Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T03:56:03.568Z Has data issue: false hasContentIssue false

Zebrafish as a possible bioindicator of organic pollutants in drinking waters with effects on reproduction: are effects cumulative or reversible?

Published online by Cambridge University Press:  03 May 2016

M. Martínez-Sales*
Affiliation:
Aquaculture and Environmental Research Group (ACUMA), Universidad Politécnica de Valencia, Camino de Vera 14, 46022, Valencia, Spain.
F. García-Ximénez
Affiliation:
Aquaculture and Environmental Research Group (ACUMA), Universidad Politécnica de Valencia, Camino de Vera 14, 46022, Valencia, Spain.
F.J. Espinós
Affiliation:
Aquaculture and Environmental Research Group (ACUMA), Universidad Politécnica de Valencia, Camino de Vera 14, 46022, Valencia, Spain.
*
All correspondence to: M. Martínez-Sales. Aquaculture and Environmental Research Group (ACUMA), Universidad Politécnica de Valencia, Camino de Vera 14, 46022, Valencia, Spain. Tel: +34 963879433. E-mail: mimarsa@alumni.upv.es

Summary

Organic pollutants are present in drinking waters due to inefficient detection and removal treatments. For this reason, zebrafish is proposed as a complementary indicator in conventional potabilization treatments. Based on the most sensitive parameters detected in our previous work, in this study we attempted to examine the possible cumulative effect between generations of environmental pollutants likely present in drinking waters, when specimens were cultured in the same water and/or the possible reversibility of these effects when cultured in control water. To this end, embryos with the chorion intact were cultured in three drinking waters from different sources and in one control water for up to 5 months in 20 l glass tanks. Four replicates were performed in all water groups. Results in water group C (tap water from a city also located in a region with intensive agricultural activity, but from the hydrological basin of the river Xúquer) revealed a non-reversible effect on fertility rate. Also in water C there was an alteration of sex ratio towards females, although in this case the alteration was reversible. A transgenerational alteration in the germ-line via an epigenetic mechanism from the previous generation is proposed as the most plausible explanation of this effect.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ankley, G.T. & Johnson, R.D. (2004). Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. Inst. Lab. Anim. Res. 45, 469–83.Google Scholar
Baroiller, J.F., Guiguen, Y. & Fostier, A. (1999). Endocrine and environmental aspects of sex differentiation in fish. Cell. Mol. Life Sci. 55, 910–31.CrossRefGoogle Scholar
Baumann, L., Holbech, H., Keiter, S., Kinnberg, K.L., Knörr, S., Nagel, T. & Braunbeck, T. (2013). The maturity index as a tool to facilitate the interpretation of changes in vitellogenin production and sex ratio in the fish sexual development test. Aquat. Toxicol. 128–129, 3442.Google Scholar
Benner, J., Helbling, D.E., Kohler, H.P.E., Wittebol, J., Kaiser, E., Prasse, C., Ternes, T.A., Albers, C.N., Aamand, J., Horemans, B., Springael, D., Walravens, E., & Boon, N. (2013). Is biological treatment a viable alternative for micropollutant removal in drinking water treatment processes? Water Res. 47, 5955–76.Google Scholar
Brand, M., Granato, M. & Nüslein-Volhard, C. (2002). Keeping and raising zebrafish. In Zebrafish. A Practical Approach (Nüslein-Volhard, C. & Dahm, R., eds). Oxford, UK: Oxford University Press, 16 pp.Google Scholar
Braw-Tal, R. (2010). Endocrine disruptors and timing of human exposure. Pediatr. Endocrinol. Rev. (PER) 8, 41–6.Google Scholar
Dahm, R. (2002). Atlas of embryonic stages of development in the zebrafish (Appendix 2). In Zebrafish. A Practical Approach (Nüslein-Volhard, C. & Dahm, R., eds). Oxford, UK: Oxford University Press, pp. 219–36.Google Scholar
Dai, Y.J., Jia, Y.F., Chen, N., Bian, W.P., Li, Q.K., Ma, Y.B., Chen, Y.L. & Pei, D.S. (2014). Zebrafish as a model system to study toxicology. Environ. Toxicol. Chem. 33, 11–7.Google Scholar
David, A. & Pancharatna, K. (2009). Developmental anomalies induced by a non-selective COX inhibitor (ibuprofen) in zebrafish (Danio rerio). Environ. Toxicol. Pharmacol. 27, 390–5.Google Scholar
Deblonde, T., Cossu-Leguille, C., Hartemann, P. (2011). Emerging pollutants in wastewater: A review of the literature. Int. J. Hyg. Environ. Health 214, 442–8.CrossRefGoogle ScholarPubMed
Duan, Z.H., Zhu, L., Zhu, L.Y., Yao, K., Zhu, X.S. (2008). Individual and joint toxic effects of pentachlorophenol and bisphenol A on the development of zebrafish (Danio rerio) embryo. Ecotox. Environ. Safe. 71, 774–80.Google Scholar
Fenske, M., Maack, G., Ensenbach, U. & Segner, H. (1999). Identification of estrogens-sensitive developmental stages of zebrafish, Danio rerio . In Proceedings of the Ninth Annual Meeting of Society of Environmental Toxicology and Chemistry, 25–29 May 1999, Leipzig, Germany.Google Scholar
Galus, M., Kirischian, N., Higgins, S., Purdy, J., Chow, J., Rangaranjan, S., Li, H., Metcalfe, C. & Wilson, J.Y. (2013). Chronic, low concentration exposure to pharmaceuticals impacts multiple organ systems in zebrafish. Aquat. Toxicol. 132–133, 200–11.CrossRefGoogle ScholarPubMed
Han, Z., Jiao, S., Shan, Z. & Zhang, X. (2011). Effects of β-endosulfan on the growth and reproduction of zebrafish (Danio rerio). Environ. Toxicol. Chem. 30, 2525–31.Google Scholar
Henn, K. (2011). Limits of the embryo toxicity test with Danio rerio as an alternative to the acute fish toxicity test. PhD Thesis. University of Heidelberg, Germany.Google Scholar
Hill, R. & Janz, D. (2003). Developmental estrogenic exposure in zebrafish (Danio rerio). I. Effects on sex ratio and breeding success. Aquat. Toxicol. 63, 417–29.Google Scholar
Hsioa, C.D. & Tsai, H.J. (2003). Transgenic zebrafish with fluorescent germ cell: a useful tool to visualize germ cell proliferation and juvenile hermaphroditism in vivo . Dev. Biol. 262, 313–23.Google Scholar
Ikehata, K., Gamal, El-Din, M. & Snyder, S.A. (2008). Ozonation and advanced oxidation treatment of emerging organic pollutants in water and wastewater. Ozone-Sci. Eng. 30, 21–6.Google Scholar
Jurewicz, J., Hanke, W., Radwan, M. & Bonde, J. (2009). Environmental factors and semen quality. Int. J. Occup. Med. Environ. Health 22, 305–29.Google Scholar
Khetan, S.K. & Collins, T.J. (2007). Human pharmaceuticals in the aquatic environment: a challenge to green chemistry. Chem. Rev. 107, 2319–64.CrossRefGoogle ScholarPubMed
Larsen, M.G., Bilberg, K. & Baatrup, E. (2009). Reversibility of estrogenic sex changes in zebrafish (Danio rerio). Environ. Toxicol. Chem. 28, 1783–5.CrossRefGoogle ScholarPubMed
Liew, W.C. & Orbán, L. (2014). Zebrafish sex: a complicated affair. Brief. Funct. Genomics 13, 172–87.CrossRefGoogle ScholarPubMed
Liu, S.Y., Jin, Q., Huang, X.H. & Zhu, G.N. (2014). Disruption of zebrafish (Danio rerio) sexual development after full life-cycle exposure to environmental levels of triadimefon. Environ. Toxicol. Pharmacol. 37, 468–75.Google Scholar
Mandrell, D., Truong, L., Jephson, C., Sarker, M., Moore, A., Lang, C., Simonich, M., & Tanguay, R. (2012). Automated zebrafish chorion removal and single embryo placement: optimizing throughput of zebrafish developmental toxicity screens. J. Lab. Automat. 17, 6674.Google Scholar
Martínez-Sales, M., García- Ximénez, F. & Espinós, F.J. (2015a). Zebrafish (Danio rerio) as a possible bioindicator of epigenetic factors present in drinking water that may affect reproductive function: Is chorion an issue? Zygote 23, 447–52.Google Scholar
Martínez-Sales, M., García- Ximénez, F. & Espinós, F.J. (2015b). Zebrafish as a possible bioindicator of organic pollutants with effects on reproduction in drinking waters. J. Environ. Sci. 32, 254–60.CrossRefGoogle Scholar
Matthews, M., Trevarrow, B. & Matthews, J. (2002). A virtual tour of the Guide for zebrafish users. Lab. Animal 31, 3440.Google ScholarPubMed
Mileva, G., Baker, S. L., Konkle, A., & Bielajew, C. (2014). Bisphenol-A: epigenetic reprogramming and effects on reproduction and behavior. Int. J. Environ. Res. Public Health 11, 7537–61.CrossRefGoogle ScholarPubMed
Nikolaou, A. (2013). Pharmaceuticals and related compounds as emerging pollutants in water: analytical aspects. Global NEST J. 15, 112.Google Scholar
Örn, S., Holbech, H., Madsen, T.H., Norrgren, L. & Petersen, G.I. (2003). Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyl testosterone. Aquat. Toxicol. 65, 397411.Google Scholar
Ouyang, Y., Nkedi-Kizza, P., Wu, Q.T., Shinde, D. & Huang, C.H. (2006). Assessment of seasonal variations in surface water quality. Water Res. 40, 3800–10.Google Scholar
Rodil, R., Quintana, J.B., Concha-Graña, E., López-Mahía, P., Muniategui-Lorenzo, S. & Prada-Rodríguez, D. (2012). Emerging pollutants in sewage, surface and drinking water in Galicia (NW Spain). Chemosphere 86, 1040–9.Google Scholar
Rusiecki, J.A., Baccarelli, A., Bollati, V., Tarantini, L., Moore, L.E. & Bonefeld-Jorgensen, E.C. (2008). Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ Health Perspect. 116, 1547–52.Google Scholar
Simão, M., Cardona-Costa, J., Pérez Camps, M. & García-Ximénez, F. (2010). Ultraviolet radiation dose to be applied in recipient zebrafish embryos for germ-line chimaerism is strain dependent. Reprod. Domest. Anim. 45, 1098–103.Google Scholar
Simon, O., Mottin, E., Geffroy, B. & Hinton, T. (2011). Effects of dietary uranium on reproductive endpoints—fecundity, survival, reproductive success—of the fish Danio rerio . Environmental Toxicology and Chemistry. 30, 220–5.Google Scholar
Skinner, M.K. (2011). Role of epigenetics in developmental biology and transgenerational inheritance. Birth Defects Res. C Embryo Today 93, 51–5.Google Scholar
Skinner, M.K., Manikkam, M. & Guerrero-Bosagna, C. (2010). Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrin. Met. 21, 214–22.CrossRefGoogle ScholarPubMed
Toft, G., Rignell-Hydbom, A., Tyrkiel, E., Shvets, M., Giwercman, A., Lindh, C.H., Pedersen, H.S., Ludwicki, J.K., Lesovoy, V., Hagmar, L., Spanó, M., Manicardi, G.C., Bonefeld-Jorgensen, E.C., Thulstrup, A.M. & Bonde, J.P. (2006). Semen quality and exposure to persistent organochlorine pollutants. Epidemiology 17, 450–8.Google Scholar
Vaughan, M., Van Egmond, R. & Tyler, C.R. (2001). The effect of temperature on sexual differentiation and development in the zebrafish (Danio rerio). In Proceedings of the 11th Annual Meeting of the Society of Environmental Toxicology and Chemistry, 610.Google Scholar
Vested, A., Giwercman, A., Bonde, J.P. & Toft, G. (2014). Persistent organic pollutants and male reproductive health. Asian J. Androl. 16, 7180.CrossRefGoogle ScholarPubMed
von der Ohe, P.C., Dulio, V., Slobodnik, J., De Deckere, E., Kühne, R., Ebert, R.U., Ginebreda, A., De Cooman, W., Schüürmann, G. & Brack, W. (2011). A new risk assessment approach for the prioritization of 500 classical and emerging organic microcontaminants as potential river basin specific pollutants under the European Water Framework Directive. Sci. Total Environ. 409, 2064–77.Google Scholar
Westerfield, M. (1995). The Zebrafish Book. Eugene, Oregon, USA: University of Oregon Press.Google Scholar
Westerfield, M. (2007). The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio), 5th edition. Eugene, Oregon, USA: University of Oregon Press.Google Scholar
Yoshizaki, G., Takeuchi, Y., Kobayashi, T., Ihara, S. & Takeuchi, T. (2002). Primordial germ cells: the blueprint for a piscine life. Fish Physiol. Biochem. 26, 312.Google Scholar