Skip to main content

Advertisement

Log in

Marine pollution risk in a coastal city: use of an eco-genotoxic tool as a stress indicator in mussels from the Eastern Aegean Sea

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Coastal areas, such as bays, estuaries, and harbors, are heavily polluted since these areas are the settlements to which toxic chemicals from industrial and domestic wastes are discharged. The genetic damage was evaluated using bioindicator mussel Mytilus galloprovincialis caused by toxic chemicals (metals and polycyclic aromatic hydrocarbons) in İzmir and Çandarlı Bays (the Eastern Aegean Sea) through comet assay. Three sampling sites from the two bays were selected and the study was conducted during the spring and autumn periods. The highest levels of DNA damage expressed as %Tail-DNA were observed in İzmir Bay (34.60 % Tail-DNA) in the spring. Analysis of the correlation between PAHs and metals in mussels and %T-DNA in the hemolymph and gill cells showed a statistically significant positive correlation between %T-DNA and ∑PAH, chromium (p < 0.05). This study determined the pollution level of the İzmir and Çandarlı Bays by using the DNA damage to the mussel, which can identify the effects of environmental pollutants at the cellular levels. These results confirm that comet assay can be used to determine the temporal and spatial differences of DNA damage, and as a suitable tool for the measurement of genotoxicity in regions with low pollutant concentrations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akcha F, Burgeot T, Narbonne JF, Garrigues P (2003) PAHs: An Ecotoxicological Perspective. Metabolic Activation of PAHs. In: Douben PET (ed) Role of DNA Adduct Formation in Induced Carcinogenesis, Wiley, pp 65–79

  • Almeida C, Pereira C, Gomes T, Bebianno MJ, Cravo A (2011) DNA damage as a biomarker of genotoxic contamination in Mytilus galloprovincialis from the South coast of Portugal. J Environ Monitor 13:2559–2567

    Article  CAS  Google Scholar 

  • Almeida C, Pereira CG, Gomes T, Cardoso C, Bebianno MJ, Cravo A (2013) Genotoxicity in two bivalve species from a coastal lagoon in the south of Portugal. Mar Environ Res 89:29–38

    Article  CAS  Google Scholar 

  • Ameur WB, de Lapuente J, El Megdiche Y, Barhoumi B, Trabelsi S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Driss MR, Borràs M (2012) Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Mar Pollut Bull 64:241–251

    Article  Google Scholar 

  • Andreatis J, Papadopoulou C (1982) A study of the distribution of chromium, cobalt, antimony and zinc in the edible mollusc Meretrix chitane from the Aegean Sea. VIth Rapp Comm Int Mer Médit CIESM, Cannes France, pp 299-303

  • Besada V, Andrade JM, Schultze F, Gonzalez JJ (2011) Comparison of the 2000 and 2005 spatial distributions of heavy metals in wild mussels from the North-Atlantic Spanish Coast. Ecotoxicol Environ Saf 74:373–381

    Article  CAS  Google Scholar 

  • Bhuvaneshwarı R, Babu Rajendran R, Kumar K (2013) Induction of DNA Damage and GADD45β gene Mutation in Zebra fish (Danio rerio) due to Environmentally Relevant Concentrations of Organochlorine Pesticides and Heavy Metals. Int J Environ Res 7(1):219–224

    Google Scholar 

  • Binelli A, Cogni D, Parolini M, Riva C, Provini A (2009) In vivo experiments for the evaluation of genotoxic and cytotoxic effects of Triclosan in Zebra mussel hemocytes. Aquat Toxicol 91:238–244

    Article  CAS  Google Scholar 

  • Brandão F, Cappello T, Raimundo J, Santos MA, Maisano M, Mauceri A, Pacheco M, Pereira P (2015) Unravelling the mechanisms of mercury hepatotoxicity in wild fish (Liza aurata) through a triad approach: bioaccumulation, metabolomic profiles and oxidative stress. Metallomics 7(9):1352–1363

    Article  Google Scholar 

  • Brunelli E, Mauceri A, Maisano M, Bernabò I, Giannetto A, De Domenico E, Corapi B, Tripepi S, Fasulo S (2011) Ultrastructural and immunohistochemical investigation on the gills of the teleost, Thalassoma pavo L. exposed to cadmium. Acta Histochem 113(2):201–213

  • Cappello T, Maisano M, D’Agata A, Natalotto A, Mauceri A, Fasulo S (2013a) Effects of environmental pollution in caged mussels (Mytilus galloprovincialis). Mar Environ Res 91:52–60

    Article  CAS  Google Scholar 

  • Cappello T, Mauceri A, Corsaro C, Maisano M, Parrino V, Lo Paro G, Messina G, Fasulo S (2013b) Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR-based metabolomics. Mar Pollut Bull 77(1-2):132–139

    Article  CAS  Google Scholar 

  • Cappello T, Maisano M, Giannetto A, Parrino V, Mauceri A, Fasulo S (2015) Neurotoxicological effects on marine mussel Mytilus galloprovincialis caged at petrochemical contaminated areas (eastern Sicily, Italy): 1H NMR and immunohistochemical assays. Comp Biochem Physiol C Toxicol Pharmacol 169:7–15

    Article  CAS  Google Scholar 

  • Cappello T, Brandão F, Guilherme S, Santos MA, Maisano M, Mauceri A, Canário J, Pacheco M, Pereira P (2016) Insights into the mechanisms underlying mercury-induced oxidative stress in gills of wild fish (Liza aurata) combining (1)H NMR metabolomics and conventional biochemical assays. Sci Total Environ 548–549:13–24

    Article  Google Scholar 

  • Cevik U, Damla N, Kobyaa AI, Bulut VN, Duran C, Dalgıc G, Bozacı R (2008) Assessment of metal element concentrations in mussel (M. galloprovincialis) in Eastern Black Sea, Turkey. J Hazard Mater 160:396–401

    Article  CAS  Google Scholar 

  • Ciacci C, Barmo C, Gallo G, Maisano M, Cappello T, D‘Agata A, Leonzio C, Mauceri A, Fasulo S, Canesi L (2012) Effects of sub-lethal, environmentally relevant concentrations of hexavalent chromium in the gills of Mytilus galloprovincialis. Aquat Toxicol 120–121:109–118

    Article  Google Scholar 

  • Claxton LD, Houk VS, Hughes TJ (1998) Genotoxicity of industrial wastes and effluents. Mutat Res 410:237–243

    Article  CAS  Google Scholar 

  • Crowe TP, Smith EL, Donkin P, Barnaby DL, Rowland SJ (2004) Measurements of sub-lethal effects on individual organisms indicates community level impacts of pollution. J Appl Ecol 41:114–123

    Article  Google Scholar 

  • D’Agata A, Cappello T, Maisano M, Parrino V, Giannetto A, Brundo MV, Ferrante M, Mauceri A (2014) Cellular biomarkers in the mussel Mytilus galloprovincialis (Bivalvia: Mytilidae) from Lake Faro (Sicily, Italy). Ital J Zool 81(1):43–54

  • Dailianis S, Tsarpali V, Melas K, Karapanagioti HK, Manariotis ID (2014) Aqueous phenanthrene toxicity after high-frequency ultrasound degradation. Aquat Toxicol 147:32–40

    Article  CAS  Google Scholar 

  • Debetto P, Luciani S (1988) Toxic effects of chromium on cellular metabolism. Sci Total Environ 71:365–367

    Article  CAS  Google Scholar 

  • FAO/WHO (2010) Joint FAO/WHO Expert Committee on Food Additives Report of the Seventy-Second Meeting of JECFA in the WHO Technical Report Series, Rome Italy, pp 3–13

  • Fasulo S, Iacono F, Cappello T, Corsaro C, Maisano M, D’Agata A, Giannetto A, De Domenico E, Parrino V, Lo Paro G, Mauceri A (2012a) Metabolomic investigation of Mytilus galloprovincialis (Lamarck 1819) caged in aquatic environments. Ecotoxicol Environ Saf 84:139–146

    Article  CAS  Google Scholar 

  • Fasulo S, Maisano M, Sperone E, Mauceri A, Bernabò I, Cappello T, D’Agata A, Tripepi S, Brunelli E (2012b) Toxicity of Foroozan crude oil to ornate wrasse (Thalassoma pavo, Osteichthyes, Labridae): ultrastructure and cellular biomarkers. Ital J Zool 79(2):182–199

    Article  CAS  Google Scholar 

  • Fernandez-Tajes J, Florez F, Pereira S, Rabade T, Laffon B, Mendez J (2011) Use of three bivalve species for biomonitoring a polluted estuarine environment. Environ Monit Assess 172:301–317

    Article  Google Scholar 

  • Ferrarese E, Andreottola G, Oprea IA (2008) Remediation of PAH contaminated sediments by chemical oxidation. J Hazard Mater 152:128–139

    Article  CAS  Google Scholar 

  • Galgani F, Martínez-Gómez C, Giovanardi F, Romanelli G, Caixach J, Cento A et al (2011) Assessment of polycyclic aromatic hydrocarbon concentrations in mussels (Mytilus galloprovincialis) from the Western basin of the Mediterranean Sea. Environ Monit Assess 177:289–300

    Article  Google Scholar 

  • Gichner T, Mukherjee A, Veleminsky J (2006) DNA staining with the fluorochromes EtBr, DAPI and YOYO-1 in the comet assay with tobacco plants after treatment with ethyl methanesulphonate, hyperthermia and DNase-I. Mutat Res 605:17–21

    Article  CAS  Google Scholar 

  • Halldórsson HP, Ericson G, Svavarsson J (2004) DNA strand breakage in mussels (Mytilus edulis L.) deployed in intertidal and subtidal zone in Reykjavík harbour. Mar Environ Res 58:763–767

    Article  Google Scholar 

  • Héberger K, Kolarevic S, Kracun-Kolarevic M, Sunjog K, Gacic Z, Kljajic Z, Milena Mitric M, Vukovic-Gaci B (2014) Evaluation of single-cell gel electrophoresis data: Combination of variance analysis with sum of ranking differences. Mutat Res 771:15–22

    Article  Google Scholar 

  • JECFA (2005). Summary and Conclusions. Joint FAO/WHO Expert Committee on Food Additives. Sixty-fourth meeting, 8-17 February, Rome, ftp://ftp.fao.org/es/esn/jecfa/jecfa64_summary.pdf

  • Jha AN (2008) Ecotoxicological applications and significance of the comet assay. Mutagenesis 23(3):207–221

    Article  CAS  Google Scholar 

  • Karacik B, Okay OS, Henkelmann B, Bernhoft S, Schramm KW (2009) Polycyclic aromatic hydrocarbons and effects on marine organisms in the Istanbul Strait. Environ Int 35:599–606

    Article  CAS  Google Scholar 

  • Kennish MJ (1998) Pollution in Estuarine and Marine Environments, Pollution Impacts on Marine Biotic Communities. Institute of Marine and Coastal Sciences, Rutgers University, New Jersey, 310p

  • Kleinjans JCS, Van Schooten FJ (2002) Ecogenotoxicology: the evolving field. Environ Toxicol Phar 11:173–179

    Article  CAS  Google Scholar 

  • Klobucar GIV, Pavlica M, Stambuk A, Hylland K, Pavlica M (2008) Detection of DNA damage in haemocytes of Mytilus galloprovincialis in the coastal ecosystems of Kastela and Trogir Bays, Croatia. Sci Total Environ 405:330–337

    Article  CAS  Google Scholar 

  • Kocatas A, Ergen Z, Katağan T, Önen M, Çınar ME, Öztürk B, Doğan A (1997) The Effects of the Pollution on the Distribution of Benthos in the Bay of Izmir. Marine Research in the Izmir Bay, September 17-19 Workshop Abstract, pp 90

  • Koprucu K (2007) Turkiye su urunleri uretiminin durumu ve değerlendirilmesi. Türk Tarım Dergisi 178:22–28 (In Turkish)

    Google Scholar 

  • Kucuksezgin F (2011) The Water Quality of Izmir Bay: A Case Study. R Environ Contam T 211:1–24

    CAS  Google Scholar 

  • Kucuksezgin F, Kacar A, Kucuksezgin G, Uluturhan E (2010) Monitoring metal contamination levels and fecal pollution in clam (Tapes decussatus) collected from Izmir Bay (Turkey). Environ Monit Assess 162(1-4):407–415

    Article  CAS  Google Scholar 

  • Kucuksezgin F, Pazı İ, Yucel-Gier G, Akçalı B, Galgani F (2013) Monitoring of heavy metal and organic compound levels along the Eastern Aegean coast with transplanted mussels. Chemosphere 93:1511–1518

    Article  CAS  Google Scholar 

  • Kumaravel TS, Jha AN (2006) Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutat Res 605:7–16

    Article  CAS  Google Scholar 

  • Langston WJ, Burt GR, Chesman BS (2007) Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals. Marine Ecological Progress Series 333:173–184

    Article  CAS  Google Scholar 

  • Lök A, Acarlı S, Serdar S, Köse A, Yıldız H (2007) Growth and mortality of Mediterranean mussel Mytilus galloprovincialis Lam., 1819, in relation to size on longline in Mersin Bay, Izmir (Turkey–Aegean Sea). Aquac Res 38:819–826

    Article  Google Scholar 

  • Luch A, Baird WM (2005) In: Luch A (ed) Carcinogenic Effects Polycyclic Aromatic Hydrocarbons, Metabolic Activation and Detoxification of Polycyclic Aromatic Hydrocarbons. Imperial College Pres, USA, pp 19–96

    Chapter  Google Scholar 

  • Maanan M (2007) Biomonitoring of heavy metals using M. galloprovincialis in Safi coastal waters, Morocco. Environ Toxicol 22:525–531

    Article  CAS  Google Scholar 

  • MAFF (1995) Monitoring and surveillance of nonradioactive contaminants in the aquatic environment and activities regulating the disposal of wastes at sea. Directorate of Fisheries Research, Lowestoft, Aquatic environment monitoring report, 44

  • Magi E, Bianco R, Ianni C, Di Carro M (2002) Distribution of polycyclic aromatic hydrocarbons in the sediments of the Adriatic Sea. Environ Pollut 119:91–98

    Article  CAS  Google Scholar 

  • Martins M, Costa PM, Ferreira AM, Costa MH (2013) Comparative DNA damage and oxidative effects of carcinogenic and non-carcinogenic sediment-bound PAHs in the gills of a bivalve. Aquat Toxicol 142–143:85–95

    Article  Google Scholar 

  • Monserrat JM, Martínez PE, Laura AG, Amado LL, Martins CMG, Pinho GLL, Chaves IS, Cravo MF, Lima JV, Bianchini A (2007) Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comp Biochem Phy C 146:221–234

    Google Scholar 

  • Moore MN, Depledge MN, Readman JW, Leonard DRP (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res 552:247–268

    Article  CAS  Google Scholar 

  • Narbonne JF, Djomo JE, Ribera D, Ferrier V, Garrigues P (1999) Accumulation kinetics of polycyclic aromatic hydrocarbons adsorbed to sediment by the mollusk Corbicula fluminea. Ecotox Environ Safe 42:1–8

    Article  CAS  Google Scholar 

  • Neser G, Unsalan D, Tekogul N, Stuer-Lauridsen F (2008) The ship breaking industry in Turkey: environmental, safety and health issues. J Clean Prod 16:350–358

    Article  Google Scholar 

  • Official Gazette (2005) TC Ministery of Forestry and Water Affairs. Su Ürünleri Yönetmeliği No: 22223 (In Turkish)

  • Official Gazette (2014) TC Ministery of Forestry and Water Affairs. Hayvan Deneyleri Etik Kurullarının Çalışma Usul ve Esaslarına Dair Yönetmelik 15 February, No: 28914 (In Turkish)

  • Okay OS, Karacık B, Güngördü A, Ozmen M, Yılmaz A, Koyunbaba NC, Yakan SD, Korkmaz V, Henkelmann B, Schramm KW (2014) Micro-organic pollutants and biological response of mussels in marinas and ship building/breaking yards in Turkey. Sci Total Environ 496:165–178

    Article  CAS  Google Scholar 

  • Orbea A, Cajaraville MP (2006) Peroxisome proliferation and antioxidant enzymes in transplanted mussels of four Basque estuaries with different levels of poly-cyclic aromatic hydrocarbon and polychlorinated biphenyl pollution. Environ Toxicol Chem 25:1616–1626

    Article  CAS  Google Scholar 

  • Parlak H, Katalay S, Büyükisik B (1999) Accumulation and Loss of Chromium by Mussels (M. galloprovincialis). B Environ Contam Tox 62:286–292

    Article  CAS  Google Scholar 

  • Petridis P, Jha AN, Langston WJ (2009) Measurements of the genotoxic potential of (xeno-) oestrogens in the bivalve mollusc Scrobicularia plana, using the Comet assay. Aquat Toxicol 94:8–15

    Article  CAS  Google Scholar 

  • Phillips DJH, Rainbow PS (1993) Biomonitoring of Aquatic trace Contaminants. Chapman and Hall, London

    Book  Google Scholar 

  • Qiao M, Wang C, Huang S, Wang D, Wang Z (2006) Composition, sources, and potential toxicological significance of PAHs in the surface sediments of the Meiliang Bay. Taihu Lake, China. Environ Int 32(1):28–33

    Article  CAS  Google Scholar 

  • Rank J, Jensen K, Jespersen PH (2005) Monitoring DNA damage in indigenous blue mussels (Mytilus edulis) sampled from coastal sites in Denmark. Mutat Res 585:33–42

    Article  CAS  Google Scholar 

  • Romeo M, Frasila C, Gnassia-Barelli M, Damiens G, Micu D, Mustata G (2005) Biomonitoring of trace metals in the Black Sea (Romania) using mussels Mytilus galloprovincialis. Water Res 39:596–604

    Article  CAS  Google Scholar 

  • Sponza D, Karaoğlu N (2002) Environmental geochemistry and pollution studies of Aliaga metal industry district. Environ Int 27(7):541–553

    Article  CAS  Google Scholar 

  • Steinert S, Streib-Montee R, Leather JM, Chadwick DB (1998) DNA damage in mussels at sites in San Diego Bay. Mutat Res Fund Mol M 399(1):65–85

    Article  CAS  Google Scholar 

  • Ucuncuoglu E, Arli O, Eronat AH (2006) Evaluating the impact of coastal land uses on water-clarity conditions from Landsat TM/ETM+ imagery: Candarli Bay, Aegean Sea. Int J Remote Sens 27(17):3627–3643

    Article  Google Scholar 

  • UNEP/FAO/IOC/IAEA (1984a) RSRM 7 Sampling of selected marine organisms and sample preparation for trace metal analysis. Reference Methods for Marine Pollution Studies No. 7 Rev. 2, UNEP, 15p

  • UNEP/FAO/IOC/IAEA (1984b) RSRM 11 Determination of total cadmium, zinc, lead and copper in selected marine organisms by flameless atomic absorption spectrophotometry. Reference Methods for Marine Pollution Studies No. 11, UNEP, 18p

  • UNEP/FAO/IOC/IAEA (1984c) RSRM 8 Determination of total mercury in selected marine organism by cold vapour atomic absorption spectrophotometry. Reference Methods for Marine Pollution Studies No. 8 Rev. 1 UNEP, 13p

  • UNEP/FAO/IOC/IAEA (1993) RSRM 6 Guidelines for monitoring chemical contaminants in the sea using marine organisms. Reference Methods for Marine Pollution Studies No. 6 UNEP, 28p

  • Valverde M, Rojas E (2009) Environmental and occupational biomonitoring using the Comet assay. Mutat Res 681:93–109

    Article  CAS  Google Scholar 

  • Wang G, Lu Y, Han J, Luo W, Shi Y, Wang T, Sun Y (2010) Hexachlorobenzene sources, levels and human exposure in the environment of China. Environ Int 36:122–130

    Article  Google Scholar 

  • Wenzl T, Simon R, Anklam E, Kleiner J (2006) Analytical methods for polycyclic aromatic hydrocarbons (PAHs) in food and the environment needed for new food legislation in the European Union. Trends Anal Chem 25:716–725

    Article  CAS  Google Scholar 

  • Wogan GN, Hecht SS, Felton JS, Conney AH, Loeb LA (2004) Environmental and chemical carcinogenesis. Semin Cancer Biol 14:473–486

    Article  CAS  Google Scholar 

  • Yakan SD, Henkelmann B, Schramm KW, Okay OS (2013) Bioaccumulation—Depuration kinetics and effects of phenanthrene on Mediterranean mussel (Mytilus galloprovincialis). J Environ Sci Heal A 48:1037–1046

    Article  CAS  Google Scholar 

  • Yang F, Zhang Q, Guo H, Zhang S (2010) Evaluation of cytotoxicity, genotoxicity and teratogenicity of marine sediments from Qingdao coastal areas using in vitro fish cell assay, comet assay and zebrafish embryo test. Toxicol in Vitro 24:2003–2011

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by The Scientific and Technological Research Council of Turkey (Project number: TUBITAK 113Y540).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Asli Kacar.

Additional information

Responsible editor: Cinta Porte

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kacar, A., Pazi, I., Gonul, T. et al. Marine pollution risk in a coastal city: use of an eco-genotoxic tool as a stress indicator in mussels from the Eastern Aegean Sea. Environ Sci Pollut Res 23, 16067–16078 (2016). https://doi.org/10.1007/s11356-016-6783-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-6783-1

Keywords

Navigation