Sediment quality of the ecoregion Engure, Gulf of Riga, assessed by using ecotoxicity tests and biomarker responses

Open access


The aim of this study was to assess sediment quality in the ecoregion Engure, western coast of the Gulf of Riga, by using sediment ecotoxicity tests with amphipods Monoporeia affinis and Pontogammarus robustoides and selected biomarkers (AChE, GST, GR, CAT, MT) measured in Macoma balthica, to represent different types of biological responses reacting to different stressors. Ecoregion Engure sediments are characterised by comparatively low concentrations of heavy metals, and the area could be considered as unpolluted. Ecotoxicity tests of ecoregion Engure sediments did not show statistically significant (> 20% mortality) toxic effects. Survival of test organisms ranged from 83 to 100% and revealed “good quality” of tested sediment. There were no established strong differences between the stations and years regarding biomarkers. The integrated biomarker response index indicated more stressful conditions in station Mērsrags, while MT activity revealed heavy metal pollution in station Engure. In general, heavy metal concentrations, ecotoxicity tests and biomarker responses indicate that the ecoregion Engure is not markedly various and anthropogenically affected.

Akcha, F., Izuel, C., Venier, P., Budzinski, H., Burgeot, T., Narbonne J.-F. (2000). Enzymatic biomarker measurement and study of DNA adduct formation in benzo[a]pyrene-contaminated mussels, Mytilus galloprovincialis. Aquat. Toxicol., 49, 269-287.

Anonymous (1993). Society of Environmental Toxicology and Chemistry. Guidance document on sediment toxicity assessment for freshwater and marine environments. In: Hill, I. R., Matthiessen, P., Heinbach F. (eds.). Workshop on Sediment Toxicity Assessment, Renesse, The Netherlands, 8-10 November 1993 (105 pp.). SETAC-Europe, Brussels.

Anonymous (1996). Microwave assisted digestion of siliceous and organically based matrices (Method 3052). Revision 0 (December 1996). In: Test Methods for Evaluating Solid Wastes: Physical/Chemical Methods, EPA SW-846, Third Ed., Vol. I, Section A, Chapter 3 (Inorganic Analytes), pp. 3052-1-3052-20, U.S. Environmental Protection Agency, Office of Solid Waste and Emergency Response, Washington, D.C. Available at: Anonymous (1997). JAMP (Joint Assessment and Monitoring Programme) Guidelines for General Biological Effects Monitoring (OSPAR Agreement 1997-7). OSPAR Commission. 22 pp (at pp. 1-12).

Anonymous (2000). Methods for Measuring the Toxicity and Bioaccumulation of Sediment Associated Contaminants with Freshwater Invertebrates. 2nd edition. Report EPA 600/R-99/064 March 2000. Washington, DC: United States Environmental Protection Agency. 212 pp.

Anonymous (2005). International Standards Organization Water Quality - Determination of Acute Toxicity of Marine and Estuarine Sediments to Amphipods. ISO/CD 16712:2005(E). First Edition. TC 147/SC5/WG2. 16 pp.

Anonymous (2006). Cabinet Regulation No. 475. Procedures regarding the Cleaning and Deepening of Surface Water Bodies and Port Basins.

Anonymous (2009a). Assessment of the Impact of Shipping on the Marine Environment. Prepared by Ware, K. OSPAR Commission. 34 pp.

Anonymous (2009b). Losses of Contaminants from Ships’ Coatings and Anodes. A Study Relating to the Netherlands Continental Shelf and the North Sea. Prepared by Tak, van der C. OSPAR Commission. 27 pp.

Anonymous (2010). Hazardous substances in the Baltic Sea-an integrated thematic assessment of hazardous substances in the Baltic Sea. Balt. Sea Environ. Proc., 120B, 1-119.

Barda, I., Purina, I., Rimsa, E., Balode, M. (2014). Seasonal dynamics of biomarkers in infaunal clam Macoma balthica from the Gulf of Riga (Baltic Sea). J. Mar. Syst., 1, 150-156.

Bat, L. (1998). Influence of sediment on heavy metal uptake by the polychaete Arenicola marina. Turkish J. Zool., 22 (4), 341-350.

Baturin, G. N., Dubinchuk V. T. (2009). Composition of ferromanganese nodules from Riga Bay (Baltic Sea). Oceonology (Marine Geology), 49 (1), 121-130.

Bellan-Santini, D. (1980). Relationship between populations of amphipods and pollution. Mar. Pollut. Bull., 11, 224-227.

Beliaeff, B., Burgeot, T. (2002). Integrated biomarker response (IBR): A useful graphical tool for ecological risk assessment. Environ. Toxicol. Chem., 21, 1316-1322.

Berezina, N. A., Strode, E., Lehtonen, K. K., Balode, M., Golubkov, S. M. (2013). Sediment quality assessment using Gmelinoides fasciatus and Monoporeia affinis (Amphipoda, Gammaridea) in the northeastern Baltic Sea. Crustaceana, 86, 780-801.

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.

Bocquene, G., Galgani, F. (1998). Biological effects of contaminants: Cholinesterase inhibition by organophosphate and carbamate compounds. ICES Tech. Mar. Environ. Sci., 22, 1-12.

Bocquene, G., Galgani, F. (1998). Biological effects of contaminants: cholinesterase inhibition by organophosphate and carbamate compounds. ICES Tech. Mar. Environ., Sci., 22, 1-12.

Bocquene, G., Galgani, F., Truquet, P. (1990). Characterization and assay conditions for use of ACHe activity from several marine species in pollution monitoring. Mar. Environ. Res., 30 (2), 75-89.

Borgmann, U., Norwood, W. P., Nowierski, M. (2005). Amphipod (Hyalella azteca) solid-phase toxicity test using high water-sediment ratios. In: Small-scale Freshwater Toxicity Investigations Toxicity Test Methods (pp. 413-436). Blaise, C., Ferard, J.-F. (eds.). Netherlands: Springer.

Bradford, M. M. (1976). A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem., 72, 248-254.

Broeg, K., Lehtonen K. K. (2006). Indices for the assessment of environmental pollution of the Baltic Sea coasts: Integrated assessment of a multi-biomarker approach. Mar. Poll. Bull., 53, 508-522.

Cairns, J. J., Mount, D. I. (1990). Aquatic toxicology. Part 2. Environ. Sci. Technol., 24, 154-161.

Carlberg, I., Mannervik, B. (1985). Glutathione reductase. Meth. Enzymol., 113, 485-490.

Cazenave, J., Bacchetta, C., Parma, M. J., Scarabotti, P. A., Wunderlin, D. A. (2009). Multiple biomarkers responses in Prochilodus lineatus allowed assessing changes in the water quality of Salado River basin (Santa Fe, Argentina). Environ. Poll., 157, 3025-3033.

Cederwall, H. (1977). Annual macrofauna production of a soft bottom in the northern Baltic Proper. In: Keegan, B. F., Ceidigh, P. O., Boaden, P. J. S. (eds.). Biology of Benthic Organisms. Proceedings of the 11th European Marine Biology Symposium, Galway, October 1976 (pp. 155-164). Oxford: Pergamon Press.

Chapman, P. M., Long, E. R. (1983). The use of bioassays as part of a comprehensive approach to marine pollution assessment. Mar. Poll. Bull., 14, 81-84.

Claiborne, A. (1985). Catalase activity. In: Greenwald, R. A. (Ed.). Handbook of Methods for Oxygen Radical Research (pp. 283-284). Boca Raton, Florida: CRC Press.

Dellali, M., Gnassia Barelli, M., Romeo, M., Aissa, P. (2001). The use of acetylcholinesterase activity in Ruditapes decussatus and Mytilus galloprovincialis in the biomonitoring of Bizerta lagoon. Comp. Biochem. Physiol., C 130, 227-235.

Damiens, G., Gnassia-Barelli, M., Loquès, F., Roméo, M., Salbert, V. (2007). Integrated biomarker responses index as a useful tool for environmental assessment evaluated using transplanted mussels. Chemosphere, 66, 574-583.

Di Giulio, R. T., Wasburn, P. C., Wenning, R. J., Winston, G.W., Jewell, C. S. (1989). Biochemical responses in aquatic animals: A review of determinants of oxidative stress. Environ. Toxicol. Chem., 8, 1103-1123.

Ellman, G. L., Courtney, K. O., Andrres, V., Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol., 7, 88-95.

Ferreira, M., Moradas-Ferreira, P., Reis-Henriques, M. A. (2005). Oxidative stress biomarkers in two resident species, mullet (Mugil cephalus) and flounder (Platichthys flesus), from a polluted site in River Douro Estuary Portugal. Aquat. Toxicol., 71, 39-48.

Fitzpatrick, P. J., O’Halloran, J., Sheehan, D., Walsh, A. R. (1997). Assessment of a glutathione S-transferase and related proteins in the gill and digestive gland of Mytilus edulis (L.), as potential organic pollution biomarkers. Biomarkers, 2, 51-56.

Fjodorova, R. (2009). Katram savs ceïð ejams [Everybody has one’s own way to go]. Grâm: Freiberga, A. (red.). Latvijas Jûrniecîbas gadagrâmata 2008 [Latvian Maritime Yearbook 2008] (352.-358. lpp.). Rîga: Latvijas Jûrniecîbas savienîba (in Latvian).

Fulton, M. H., Key, P. B. (2001). Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticides exposure and effects. Envion. Toxicol. Chem., 20, 37-45.

George, S. G., Olsson, P. E. (1994). Metallothioneins as indicators of trace metal pollution. In: Kramer, K. J. M. (Ed.). Biomonitoring of Coastal Waters and Estuaries (pp. 151-178). Boca Raton, FL: CRC Press. Glasby, G. P., Emelyanov, E. M., Zhamoida, V. A., Baturin, G. N., Leipe, T., Bahlo, R., Bonacker, P. (1997). Environments of formation of ferromanganese concretions in the Baltic Sea: A critical review. In: Nicholson, K., Hein, J. R., Bühn, B., Dasgupta, S. (eds.). Manganese, Mineralization: Geochemistry and Mineralogy of Terrestrial and Marine Deposits. Geological Society Special Publication, Vol. 119 (pp. 213-237). London.

Guilhermino, L., Barros, B., Silva, M. C., Soares, A. M. V. M. (1998). Should the use of inhibition of cholinesterases as a specific biomarker for organophosphate and carbamate pesticides be questioned? Biomarkers, 3, 157-163.

Habig, W. H., Pabst, M. J., Jakoby, W. B. (1974). Glutathione S-transferases - the first enzymatic step in mercapturic acid formation. J. Biol. Chem., 249, 7130-7139.

Hansen, P. D. (2003). Biomarkers. In: Markert, B. A., Breure, A. M., Zechmeister, H. G. (eds.). Bioindicators and Biomonitors (pp. 203-220). Oxford: Elsevier Science Ltd.

Hay, M. E., Stachowicz, J., Cruz-Rivera, E., Bullard, S., Deal, M. S., Lindquist, N. (1998). Bioassays with marine and freshwater macroorganisms.

In: Haynes, K. F., Millar, J. G. (eds.). Methods in Chemical Ecology. 2. Bioassay Methods (pp. 39-141). New York: Chapman and Hall.

Ingersoll, C. G. (1995). Sediment tests. In: Fundamentals of Aquatic Toxicology. 2nd edn. Effects, Environmental Fate, and Risk Assessment (pp. 231-255). Rand, G. M. (Ed.). Washington D.C.: Taylor and Francis Publ.

John, D. A., Leventhal, J. S. (1995). Bioavailability of metals. Ch. 2. In: Preliminary Compilation of Descriptive Geoenvironmental Mineral Deposit Models (pp. 10-19). Edward A. du Bray (Ed.). Denver, Colorado: U.S. Department of the Interior U.S. Geological Survey.

Kankaanpää, H., Vuorinen, P., Sipiä, V., Keinänen, M. (2002). Acute effects of Nodularia spumigena and bioaccumulation of nodularin to brown trout (Salmo trutta L.) under laboratory conditions. Aquat. Toxicol., 61, 155-168.

Kruschwitz, L. G. (1987). Environmental factors controlling reproduction of the amphipod Hyalella azteca. Proc. Okla. Acad. Sci., 58, 16-21.

Kulikova, I., Seisuma, Z. (2005). Spatial and temporal distribution of metal in sediments of the Gulf of Riga (the Baltic Sea). Ekologija (Lithuania), 2, 6-10.

Lehtonen, K. K., Leinio, S., Schneider, R., Leivuori, M. (2006). Biomarkers of pollution effects in the bivalves Mytilus edulis and Macoma balthica collected from the southern coast of Finland (Baltic Sea). Mar. Ecol. Prog. Ser., 322, 155-168.

Lehtonen, K. K., Kankaanpää, H., Leinio, S., Sipia, V. O., Pflugmacher, S., Sandberg-Kilpi, E. (2003). Accumulation of nodularin-like compounds from the cyanobacteria Nodularia spumigena and changes in acetylcholinesterase activity in the clam Macoma balthica during short-term laboratory exposure. Aquat. Toxicol., 64, 461-476.

Lehtonen, K. K. (2004). Seasonal variations in the physiological condition of the benthic amphipods Monoporeia affinis and Pontoporeia femorata in the Gulf of Riga (Baltic Sea). Aquatic Ecol., 38 (3), 441-456.

Leiniö, S., Lehtonen, K. K. (2005). Seasonal variability in biomarkers in the bivalves Macoma balthica and Mytilus edulis from the northern Baltic Sea. Comp. Biochem. Physiol., C 40, 408-421.

Livingstone, D. R. (2001). Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar. Pollut. Bull., 42, 656-666.

Livingstone, D. R., Lips, F., Garcia Martinez, P., Pipe, R. K. (1992). Antioxidant enzymes indigestive gland of the common mussel, Mytilus edulis L. Mar. Biol., 112, 265-276.

Luoma, S. N., Ho, K. T. (1993). The appropriate uses of marine and estuarine sediment bioassays. In: The Handbook of Ecotoxicology (pp. 193-226). Calow, P. (ed.). Oxford: Blackwell.

Luoma, S. N. (1983). Bioavailability of trace metals to aquatic organisms: A review. Sci. Total Environ., 28, 1-22.

Manduzio, H., Monsinjon, T., Galap, C., Leboulenger, F., Rocher, B. (2004). Seasonal variations in antioxidant defenses in blue mussels Mytilus edulis collected from a polluted area: Major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat. Ecol., 70, 83-93.

Massy, V., Williams, C. H. (1965). On the reaction mechanism of yeast glutathione reductase. J. Biol. Chem., 240, 4470-4481.

Martin-Diaz, M. L., Blasco, J., Sales, D., Del Valls, T. A. (2008). Field validation of a battery of biomarkers to assess sediment quality in Spanish ports. Environ. Poll., 151, 631-640.

Paris-Palacios S., Biagianti-Risbourg S., Vernet G. (2000). Biochemical and (ultra)structural hepatic perturbations of Brachydanio rerio (Teleostei, Cyprinidae) exposed to two sublethal concentrations of copper sulfate. Aquat. Toxicol., 50, 109-124.

Pfeifer, S., Schiedek, D., Dippner, J. (2005). Effect of temperature and salinity on acetylcholinesterase activity, a common pollution biomarker, in Mytilus sp. from the south-western Baltic Sea. J. Exp. Mar. Biol. Ecol., 320, 93-103.

Poikâne, R. (2008). The role of suspended particulate matter and sediment in the dynamics of metals in the gulf of Riga. Doctoral Thesis. University of Latvia, Rîga. 157 pp.

Rand, G. M., Wells, P. G., McCarty, L. S. (1995). Introduction to aquatic toxicology. In: Fundamentals of Aquatic Toxicology. 2nd edn. Effects, Environmental Fate, and Risk Assessment (pp. 3-67). Rand, G. M. (Ed.). Washington D.C.: Taylor and Francis Publ.

Reynoldson, T. B., Day, K. E. (1993). Freshwater sediments. In: Handbook of Ecotoxicology, Vol. 1 (pp. 83-100). Calow, P. (Ed.). London: Oxford Blackwell Scientific Publishers.

Reynoldson, T. B. (1987). Interactions between sediment contaminants and benthic organisms. In: Thomas, R., Evans, R., Hamilton, A., Munavar, M., Reynoldson, T., Sadar H. (eds.). Ecological Effects in situ Sediment Contaminants. Dr. W. Junk Publishers. Reprinted from: Hydrobiologia, 149, 53-66.

Robillard, S., Beauchamp, G., Laulier, M. (2003). The role of abiotic factors and pesticide levels on enzymatic activity in the freshwater mussel Anadonta cygnea at three different exposure sites. Comp. Biochem. Physiol., C 135, 49-59.

Roméo, M., Hoarau, P., Garello, G., Gnassia-Barelli, M., Girard, J. P. (2003). Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environ. Poll., 122, 369-378.

Seisuma, Z., Kulikova, I. (2012). Distribution of metal concentrations in sediments of the coastal zone of the Gulf of Riga and open part of the Baltic Sea. Oceanology, 52 (6), 780-784.

Sherrat, P. J., Hayes, J. D. (2002). Glutathione-S-transferases. In: Ioanides, C. (Ed.). Enzyme Systems that Metabolize Drugs and Other Xenobiotics (pp. 319-352). John Wiley & Sons, LTD.

Stiebriṇš, O., Väling, P. (1996). Bottom Sediments of the Gulf of Riga. Riga, 54 pp.

Stokenberga, D. (2012). Mçrsraga osta plâno jaunus attîstîbas virzienus [Mçrsrags Port plans new development directions]. Grâm.: Freiberga, A. (red.). Latvijas Jûrniecîbas gadagrâmata 2011 [Latvian Maritime Yearbook 2011] (430.-431. lpp.]. Rîga: Latvijas Jûrniecîbas savienîba (in Latvian).

Strâķe, S., Poikâne, R., Putna, I., Pfeifere, M., Jansons, M., Balode, M., Nakari, T., Sainio, P., Schultz, E., Munne, P. (2011). WP3 Innovative Approaches to Chemical Control of Hazardous Substances: National Report of Latvia. Rîga: Latvian Institute of Aquatic Ecology. 75 pp.

Strode, E., Balode, M. (2013). Toxico-resistance of Baltic amphipod species to heavy metals. Crustaceana, 86 (7-8), 1007-1024. Swartz, R. C., Ditsworth, G. R., Schults, D. W., Lamberson, J. O. (1985a) Sediment toxicity to a marine infaunal amphipod: Cadmium and its interaction with sewage sludge. Mar. Environ. Res., 18, 133-153.

Swartz, R. C., De Ben, W. A., Jones, J. K. P., Lamberson, J. O., Cole, F. A. (1985b). Phoxocephalid amphipod bioassay for marine sediment toxicity. In: Cardwell, R. D., Purdy, R., Bahner, R. C. (eds.). Aquatic Toxicology and Hazard Assessment: Seventh Symposium. ASTM STP 854 (pp. 284-307). Philadelphia, PA: American Society for Testing and Materials.

Swartz, R. C., Deben, W. A., Sercu, K. A., Lamberson, J. O. (1982). Sediment toxicity and the distribution of amphipods in Commencement Bay, Washington. Mar. Pollut. Bull., 13, pp. 359-364.

Torres, M. A., Testa, C. P., Gáspari, C., Masutti, M. B., Panitz, C. M. N., Curi-Pedrosa, R., Alves de Almeida, E., Di Mascio, P., Filho, D.W. (2002). Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Mar. Poll. Bull., 44, 923-932.

Trautmann, N. M., Carlsen, W. C., Krasny, M. E., Cunningham, C. M. (2001). Assessing Toxic Risk: Student Edition and Teacher’s Guide. Arlington, VA: National Science Teachers Association. 106 pp.

Tsangaris, C., Cotou, E., Papathanassiou, E., Nicolaidou, A. (2010). Assessment of contaminant impacts in a semi-enclosed estuary (Amvrakikos Gulf, NWGreece): Bioenergetics and biochemical biomarkers in mussels. Environ. Monit. Assess., 161, 259-269.

Van der Oost, R., Beyer, J., Vermeulen, N. P. E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environ. Toxicol. Pharmacol., 13, 57-149.

Verlecar, X. N., Jena, K. B., Chainy, G. B. N. (2008). Seasonal variation of oxidative biomarkers in gills and digestive gland of green-lipped mussel Perna viridis from Arabian Sea. Est. Coastal Shelf Sci., 76, 745-752.

Viarengo, A., Ponzano, E., Dondero, F., Fabbri, R. (1997). A simple spectrophotometric method for metallothionein evaluation in marine organisms: An application to Mediterranean and Antarctic molluscs. Mar. Environ. Res., 44, 69-84.

Viarengo, A., Burlano, B., Dondero, F., Marro, A., Fabbro, R. (1999). Metallothionein as a tool in biomonitoring programmes. Biomarkers, 4, 455-466

Viarengo, A., Burlando, B., Ceratto, N., Panfoli, I. (2000). Antioxidant role of metallothioneins: A comparative overview. Cell. Mol. Biol. (Noisy-le-grand), 46, 407-417.

Widdows, J. (1993). Marine and estuarine invertebrate toxicity tests. In: Calow, P. (ed.). Handbook of Ecotoxicology. Vol. 1 (pp. 145-166). London: Oxford Blackwell Science Publoshers.

Wiklund, E. A.-K., Vilhelmsson, S., Wiklund, J. S., Eklund, B. (2009). Contaminants and habitat choice in the Baltic Sea: Behavioural experiments with the native species, Monoporeia affinis, and the invasive genus, Marenzelleria. Estuarine, Coastal Shelf Sci., 81 (2), 238-246.

Zhong, H., Kraemer, L., Evans, D. (2013). Influence of contact time and sediment composition on the bioavailability of Cd in sediments. Environ. Poll. 173, 11-16.

Journal Information

CiteScore 2017: 0.22

SCImago Journal Rank (SJR) 2017: 0.127
Source Normalized Impact per Paper (SNIP) 2017: 0.211

Cited By


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 189 189 10
PDF Downloads 53 53 6