Skip to main content
SpringerLink
Log in

Assessment of contaminant impacts in a semi-enclosed estuary (Amvrakikos Gulf, NW Greece): Bioenergetics and biochemical biomarkers in mussels

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

A combination of bioenergetics and biochemical biomarkers in mussels was applied to assess possible pollution impacts in a protected semi-enclosed estuary (Amvrakikos Gulf, NW Greece) that receives pesticide discharges through riverine transport. Scope for growth, a physiological condition index representing the energy budget of the organism, was applied to detect general stress effects on the health status of mussels. The low energy budgets of mussels revealed stress conditions and provided early warning signals of possible consequences at higher levels of biological organization. Biochemical markers of exposure confirmed a risk of pesticide contamination. Decreased acetylcholinesterase activities indicated exposure to organophosphate and carbamate pesticides. Responses of the antioxidant enzyme glutathione peroxidase suggested the presence of contaminants capable of reactive oxygen species production that could be related to organochlorine pesticide contamination in the area. On the other hand, metallothionein levels implied low metal contamination.

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

Similar content being viewed by others

References

  • Albanis, T. A., & Hela, D. G. (1998). Pesticide concentrations in Louros river and their fluxes into the marine environment. International Journal of Environmental Analytical Chemistry, 70, 105–120. doi:10.1080/03067319808032608.

    Article  CAS  Google Scholar 

  • Albanis, T. A., Danis, T. G., & Hela, G. H. (1995). Transportation of pesticides in estuaries of Louros and Arachthos rivers (Amvrakikos Gulf, N.W. Greece). The Science of the Total Environment, 171, 85–93. doi:10.1016/0048-9697(95)04667-5.

    Article  CAS  Google Scholar 

  • Bayne, B. L., & Widdows, J. (1978). The physiological ecology of two populations of Mytilus edulis. Oecologia, 37, 137–162. doi:10.1007/BF00344987.

    Article  Google Scholar 

  • Bayne, B. L., Brown, D. A., Burns, K., Dixon, D. R., Ivanovici, A., Livingstone, D. R., et al. (1985). The effects of stress and pollution on marine animals. New York: Praeger.

    Google Scholar 

  • Bocchetti, R., & Regoli, F. (2006). Seasonal variability of oxidative biomarkers, lysosomal parameters, metallothioneins and peroxisomal enzymes in the Mediterranean mussel Mytilus galloprovincialis from Adriatic Sea. Chemosphere, 65, 913–921. doi:10.1016/j.chemosphere.2006.03.049.

    CAS  Google Scholar 

  • Bocquené, G. (1993). Assessment of biological water quality using acetylcholinesterase (ACHE) inhibition measurement. In UNEP/FAO/IOC: Selected techniques for monitoring biological effects of pollutants in marine organisms. MAP technical report Series no. 71. UNEP, Athens (pp 105–111).

  • Bocquené, G., & Galgani, F. (1991). L’acétylcholinésterase chez les organismes marins, outil de surveillance des effets des pesticides organophosphorés et carbamates. Oceanis, 17, 439–448.

    Google Scholar 

  • Bocquené, G., Galgani, F., Burgeot, T., Le Dean, L., & Truquet, P. (1993). Acetylcholinesterase levels in marine organisms along French coasts. Marine Pollution Bulletin, 26, 101–106. doi:10.1016/0025-326X(93)90099-6.

    Article  Google Scholar 

  • Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 772, 248–264. doi:10.1016/0003-2697(76)90527-3.

    Article  Google Scholar 

  • Cossu, C., Doyotte, A., Jacquin, M. C., Babut, M., Exinger, A., & Vasseur, P. (1997). Glutathione reductase, selenium-dependent glutathione peroxidase, glutathione levels and lipid peroxidation in freshwater bivalves, Unio tumidus, as biomarkers of aquatic contamination in field studies. Ecotoxicology and Environmental Safety, 38, 122–131. doi:10.1006/eesa.1997.1582.

    Article  CAS  Google Scholar 

  • Cotou, E., & Papathanassiou, E. (1996). Physiological responses of marine indicator organisms to global pollution. MAP Technical Report Series, 103, 43–55.

    Google Scholar 

  • Cotou, E., Vagias, C., Rapti, T., & Roussis, V. (2001). Metallothionein levels in the bivalves Callista chione and Venus verrucosa from two Mediterranean sites. Zeitschrift fuer Naturforschung, C. Biosciences, 56, 848–852.

    CAS  Google Scholar 

  • Cotou, E., Papathanassiou, E., & Tsangaris, C. (2002). Assessing the quality of marine coastal environments: comparison of scope for growth and Microtox® bioassay results of pollution gradient areas in eastern Mediterranean (Greece). Environmental Pollution, 119, 141–149. doi:10.1016/S0269-7491(01)00337-2.

    Article  CAS  Google Scholar 

  • Doyotte, A., Cossu, C., Jacquin, M. C., Babut, M., & Vasseur, P. (1997). Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalves Unio tumidus. Aquatic Toxicology (Amsterdam, Netherlands), 39, 93–110. doi:10.1016/S0166-445X(97)00024-6.

    CAS  Google Scholar 

  • Ellman, G. L. (1958). A colorimetric method for determining low concentrations of mercaptans. Archives of Biochemistry and Biophysics, 74, 443–450. doi:10.1016/0003-9861(58)90014-6.

    Article  CAS  Google Scholar 

  • Ellman, G. L., Courtney, K. D., Andres, V., Jr, & Featherstone, R. M. (1961). A new and rapid colorimeric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7, 88–95. doi:10.1016/0006-2952(61)90145-9.

    Article  CAS  Google Scholar 

  • El-Shenawy, N. S., Greenwood, R., Ismail, M., Abdel-Nabi, I. M., & Nabil, Z. I. (2006) Effect of atrazine and lindane on the scope for growth of marine mussel Mytilus edulis. Acta Zoologica Sinica, 52(4), 712–723.

    CAS  Google Scholar 

  • Escartin, E., & Porte, C. (1997). The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environmental Toxicology and Chemistry, 16, 2090–2095. doi:10.1897/1551-5028(1997)016<2090:TUOCAC>2.3.CO;2.

    Article  CAS  Google Scholar 

  • Gamble, S. C., Goldfarb, P. S., Porte, C., & Livingstone, D. R. (1995). Glutathione peroxidase and other antioxidant enzyme function in marine invertebrates (Mytilus edulis, Pecten maximus, Carcinus maenas and Asterias rubens). Marine Environmental Research, 39, 191–195. doi:10.1016/0141-1136(94)00031-J.

    Article  CAS  Google Scholar 

  • Gnaiger, E. (1983). Heat dissipation and energetic efficiency in animal anoxibiosis: economy contra power. The Journal of Experimental Zoology, 228, 471–490. doi:10.1002/jez.1402280308.

    Article  CAS  Google Scholar 

  • Guelorget, O., Frisoni, G. F., Monti, D., & Perthuisot, J. P. (1986). Contribution a l’etude ecologique des lagunes septentrionales de la baie d’Amvrakia (Grece). Oceanologica Acta, 9, 9–17.

    Google Scholar 

  • Hatzianestis, J., Sklivagou, E., & Georgakopoulou, E. (2001). Levels of chlorinated compounds in marine organisms from Greek waters. In Proceedings of the 7th international conference on environmental science and technology, Ermoupolis, Syros I, Greece, 3–6 September (Vol. 1, pp. 310–317).

  • Hela, D. G., Albanis, T., & Anafnostou, C. (2000). Concentration levels of pesticide residues in coastal sediments of Amvrakikos Gulf. In Proceedings of the 6th Hellenic symposium on oceanography and fisheries, Chios, Greece, 23–26 May (Vol. 1, pp. 517–522).

  • Ivankoviċ, D., Pavièic, J., Erk, M., & Filipovic-Marijic, V. (2005). Evaluation of the Mytilus galloprovibciallis Lam. digestive gland metallothionein as a biomarker in a long term field study: Seasonal and spatial variability. Marine Pollution Bulletin, 50, 1303–1313. doi:10.1016/j.marpolbul.2005.04.039.

    Article  Google Scholar 

  • Karageorgis, A. P., & Hatzianestis, I. (2003). Surface sediment chemistry in the Olympic Games 2004 Sailing Center (Saronikos Gulf). Meditterannean Marine Science, 4, 5–22.

    Google Scholar 

  • Lemaire, P., & Livingstone, D. R. (1993). Pro-oxidant/antioxidant processes and organic xenobiotic interactions in marine organisms, in particular the flounder Platicthys flesus and the mussel Mytilus edulis. Trends in Comparative Biochemistry and Physiology, 1, 119–1150.

    Google Scholar 

  • Livingstone, D. R. (2001). Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42, 656–666. doi:10.1016/S0025-326X(01)00060-1.

    Article  CAS  Google Scholar 

  • Livingstone, D. R., Lips, F., Garcia Martinez, P., & Pipe, R. K. (1992). Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Marine Biology (Berlin), 112, 265–276. doi:10.1007/BF00702471.

    Article  CAS  Google Scholar 

  • Mackay, E. A., Overnell, J., Dumbar, B., Davindson, I., Hunziker, P. E., Kägi, J. H., et al. (1993). Complete amino acid sequences of five dimeric and four monomeric forms of metallothionein from the edible Mytilus edulis. European Journal of Biochemistry, 218, 183–194. doi:10.1111/j.1432-1033.1993.tb18364.x.

    Article  CAS  Google Scholar 

  • Moreira, S. M., & Guilhermino, L. (2005). The use of Mytilus galloprovincialis acetylcholinesterase and glutathione S-transferases activities as biomarkers of environmental contamination along the Northwest Portuguese coast. Environmental Monitoring and Assessment, 105, 309–325. doi:10.1007/s10661-005-3854-z.

    Article  CAS  Google Scholar 

  • National Center for Marine Research (2000). Development and implementation of new techniques for pollution control, protection and management of Amvrakikos Gulf. PENED project 360, Final Report, Athens.

  • Nesto, N., Bertoldo, M., Nasci, C., & Da Ros, L. (2004). Spatial and temporal variation of biomarkers in mussels (Mytilus galloprovincialis) from the Lagoon of Venice, Italy. Marine Environmental Research, 58, 287–291. doi:10.1016/j.marenvres.2004.03.073.

    Article  CAS  Google Scholar 

  • Nicolaidou, A., Petrou, K., Kormas, K. A., & Reizopoulou, S. (2006). Inter-annual variability of soft bottom macrofaunal communities in two Ionian Sea Lagoons. Hydrobiologia, 555, 89–98. doi:10.1007/s10750-005-1108-2.

    Article  Google Scholar 

  • Raspor, B., Dragun, Z., Erk, M., Ivankoviċ, D., & Pavičiċ, J. (2004). Is the digestive gland of Mytilus galloprovincialis a tissue of choice for estimating cadmium exposure by means of metallothioneins? The Science of the Total Environment, 333, 99–108. doi:10.1016/j.scitotenv.2004.05.008.

    Article  CAS  Google Scholar 

  • Readman, J. W., Albanis, T. A., Barcelo, D., Galassi, S., Tronczynski, J., & Gabrielides, G. E. (1993). Herbicide contamination of mediterranean estuarine waters: Results from a MED POL pilot survey. Marine Pollution Bulletin, 26, 613–619. doi:10.1016/0025-326X(93)90500-J.

    Article  CAS  Google Scholar 

  • Reid, D. J., & Mac Farlane, G. R. (2003). Potential biomarkers of crude oil exposure in the gastropod mollusc Austrocochlea porcata: Laboratory and manipulative field studies. Environmental Pollution, 123, 147–155. doi:10.1016/S0269-7491(03)00209-4.

    Article  Google Scholar 

  • Reizopoulou, S., Thessalou-Legaki, M., & Nicolaidou, A. (1996). Assessment of disturbance in Mediterranean lagoons: An evaluation of methods. Marine Biology (Berlin), 125, 189–197. doi:10.1007/BF00350773.

    Article  Google Scholar 

  • Sheehan, D., & Power, A. (1999). Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comparative Biochemistry and Physiology, 123C, 193–199.

    CAS  Google Scholar 

  • Solé, M., Porte, C., & Albaiges, J. (1994). Mixed function oxygenase components and antioxidant enzymes in different marine bivalves: Its relation with contaminant body burdens. Aquatic Toxicology (Amsterdam, Netherlands), 30, 271–283. doi:10.1016/0166-445X(94)90064-7.

    Google Scholar 

  • Solé, M., Porte, C., & Albaiges, J. (1995). Seasonal variation in the mixed-function oxygenase system and antioxidant enzymes of the mussel Mytilus galoprovonciallis. Environmental Toxicology and Chemistry, 14, 157–164. doi: 10.1897/1552-8618(1995)14[157:SVITMO]2.0.CO;2.

    Article  Google Scholar 

  • Tsangaris, C., Strogyloudi, E., & Papathanassiou, E. (2004). Measurement of biochemical markers of pollution in mussels Mytilus galloprovincialis from coastal areas of the Saronicos Gulf (Greece). Mediterranean Marine Science, 5(1), 175–186.

    Google Scholar 

  • Tsangaris, C., Papathanassiou, E., & Cotou, E. (2007). Assessment of the impact of heavy metal pollution from a ferro-nickel smelting plant using biomarkers. Ecotoxicology and Environmental Safety, 66, 232–243. doi:10.1016/j.ecoenv.2006.03.011.

    Article  CAS  Google Scholar 

  • Viarengo, A., Ponzano, E., Dondero, F., & Fabbri, R. (1997). A simple spectrophotometric method for metallothionein evaluation in marine organisms: application to mediterranean and antartic molluscs. Marine Environmental Research, 44, 69–84. doi:10.1016/S0141-1136(96)00103-1.

    Article  CAS  Google Scholar 

  • Viarengo, A., Burlando, B., Dondero, F., Marro, A., & Fabbri, R. (1999). Metallothionein as a tool in biomonitoring programmes. Biomarkers, 4, 455–466. doi:10.1080/135475099230615.

    Article  CAS  Google Scholar 

  • Viarengo, A., Lowe, D., Bolognesi, C., Fabbri, E., & Koehler, A. (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, 146(Part C), 281–300.

    CAS  Google Scholar 

  • Widdows, J., & Donkin, P. (1992). Mussels and environmental contaminants: Bioaccumulation and physiological aspects. In E. M. Gosling (Ed.), The mussel Mytilus: Ecology, physiology, genetics and culture (pp. 383–424). Amsterdam: Elsevier.

    Google Scholar 

  • Widdows, J., & Salked, P. (1993). Practical procedures for measurement of Scope for Growth. In UNEP/FAO/IOC: Selected Techniques for monitoring biological effects of pollutants in marine organisms. MAP technical report series no. 71. UNEP, Athens (pp 147–172).

  • Widdows, J., Fieth, P., & Worrall, C. M. (1979). Relationships between seston, available food and feeding activity in the common mussel Mytilus edulis. Marine Biology (Berlin), 50, 195–207. doi:10.1007/BF00394201.

    Article  CAS  Google Scholar 

  • Widdows, J., Donkin, P., Brinsley, M. D., Evans, S. V., Salked, P. N., Franklin, A., et al. (1995). Scope for growth and contaminant levels in North Sea mussels Mytilus edulis. Marine Ecology Progress Series, 127, 131–148. doi:10.3354/meps127131.

    Article  CAS  Google Scholar 

  • Widdows, J., Nasci, C., & Fossato, V. U. (1997). Effects of pollution on the scope for growth of mussels (Mytilus galloprovincialis) from the Venice Lagoon. Italy. Marine Environmental Research, 43, 69–79. doi:10.1016/0141-1136(96)00003-7.

    Article  CAS  Google Scholar 

  • Widdows, J., Donkin, P., Staff, F. J., Matthiessen, P., Law, R. J., Allen, Y. T., et al. (2002). Measurement of stress effects (scope for growth) and contaminant levels in mussels (Mytilus edulis) collected from the Irish Sea. Marine Environmental Research, 53, 327–356. doi:10.1016/S0141-1136(01)00120-9.

    Article  CAS  Google Scholar 

  • Winston, G. W., & Di Giulio, R. T. (1991). Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology (Amsterdam, Netherlands), 19, 137–161. doi:10.1016/0166-445X(91)90033-6.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Oceanography, Hellenic Center for Marine Research (HCMR), 46.7 km, Athinon–Souniou Avenue, P.O. Box 712, 190 13, Anavyssos, Greece

    Catherine Tsangaris & Enangelos Papathanassiou

  2. Institute of Aquaculture, Hellenic Center for Marine Research (HCMR), Agios Kosmas, 16610, Elliniko, Greece

    Efthimia Cotou

  3. Department of Zoology–Marine Biology, University of Athens, Panepistimioupolis, 15784, Athens, Greece

    Artemis Nicolaidou

Authors
  1. Catherine Tsangaris
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Efthimia Cotou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enangelos Papathanassiou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Artemis Nicolaidou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Catherine Tsangaris.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsangaris, C., Cotou, E., Papathanassiou, E. et al. Assessment of contaminant impacts in a semi-enclosed estuary (Amvrakikos Gulf, NW Greece): Bioenergetics and biochemical biomarkers in mussels. Environ Monit Assess 161, 259–269 (2010). https://doi.org/10.1007/s10661-008-0743-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-008-0743-2

Keywords

Search

Navigation