Impact of Endocrine Disruptors on Vitellogenin Concentrations in Wild Brown Trout (Salmo trutta trutta)

Abstract

The adverse effects of endocrine disruptors (EDs) on aquatic wildlife and human health represent a current issue of high public concern. Substantial knowledge of the level of estrogenic EDs in fish has accumulated from field surveys. For this purpose, a survey of wild brown trout (Salmo trutta trutta) was carried out to assess the incidence of EDs in the feral fish population living in the Liri river (Abruzzi, Italy). The results of this study show that this aquatic environment possesses an estrogenic potency that triggered the increase of vitellogenin levels in both female and male trouts. Fish exposed to different pesticides and urban waste in downstream river showed higher vitellogenin levels in comparison to the headwater site. Furthermore, some trouts coming from the downstream reported the presence of several pesticides and fungicides, some of these banned several years ago.

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

References

  1. Andersson C, Katsiadaki I, Lundstedt-Enkel K, Örberg J (2007) Effects of 17α-ethynylestradiol on EROD activity, spiggin and vitellogenin in three-spined stickleback (Gasterosteus aculeatus). Aquat Toxicol 83(1):33–42

    CAS  Article  Google Scholar 

  2. Arta Abruzzo (2014) Monitoraggio dei prodotti fitosanitari nelle acque superficiali e sotterranee ai sensi della Parte Terza del D.Lgs 152/06 e s.m.i. https://bura.regione.abruzzo.it/2015/Allegati/Spe_62_doc0_4.pdf. Accessed 25 May 2020

  3. Beresford N, Baynes A, Kanda R (2016) Use of a battery of chemical and ecotoxicological methods for the assessment of the efficacy of wastewater treatment processes to remove estrogenic potency. J Vis Exp JoVE 115:e54243

    Google Scholar 

  4. Bugel SM, White LA, Cooper KR (2011) Decreased vitellogenin inducibility and 17β-estradiol levels correlated with reduced egg production in killifish (Fundulus heteroclitus) from Newark Bay. NJ Aquat Toxicol 105(1–2):1–12

    CAS  Google Scholar 

  5. Datta SN, Kaur VI, Dhawan A, Jassal G (2013) Estimation of length-weight relationship and condition factor of spotted snakehead Channa punctata (Bloch) under different feeding regimes. SpringerPlus 2(1):436

    Article  Google Scholar 

  6. Depiereux S, Liagre M, Danis L (2014) Intersex occurrence in rainbow trout (Oncorhynchus mykiss) male fry chronically exposed to ethynylestradiol. PLoS ONE 9(7):e98531

    Article  Google Scholar 

  7. Di Giulio R, Hinton DE (2008) Biomarkers. In The toxicology of fishes, 1st edn. CRC Press/Taylor and Francis Group, Boca Raton, p 703

  8. EN 27 828 (1994) Water quality—methods for biological sampling—guidance on handnet sampling of aquatic benthic macroinvertebrates. (ISO 7828: 1985)

  9. European Food Safety Authority (EFSA), Arena M, Auteri D, Barmaz S, Bellisai G, Brancato A, Court Marques D (2017) Peer review of the pesticide risk assessment of the active substance chlorpropham. EFSA J 15(7):e04903

    Google Scholar 

  10. European Food Safety Authority (EFSA), Arena M, Auteri D, Barmaz S, Bellisai G, Brancato A, Court Marques D (2018) Peer review of the pesticide risk assessment of the active substance tolclofos-methyl. EFSA J 16(1):e05130

    Google Scholar 

  11. Ghetti PF (1997) I macroinvertebrati nel controllo della qualità di ambienti di acque correnti. Indice Biotico Esteso (I.B.E.). Manuale di applicazione. Provincia Autonoma di Trento, Trento, p 222

  12. Gupta PK (2017) Herbicides and fungicides. In: Gupta RC (ed) Reproductive and developmental toxicology. Academic Press/Elsevier, Cambridge, pp 657–679

    Google Scholar 

  13. Gustavo G, Alberto MSF, Eugenia MSA, Anabella F, Martin ST, Vanesa MS, Aloranti C (2014) Comprehesive assement of estrogenic contamination of surface waters of the river basin suquia. Euro Sci J 3:297–302

    Google Scholar 

  14. Hiramatsu N, Todo T, Sullivan CV (2015) Ovarian yolk formation in fishes: molecular mechanisms underlying formation of lipid droplets and vitellogenin-derived yolk proteins. Gen Comp Endocrinol 221:9–15

    CAS  Article  Google Scholar 

  15. Kiyama R, Wada-Kiyama Y (2015) Estrogenic endocrine disruptors: molecular mechanisms of action. Environ Int 83:11–40

    CAS  Article  Google Scholar 

  16. Kolanczyk RC, Serrano JA, Tapper MA, Schmieder PK (2018) A comparison of fish pesticide metabolic pathways with those of the rat and goat. Regul Toxicol Pharmacol 94:124–143

    CAS  Article  Google Scholar 

  17. Körner O, Vermeirssen ELM, Burkhardt-Holm P (2007) Reproductive health of brown trout inhabiting Swiss rivers with declining fish catch. Aquat Sci 64:26–40

    Article  Google Scholar 

  18. Körner O, Kohno S, Schönenberger R, Suter MJF, Knauer K, JrLJ G, Burkhardt-Holm P (2008) Water temperature and concomitant waterborne ethinylestradiol exposure affects the vitellogenin expression in juvenile brown trout (Salmo trutta). Aquat Toxicol 90(3):188–196

    Article  Google Scholar 

  19. Li Y, Wang J, Zheng M, Zhang Y, Ru S (2018) Development of ELISAs for the detection of vitellogenin in three marine fish from coastal areas of China. Mar Pollut Bull 133:415–422

    CAS  Article  Google Scholar 

  20. Mnif W, Hassine AIH, Bouaziz A, Bartegi A, Thomas O, Roig B (2011) Effect of endocrine disruptor pesticides: a review. Int J Environ Res Public Health 8(6):2265–2303

    CAS  Article  Google Scholar 

  21. Nagler JJ, Davis TL, Modi N, Vijayan MM, Schultz I (2010) Intracellular, not membrane, estrogen receptors control vitellogenin synthesis in the rainbow trout. Gen Comp Endocrinol 167(2):326–330

    CAS  Article  Google Scholar 

  22. Nikoleris L, Hultin CL, Hallgren P, Hansson MC (2016) 17α-Ethinylestradiol (EE2) treatment of wild roach (Rutilus rutilus) during early life development disrupts expression of genes directly involved in the feedback cycle of estrogen. Comp Biochem Physiol C Toxicol Pharmacol 180:56–64

    CAS  Article  Google Scholar 

  23. Ondarza PM, Gonzalez M, Fillmann G, Miglioranza KSB (2014) PBDEs, PCBs and organochlorine pesticides distribution in edible fish from Negro River basin, Argentinean Patagonia. Chemosphere 94:135–142

    CAS  Article  Google Scholar 

  24. Pacioni E, Petitta M, Burri E, Fanelli M, Mazzeo P, Ruggieri F (2010) Influence of surface/groundwater interaction on pollution by pesticides in farmlands of the Fucino Plain, central Italy. Environ Earth Sci 61:201–216

    CAS  Article  Google Scholar 

  25. Satya S, Wade M, Hass U (2012) Guidance document on standardised test guidelines for evaluating chemicals for endocrine disruption. https://www.oecd.org/chemicalsafety/testing/50459967.pdf. Accessed 15 April 2020

  26. Schug TT, Johnson AF, Birnbaum LS (2016) Minireview: endocrine disruptors: past lessons and future directions. Mol Endocrinol 30(8):833–847

    CAS  Article  Google Scholar 

  27. Silva JM, de Brito Santos FL, Santos RV, de Oliveira BE, Santos EL, Santana AEG, Abreu FC (2017) Determination of genotoxic effect of trifluralin on Colossoma macropomum (Teleostei: Characidae: Serrasalminae, Cuvier, 1816) using a multibiomarker approach. Ecotoxicol Environ Contam 12(1):85–93

    Google Scholar 

  28. Sumpter JP (1985) The purification, radioimmunoassay and plasma levels of vitellogenin from the rainbow trout, Salmo gairdneri. In: Lofts B, Holmes WN (eds) Current trends in comparative endocrinology. Hong Kong University Press, Hong Kong, p 355

    Google Scholar 

  29. Tabassum H, Ashafaq M, Khan J, Shah MZ, Raisuddin S, Parvez S (2016) Short term exposure of pendimethalin induces biochemical and histological perturbations in liver, kidney and gill of freshwater fish. Ecol Indic 63:29–36

    CAS  Article  Google Scholar 

  30. Tada N, Nakao A, Hoshi H, Saka M, Kamata Y (2008) Vitellogenin, a biomarker for environmental estrogenic pollution, of Reeves' pond turtles: analysis of similarity for its amino acid sequence and cognate mRNA expression after exposure to estrogen. J Vet Med Sci 70(3):227–234

    CAS  Article  Google Scholar 

  31. Turano MJ, Borski RJ, Daniels HV (2007) Compensatory growth of pond-reared hybrid Striped bass, Morone chrysops × Morone saxatilis, fingerlings. J World Aquacult Soc 38:250–261

    Article  Google Scholar 

  32. Ündeğer Ü, Schlumpf M, Lichtensteiger W (2010) Effect of the herbicide pendimethalin on rat uterine weight and gene expression and in silico receptor binding analysis. Food Chem Toxicol 48(2):502–508

    Article  Google Scholar 

  33. Vermeirssen ELM, Körner O, Schönenberger R, Suter MJF, Burkhardt-Holm P (2005) Characterization of environmental estrogens in river water using a three pronged approach: active and passive water sampling and the analysis of accumulated estrogens in the bile of caged fish. Environ Sci Technol 39:8191–8198

    CAS  Article  Google Scholar 

  34. Vives I, Grimalt JO, Ventura M, Catalan J, Rosseland BO (2005) Age dependence of the accumulation of organochlorine pollutants in brown trout (Salmo trutta) from a remote high mountain lake (Redo, Pyrenees). Environ Pollut 133(2):343–350

    CAS  Article  Google Scholar 

  35. Yamamoto FY, Garcia JRE, Kupsco A, Oliveira Ribeiro CA (2017) Vitellogenin levels and others biomarkers show evidences of endocrine disruption in fish species from Iguaçu River—Southern Brazil. Chemosphere 186:88–99

    CAS  Article  Google Scholar 

  36. Yilmaz O, Prat F, Ibañez AJ, Amano H, Koksoy S, Sullivan CV (2015) Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: Status and perspectives on multiplicity and functioning of vitellogenins. Gen Comp Endocrinol 221:16–22

    CAS  Article  Google Scholar 

  37. Zhang T, Qu Z, Li B, Yang Z (2019) Simultaneous determination of atrazine, pendimethalin, and trifluralin in fish samples by QuEChERS extraction coupled with gas chromatography-electron capture detection. Food Anal Methods 12(5):1179–1186

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Monia Perugini.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 444 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zezza, D., Bisegna, A., Angelozzi, G. et al. Impact of Endocrine Disruptors on Vitellogenin Concentrations in Wild Brown Trout (Salmo trutta trutta). Bull Environ Contam Toxicol (2020). https://doi.org/10.1007/s00128-020-02916-8

Download citation

Keywords

  • Vitellogenin
  • Pesticides
  • Agricultural sewage
  • Fish
  • Endocrine disruptors