Abstract
This study aimed to investigate the effects of endocrine disruptors 17β-estradiol (E2) and 17α-ethinylestradiol (EE2) on Nile tilapia (Oreochromis niloticus) development, focusing on gonadal histological factors. Concentrations of estrogens E2 and EE2 ranging from 250 to 1000 ng·L−1 can produce intersex individuals, significantly decreasing the condition factor as the concentrations increased. These concentrations could also induce the development of morphological anomalies. Increasing the concentration of estrogens by one order of magnitude (µg·L−1) was lethal for Nile tilapia larvae, with no effect on the incubation time and percentage of larvae hatching. Additionally, morphological anomalies and developmental problems were observed. Estrogens applied at a concentration of 160 µg·L−1 for 28 days caused the birth of a small number of intersex individuals in Nile tilapia, but generated almost entirely female populations in hormonal treatments. Furthermore, the gonads of fish exposed to the estrogens were smaller and less developed, without any significant difference between E2 and EE2. Variation in the exposure time (one to 4 weeks) of Nile tilapia to estrogens (160 µg·L−1) resulted in the appearance of intersex individuals and the development of morphological anomalies, regardless of the exposure time.
Similar content being viewed by others
References
Adeel, M., Song, X., Wang, Y., Francis, D., & Yang, Y. (2017). Environmental impact of estrogens on human, animal and plant life: A critical review. Environment International, 99, 107–119. https://doi.org/10.1016/j.envint.2016.12.010
Adeogun, A. O., Onibonoje, K., Ibor, O. R., Omiwole, R. A., Chukwuka, A. V., Ugwumba, A. O., & Arukwe, A. (2016). Endocrine-disruptor molecular responses, occurrence of intersex and gonado-histopathological changes in tilapia species from a tropical freshwater dam (Awba Dam) in Ibadan, Nigeria. Aquatic Toxicology, 174, 10–21. https://doi.org/10.1016/j.aquatox.2016.02.002
Alcántar-Vázquez, J. P. (2018). Sex proportion in Nile tilapia Oreochromis niloticus fed estrogen mixtures: A case of paradoxical masculinization. Latin American Journal of Aquatic Research, 46(2), 337–345. https://doi.org/10.3856/vol46-issue2-fulltext-9
Américo-Pinheiro, J. H. P., da Cruz, C., Aguiar, M. M., Torres, N. H., Ferreira, L. F. R., & Machado-Neto, J. G. (2020). Histological changes in targeted organs of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentrations of the pesticide carbofuran. Water, Air, and Soil Pollution, 231, 228. https://doi.org/10.1007/s11270-020-04628-5
Boscolo, C. N. P., Pereira, T. S. B., Batalhão, I. G., Dourado, P. L. R., Schlenk, D., & de Almeida, E. A. (2017). Diuron metabolites act as endocrine disruptors and alter aggressive behavior in Nile tilapia (Oreochromis niloticus). Chemosphere, 191, 832–838. https://doi.org/10.1016/j.chemosphere.2017.10.009
Coelho, L. H. G., de Jesus, T. A., Kohatsu, M. Y., Poccia, G. T., Chicarolli, V., Helwig, K., Roberts, C. H. J., Teedon, P., & Pahl, O. (2020). Estrogenic hormones in São Paulo waters (Brazil) and their relationship with environmental variables and Sinapis alba phytotoxicity. Water Air Soil Pollut 231, 150 (2020). https://doi.org/10.1007/s11270-020-04477-2
Czarny, K., Szczukocki, D., Krawczyk, B., Zieliński, M., Miękoś, E., & Gadzała-Kopciuch, R. (2017). The impact of estrogens on aquatic organisms and methods for their determination. Critical Reviews in Environmental Science and Technology, 47(11), 1–55. https://doi.org/10.1080/10643389.2017.1334458
Dammann, A. A., Shappell, N. W., Bartell, S. E., & Schoenfuss, H. L. (2011). Comparing biological effects and potencies of estrone and 17β-estradiol in mature fathead minnows, Pimephales promelas. Aquatic Toxicology, 105, 559–568. https://doi.org/10.1016/j.aquatox.2011.08.011
FAO (Roma), 2020. The State of World Fisheries and Aquacultura 2020: Meeting the sustainable development goals. Access: Aug 30th 2021.
Goswami, L., Vinoth Kumar, R., Borah, S. N., Arul Manikandan, N., Pakshirajan, K., & Pugazhenthi, G. (2018). Membrane bioreactor and integrated membrane bioreactor systems for micropollutant removal from wastewater: A review. Journal of Water Process Engineering, 26, 314–328. https://doi.org/10.1016/j.jwpe.2018.10.024
Hamid, N., Junaid, M., & Pei, D. S. (2021). Combined toxicity of endocrine-disrupting chemicals: A review. Ecotoxicology and Environmental Safety, 215, 112136. https://doi.org/10.1016/j.ecoenv.2021.112136
Harb, M., Lou, E., Smith, A. L., & Stadler, L. B. (2019). Perspectives on the fate of micropollutants in mainstream anaerobic wastewater treatment. Current Opinion in Biotechnology, 57, 94–100. https://doi.org/10.1016/j.copbio.2019.02.022
Hassell, K., Pettigrove, V., Beresford, N., Jobling, S., & Kumar, A. (2016). No evidence of exposure to environmental estrogens in two feral fish species sampled from the Yarra River, Australia: A comparison with Northern Hemisphere studies. Ecotoxicology and Environmental Safety, 131, 104–117. https://doi.org/10.1016/j.ecoenv.2016.05.004
Huang, G. Y., Liu, Y. S., Chen, X. W., Liang, Y. Q., Liu, S. S., Yang, Y. Y., Hu, L. X., Shi, W. J., Tian, F., Zhao, J. L., Chen, J., & Ying, G. G. (2016). Feminization and masculinization of western mosquitofish (Gambusia affinis) observed in rivers impacted by municipal wastewaters. Scientific Reports, 06(01), 1–11. https://doi.org/10.1038/srep20884
Khanzada, N. K., Farid, M. U., Kharraz, J. A., Choi, J., Tang, C. Y., Nghiem, L. D., Jang, A., & An, A. K. (2019). Removal of organic micropollutants using advanced membrane-based water and wastewater treatment: A review. Journal of Membrane Science, 598, 117672. https://doi.org/10.1016/j.memsci.2019.117672
Koger, C. S., The, S. J., & Hinton, D. E. (2000). Determining the sensitive developmental stages of intersex induction in medaka (Oryzias latipes) exposed to 17β-estradiol or testosterone. Marine Environmental Research, 50(1–5), 201–206. https://doi.org/10.1016/S0141-1136(00)00068-4
Lange, R., Hutchinson, T. H., Croudace, C. P., Siegmund, F., Schweinfurth, H., Hampe, P., Panter, G. H., & Sumpter, J. P. (2001). Effects of the synthetic estrogen 17 α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environmental Toxicology Chemistry, 20, 1216–1227. https://doi.org/10.1002/etc.5620200610
Luzio, A., Monteiro, S. M., Rocha, E., Fontaínhas-Fernandes, A. A., & Coimbra, A. M. (2016). Development and recovery of histopathological alterations in the gonads of zebrafish (Danio rerio) after single and combined exposure to endocrine disruptors (17α-ethinylestradiol and fadrozole). Aquatic Toxicology, 175, 90–105. https://doi.org/10.1016/j.aquatox.2016.03.014
Martinez-Bengochea, A., Doretto, L., Rosa, I. F., Oliveira, M. A., Silva, C., Silva, D. M. Z. A., Santos, G. R., Santos, J. F. S., Avelar, M. M., Silva, L. V., Lucianelli-Junior, D., Souza, E. R. B., Silva, R. C., Stewart, A. B., Nakaghi, L. S. O., Valentin, F. N., & $ Nóbrega, R. H. . (2020). Effects of 17β-estradiol on early gonadal development and expression of genes implicated in sexual differentiation of a South American teleost Astyanax Altiparanae. Comparative Biochemistry and Physiology Part b: Biochemistry and Molecular Biology, 248–249, 110467. https://doi.org/10.1016/j.cbpb.2020.110467
Meijide, F. J., Rey Vázquez, G., Piazza, Y. G., Babay, P. A., Itria, R. F., & Lo Nostro, F. L. (2016). Effects of waterborne exposure to 17β-estradiol and 4-tert-octylphenol on early life stages of the South American cichlid fish Cichlasoma dimerus. Ecotoxicology and Environmental Safety, 124, 82–90. https://doi.org/10.1016/j.ecoenv.2015.10.004
Niemuth, N. J., & Klaper, R. D. (2015). Emerging wastewater contaminant metformin causes intersex and reduced fecundity in fish. Chemosphere, 135, 38–45. https://doi.org/10.1016/j.chemosphere.2015.03.060
Niemuth, N. J., Jordan, R., Crago, J., Blanksma, C., Johnson, R., & Klaper, R. D. (2014). Metformin exposure at environmentally relevant concentrations causes potential endocrine disruption in adult male fish. Environmental Toxicology and Chemistry [s.l.], 34(2), 291–296. https://doi.org/10.1002/etc.2793
Ofrydopoulou, A., Nannou, C., Evgenidou, E., Christodoulou, A., & Lambropoulou, D. (2022). Assessment of a wide array of organic micropollutants of emerging concern in wastewater treatment plants in Greece: Occurrence, removals, mass loading and potential risks. Science of the Total Environment, 802, 149860. https://doi.org/10.1016/j.scitotenv.2021.149860
Pawlowski, S., van Aerle, R., Tyler, C., & Braunbeck, T. (2004). Effects of 17α-ethinylestradiol in a fathead minnow (Pimephales promelas) gonadal recrudescence assay. Ecotoxicology and Environmental Safety [s.l.], 57(3), 330–345. https://doi.org/10.1016/j.ecoenv.2003.07.019
Proctor, K., Petrie, B., Lopardo, L., Camacho Munoz, D., Rice, J., Barden, R., Arnot, T., & Kasprzyk-Hordern, B. (2021). Micropollutant fluxes in urban environment – A catchment perspective. Journal of Hazardous Materials, 401, 123745. https://doi.org/10.1016/j.jhazmat.2020.123745
Ribeiro, A. R., Nunes, O. C., Pereira, M. F., & Silva, A. M. (2015). An overview on the advanced oxidation processes applied for the treatment of water pollutants defined in the recently launched Directive 2013/39/EU. Environment International, 75, 33–51. https://doi.org/10.1016/j.envint.2014.10.027
Solaun, O., Rodríguez, J. G., Menchaca, I., Lopez-Garcia, E., Martinez, E., Zonja, B., Postigo, C., de Alda, M. L., Barcelo, D., Borja, A., Manzanos, A., & Larreta, J. (2021). Contaminants of emerging concern in the Basque coast (N Spain): Occurrence and risk assessment for a better monitoring and management decisions. Science of the Total Environment, 765, 142765. https://doi.org/10.1016/j.scitotenv.2020.142765
Song, W., Lu, H., Wu, K., Zhang, Z., Shuk-Wa Lau, E., & Ge, W. (2020). Genetic evidence for estrogenicity of bisphenol A in zebrafish gonadal differentiation and its signalling mechanism. Journal of Hazardous Materials, 386, 121886. https://doi.org/10.1016/j.jhazmat.2019.121886
Tirado, J. O., Valladares, L., Muñoz, D., Caza, J., Manjunatha, B., & Kundapur, R. R. (2017). Levels of 17β-estradiol, vitellogenin, and prostaglandins during the reproductive cycle of Oreochromis niloticus. Latin American Journal of Aquatic Research, 45(5), 930–936. https://doi.org/10.3856/vol45-issue5-fulltext-8
Toft, G., & Baatrup, E. (2003). Altered sexual characteristics in guppies (Poecilia reticulata) exposed to 17β-estradiol and 4-tert-octylphenol during sexual development. Ecotoxicology and Environmental Safety, 56(2), 228–237. https://doi.org/10.1016/S0147-6513(02)00138-0
Tolosa, E. M. C., Behmer, O. A., & Rodrigues, C. J. (2003). Manual de técnicas para histologia normal e patológica. São Paulo: Manole, 2003, 341.
Urushitani, H., Shimizu, A., Katsu, Y., & Iguchi, T. (2002). Early estrogen exposure induces abnormal development of Fundulus heteroclitus. Journal of Experimental Zoology, 293(7), 693–702. https://doi.org/10.1002/jez.10161
Priyan, V. V., Shahnaz, T., Suganya, E., Sivaprakasam, S., & Narayanasamy, S. (2021). Ecotoxicological assessment of micropollutant Diclofenac biosorption on magnetic sawdust: Phyto, Microbial and Fish toxicity studies. Journal of Hazardous Materials, 403, 123532. https://doi.org/10.1016/j.jhazmat.2020.123532
Vidal, C. B., Barbosa, P. G. A., Pessoa, G. P., Buarque, P. C., Nascimento, J. G. S., Farias-Filho, A. L., Paz, M. S., dos Santos, A. B., Cavalcante, R. M., & Nascimento, R. F. (2020). Multiresidue determination of endocrine disrupting compounds in sewage treatment plants (SPE-HPLC-DAD). J. Braz. Chem. Soc., 31(12), 2518–2530. https://doi.org/10.21577/0103-5053.20200127
Woodling, J. D., Lopez, E. M., Maldonado, T. A., Norris, D. O., & Vajda, A. M. (2006). Intersex and other reproductive disruption of fish in wastewater effluent dominated Colorado streams. Comparative Biochemistry and Physiology, Part C, 144, 10–15. https://doi.org/10.1016/j.cbpc.2006.04.019
Xie, Q. P., Li, B. B., Wei, F. L., Yu, M., Zhan, W., Liu, F., & Lou, B. (2021). Growth and gonadal development retardations after long-term exposure to estradiol in little yellow croaker Larimichthys Polyactis. Ecotoxicology and Environmental Safety, 222, 112462. https://doi.org/10.1016/j.ecoenv.2021.112462
Zhang, D., Liu, W., Wang, S., Zhao, J., Xu, S., Yao, H., Wang, H., Bai, L., Wang, Y., Gu, H., Tao, J., & Shi, P. (2021). Risk assessments of emerging contaminants in various waters and changes of microbial diversity in sediments from Yangtze River chemical contiguous zone, Eastern China. Science of the Total Environment, 803, 149982. https://doi.org/10.1016/j.scitotenv.2021.149982
Funding
The authors would like to thank the National Council for Scientific and Technological Development (CNPq), Process nº 481985/2012–3, for the financial support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pacheco Passos Neto, O., Bezerra dos Santos, A., Feitosa Silva, J.R. et al. Alterations in the Development and Gonadal Structure of Nile Tilapia (Oreochromis niloticus) Exposed to Natural and Synthetic Estrogens. Water Air Soil Pollut 232, 448 (2021). https://doi.org/10.1007/s11270-021-05375-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-021-05375-x