Skip to main content
SpringerLink
Log in

Assessment of Water Pollution in the Tronto River (Italy) by Applying Useful Biomarkers in the Fish Model Carassius auratus

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The Tronto River (southern Marche region of central Italy) is located in an area with neighboring industrial activities and is contaminated with domestic and industrial wastewater. Water quality data analyses revealed the presence of a mixture of low levels of heavy metals and organic compounds. The effects of long-term exposure to Tronto River water on juvenile Carassius auratus were evaluated with an integrated approach using xenoestrogens biomarkers, such as vitellogenin (VTG) and ER β-1 mRNA expression, and stress parameters (i.e., cortisol and glucose in the blood and glycogen in the liver). Treatment with Tronto River water did not induce VTG synthesis in fish and did not affect ER β-1 mRNA expression. Moreover, cortisol titers found in the plasma of fish exposed to Tronto River water were lower than those found in the control group. Regarding energy parameters, treatment with Tronto River water induced an increase in plasma glucose and a depletion of liver glycogen reserves.

The effects of Tronto River water were studied in parallel with those of 4-NP and CdCl2. The 4-NP at the dose of 22 μg/L induced the synthesis of peripheral vitellogenin and increase of ER β-1 titers; on the contrary, CdCl2 exposure at the concentration of 22 μg/L did not induce significant changes on plasma VTG and/or hepatic ER β-1 levels. In addition, no significant changes in plasma cortisol levels in fish exposed to 4-NP or CdCl2 were found. Fish exposed to CdCl2 displayed liver glycogen depletion, but no significant increase in plasma glucose was observed. On the contrary, a 30-day exposure to 4-NP induced only a slight decrease of glycogen reserves without any changes in plasma glucose levels.

In conclusion, our study demonstrated that long-term exposure of juvenile goldfish to the water of the Tronto River significantly affects both stress and energy parameters. There is evidence that pollutants, present in Tronto River water, were not able to induce xenoestrogenic effects but caused a functional impairment of the hypothalamum–pituitary–interrenal axis.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • ARPAM (2005) Available from http://www.213.26.167.177/carto/Fiumi/StampaDettagli.asp?xmin=2382188.4422110547&ymin=4712771.356783919&xmax=2475188.4422110556&ymax=4789414.572864322&prj=qa&dt=2005&cod=7/TR

  • ARPAM (2006) Available from http://www.213.26.167.177/carto/Fiumi/StampaDettagli.asp?xmin=2382188.4422110547&ymin=4712771.356783919&xmax=2475188.4422110556&ymax=4789414.572864322&prj=qa&dt=2006&cod=7/TR

  • Arukwe A, Goksoyr A (1998) Xenobiotics, xenoestrogens and reproduction disturbances in fish. Sarsia 83:225–241

    Google Scholar 

  • Arukwe A, Goksoyr A, Thibaut R, Cravedi JP (2000) Metabolism and organ distribution of nonylphenol in Atlantic salmon (Salmo salar). Mar Environ Res 50:141–145

    Article  CAS  Google Scholar 

  • Baldi P, Long AD (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17:509–519

    Article  CAS  Google Scholar 

  • Box GEP, Tiao GC (1992) Bayesian inference in statistical analysis. Wiley, New York, pp 92–112

    Google Scholar 

  • Brodeur JC, Daniel C, Ricard AC, Hontela A (1998) In vitro response to ACTH of the interrenal tissue of rainbow trout (Oncorhynchus mykiss) exposed to cadmium. Aquat Toxicol 42:103–113

    Article  CAS  Google Scholar 

  • Brodeur JC, Sherwood G, Rasmussen JB, Hontela A (1997) Impaired cortisol secretion in yellow perch (Perca flavescens) from lakes contaminated by heavy metals: in vivo and in vitro assessment. Can J Fish Aquat Sci 54:2752–2758

    Article  CAS  Google Scholar 

  • Cakmak G, Togan I, Severcan F (2006) 17β-estradiol induced compositional, structural and functional hanges in rainbow trout liver, revealed by FT-IR spectroscopy: a comparative study with nonylphenol. Aquat. Toxicol 77:53–63

    Article  CAS  Google Scholar 

  • Carnevali O, Mosconi G, Habibi HR, Elia AC, Cardinali M, Polzonetti-Magni AM (2003) Validation of an enzyme linked immunosorbent assay (ELISA) for Cyprinus carpio L. vitellogenin, as a biomarker of reproductive disorders. Chemistry and Ecology 1:5–13

    Article  CAS  Google Scholar 

  • De Zwart D (1995) Monitoring water quality in the future. Volume 3: Biomonitoring. National Institute of Public Health and Environmental Protection (RIVM), Bilthoven, The Netherlands

    Google Scholar 

  • Foran CM, Peterson BN, Benson WH (2002) Influence of parental and developmental cadmium exposure on endocrine and reproductive function in Japanese medaka (Oryzias latipes). Comp Biochem Physiol C 133:345–354

    Article  Google Scholar 

  • Fu H, Steinebach OM, van den Hamer CJA, Balm PHM, Lock RAC (1990) Involvement of cortisol and metallothionein-like proteins in the physiological responses of tilapia (Oreochromis mossambucus) to sublethal cadmium stress. Aquat Toxicol 16:257–270

    Article  CAS  Google Scholar 

  • Gimeno L, Ferrando MD, Sanchez S, Gimeno LO, Andreu E (1995) Pesticide effects on eel metabolism. Sci Total Environ 31:153–157

    CAS  Google Scholar 

  • Hontela A (1997) Endocrine and physiological responses of fish to xenobiotics: role of glucocorticosteroid hormones. Rev Toxicol 1:1–46

    CAS  Google Scholar 

  • Hontela A (2005) Adrenal toxicology: environmental pollutants and the HPI axis. In: Mommsen TP, Moon TW (eds) Biochemistry and Molecular Biology of Fishes. Vol. 6, Environmental Toxicology. Elsevier BV, Netherlands, Amsterdam, p 331–363

    Google Scholar 

  • Hontela A, Dumont P, Duclos D, Fortin R (1995) Endocrine and metabolic dysfunction in yellow perch, Perca flavescens, exposed to organic contaminants and heavy metals in the St. Lawrence River Environ Toxicol Chem 14:725–731

    Article  CAS  Google Scholar 

  • Hontela A, Rasmussen JB, Audet C, Chevalier G (1992) Impaired cortisol stress response in fish from environments polluted by PAHs, PCBs, and mercury. Arch Environ Contam Toxicol 34:377–381

    Google Scholar 

  • Kemp A, Kits Van Heijningen AJM (1954) A colorimetric micro-method for the determination of glycogen in tissues. Biochem J 56:646–647

    CAS  Google Scholar 

  • Lacroix A, Hontela A (2004) A comparative assessment of the adrenotoxic effects of cadmium in two teleost species, rainbow trout, Oncorhynchus mykiss, and yellow perch, Perca flavescens. Aquat Toxicol 67:13–21

    Article  CAS  Google Scholar 

  • Le Guevel R, Petit FG, Le Goff P, Metivier R, Valotaire Y, Pakdel F (2000) Inhibition of rainbow trout (Oncorhynchus mykiss) estrogen receptor activity by cadmium. Biol Reprod 63:259–266

    Article  CAS  Google Scholar 

  • Levesque H, Moon TW, Campbell PGC, Hontela A (2002) Seasonal variation in carbohydrate and lipid metabolism of cortisol-impaired metalexposed yellow perch (Perca flavescens). Aquat Toxicol 60:257–267

    Article  CAS  Google Scholar 

  • McCormick S, O’Dea MF, Moeckel AM, Lerner DT, Björnsson BT (2005) Endocrine disruption of parr-smolt transformation and seawater tolerance of Atlantic salmon by 4-nonylphenol and 17β-estradiol. Gen Comp Endocrinol 142:280–288

    Article  CAS  Google Scholar 

  • Nolan DT, Spanings FAT, Ruane NM, Hadderingh RH, Jenner HA, Wendelaar Bonga SE (2003) Exposure to water from the lower Rhine induces a stress response in the rainbow trout Oncorhynchus mykiss. Arch Environ Contam Toxicol 45:247–257

    Article  CAS  Google Scholar 

  • Norris OD (2000) Endocrine disruptors of the stress axis in natural populations: How can we tell? Am Zool 40:393–401

    Article  CAS  Google Scholar 

  • Pereira JJ, Mercaldo-Allen R, Kuropat C, Luedke D, Sennefelder G (1993) Effect of cadmium accumulation on serum vitellogenin levels and hepatosomatic and gonadosomatic indices of winter flounder (Pleuronectes americanus). Arch Environ Contam Toxicol 24:427–431

    Article  CAS  Google Scholar 

  • Pratap HB, Wendelaar Bonga SE (1990) Effect of waterborne cadmium on plasma cortisol and glucose in the cichlid fish Oreochromis mossambicus. Comp Biochem Physiol C 95:313–317

    Article  Google Scholar 

  • Ricard AC, Daniel C, Andersen P, Hontela A (1998) Effects of subchronic exposure to cadmium chloride on endocrine and metabolic functions in rainbow trout Oncorhynchus mykiss. Arch Environ Contam Toxicol 34:377–381

    Article  CAS  Google Scholar 

  • Roche H, Buet A, Ramade F (2002) Accumulation of lipophilic microcontaminants and biochemical responses in eels from the Biosphere Reserve of Camargue. Ecotoxicology 11:9–18

    Article  Google Scholar 

  • Sancho E, Ferrando MD, Andreu E (1998) Effects of sublethal exposure to a pesticide on levels of energetic compounds in Anguilla anguilla. J Environ Sci Health 33B:411–424

    Google Scholar 

  • Santos MA, Pacheco M (1996) Anguilla anguilla L. Stress biomarkers recovery in clean water and secondary-treated pulp mill effluent. Ecotoxicol Environ Toxicol Safety 35:96–100

    Article  CAS  Google Scholar 

  • Sangalang GB, O’Halloran MJ (1972) Cadmium-induced testicular injury and alterations of androgen synthesis in brook trout. Nature 240:470–471

    Article  CAS  Google Scholar 

  • Scott GR, Sloman KA, Rouleau C, Wood CM (2003) Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 2061779–1790

  • Shaffi SA, Manohar YR, Nandan MJ (2001) Influence of protective agents on metal induced respiratory distress in Labeo rohita (Ham). Bull Environ Contam Toxicol 66:611–616

    CAS  Google Scholar 

  • Snedecor GW, Cochran WG (1989) Statistical methods. Iowa State University Press, Ames, p 491

    Google Scholar 

  • Sokal R, Rohlf F (1996) Biometry. W.H. Freeman, New York, p 887

    Google Scholar 

  • Soverchia L, Ruggeri B, Palermo F, et al. (2005) Modulation of vitellogenin synthesis through estrogen receptor beta-1 in goldfish (Carassius auratus) juveniles exposed to 17β-estradiol and nonylphenol. Toxicol Appl Pharmacol 209:236–243

    Article  CAS  Google Scholar 

  • Stoica A, Katzenellenbogen BS, Martin MB (2000) Activation of estrogen receptor-α by the heavy metal cadmium. Mol Endocrinol 4:545–553

    Article  Google Scholar 

  • Strmac M, Braunbeck T (1999) Effects of triphenyltin acetate on survival, hatching success, and liver ultrastructure of early life stages of zebrafish (Brachydanio rerio). Ecotoxicol Environ Safety 44:25–39

    Article  CAS  Google Scholar 

  • Teles M, Maria VL, Pacheco M, Santos MA (2003) Effects on plasma cortisol, lactate and glucose in Anguilla anguilla L. exposed to pulp mill effluents components. Environ Int 10931–6

  • Teles M, Pacheco M, Santos MA (2004) Responses of European eel (Anguilla anguilla L.) in two polluted environments: in situ experiments. Ecotoxicol Environ Safety 58:373–378

    Article  CAS  Google Scholar 

  • Thomas P (1990) Teleost model for studying the effects of chemicals on female reproductive endocrine function. J Exp Zool 4(Suppl):126–128

    Article  CAS  Google Scholar 

  • Tilton SC, Foran CM, Benson WH (2003) Effects of cadmium on the reproductive axis of Japanese medaka (Oryzias latipes). Comp Biochem Physiol C 136:265–76

    Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Versteeg D, Giesy JP (1986) The histological and biochemical effects of cadmium exposure in the bluegill sunfish (Lepomis macrochirus). Ecotoxicol Environ Safety 11:31–43

    Article  CAS  Google Scholar 

  • Vijayan MM, Moon TW (1992) Acute handling stress alters hepatic glycogen metabolism in food-deprived-rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 49:2260–2266

    Article  CAS  Google Scholar 

  • Vijayan MM, Pereira C, Grau EG, Iwama GK (1997) Metabolic responses associated with confinement stress in tilapia: the role of cortisol. Comp Biochem Physiol C 116:89–95

    Article  Google Scholar 

  • Vitali M, Ensabella F, Stella D, Guidotti M (2004) Nonylphenols in freshwaters of the hydrologic system of an Italian district: association with human activities and evaluation of human exposure. Chemosphere 57:1637–1647

    Article  CAS  Google Scholar 

  • Walter GL, Jones PD, Giesy JP (2000) Pathologic alterations in adult rainbow trout, Oncorhynchus mykiss, exposed to dietary 2,3,7,8-tetrachlorodibenzo-p-dioxin. Aquat Toxicol 50:287–299

    Article  CAS  Google Scholar 

  • Yadetie A, Arukwe A, Goksøyr A, Male R (1999) Induction of hepatic estrogen receptor in juvenile Atlantic salmon in vivo by the environmental estrogen, 4-nonylphenol. Sci Total Environ 233:201–210

    Article  CAS  Google Scholar 

  • Yao Z, Van der Kraak GJ, Squires EJ (1996) Effect of heavy metals on in vitro vitellogenin production from cultured hepatocytes of goldfish. In: Proceedings of the 3rd International Symposium on Fish Endocrinology, Hakodate, p 172

Download references

Author information

Authors and Affiliations

  1. Dipartimento di Scienze Morfologiche e Biochimiche Comparate, Università degli Studi di Camerino, via Gentile III da Varano, 62032, Camerino, MC, Italy

    F. A. Palermo, G. Mosconi & A. M. Polzonetti-Magni

  2. Centro Universitario di Ricerca per lo Sviluppo e la Gestione delle Risorse dell’Ambiente Marino e Costiero (UNICRAM), Università degli Studi di Camerino, Lungomare A. Scipioni 6, 63039, San Benedetto del Tronto, AP, Italy

    F. A. Palermo & A. M. Polzonetti-Magni

  3. Dipartimento di Biologia Molecolare Cellulare Animale, Università degli Studi di Camerino, via Gentile III da Varano, 62032, Camerino, MC, Italy

    M. Angeletti

Authors
  1. F. A. Palermo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Mosconi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Angeletti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. M. Polzonetti-Magni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. A. Palermo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Palermo, F.A., Mosconi, G., Angeletti, M. et al. Assessment of Water Pollution in the Tronto River (Italy) by Applying Useful Biomarkers in the Fish Model Carassius auratus . Arch Environ Contam Toxicol 55, 295–304 (2008). https://doi.org/10.1007/s00244-007-9113-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-007-9113-2

Keywords

Search

Navigation