Abstract
Toxin-producing cyanobacteria in lakes and reservoirs form a threat to humans as well as various forms of aquatic life. This study examined the occurrence and distribution of Microcystins (MCYST) in the shallow eutrophic lake Pamvotis (Greece). MCYST concentrations in the tissues (liver, kidneys, intestine, gonads, brain and muscle) of the fish species Carassius gibelio were also examined. Tests were performed with an enzyme-linked immunosorbent assay (ELISA). MCYST concentration in water and in the scum of Lake Pamvotis were highest during the warm period (April—October, 2005). Phytoplankton samples were dominated by the genera Microcystis and Anabaena during the same period. MCYST values were always below the WHO Guide level for recreational waters but much higher than the WHO Guide level for drinking water. It was found that MCYST can accumulate in the fish tissues of C. gibelio. Even though the target organ for MCYST is the liver, in our study MCYST were found also in the rest of C. gibelio tissues in the following order: intestine> kidney> > brain>gonads> muscle. Muscle tissue contained concentrations of microcystins that correspond to 0.096 μg/kg/day well above the recommended limit for human consumption (0.04 μg/Kg/day).
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Albanis, T., Pomonis, P., & Sdoukos, A. (1986). Seasonal fluctuation of organochlorine and triazines pesticides in the aquatic system of Ioannina basin (Greece). The Science of the Total Environment, 58, 243–253.
Albay, M., Akcaalan, R., Tufekci, H., Metcalf, J., Beattie, K., & Codd, G. (2003). Depth profiles of cyanobacterial hepatotoxins (microcystins) in three Turkish freshwater lakes. Hydrobiologia, 505, 89–95.
Anagnostidis, K., & Economou, A. (1980). Limnological studies of Lake Pamvotis (Ioannina) Greece. Archiv für Hydrobiologie, 89, 313–342.
A.P.H.A. (1989). Standard methods for the examination of water and wastewater (17th ed.). Washington: American Public Health Association.
Beveridge, M. C. M., Baird, D. J., Rahmatullah, S. M., Lawton, L. A., Beatie, K. A, & Codd, G. A. (1993). Grazing rates on toxic and non-toxic strains of cyanobacteria by Hypophthalmichthys molitrix and Oreochromis niloticus. Journal of Fish Biology, 43, 901–907.
Briand, J. F., Jacket, S., Bernard, C., & Humbert, J. F. (2003). Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. Veterinary Research, 34, 361–377.
Carmichael, W. W. (1992). Cyanobacteria secondary metabolites-cyanotoxins. Journal of Applied Bacteriology, 72, 445–459.
Chorus, I. (2001). Cyanotoxins, occurrence, causes, consequences. Berlin: Springer.
Chorus, I., & Bartram, J. (1999). (Eds.), Toxic cyanobacteria in water. A guide to public health consequences, monitoring and management (p. 416). London: E & FN Spon, WHO.
Codd, G. A. (1995). Cyanobacterial toxins: occurrence, properties and biological significance. Water Science and Technology, 32, 149–156.
Cook, C., Vardaka, E., & Lanaras, T. (2004). Toxic cyanobacteria in Greek freshwaters, 1997–2000: Occurrence, toxicity and impacts in the Mediterranean region. Acta Hydrochimica Et Hydrobiologica, 32, 107–124.
Dietrich, D. R., & Hoeger, S. (2005). Guidance values for microcystins in water and cyanobacterial products (blue-green algal supplements): A reasonable or misguided approach? Toxicology and Applied Pharmacology, 203(3), 273–289.
Ernst, B., Dietz, L., Hoeger, S., & Dietrich, D. (2005). Recovery of MC-LR in fish liver Tissue. Environmental Toxicology, 20(4), 449–458.
Falconer, I. R. (1993). Algal toxins in seafood and drinking water. London: Academic.
Falconer, I. R. (2001). Toxic cyanobacterial bloom problems in Australian waters: Risk and impacts on human health. Phycologia, 40, 228–233.
Falconer, I., Dornbush, M., Moran, G., & Yeung, S. (1992). Effect of the cyanobacterial toxins from Microcystis aeruginosa on isolated enterocytes from the chicken small intestine. Toxicon, 30, 790–793.
Fisher, W., & Dietrich, D. (2000). Pathological and biochemical characterization of MC-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicology and Applied Pharmacology, 16, 73–81.
Fisher, W., Garthwaite, I., Miles, C., Ross, C., Aggen, J., Chamberlin, R., et al. (2001). Congener-Independent Immunoassay for Microcystins and Nodularins Environ. Science & Technologie, 35, 4849–4856.
Fujii, K., Sivonen, K., Nakano, T., & Harada, K.-I. (2002). Structural elucidation of cyanobacterial peptides encoded by peptide synthetase gene in Anabaena species. Tetrahedron, 58, 6863–6871.
Gkelis, S., Harjunpa, V., Lanaras, T., & Sivonen, K. (2005). Diversity of Hepatotoxic Microcystins and Bioactive Anabaenopeptins in Cyanobacterial Blooms from Greek Freshwaters. Environmental Toxicology, 20(3), 249–256.
Harada, K., Tsuyoshi, M., Takayuki, S., Kiyonaga, F., Fumio, K., Ho-dong, P., et al. (2001). Co-production of Microcystins and Aeruginopeptins by natural cyanobacterial bloom. Environmental Toxicology, 16, 298–305.
Havens, K. E., James, R. T., East, T. L., & Smith, V. H. (2003). N:P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environmental Pollution, 122, 379–390.
Jacket, C., Thermes, V., de Luze, A., Puiseux-Dao, S., Bernard, C., Joly, J.-S., et al. (2004). Effects of MC-LR on development of medaka fish embryos (Oryzias latipes). Toxicon, 43, 141–147.
Janse, I., Kardinaal, W., Meima, M., & Zwart, G. (2003). High resolution differentiation of cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Applied and Environmental Microbiology, 69, 6634–6643.
Kagalou, I., Papastergiadou, E., & Leonardos, I. (2007). Long term changes on eutrophication process in a shallow Mediterranean lake ecosystem of W.Greece: Response after the reduction of external load. Journal of Environmental Management (2007), doi:10.1016/j.jcnvman.2007.01.039.
Kagalou, I., Papastergiadou, E., Tsimarakis, G., & Petridis, D. (2003a). Evaluation of the trophic state of Lake Pamvotis Greece, a shallow urban Lake. Hydrobiologia, 506–509, 745–752.
Kagalou, I., Petridis, D., & Tsimarakis, G. (2003b). Seasonal variation of water quality parameters in a shallow lake (Lake Pamvotis, Greece) and effects on phytoplankton, zooplankton communities. Journal of Freshwater Ecology, 18, 199–206.
Kagalou, I., Tsimarakis, G., & Patsias, A. (2001). Phytoplankton dynamics and physical-chemical features of a shallow lake (Lake Pamvotis-Greece). Fresenius Environmental Bulletin, 10(12), 845–849.
Kankaanpaa, H., Holliday, J., Schroder, K., Goddard, T., von Fister, R., & Carmichael, W. (2005). Cyanobacteria and prawn farming in nothern New South Wales, Australia — A case study on cyanobacteria diversity and hepatotoxin bioaccumulation. Toxicology and Applied Pharmacology, 203, 243–256.
Kardinaal, W., Janse, I., Visser, P., & Zwart, G. (2005). Dynamics of toxic cyanobacteria in Dutch lakes revealed by molecular techniques. In Shallow lakes international conference, 5–10 June, Dalfsen, The Netherlands.
Keshavanath, P., Beveridge, M. C. M., Baird, D. J., Lawton, L. A., Nimmo, A., & Codd, G. A. (1994). The functional grazing response of a phytoplanktivorous fish Oreochromis niloticus to mixtures of toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa. Journal of Fish Biology, 45, 123–129.
Klaassen, C., & Watkins, B. (1984). Mechanisms of bile formation, hepatic uptake, and biliary excretion. Pharmacological Reviews, 36, 1–67.
Kolmakov, V., & Gladyshev, M. (2003). Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crusian carp. Aquatic Ecology, 37, 237–242.
Kotak, B. G., Lam, A. K.-Y., Prepas, E. E., Hrudey, S. E., & Kenefick, S. L. (1995). Variability of the hepatotoxin, microcystin-LR, in hypereutrophic drinking water lakes. Journal of Phycology, 31, 248–263.
Kotak, B. G., Zurawell, R., Prepas, E., & Holmes, C. (1996). Microcystin-LR concentration in aquatic food web compartments from lakes of varying trophic status. Canadian Journal of Fisheries and Aquatic Sciences, 53, 1974–1985.
Kusuhara, H., Suzuki, H., Naito, M., Tsuruo, T., & Sugiyama, Y. (1998). Characterization of efflux transport of organic anions in amouse brain capillary entothelial cell line. Journal of Pharmacology and Experimental Therapeutics, 285, 1260–1265.
Lam, A. K.-Y., Fedorak, P. M., & Prepas, E. E. (1995). Biotransformation of the cyanobacterial hepatotoxin microcystin-LR, as determined by HPLC and protein phosphatase bioassay. Environmental Science & Technology, 29, 242–246.
Lampert, W. (1981). Toxicity of the blue-green alga Microcystis aeruginosa: Effective defense mechanism against grazing pressure by Daphnia. Verhandlungen. Internationale Vereinigung feur Theortische und Angewandte Limnologie, 21, 1436–1440.
Li, X., Liu, Y., Song, L., & Liu, J. (2003). Responses of antioxidant systems in the hepatocytes of common carp (Cyprinus carpio) to the toxicity of MC-LR. Toxicon, 42, 85–89.
Lindholm, T., Vesterkvist, P., Spoof, L., Lundberg-Niinistö, C., & Meriluoto, J. (2003). Microcystin occurrence in lakes in Åland, SW Finland. Hydrobiologia, 505, 129–138.
MacKintosh, C., Beattie, K. A., Klumpp, S., Cohen P., & Codd, G. A. (1990). Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatase 1 and 2A from both mammals and higher plants. FEBS Letters, 264, 187–192.
Magalhães, V. F., Soares, R., & Azevedo, S. (2001). Microcystin contamination in fish from the Jacarepagua Lagoon (Rio de Janeiro, Brazil): Ecological implication and human health risk. Toxicon, 39, 1077–1085.
Malbrouck, C., & Kestemont, P. (2006). Effects of microcystins on fish. Environmental Toxicology and Chemistry, 25(1), 72–86.
Metcalf, J. S., Bell, S. G., & Codd, G. A. (2000). Production of novel polyclonal antibodies against the cyanobacterial toxin microcystin-LR and their application for the detection and quantification of microcystins and nodularin. Water Research, 34(10), 2761–2769.
Mitraki, G. H., Crisman, T., & Zalidis, G. (2004). Lake Koronia, Greece: Shift from autotrophy to eterotrophy with cultural eutrophication and progressive water-level reduction. Limnologica, 34, 110–116.
Mohamed, Z. A., Carmichael, W. W., & Hussein, A. A. (2003). Estimation of microcystins in the freshwater fish Oreochromis niloticus in an Egyptian fish farm containing a Microcystis bloom. Environmental Toxicology, 18, 137–141.
Moss, B. (1980). Ecology of freshwaters. Oxford: Blackwell.
Moustaka-Gouni, M. (1993). Phytoplankton succession and diversity in a warm monomictic, relatively shallow lake: Lake Volvi, Macedonia, Greece. Hydrobiologia, 249, 33–42.
Naselli-Flores, L., & Barone, R. (2005). Water-level fluctuation in Mediterranean reservoirs: Setting a dewatering threshold as a management tool to improve water quality. Hydrobiologia, 548, 85–99.
Northcott, M. E., Beveridge, M. C. M., & Ross, L. G. (1991). A laboratory investigation of the filtration and ingestion rates of the tilapia Oreochromis niloticus, feeding on two species of bluegreen algae. Environmental Biology of Fishes, 31, 75–85.
Prescott, G. W. (1978). How to know the freshwater phytoplankton. (3ed.) Cambridge, UK: Cambridge University Press.
Romero, J., Kagalou, I., Imberger, J., Hela, D., Kotti, M., Bartzokas, A., et al. (2002). Seasonal water quality of shallow and eutrophic Lake Pamvotis, Greece: Implications for restoration. Hydrobiologia, 474, 91–105.
Sipia, V., Lahti, K., Kankaanpaa, H., Vuorinen, P., & Meriluoto, J. (2002). Screening for cyanobacterial hepatotoxins in herring and salmon from the Baltic Sea. Aquatic Ecosystem Health & Management, 5(4), 451–456.
Soares, R., Magalhaes, V., & Azevedo, S. (2004). Accumulation and depuration of microcystins (cyanobacteria hepatotoxins) in Tilapia rendalli (Cichlidae) under laboratory conditions. Aquatic Toxicology, 70, 1–10.
Specziar, A., Biro, P., & Tolg, L. (1998). Feeding and competition of five cyprinid fishes in different habitats of the Lake Balaton littoral zone, Hungary. Italian Journal of Zoology, 65, 331–336.
Specziár, A., Tölg, L., & Biró, P. (1997). Feeding strategy and growth of cyprinids in the littoral zone of Lake Balaton. Journal of Fish Biology, 51, 1109–1124.
Stalikas, C., Pilidis, G., & Karayanis, M. (1994). Heavy metal concentration in sediments of Lake Pamvotis and Kalamas River in North-Western Greece. Fresenius Environmental Bulletin, 3, 575–579.
Temponeras, M., Kristiansen, J., & Moustaka-Gouni, M. (2000). Seasonal variation in phytoplankton composition and physical-chemical features of the shallow Lake Doirani, Macedonia, Greece. Hydrobiologia, 424, 109–122.
Tencalla, F. G., Dietrich, D. R., & Schlatter, C. (1994). Toxicity of Microcystis aeruginosa peptide toxin to yearling rainbow trout (Oncorhyunchus mykiss). Aquatic Toxicology, 30, 215–224.
Tryfon, E., Moustaka-Gouni, M., Nicolaidis, G., & Tsekos, I. (1994). Phytoplankton and physical-chemical features of a shallow Lake Mikri Prespa, Macedonia, Greece. Archiv für Hydrobiologie, 131, 477–494.
Uterhmole, H. (1958). Zur vervollkommnung der quantitativen phytoplakton-methodik. Mitteilungen. Internationale Vereinigung feur Theortische und Angewandte Limnologie, 9, 1–38.
Vardaka, E., Moustaka-Gouni, M., Cook, E., & Lanaras, T. (2005). Cyanobacterial blooms and water quality in Greek waterbodies. Journal of Applied Phycology, 17, 391–401.
Vasconcelos, V. M. (1995). Uptake and depuration of the heptapeptide toxin microcystin-LR in Mutilus galloprovincialis. Aquatic Toxicology, 32, 22.
Vasconcelos, V. M., Sivonen, K., Evans, W. R., Carmichael, W. W., & Namikoshi, M. (1996). Hepatotoxic microcystin diversity in cyanobacterial blooms collected in Portuguese freshwaters. Water Research, 30(10), 2377–2384.
WHO (1998). Blue-green algae in inland waters: Assessment and control of risks to public health. WHO Document, Annex G.
Williams, D. E., Craig, M., Dawe, S. C., Kent, M. L., Andersen, R. J., & Holmes, C. F. B. (1997a). 14C labeled microcystin-LR administrated to atlantic salmon via intraperitoneal injection provides in vivo evidence for covalent binding of microcystin-LR in salmon livers. Toxicon, 35(6), 985–989.
Williams, D. E., Craig, M., Dawe, S. C., Kent, M. L., Holmes, C. F. B., & Andersen, R. J. (1997b). Evidence for a covalent bound form of microcystin-LR in salmon liver and dungeness crab larval. Chemical Research in Toxicology, 10(4), 460–463.
Xie, L., Xie, P., Guo, L., Li, L., Miyabara, Y., & Park, H. D. (2005). Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environmental Toxicology, 20, 293–300.
Zar, J. H. (1999). Biostatistical analysis (4th ed.). New Jersey: Prentice-Hall.
Zhang, X., Xie, P., Hao, L., Guo, N., Gong, Y., Hu, X., et al. (2006). Effects of the phytoplanktivorous silver carp (Hypophthalmichtys molitrixon) on plankton and the hepatotoxic microcystins in an ecosystem experiment in a eutrophic lake, Lake Shichahai in Beijing. Aquaculture, 257, 173–186.
Zimba, P., Khoo, L., Ganut, P., Brittain, S., & Carmichael, W. (2001). Confirmation of catfish, Ictalurus punctatus (Rafinesque),mortality from microcystins toxins. Journal of Fish Diseases, 24, 41–47.
Zurawell, R., Chen, H., Burke, J., & Prepas, E. (2005). Hepatoxin cyanobacteria: A review of the biological importance of microcystins in freshwater environments. Journal of Toxicology and Environmental Health, Part B, 8, 1–37.
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Kagalou, I., Papadimitriou, T., Bacopoulos, V. et al. Assessment of microcystins in lake water and the omnivorous fish (Carassius gibelio, Bloch) in Lake Pamvotis (Greece) containing dense cyanobacterial bloom. Environ Monit Assess 137, 185–195 (2008). https://doi.org/10.1007/s10661-007-9739-6
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DOI: https://doi.org/10.1007/s10661-007-9739-6