Skip to main content
SpringerLink
Log in

Comparative study of the genotoxic response of freshwater mussels Unio tumidus and Unio pictorum to environmental stress

  • FRESHWATER BIVALVES
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Genotoxic response of freshwater mussels U. tumidus and U. pictorum to environmental stress was studied using comet assay on hemocytes and gill cells. The mussels were acclimated to controlled laboratory conditions for 10 days, and then exposed at 4 sites in the Sava and Danube rivers in the area of the city of Belgrade. Samples of each species were taken after 7, 14, and 30 days of exposure. The mussels sampled immediately after acclimation served as controls. Genotoxic response in both species was induced earlier at sites receiving untreated wastewaters from the city’s main collectors (7 days), than at the site receiving only domestic wastewaters from small settlements located upstream from the city (30 days). There was a correlation between the comet tail intensity values in tissues of exposed mussels and the concentrations of zinc, copper, iron, and arsenic at the exposure sites. The genotoxic responses in both tissues of U. pictorum and in hemocytes of U. tumidus were similar, while U. tumidus gill cells failed to exhibit significant genotoxic response at two sites. These findings, together with higher mortality of U. tumidus at the most polluted sites, promote U. pictorum as a model for genotoxicity monitoring in freshwater environments.

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

Similar content being viewed by others

References

  • Ahmed, M. K., M. Habibullah-Al-Mamun, M. A. Hossain, M. Arif, E. Parvin, M. S. Akter, M. S. Khan & M. M. Islam, 2011. Assessing the genotoxic potentials of arsenic in tilapia (Oreochromis mossambicus) using alkaline comet assay and micronucleus test. Chemosphere 84: 143–149.

    Article  CAS  PubMed  Google Scholar 

  • Aldridge, D. C., 1999. The morphology, growth and reproduction of Unionidae (Bivalvia) in a Fenland waterway. Journal of Molluscan Studies 65: 47–60.

    Article  Google Scholar 

  • Ali, D., S. Alarifi, S. Kumar, M. Ahamed & M. A. Siddiqui, 2012. Oxidative stress and genotoxic effect of zinc oxide nanoparticles in freshwater snail Lymnaea luteola L. Aquatic Toxicology 15: 124–125.

    Google Scholar 

  • Amiard, J. C., C. Amiard-Triquet, S. Barka, J. Pellerin & P. S. Rainbow, 2006. Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquatic Toxicology 76: 160–202.

    Article  CAS  PubMed  Google Scholar 

  • Andral, B., J. Y. Stanisiere, D. Sauzade, E. Damier, H. Thebault, F. Galgani & P. Boissery, 2004. Monitoring chemical contamination levels in the Mediterranean based on the use of mussel caging. Marine Pollution Bulletin 49: 704–712.

    Article  CAS  PubMed  Google Scholar 

  • Arbuckle, K. E. & J. A. Downing, 2002. Freshwater mussel abundance and species richness: GIS relationships with watershed land use and geology. Canadian Journal of Fisheries and Aquatic Sciences 59: 310–316.

    Article  Google Scholar 

  • Bagdonas, E. & M. Z. Vosyliene, 2006. A study of toxicity and genotoxicity of copper, zinc and their mixture to rainbow trout (Oncorhynchus Mykiss). Biologija 1: 8–13.

    Google Scholar 

  • Bauer, G. & K. Wachtler, 2001. Ecology and evolution of the freshwater mussels unionoida. In Bauer, G. & K. Wachtler. (eds), Ecological Studies. Vol. 145. Berlin: Springer.

  • Bauer, G., S. Hochwald & W. Silkenat, 1991. Spatial distribution of freshwater mussels: the role of host fish and metabolic rate. Freshwater Biology 26: 377–386.

    Article  Google Scholar 

  • Binelli, A., C. Riva & A. Provini, 2007. Biomarkers in zebra mussel for monitoring and quality assessment of Lake Maggiore (Italy). Biomarkers 12: 349–368.

    Article  CAS  PubMed  Google Scholar 

  • Bocquené, G., S. Chantereau, C. Clérendeau, E. Beausir, D. Ménard, B. Raffin, C. Minier, T. Burgeot, A. P. Leszkowicz & J. F. Narbonne, 2004. Biological effects of the “Erika” oil spill on the common mussel (Mytilus edulis). Aquatic Living Resources 17: 309–316.

    Article  Google Scholar 

  • Bolognesi, C., A. Buschini, E. Branchi, P. Carboni, M. Furlini, A. Martino, M. Monteverde, P. Poli & C. Rossi, 2004. Comet and micronucleus assays in zebra mussel cells for genotoxicity assessment of surface drinking water treated with three different disinfectants. Science of the Total Environment 333: 127–136.

    Article  CAS  PubMed  Google Scholar 

  • Claxton, L. D., V. S. Houk & T. J. Hughes, 1998. Genotoxicity of industrial wastes and effluents. Mutation Research 410: 237–243.

    Article  CAS  PubMed  Google Scholar 

  • Coffinet, S., C. Cossu-Leguille, A. Bassères, J. F. Gonnet & P. Vasseur, 2008. Response of the bivalve Unio tumidus and freshwater communities in artificial streams for hazard assessment of methyl methacrylate. Environmental Toxicology and Chemistry 27: 1371–1382.

    Article  CAS  PubMed  Google Scholar 

  • Collins, A. R., A. Oscoz, G. Brunborg, I. Gaiva, L. Giovannelli, M. Kruszewski, C. C. Smith & R. Stetina, 2008. The comet assay: topical issues. Mutagenesis 23: 143–151.

    Google Scholar 

  • Conners, E. D. & C. M. Black, 2004. Evaluation of lethality and genotoxicity in the freshwater mussel Utterbackia imbecillis (Bivalvia: Unionidae) exposed singly and in combination to chemicals used in Lawn Care. Archives of Environmental Contamination and Toxicology 46: 362–371.

    Article  CAS  PubMed  Google Scholar 

  • Cossu, C., A. Doyotte, M. Babut, A. Exinger & P. Vasseur, 2000. Antioxidant biomarkers in freshwater bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicology and Environmental Safety 45: 106–121.

    Article  CAS  PubMed  Google Scholar 

  • De Kock, W. C. & K. J. M. Kramer, 1994. Active biomonitoring (ABM) by translocation of Bivalves mollusks. In Kramer, K. J. M. (ed.), Biomonitoring of Coastal Waters and Estuaries. CRC Press, Boca Raton, FL: 51–84.

    Google Scholar 

  • De Lafontaine, Y., F. Gagne, C. Blaise, G. Costan, P. Gagnon & H. M. Chan, 2000. Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquatic Toxicology 50: 51–71.

    Article  PubMed  Google Scholar 

  • Dixon, D. R., A. M. Pruski, L. R. J. Dixon & A. N. Jha, 2002. Marine invertebrate eco-genotoxicity: a methodological overview. Mutagenesis 17: 495–507.

    Article  CAS  PubMed  Google Scholar 

  • European Commission, 2006. Directive 2006/7/EEC, Directive concerning management of bathing water quality and repealing Directive 76/160/EEC. Official Journal of European Communities L. 64: 37–51.

    Google Scholar 

  • Ferrari, B., N. Paxeus, R. Lo Giudice, A. Pollio & J. Garric, 2003. Ecotoxicological impact of pharmaceuticals found in treated waste waters: study of carbamazepine, clofibric acid and diclofenac. Ecotoxicology and Environmental Safety 55: 359–370.

    Article  CAS  PubMed  Google Scholar 

  • Grover, S. & S. Kaur, 1999. Genotoxicity of wastewater samples from sewage and industrial effluent detected by the Allium root anaphase aberration and micronucleus assays. Mutation Research 426: 183–188.

    Article  CAS  PubMed  Google Scholar 

  • Guidi, P., G. Frenzilli, M. Benedetti, M. Bernardeschi, A. Falleni, D. Fattorini, F. Regoli, V. Scarcelli & M. Nigro, 2010. Antioxidant, genotoxic and lysosomal biomarkers in the freshwater bivalve (Unio pictorum) transplanted in a metal polluted river basin. Aquatic Toxicology 100: 75–83.

    Article  CAS  PubMed  Google Scholar 

  • Halling, S., N. Nors, P. F. Lanzky, F. Ingerslev, L. Holten & S. E. Jorgensen, 1998. Occurrence, fate and effects of pharmaceutical substances in the environment—a review. Chemosphere 36: 357–393.

    Article  Google Scholar 

  • ICPDR, 2002. Water Quality in the Danube River Basin. TNMN Yearbook 2002. http://www.icpdr.org/icpdr-pages/tnmn_yearbooks.htm.

  • Jha, A. N., 2004. Genotoxicological studies in aquatic organisms: an overview. Mutation Research 552: 1–17.

    Article  CAS  PubMed  Google Scholar 

  • Jha, A. N., 2008. Ecotoxicological application and significance of the comet assay. Mutagenesis 23: 207–221.

    Article  CAS  PubMed  Google Scholar 

  • Klobučar, G., M. Pavlica, R. Erben & D. Papeš, 2003. Application of the micronucleus and comet assays to mussel Dreissena polymorpha haemocytes for genotoxicity monitoring of freshwater environments. Aquatic Toxicology 64: 15–23.

    Article  PubMed  Google Scholar 

  • Klobučar, G., A. Štambuk, K. Hylland & M. Pavlica, 2008. Detection of DNA damage in haemocytes of Mytilus galloprovincialis in the coastal ecosystems of Kaštela and Trogir Bays, Croatia. Science and Total Environment 405: 330–337.

    Article  Google Scholar 

  • Kolarević, S., J. Knežević-Vukčević, M. Paunović, J. Tomović, Z. Gačić & B. Vuković-Gačić, 2011. Antropogenic impact on water quality of the River Danube in Serbia: microbiological analysis and genotoxicity monitoring. Archives of Biological Science 63: 1209–1217.

    Article  Google Scholar 

  • Lehtonen, K. K., D. Schiedek, A. Köhler, T. Lang, P. J. Vuorinen, L. Förlin, J. Barŝiené, J. Pempkowiak & J. Gercken, 2006. The BEEP project in the Baltic Sea: overview of results and outline for a regional biological effects monitoring strategy. Marine Pollution Bulletin 53: 523–537.

    Article  CAS  PubMed  Google Scholar 

  • Makala, P. & A. O. J. Oikari, 1990. Uptake and body distribution of chlorinated phenolic in the freshwater mussel, Anodonta atina L. Ecotoxicology and Environmental Safety 20: 354–362.

    Article  Google Scholar 

  • Millward, G. E., S. Kadam & A. N. Jha, 2012. Tissue-specific assimilation, depuration and toxicity of nickel in Mytilus edulis. Environmental Pollution 162: 406–412.

    Article  CAS  PubMed  Google Scholar 

  • Nigro, M., A. Falleni, I. Del Barga, V. Scarcelli, P. Lucchesi, F. Regoli & G. Frenzilli, 2006. Cellular biomarkers for monitoring estuarine environments: transplanted versus native mussels. Aquatic Toxicology 77: 339–347.

    Article  CAS  PubMed  Google Scholar 

  • Olive, P. L. & P. B. Judit, 2006. The comet assay: a method to measure DNA damage in individual cells. British Columbia Cancer Research Center. doi:10.1038/nprot.2006.5675.

  • Pampanin, D. M., L. Camus, A. Gomiero, I. Marangon, E. Volpato & C. Nasci, 2005. Susceptibility to oxidative stress of mussels (Mytilus galloprovincialis) in the Venice Lagoon (Italy). Marine Pollution Bulletin 50: 1548–1557.

    Article  CAS  PubMed  Google Scholar 

  • Parolini, M., A. Binelli & A. Provini, 2011. Assessment of the potential cyto-genotoxicity of the nonsteroidal anti-inflammatory drug (NSAID) diclofenac on the zebra mussel (Dreissena polymorpha). Water, Air, Soil, Pollution 217: 589–601.

    Article  CAS  Google Scholar 

  • Pavlica, M., G. Klobučar, N. Mojaš, R. Erben & D. Papeš, 2001. Detection of DNA damage in haemocytes of zebra mussel using comet assay. Mutation Research 490: 209–214.

    Article  CAS  PubMed  Google Scholar 

  • Ramírez, O. A. & F. P. García, 2005. Genotoxic damage in zebra fish (Danio rerio) by arsenic in waters from Zimapan, Hidalgo, Mexico. Mutagenesis 20: 291–295.

    Article  PubMed  Google Scholar 

  • Ravera, O., 2001. Monitoring of the aquatic environment by species accumulators of pollutants: a review, in: Ravera, O. (eds), Scientific and legal aspects of biological monitoring in freshwater. Journal of Limnology 60: 63–72.

    Google Scholar 

  • Regoli, F., G. Frenzilli, R. Bocchetti, F. Annarumma, V. Scarcelli, D. Fattorini & M. Nigro, 2004. Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis during a field translocation experiment. Aquatic toxicology 68: 167–178.

    Article  CAS  PubMed  Google Scholar 

  • Richardson, M. L. & J. M. Bowron, 1985. The fate of pharmaceutical chemicals in the aquatic environment. Journal of Pharmacy and Pharmacology 37: 1–12.

    Article  CAS  PubMed  Google Scholar 

  • Rocher, B., J. Le Goff, L. Peluhet, M. Briand, H. Manduzio & J. Gallois, 2006. Genotoxicant accumulation and cellular defence activation in bivalves chronically exposed to waterborne contaminants from the Seine River. Aquatic Toxicology 79: 65–77.

    Article  CAS  PubMed  Google Scholar 

  • Roméo, M., P. Hoarau, G. Garello, M. Gnassia-Barelli & J. P. Girard, 2003. Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environmental Pollution 122: 369–378.

    Article  PubMed  Google Scholar 

  • Schwalb, A. N. & M. T. Pusch, 2007. Horizontal and vertical movements of unionid mussels in a lowland river. Journal of the North American Benthological Society 26: 261–272.

    Article  Google Scholar 

  • Singh, N. P., M. T. McCoy, R. R. Tice & E. L. Schneider, 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research 175: 184–191.

    Article  CAS  PubMed  Google Scholar 

  • Smolders, R., L. Bervoets, V. Wepener & R. Blust, 2003. A conceptual framework for using mussels as biomonitors in whole effluent toxicity. Human and Ecological Risk Assessment 9: 741–760.

    Article  CAS  Google Scholar 

  • Soares-da-Silva, I. M., J. Ribeiro, C. Valongo, R. Pinto, M. Vilanova, R. Bleher & J. Machado, 2002. Cytometric, morphologic and enzymatic characterization of haemocytes in Anodonta cygnea. Comp. Biochem Physiol. Part A: Mol. Integr. Physiol. 132: 541–553.

    Google Scholar 

  • Štambuk, A., M. Pavlica, L. Malović & G. Klobučar, 2008. Persistance of DNA damage in the freshwater mussel Unio pictorum upon exposure to ethyl methanesulphonate and hydrogen peroxide. Environmental and Molecular Mutagenesis 49: 217–225.

    Article  PubMed  Google Scholar 

  • Štambuk, A., M. Pavlica, G. Vignjević, B. Bolarić & G. Klobučar, 2009. Assessment of genotoxicity in polluted freshwaters using caged painter’s mussel, Unio pictorum. Ecotoxicology 18: 430–439.

    Article  PubMed  Google Scholar 

  • StatSoft, Inc., 2001. STATISTICA for Windows [Computer program manual]. Tulsa, OK: StatSoft, Inc., http://www.statsoft.com.

  • Sunjog, K., Z. Gačić, S. Kolarević, Z. Višnjić-Jeftić, I. Jarić, J. Knežević-Vukčević, B. Vuković-Gačić, & M. Lenhardt, 2012. Heavy metal accumulation and the genotoxicity in Barbel (Barbus barbus) as indicators of the Danube river pollution. The Scientific World Journal. doi:10.1100/2012/351074.

  • Viarengo, A., D. Lowe, C. Bolognesi, E. Fabbri & A. Koehler, 2007. The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comparative biochemistry and physiology. Toxicology & Pharmacology 146: 281–300.

    CAS  Google Scholar 

  • White, P. & J. B. Rasmussen, 1998. The genotoxic hazard of domestic wastes in surface waters. Mutation Research 410: 223–236.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, J. T., P. L. Pascoe, J. M. Parry & D. R. Dixon, 1998. Evaluation of the comet assay as a method for the detection of DNA damage in the cells of a marine invertebrate, Mytilus edulis L. (Mollusca: Pelecypoda). Mutation Research 399: 87–95.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This research received funding from the European Community’s FP7/2007-2013 Agreement No. 265264.

Author information

Authors and Affiliations

  1. Faculty of Biology, Chair of Microbiology, Centar for Genotoxicology and Ecogenotoxicology, University of Belgrade, Studentski trg 16, 11000, Belgrade, Serbia

    Branka Vuković-Gačić, Stoimir Kolarević, Karolina Sunjog & Jelena Knežević-Vukčević

  2. Institute for Biological Research Siniša Stanković, University of Belgrade, Bulevar Despota Stefana 142, 11060, Belgrade, Serbia

    Jelena Tomović & Momir Paunović

  3. Institute for Multidisciplinary Research, University of Belgrade, Kneza Višeslava 1, 11000, Belgrade, Serbia

    Karolina Sunjog & Zoran Gačić

Authors
  1. Branka Vuković-Gačić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stoimir Kolarević
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karolina Sunjog
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jelena Tomović
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jelena Knežević-Vukčević
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Momir Paunović
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zoran Gačić
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stoimir Kolarević.

Additional information

Guest editors: Manuel P. M. Lopes-Lima, Ronaldo G. Sousa, Simone G. P. Varandas, Elsa M. B. Froufe & Amílcar A. T. Teixeira / Biology and Conservation of Freshwater Bivalves

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vuković-Gačić, B., Kolarević, S., Sunjog, K. et al. Comparative study of the genotoxic response of freshwater mussels Unio tumidus and Unio pictorum to environmental stress. Hydrobiologia 735, 221–231 (2014). https://doi.org/10.1007/s10750-013-1513-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-013-1513-x

Keywords

Search

Navigation