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Exposure to 17β estradiol causes erosion of sexual dimorphism in Bluegill (Lepomis macrochirus)

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Abstract

Estrogenic compounds including 17β estradiol (or E2) are known to negatively affect the reproductive system of many animals, including fish, leading to feminization, altered sex ratio, reduced fecundity, and decreased gonadosomatic index. The objective of this study was to evaluate the effects of varying concentrations of water-soluble 17β estradiol exposure on the external morphology of Bluegill. An experiment was set up where fish were individually maintained in 10-g tanks and exposed to 17β estradiol concentrations of 40 and 80 ng/L or no 17β estradiol exposure (the control). Fish were exposed for 21 days, with 17β estradiol replenished each week to account for 17β estradiol half-life. Fish were photographed laterally before and after the 21-day exposure to 17β estradiol. Landmark-based geometric morphometrics were conducted in MorphoJ and canonical variate and discriminant function analysis were used to compare the morphological changes in the fish under 17β estradiol exposure. The results showed that 17β estradiol exposure caused male dimorphic characters to change in Bluegill by becoming less prevalent. Specifically, there was a narrowing of the caudal peduncle, smaller nape protrusion, reduced opercular flap and pectoral fin, and a deeper body in the exposed groups compared with control fish under both concentrations. This research highlights the widespread effects of 17β estradiol on fish health beyond the reproductive system, which could have important conservation implications by affecting mate selection and reducing reproductive success.

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References

  • Akhavan SR, Falahatkar B, Gilani MHT, Lokman PM (2015) Effects of estradiol-17β implantation on ovarian growth, sex steroid levels and vitellogenin proxies in previtellogenic sturgeon Huso. Anim Reprod Sci 157:1–10

    Article  CAS  Google Scholar 

  • Bell AM (2001) Effects of an endocrine disrupter on courtship and aggressive behaviour of male three-spined stickleback, Gasterosteus aculeatus. Anim Behav 62(4):775–780

    Article  Google Scholar 

  • Bolotovskiy AA, Levina MA, DeFaveri J, Merilä J, Levin BA (2018) Heterochronic development of lateral plates in the three-spined stickleback induced by thyroid hormone level alterations. PLoS One 13:e0194040–e0194040. https://doi.org/10.1371/journal.pone.0194040

    Article  CAS  Google Scholar 

  • Bookstein FL (1997) Morphometric tools for landmark data: geometry and biology: Cambridge University Press.

  • Cadrin SX (2013) Morphometric landmarks. Stock identification methods. 2nd ed. London, UK: Elsevier, 109-128.

  • 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(1):55–66

    Article  CAS  Google Scholar 

  • Cavalcanti MJ, Monteiro LR, Lopes P (1999) Landmark-based morphometric analysis in selected species of serranid fishes (Perciformes: Teleostei). Zoological Studies-Taipei 38(3):287–294

    Google Scholar 

  • Christiansen T, Korsgaard B, Jespersen A (1998) Effects of nonylphenol and 17 beta-oestradiol on vitellogenin synthesis, testicular structure and cytology in male eelpout Zoarces viviparus. J Exp Biol 201:179 LP–179192

    Google Scholar 

  • Clotfelter ED, Ardia DR, McGraw KJ (2007) Red fish, blue fish: trade-offs between pigmentation and immunity in Betta splendens. Behav Ecol 18:1139–1145. https://doi.org/10.1093/beheco/arm090

    Article  Google Scholar 

  • Cooke SJ, Weatherhead PJ, Wahl DH, Philipp DP (2008) Parental care in response to natural variation in nest predation pressure in six sunfish (Centrarchidae: Teleostei) species. Ecol Freshw Fish 17:628–638. https://doi.org/10.1111/j.1600-0633.2008.00314.x

    Article  Google Scholar 

  • Cooper WJ, Westneat MW (2009) Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches. BMC Evol Biol 9(1):24

    Article  Google Scholar 

  • Dujardin J-P, Kaba D, Solano P, Dupraz M, McCoy K, Jaramillo-O N (2014) Outline-based morphometrics, an overlooked method in arthropod studies? Infect Genet Evol 28:704–714

    Article  Google Scholar 

  • Ehlinger TJ (1997) Male Reproductive Competition and sex-specific growth patterns in Bluegill. North Am J Fish Manag 17:508–515. https://doi.org/10.1577/1548-8675(1997)017<0508:MRCASS>2.3.CO;2

    Article  Google Scholar 

  • Ehlinger TJ, Wilson DS (1988) Complex foraging polymorphism in bluegill sunfish. Proc Natl Acad Sci 85(6):1878–1882

    Article  CAS  Google Scholar 

  • Elliott SM, Kiesling RL, Jorgenson ZG, Rearick DC, Schoenfuss HL, Fredricks KT, Gaikowski MP (2014) Fathead minnow and bluegill sunfish life-stage responses to 17β-estradiol exposure in outdoor mesocosms. JAWRA J Am Water Resour Assoc 50(2):376–387

    Article  CAS  Google Scholar 

  • Fritts AK, Stodola AP, Douglass SA, Vinsel RM (2016) Investigation of freshwater mussel glochidia presence on Asian carp and native fishes of the Illinois river. Freshwater Mollusk Biology and Conservation 19:22–28

    Article  Google Scholar 

  • Garcia MJ, Ferro JM, Mattox T et al (2016) Phenotypic differences between the sexes in the sexually plastic mangrove rivulus fish ( Kryptolebias marmoratus ). 988–997. https://doi.org/10.1242/jeb.124040

  • Gimeno S, Komen H, Jobling S, Sumpter J, Bowmer T (1998) Demasculinisation of sexually mature male common carp, Cyprinus carpio, exposed to 4-tert-pentylphenol during spermatogenesis. Aquat Toxicol 43(2):93–109

    Article  CAS  Google Scholar 

  • Gross MR, Charnov EL (1980) Alternative male life histories in bluegill sunfish. Proc Natl Acad Sci 77:6937 LP–6936940. https://doi.org/10.1073/pnas.77.11.6937

    Article  Google Scholar 

  • Gunatilake SR, Craver S, Kwon J-W, Xia K, Armbrust K, Rodriguez JM, Mlsna TE (2013) Analysis of estrogens in wastewater using solid-phase extraction, QuEChERS cleanup, and liquid chromatography/tandem mass spectrometry. J AOAC Int 96(6):1440–1447

    Article  CAS  Google Scholar 

  • Heffron K, Gaines K, Novak J, Canam T, Collard D (2016) 17β-Estradiol influent and effluent concentrations in wastewater: demographic influences and the risk to environmental health. Environ Monit Assess 188(5):288

    Article  CAS  Google Scholar 

  • Ibañez AL, Cowx IG, O’higgins P (2007) Geometric morphometric analysis of fish scales for identifying genera, species, and local populations within the Mugilidae. Can J Fish Aquat Sci 64(8):1091–1100

    Article  Google Scholar 

  • Ibor OR, Adeogun AO, Fagbohun OA, Arukwe A (2016) Gonado-histopathological changes, intersex and endocrine disruptor responses in relation to contaminant burden in Tilapia species from Ogun River, Nigeria. Chemosphere 164:248–262

    Article  CAS  Google Scholar 

  • Imai S, Koyama J, Fujii K (2005) Effects of 17β-estradiol on the reproduction of Java-medaka (Oryzias javanicus), a new test fish species. Mar Pollut Bull 51(8):708–714

    Article  CAS  Google Scholar 

  • Jennings MJ, Philipp DP (1992) Female choice and male competition in longear sunfish. Behav Ecol 3:84–94. https://doi.org/10.1093/beheco/3.1.84

    Article  Google Scholar 

  • Jürgens MD, Holthaus KI, Johnson AC, Smith JJ, Hetheridge M, Williams RJ (2002) The potential for estradiol and ethinylestradiol degradation in English rivers. Environ Toxicol Chem 21(3):480–488

    Article  Google Scholar 

  • Karki NP, Carlsward BS, Maia A (2018) Histological changes in the liver tissues of bluegill sunfish (Lepomis macrochirus) after exposure to 17-β estradiol. Nepal J Agric Sci 17:46–53

    Google Scholar 

  • Klingenberg C (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  Google Scholar 

  • Länge R, Hutchinson TH, Croudace CP, Siegmund F, Schweinfurth H, Hampe P, Panter GH, Sumpter JP (2001) Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ Toxicol Chem 20(6):1216–1227

    Article  Google Scholar 

  • Langerhans RB, Layman CA, Langerhans AK, Dewitt TJ (2003) Habitat-associated morphological divergence in two Neotropical fish species. Biol J Linn Soc 80(4):689–698

    Article  Google Scholar 

  • Laurent P, Perry SF (1991) Environmental effects on fish gill morphology. Physiol Zool 64(1):4–25

    Article  Google Scholar 

  • Maunder RJ, Matthiessen P, Sumpter JP, Pottinger TG (2007) Impaired reproduction in three-spined sticklebacks exposed to ethinyl estradiol as juveniles. Biol Reprod 77:999–1006. https://doi.org/10.1095/biolreprod.107.062240

    Article  CAS  Google Scholar 

  • Mitteroecker P, Gunz P (2009) Advances in geometric morphometrics. Evol Biol 36(2):235–247

    Article  Google Scholar 

  • Mojekwu T, Anumudu C (2015) Advanced techniques for morphometric analysis in fish. J Aquac Res Dev 6(8)

  • O’Reilly K, Horn M (2004) Phenotypic variation among populations of Atherinops affinis (Atherinopsidae) with insights from a geometric morphometric analysis. J Fish Biol 64(4):1117–1135

    Article  Google Scholar 

  • Olivereau M, Olivereau J (1979) Effect of estradiol-17 β on the cytology of the liver, gonads and pituitary, and on plasma electrolytes in the female freshwater eel. Cell Tissue Res 199(3):431–454

    Article  CAS  Google Scholar 

  • Ortiz-Zarragoitia M, Cajaraville MP (2005) Effects of selected xenoestrogens on liver peroxisomes, vitellogenin levels and spermatogenic cell proliferation in male zebrafish. Comp Biochem Phys Part C: Toxicol Pharmacol 141(2):133–144

    Article  Google Scholar 

  • Park PJ, Aguirre WE, Spikes DA, Miyazaki JM (2013) Landmark-based geometric morphometrics: what fish shapes can tell us about fish evolution. Proceedings of the Association for Biology Laboratory Education 34:361–371

    CAS  Google Scholar 

  • Parrott JL, Blunt BR (2005) Life-cycle exposure of fathead minnows (Pimephales promelas) to an ethinylestradiol concentration below 1 ng/L reduces egg fertilization success and demasculinizes males. Environ Toxicol 20(2):131–141

    Article  CAS  Google Scholar 

  • Paukert CP, Willis DW, Bouchard MA (2004) Movement, home range, and site fidelity of bluegills in a Great Plains lake. N Am J Fish Manag 24(1):154–161

    Article  Google Scholar 

  • Purdom C, Hardiman P, Bye V, Eno N, Tyler C, Sumpter J (1994) Estrogenic effects of effluents from sewage treatment works. Chem Ecol 8(4):275–285

    Article  CAS  Google Scholar 

  • Ramler D, Palandačić A, Delmastro GB, Wanzenböck J, Ahnelt H (2016) Morphological divergence of lake and stream phoxinus of Northern Italy and the Danube basin based on geometric morphometric analysis. Ecol Evol 7(2):572–584

    Article  Google Scholar 

  • Schnitzler JG, Frederich B, Dussenne M, Klaren PH, Silvestre F, Das K (2016) Triclosan exposure results in alterations of thyroid hormone status and retarded early development and metamorphosis in Cyprinodon variegatus. Aquat Toxicol 181:1–10

    Article  CAS  Google Scholar 

  • Schultz K (2010) Ken Schultz’s field guide to freshwater fish: John Wiley and Sons.

  • Shukla R, Bhat A (2017) Morphological divergences and ecological correlates among wild populations of zebrafish (Danio rerio). Environ Biol Fish 100(3):251–264

    Article  Google Scholar 

  • Sowers AD, Gaworecki KM, Mills MA, Roberts AP, Klaine SJ (2009) Developmental effects of a municipal wastewater effluent on two generations of the fathead minnow, Pimephales promelas. Aquat Toxicol 95(3):173–181

    Article  CAS  Google Scholar 

  • Stundl J, Pospisilova A, Jandzik D, Fabian P, Dobiasova B, Minarik M, Metscher BD, Soukup V, Cerny R (2019) Bichir external gills arise via heterochronic shift that accelerates hyoid arch development. Elife 8:e43531. https://doi.org/10.7554/eLife.43531

    Article  Google Scholar 

  • Wang H-P, Gao Z, Beres B, Ottobre J, Wallat G, Tiu L, Rapp D, O’Bryant P, Yao H (2008) Effects of estradiol-17β on survival, growth performance, sex reversal and gonadal structure of bluegill sunfish Lepomis macrochirus. Aquaculture 285(1):216–223

    Article  CAS  Google Scholar 

  • Warner RR (1988) Sex change and the size-advantage model. Trends Evol Ecol 3:133–136

    Article  CAS  Google Scholar 

  • Willis S, Winemiller K, Lopez-Fernandez H (2005) Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia 142(2):284–295

    Article  CAS  Google Scholar 

  • Wright-Walters M, and Volz C (2009) Municipal wastewater concentrations of pharmaceutical and xeno-estrogens: wildlife and human health implications. Paper presented at the Proceedings of the 2007 national conference on environmental science and technology.

  • Zaroogian G, Gardner G, Horowitz DB, Gutjahr-Gobell R, Haebler R, Mills L (2001) Effect of 17β-estradiol, o, p′-DDT, octylphenol and p, p′-DDE on gonadal development and liver and kidney pathology in juvenile male summer flounder (Paralichthys dentatus). Aquat Toxicol 54(1):101–112

    Article  CAS  Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets DH (2012) Geometric morphometrics fo biologists: a primer, 2nd edn. Academic Press, Waltham, MA

    Google Scholar 

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Acknowledgments

We would like to thank Tom Canam and Jim Novak for help with the early conceptual framework for this project. Tom Canam also provided feedback on an earlier version of this manuscript. The fish collection would not have been possible without the help of Cassi Moody-Carpenter, Bethany Hoster, and Camden Nix. Bethany and Camden along with other members of the Colombo, Maia, and Gaines labs helped with fish care and maintenance.

Funding

Funding for this project was provided by the Illinois Water Resources Center (Subaward 2011-03502-07) to A. Maia. Additional funding was available through the Department of Biological Sciences, the College of Sciences, and the Graduate School at Eastern Illinois University.

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Correspondence to Anabela Maia.

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A protocol to conduct this study was approved by Institutional Animal Care and Use Committee (Eastern Illinois University IACUC Protocol approval number 15-004).

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Karki, N.P., Colombo, R.E., Gaines, K.F. et al. Exposure to 17β estradiol causes erosion of sexual dimorphism in Bluegill (Lepomis macrochirus). Environ Sci Pollut Res 28, 6450–6458 (2021). https://doi.org/10.1007/s11356-020-10935-5

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