (2000) Ecoepidemiology of the effects of pollution on reproduction and survival of early life stages in teleosts. Fish Fish 1:41–72

    Google Scholar 

  59. Rosen D, Bailey R (1963) The poeciliid fishes (Cyprinodontiformes), their structure, zoo-geography, and systematics. B Am Mus Nat Hist 126:1–176

    Google Scholar 

  60. Rosen D, Gordon M (1953) Functional anatomy and evolution of male genitalia in poeciliid fishes. Zoologica 38:1–47

    Google Scholar 

  61. Saaristo M, Craft J, Lehtonen K, Lindstrom K (2009) Sand goby (Pomatoschistus minutus) males exposed to endocrine disrupting chemical fail in nest and mate competition. Horm Behav 56:315–321

    CAS  Google Scholar 

  62. Salla R et al (2016) Impact of an environmental relevant concentration of 17α-ethinylestradiol on the cardiac function of bullfrog tadpoles. Chemosphere 144:1862–1868

    CAS  Google Scholar 

  63. Sarat M, Rambabu C (2012) A validated simultaneous RP-HPLC method for determination of desogestrel and ethinyl estradiol tablets. Int J Pharm Pharm Sci 4:115–119

    CAS  Google Scholar 

  64. Scholz S, Gutzeit H (2000) 17-a-ethynylestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). Aquat Toxicol 50:363–373

    CAS  Google Scholar 

  65. Schultz I, Skillman A, Nicolas J, Cyr D, Nagler J (2003) Short-term exposure to 17a-ethynylestradiol decreases the fertility of sexually maturing male rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 22:1272–1280

    CAS  Google Scholar 

  66. Schwindt A, Winkelman D, Keteles K, Murphy M, Vajda A (2014) An environmental oestrogen disrupts fish population dynamics through direct and transgenerational effects on survival and fecundity. J Appl Ecol 51:582–591

    CAS  Google Scholar 

  67. Scrimshaw N (1944) Embryonic growth in the viviparous poeciliid, Heterandria formosa. Biol Bull 87:37–51

    Google Scholar 

  68. Segner H, Navas J, Schafers C, Wenzel A (2003) Potencies of estrogenic compounds in in vitro screening assays and in life cycle tests with zebrafish in vivo. Ecotox Environ Safe 54:315–322

    CAS  Google Scholar 

  69. Shifren J, Schiff I (2010) Role of hormone therapy in the management of menopause. Obstet Gynecol 115:839–855

    CAS  Google Scholar 

  70. Silva P et al (2012) Testing the effects of ethinylestradiol and of an environmentally relevant mixture of xenoestrogens as found in the Douro River (Portugal) on the maturatioin of fish gonads: a stereological study using the zebrafish (Danio rerio) as model. Aquat Toxicol 124–125:1–10

    Google Scholar 

  71. Snyder S, Keith T, Verbrugge D, Snyder E, Gross T, Kannan K, Giesy J (1999) Analytical methods for detection of selected estrogenic compounds in aqueous mixtures. Environ Sci Technol 33:2814–2820

    CAS  Google Scholar 

  72. Sole’ M, Raldua D, Piferrer F, Barcelo’ D, Porte C (2003) Feminization of wild carp, Cyprinus carpio, in a polluted environment: plasma steroid hormones, gonadal morphology and xenobiotic metabolizing system. Comp Biochem Phys C 136:145–156

    Google Scholar 

  73. Sorensen P, Goetz F (1993) Pheromonal and reproductive function of F-prostaglandins and their metabolites in teleost fish. J Lipid Mediators 6:385–393

    CAS  Google Scholar 

  74. Stacey N, Peter R (1979) Central action of prostaglandins in spawning behavior of female goldfish. Physiol Behav 22:1191–1196

    CAS  Google Scholar 

  75. Sumpter J (2005) Endocrine disrupters in the aquatic environment: an overview. Acta Hydroch Hydrob 33:9–16

    CAS  Google Scholar 

  76. Sun L, Yong W, Chu X, Lin J (2009) Simultaneous determination fo 15 steroidal oral contraceptives in water using splid-phase disk extraction followed by high performance liquid chromatography-tandem mass spectrometry. J Chromatogr A 1216:5416–5423

    CAS  Google Scholar 

  77. Tamschick S et al (2016) Sex reversal assessments reveal different vulnerability to endocrine disruption between deeply diverged anuran lineages. Sci Reg. https://doi.org/10.1038/srep23825

    Article  Google Scholar 

  78. Ternes T, Stumpf M, Mueller J, Haberer K, Wilken R, Servos M (1999) Behavior and occurrence of estrogens in municipal sewage treatment plants-I. Investigations in Germany, Canada and Brazil. Sci Total Environ 225:81–90

    CAS  Google Scholar 

  79. Teta C, Naik Y (2016) Vitellogenin induction and reduced fecundity in zebrafish exposed to effluents from the city of Bulawayo, Zimbabwe. Chemosphere 167:282–290

    Google Scholar 

  80. Travis J, Farr J, Henrich S, Cheong R (1987) Testing theories of clutch overlap with the reproductive ecology of Heterandria formosa. Ecology 68:611–623

    Google Scholar 

  81. Trexler J, Travis J, Trexler M (1990) Phenotypic plasticity in the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). II. Laboratory experiment. Evolution 44:157–167

    Google Scholar 

  82. Trudeau V, Metcalfe C, Mimeault C, Moon T (2005) Pharmaceuticals in the environment: drugged fish? Biochem Mol Biol Fishes 6:475–493

    CAS  Google Scholar 

  83. Turner C (1937) Reproductive cycles and superfetation in poeciliid fishes. Biol Bull 72:145–164

    Google Scholar 

  84. Van Aerle R, Nolanusan M, Jobling S, Christiansen L, Sumpter J, Tyler C (2001) Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ Toxicol Chem 20:2841–2847

    Google Scholar 

  85. Van den Belt K, Verheyen R, Witters H (2003) Effects of 17a-ethinylestradiol in a partial life-cycle test with zebrafish (Danio rerio): effects on growth, gonads and female reproductive success. Sci Total Environ 309:127–137

    Google Scholar 

  86. Versonnen B, Arijs K, Verslycke T, Lema W, Janssen C (2003) In vitro and in vivo estrogenicity and toxicity of o-, m-, and p-dichlorobenzene. Environ Toxicol Chem 22:329–335

    CAS  Google Scholar 

  87. Vieno N, Harkki H, Tuhkanen T, Kronberg L (2007) Occurrence of pharmaceuticals in river water and their elimination in a pilot-scale drinking water treatment plant. Environ Sci Technol 41:5077–5084

    CAS  Google Scholar 

  88. Wang L et al (2011) Assessing estrogenic activity in surface water and sediment of the Liao River systems in northeast China using combined chemical and biological tools. Environ Pollut 159:148–156

    CAS  Google Scholar 

  89. Williams R (2005) Human pharmaceuticals: assessing the impacts on aquatic ecosystems. Alan Press/ACG Publishing, Lawrence

    Google Scholar 

  90. World Health Organization (WHO) (2012) State of the science of endocrine disrupting chemicals- 2012. World Health Organization, International Programme on Chemical Safety, Geneva

    Google Scholar 

  91. Xu J, Wu L, Chen W, Jiang P, Chang A (2009) Pharmaceuticals and personal care products (PPCPs) and endocrine disrupting compounds (EDCs) in runoff from a potato field irrigated with treated wastewater in Southern California. J Health Sci 55:306–310

    CAS  Google Scholar 

  92. Yan Z, Lu G, Liu J, Jin S (2012) An integrated assessment of estrogenic contamination and feminization risk in fish in Taihu Lake, China. Ecotox Environ Safe 84:334–340

    CAS  Google Scholar 

  93. Yang Y, Gray J, Furlong E, Davis J, ReVello R, Borch T (2012) Steroid hormone runofff from agricultural test plots applied with municipal biosolids. Environ Sci Technol 45:2746–2754

    Google Scholar 

  94. Ying G, Rai K, Ying-Jun R (2002) Occurrence and fate of hormone steroids in the environment. Environ Int 28:545–551

    CAS  Google Scholar 

  95. Ying G, Kookana R, Kumar A, Mortimer M (2009) Occurrence and implications of estrogens and xenoestrogens in sewage effluents and receiving waters from South East Queensland. Sci Total Environ 407:5147–5155

    CAS  Google Scholar 

  96. Zhang Z, Feng Y, Gao P, Wang C, Ren N (2011) Occurrence and removal efficiencies of eight EDCs and estrogenicity in a STP. J Environ Monit 13:1366–1373

    CAS  Google Scholar 

  97. Zou Y, Zhang K, Zhou S (2013) Determination of estrogenic steroids and microbial and photochemical degradation of 17α-ethinylestradiol (EE2) in lake surface water: a case study. Environ Sci Process Impacts 15:1529–1535

    Google Scholar 

Download references

Acknowledgements

The authors greatly appreciate the editorial comments from S. Duke-Sylvester, B. Felgenhauer, P. Leberg, and J. McLachlan, and the logistical support provided by J. Adeyemi, S. Volt, J. Hill, E. Blankson, A. Cazan, A. Oguma, A. Kascak, A. Pant, Q. Jackson, L. Carrier, and the staff of the UL Lafayette Ecology Center.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Latonya M. Jackson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 473 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jackson, L.M., Klerks, P.L. Impact of Long-Term Exposure to 17α-Ethinylestradiol in the Live-Bearing Fish Heterandria formosa. Arch Environ Contam Toxicol 77, 51–61 (2019). https://doi.org/10.1007/s00244-019-00600-5

Download citation