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Ecotoxicology

, Volume 21, Issue 4, pp 1155–1166 | Cite as

Assessment of microcystin distribution and biomagnification in tissues of aquatic food web compartments from a shallow lake and evaluation of potential risks to public health

  • Theodoti Papadimitriou
  • Ifigenia Kagalou
  • Constantinos Stalikas
  • Georgios Pilidis
  • Ioannis D. LeonardosEmail author
Article

Abstract

The objectives of this study were: (1) to examine the distribution and bioaccumulation of microcystins in the main components of the food web (phytoplankton, zooplankton, crayfish, shrimp, mussel, snail, fish, frog) of Lake Pamvotis (NW Greece), (2) to investigate the possibility of microcystin biomagnification and (3) to evaluate the potential threat of the contaminated aquatic organisms to human health. Significant microcystin concentrations were detected in all the aquatic organisms during two different periods, with the higher concentrations observed in phytoplankton and the lower in fish species and frogs. This is the first study reporting microcystin accumulation in the body of the freshwater shrimp Atyaephyra desmsaresti, in the brain of the fish species common carp (Cyprinus carpio) and in the skin of the frog Rana epirotica. Although there was no evidence for microcystin biomagnification, the fact that microcystins were found in lake water and in the tissues of aquatic organisms, suggests that serious risks to animal and public health are possible to occur. In addition, it is likely to be unsafe to consume aquatic species harvested in Lake Pamvotis due to the high-concentrations of accumulated microcystins.

Keywords

Microcystins Aquatic organisms Biomagnification Health risks Food web Ecotoxicology 

References

  1. Adamovsky O, Kopp R, Hilscherova K, Babica P, Palikova M, Paskova V, Navratil S, Blaha L (2007) Microcystin kinetics (bioaccumulation, elimination) and biochemical responses in common carp and silver carp exposed to toxic cyanobacterial blooms. Environ Toxicol Chem 26:687–2693CrossRefGoogle Scholar
  2. Albay M, Akcaalan R, Tufekci H, Metcalf J, Beattie K, Codd G (2003) Depth profiles of cyanobacterial hepatotoxins (microcystins) in three Turkish freshwater lakes. Hydrobiology 505:89–95CrossRefGoogle Scholar
  3. Amorim A, Vasconcelos V (1999) Dynamics of microcystins in the mussel Mytilus galloprovincialis. Toxicon 37:1041–1052CrossRefGoogle Scholar
  4. Anagnostidis K, Economou-Amilli A (1980) Limnological studies on Lake Pamvotis (Ioannina), Greece I. Hydroclimatology, phytoplankton-periphyton with special reference to the valence of some microorganisms from sulphureta as bioindicators. Arch Hydrobiol 89:313–342Google Scholar
  5. Anastasiadou Ch, Koukouras A, Mavidis M, Chartosia N, Mostakim Md, Christodoulou M, Aslanoglou Ch (2004) Morphological variation in Atyaephyra desmarestii (Millet, 1831) within and among populations over its geographical range. Mediterr Mar Sci 5(2):5–13Google Scholar
  6. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726CrossRefGoogle Scholar
  7. Babcock-Jackson L, Carmichael WW, Culver DA (2002) Dreissenid mussels increase exposure of benthic and pelagic organisms to toxic microcystins. Verh Internat Verein Limnol 28:1082–1085Google Scholar
  8. Beresovsky D, Hadas O, Livne A, Sukenik A, Kaplan A, Carmeli S (2006) Toxins and biologically active secondary metabolites of Microcystis sp. isolated from Lake Kinneret. Israel J Chem 46:79–87CrossRefGoogle Scholar
  9. Briand JF, Robillot C, Quiblier-Lloberas C, Bernard C (2002) A perennial bloom Planktothrix agardhii (Cyanobacteria) in a shallow eutrophic French lake: limnological and microcystin production studies. Arch Hydrobiol 153:605–622Google Scholar
  10. Carbis CR, Mitchell GF, Anderson JW, McCauley I (1996) The effects of microcystins on the serum biochemistry of carp, Cyprinus carpio L., when the toxins are administered by gavage, immersion and intraperitoneal routes. J Fish Dis 19:151–159CrossRefGoogle Scholar
  11. Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 270:78–86CrossRefGoogle Scholar
  12. Carmichael WW (1997) The Cyanotoxins. In: Callow J (ed) Advances in botanical research, vol. 27. Academic Press, London, pp 211–256Google Scholar
  13. Chen J, Xie P (2005a) Seasonal dynamics of the hepatotoxic microcystins in various organs of four freshwater bivalves from the large eutrophic Lake Taihu of subtropical China and the risk to human consumption. Environ Toxicol 20:572–584CrossRefGoogle Scholar
  14. Chen J, Xie P (2005b) Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in two freshwater shrimps. Palaemon modestus and Macrobrachium nipponensis, from a large shallow, eutrophic lake of the subtrophical China. Toxicon 45:615–625CrossRefGoogle Scholar
  15. Codd GA (1995) Cyanobacterial toxins: occurrence, properties and biological significance. Water Sci Technol 32:149–156Google Scholar
  16. Codd GA (2000) Cyanobacterial toxin, the perception of water quality, and the prioritisation if eutrophication control. Ecol Eng 16:51–60CrossRefGoogle Scholar
  17. de Figueiredo DR, Azeiteiro UM, Esteves SM, Goncalves FJ, Pereira MJ (2004) Microcystin-producing blooms—a serious global public health issue. Ecotox Environ Saf 59:151–163CrossRefGoogle Scholar
  18. DeMott WR (1999) Foraging strategies and growth inhibition in five daphnids feeding on mixtures of a toxic cyanobacterium and green alga. Freshw Biol 42:263–274CrossRefGoogle Scholar
  19. Duy TN, Lam PKS, Shaw GR, Connell DW (2000) Toxicology and risk assessment of freshwater cyanobacterial (Blue- Green Algal) toxins in water. Rev Environ Contam Toxicol 163:113–186Google Scholar
  20. Dvorakova D, Dvorakova K, Blaha L, Marsalek B, Knotkova Z (2002) Effects of cyanobacterial biomass and purified microcystins on malformations in Xenopus laevis: teratogenesis assay (FETAX). Environ Toxicol 17:547–555CrossRefGoogle Scholar
  21. Engström-Öst J, Lehtiniemi M, Green S, Kozlowsky-Suzuki B, Viitasalo M (2002) Does cyanobacterial toxin accumulate in mysid shrimps and fish via copepods? J Exp Mar Biol Ecol 276:95–107CrossRefGoogle Scholar
  22. Ernst B, Dietz L, Hoeger SJ, Dietrich DR (2005) Recovery of MC-LR in fish liver tissue. Environ Toxicol 20:449–458CrossRefGoogle Scholar
  23. Falconer IR, Humpage AR (2005) Health risk assessment of cyanobacterial (blue-green algal) toxins in drinking water. Int J Environ Res Public Health 2:43–50CrossRefGoogle Scholar
  24. Ferrão-Filho AS, Kozlowsky-Suzuki Betina (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9:2729–2772CrossRefGoogle Scholar
  25. Ferrão-Filho AS, Domingos P, Azevedo SMFO (2002) Influences of a Microcystis aeruginosa Kützing bloom on zooplankton populations in Jacarepaguá Lagoon (Rio de Janeiro, Brazil). Limnologica 32:295–308CrossRefGoogle Scholar
  26. Fischer W, Dietrich D (2000a) Pathological and biochemical characterization of MC-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicol Appl Pharmacol 164:73–81CrossRefGoogle Scholar
  27. Fischer WJ, Dietrich DR (2000b) Toxicity of the cyanobacterial cyclic heptapeptide toxins microcystin-LR and-RR in early life-stages of the African clawed frog (Xenopus laevis). Aquat Toxicol 49:189–198CrossRefGoogle Scholar
  28. Fischer WJ, Altheimer S, Cattori V, Meier PJ, Dietrich DR, Hagenbuch B (2005) Organic anion transporting polypeptides expressed in liver and brain mediate uptake of microcystin. Toxicol Appl Pharmacol 203:257–263CrossRefGoogle Scholar
  29. Ghazali I, Saqrane S, Carvalho AP, Ouahid Y, Oudra B, Del Campo FF, Vasconcelos V (2009) Compensatory growth induced in Zebrafish Larvae after pre-exposure to a Microcystis aeruginosa natural bloom extract containing microcystins. Int J Mol Sci 10:133–146CrossRefGoogle Scholar
  30. Gkelis S, Lanaras T, Sivonen K (2006) The presence of microcystins and other cyanobacterial bioactive peptides in aquatic fauna collected from Greek freshwaters. Aquat Toxicol 78(1):32–41CrossRefGoogle Scholar
  31. Gromov B, Mamkaeva K, Filatova E (1997) Effect of toxigenic strains of cyanobacterium Microcystis aeruginosa on the larvae of frog Rana temporaria. Doklady Akademii Nauk (Proceedings of the Russian Academy of Science) 356:422–423 (Original article in Russian)Google Scholar
  32. Guo N, Xie P (2006) Development of tolerance against toxic Microcystis aeruginosa in three cladocerans and the ecological implications. Environ Pollut 143:513–518CrossRefGoogle Scholar
  33. Gustafsson S, Hansson L (2004) Development of tolerance against toxic cyanobacteria in Daphnia. Aquat Ecol 38:37–44CrossRefGoogle Scholar
  34. Gustafsson S, Rengefors K, Hansson LA (2005) Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects. Ecology 86:2561–2567CrossRefGoogle Scholar
  35. Habdija I, Latjner J, Belinic I (1995) The contribution of gastropod biomass in macrobenthic communities of a karstic river. Int Rev Ges Hydrobiol 80:103–110CrossRefGoogle Scholar
  36. Hansson L, Gustafsoson S, Rengefors K, Bomark L (2007) Cyanobacterial chemical warfare affects zooplankton community composition. Freshw Biol 52:1290–1301CrossRefGoogle Scholar
  37. Hooser SB (2000) Fulminant hepatocyte apoptosis in vivo following microcystin-LR administration to rats. Toxicol Pathol 28:726–733CrossRefGoogle Scholar
  38. Hooser SB, Beasley VR, Lovell RA, Carmichael WW, Haschek WM (1989) Toxicity of microcystin LR, a cyclic heptapeptide hepatotoxin from Micocystis aeruginosa, to rats and mice. Vet Pathol 26:246–252CrossRefGoogle Scholar
  39. Ibelings BW, Bruning K, de Jonge J, Wolfstein K, Dionisio PLM, Postma J, Burger T (2005) Distribution of microcystins in a lake foodweb: no evidence for biomagnification. Microbial Ecol 49(4):487–500CrossRefGoogle Scholar
  40. Kagalou I, Papastergiadou E, Tsimarakis G, Petridis D (2003) Evaluation of the trophic state of Lake Pamvotis Greece, a shallow urban Lake. Hydrobiology 506–509:745–752CrossRefGoogle Scholar
  41. Kagalou I, Papadimitriou T, Bacopoulos V, Leonardos I (2008) Assessment of microcystins in lake water and the omnivorous fish (Carassius gibelio, Bloch) in Lake Pamvotis (Greece) containing dense cyanobacterial bloom. Environ Monit Assess 137:185–195CrossRefGoogle Scholar
  42. Karjalainen M, Reinikainen M, Spoof L, Meriluoto JAO, Sivonen K (2005) Trophic transfer of cyanobacterial toxins from zooplankton to planktivores: consequences for pike larvae and mysid shrimps. Environ Toxicol 20(3):354–362CrossRefGoogle Scholar
  43. Khan TA (2003) Dietary studies on exotic carp (Cyprinus carpio L.) from two lakes of western Victoria, Australia. Aquat Sci 65:272–286CrossRefGoogle Scholar
  44. Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681–684CrossRefGoogle Scholar
  45. Kotak BJ, Semalulu S, Friytz DL, Prepas EE, Hrudey SE, Coppock RW (1996) Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss). Toxicon 34:517–525CrossRefGoogle Scholar
  46. Kotti M, Vlessidis A, Evmiridis N (2000) Determination of phosphorous and nitrogen in the sediment of Lake Pamvotis (Greece). Int J Environ Anal Chem 78(3–4):455–467CrossRefGoogle Scholar
  47. Lance E, Brient L, Bormans M, Gérard C (2006) Interactions between cyanobacteria and Gastropods I. Ingestion of toxic Planktothrix agardhii by Lymnaea stagnalis and the kinetics of microcystin bioaccumulation and detoxification. Aquat Toxicol 79:140–148CrossRefGoogle Scholar
  48. Lawton LA, Edwards C, Codd GA (1994) Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119:1525–1530CrossRefGoogle Scholar
  49. Leonard JA, Pearl HW (2005) Zooplankton community structure, micro-zooplankton grazing impact, and seston energy content in the St. Johns River system, Florida as influenced by the toxic cyanobacterium Cylindrospermopsis raciborskii. Hydrobiology 537:89–97CrossRefGoogle Scholar
  50. Li XY, Chung IK, Kim JI, Lee JA (2004) Subchronic oral toxicity of microcystin in common carp (Cyprinus carpio L.) exposed to microcystis under laboratory conditions. Toxicon 44:821–827CrossRefGoogle Scholar
  51. Liras V, Lindberg M, Nyström P, Annadotter H, Lawton L, Graf B (1998) Can ingested cyanobacteria be harmful to the signal crayfish (Pacifastacus leniusculus). Freshw Biol 39:233–242CrossRefGoogle Scholar
  52. Mackie GL (1984) Bivalves. In: Wilbur KM (ed) The Mollusca, vol. 7, reproduction. Academic Press, Orlando, pp 351–418Google Scholar
  53. Magalhães VF, Soares R, Azevedo S (2001) Microcystin contamination in fish from the Jacarepagua Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk. Toxicon 39:1077–1085CrossRefGoogle Scholar
  54. Magalhães VF, Marinho MM, Domingos P, Oliveira AC, Costa SM, Azevedo LO, Azevedo SMFO (2003) Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ). Toxicon 42:289–295CrossRefGoogle Scholar
  55. Malbrouck C, Kestemont P (2006) Effects of microcystins on fish. Environ Toxicol Chem 25:72–86CrossRefGoogle Scholar
  56. Malbrouck C, Trausch G, Devos P, Kestemont P (2003) Hepatic accumulation and effects of microcystin-LR on juvenile goldfish Carassius auratus L. Comp Biochem Physiol Part C 135(1):39–48CrossRefGoogle Scholar
  57. Martins JC, Vasconcelos VM (2009) Microcystin dynamics in aquatic organisms. J Toxicol Environ Health 12:65–82Google Scholar
  58. Oberemm A, Becker J, Codd GA, Steinberg C (1999) Effects of cyanobacterial toxins and aqueous crude extracts of cyanobacteria on the development of fish and amphibians. Environ Toxicol 14:77–88CrossRefGoogle Scholar
  59. Ozawa K, Yokoyama A, Ishikawa K, Kumagai M, Watanabe MF, Park HD (2003) Accumulation and depuration of microcystin produced by the cyanobacterium Microcystis in a freshwater snail. Limnology 4:131–138CrossRefGoogle Scholar
  60. Paliková M, Krejč R, Hilscherová K, Babica P, Navratil S, Kopp R, Blaha L (2007) Effect of different cyanobacterial biomasses and their fractions with variable microcystin content on embryonal development of carp (Cyprinus carpio L.). Aquat Toxicol 81: 312–318Google Scholar
  61. Papadimitriou T (2010) Effects of Microcystins on aquatic organisms. Dissertation, University of IoanninaGoogle Scholar
  62. Papadimitriou T, Kagalou I, Bacopoulos V, Leonardos I (2010) Accumulation of microcystins in water and fish tissues: an estimation of risks associated with microcystins in most of the Greek lakes. Environ Toxicol 25(4):418–427CrossRefGoogle Scholar
  63. Papadimitriou T, Armeni E, Stalikas C, Kagalou I, Leonardos I (2011) Detection of microcystins in Pamvotis lake water and assessment of cyanobacterial bloom toxicity. Environ Monit Assess. doi: 10.1007/s10661-011-2169-5
  64. Pennak RW (1978) Freshwater invertebrates of the United States. Wiley-Interscience, New York. 2nd edn, 803 ppGoogle Scholar
  65. Prepas EE, Kotak BG, Campbell LM, Evans JC, Hrudey SE, Holmes CF (1997) Accumulation and elimination of cyanobacterial hepatotoxins by the freshwater clam Anodonta grandis simpsonia. Can J Fish Aquat Sci 54:41–46Google Scholar
  66. Ressom R, Soong FS, Fitzgerald J, Turczynowicz L, El Saadi O, Roder D, Maynard T, Falconer IR (1994) Health effects of toxic cyanobacteria (blue-green algae). National Health and Medical Council, Australian Government Publishing Service, CanberraGoogle Scholar
  67. Rohrlack T, Dittman E, Borner T, Christoffersen K (2001) Effects of cell-bound microcystins on survival and feeding of Daphnia spp. Appl Environ Microbiol 67(8):3523–3529CrossRefGoogle Scholar
  68. Rohrlack T, Christoffersen K, Dittmann E, Nogueira I, Vasconcelos V, Borner T (2005) Ingestion of microcystins by Daphnia: intestinal uptake and toxic effects. Limnol Oceanogr 50:440–448CrossRefGoogle Scholar
  69. Romo S, Francisca F, Youness O, Ángel B-S (2011) Assessment of microcystins in lake water and fish (Mugilidae, Liza sp.) in the largest Spanish coastal lake. Environ Monit Assess 184:939–949CrossRefGoogle Scholar
  70. Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50:1565–1570CrossRefGoogle Scholar
  71. Sipia V, Lahti K, Kankaanpaa H, Vuorinen P, Meriluoto J (2002) Screening for cyanobacterial hepatotoxins in herring and salmon from the Baltic Sea. Aquat Ecosyst Health Manag 5(4):451–456CrossRefGoogle Scholar
  72. Sipiä VO, Karlsson KM, Meriluoto JAO, Kankaanpää HT (2004) Eiders (Somateria mollissima) obtain nodularin, a cyanobacterial hepatotoxin, in Baltic Sea food web. Environ Toxicol Chem 23:1256–1260CrossRefGoogle Scholar
  73. Tencalla F, Dietrich D, Schlatter C (1994) Toxicity of Microcystis aeruginosa peptide toxin to yearling raibowtrout (Oncorhynchus mykiss). Aquat Toxicol 30:215–224CrossRefGoogle Scholar
  74. Thostrup L, Christoffersen K (1999) Accumulation of microcystin in Daphnia magna feeding on toxic Microcystis. Archiv fūr Hydrobiologie 145:447–467Google Scholar
  75. Vardaka E, Moustaka-Gouni M, Cook CM, Lanaras T (2005) Cyanobacterial blooms and water quality in Greek waterbodies. J Appl Phycol 17:391–401CrossRefGoogle Scholar
  76. Vareli K, Pilidis G, Mavrogiorgou MC, Briasoulis E, Sainis I (2009) Molecular characterization of cyanobacterial diversity and yearly fluctuations of microcystin loads in a suburban Mediterranean lake (Lake Pamvotis, Greece). J Environ Monit 11:1506–1512CrossRefGoogle Scholar
  77. Vasconcelos VM (2006) Eutrophication, toxic cyanobacteria and cyanotoxins: when ecosystems cry for help. Limnetica 25(1–2):425–432Google Scholar
  78. White SH, Duivenvoorden LJ, Fabbro LD, Eaglesham GK (2007) Mortality and toxin bioaccumulation in Bufo marinus following exposure to Cylindrospermopsis raciborskii cell extracts and live cultures. Environ Pollut 147:158–167CrossRefGoogle Scholar
  79. WHO (1998) Cyanobacterial toxins: microcystin-LR. In: Guidelines for drinking water quality (ed) Addendum to vol. 2. Health criteria and other supporting information, 2nd edn. World Health Organization, Geneva, pp. 95–110Google Scholar
  80. Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites: a short review. Toxicol Appl Pharmacol 203:201–218CrossRefGoogle Scholar
  81. Xie LQ, Xie P, Ozawa K, Honma T, Yokoyama A, Park HD (2004) Dynamics of microcystins-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environ Pollut 127:431–439CrossRefGoogle Scholar
  82. Xie L, Yokoyama A, Nakamura K, Park H (2007) Accumulation of microcystins in various organs of the freshwater snail Sinotaia histrica and three fishes in a temperate lake, the eutrophic Lake Suwa, Japan. Toxicon 49:646–652CrossRefGoogle Scholar
  83. Yokoyama A, Park HD (2003) Depuration kinetics and persistence of the cyanobacterial toxin microcystin-LR in the freshwater bivalve Unio douglasiae. Environ Toxicol 18:61–67CrossRefGoogle Scholar
  84. Yu SZ (1995) Primary prevention of hepatocellular carcinoma. J Gastroenterol Hepatol 10:674–682CrossRefGoogle Scholar
  85. Zhang DW, Xie P, Liu YQ, Qiu T (2009) Transfer, distribution and bioaccumulation of microcystins in the aquatic food web in Lake Taihu, China, with potential risks to human health. Sci Total Environ 407:2191–2199CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Theodoti Papadimitriou
    • 1
  • Ifigenia Kagalou
    • 2
  • Constantinos Stalikas
    • 3
  • Georgios Pilidis
    • 1
  • Ioannis D. Leonardos
    • 1
    Email author
  1. 1.Biological Applications and Technology DepartmentUniversity of IoanninaIoanninaGreece
  2. 2.Ichthyology and Aquatic Environment DepartmentUniversity of ThessalyVolosGreece
  3. 3.Department of ChemistryUniversity of IoanninaIoanninaGreece

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