Berillis PANAGIOTIS, Papadimitriou THEODOTI, Petridou EVI, Kormas KONSTANTINOS, Kagalou IFIGENIA

Brain and liver histopathological examination of Carassius gibelio from A newly reconstructed lake with toxic cyanobacteria

Lake Karla, Greece, is a partially reconstructed lake. The lake s water filling process started in September 2009. Existing evidence based on the prevailing microorganisms and cyanotoxin levels in the lake in 2010 suggested that the lake could have a negative effect on its biota. By investigating whether Carassius gibelio individuals bear brain and liver histopathological findings, this study complements the data now available from the first year of L. Karla s reconstruction. Based on the 16S rRNA gene diversity, the potentially toxic cyanobacteria Anabaenopsis sp. and Planktothrix were shown to be present in the lake s water in May 2011. C. gibelio specimens were collected a month later. Histopathological alterations in the liver of the individuals, namely picnotic nuclei, loss of structure and hemorrhagic regions, were detected by microscopic examination. Picnotic nuclei, loss of the liver structure and hemorrhagic regions were detected. These alterations may be associated with the occurrence of cyanobacterial toxins possibly produced by the potentially toxic cyanobacterial species found in the water column. No alterations were found in the brain, probably due to the existence of the blood-brain barrier.

PDF

___

Ananiadis, C.I. 1959. Limnological study of Lake Karla. Bulletin de lInstitut Oc ́eanographique, 1083: 119.

Bartram, J., Burch, M., Falconer, I.R., Jones, G. and Kuiper-Goodman, T. 1999. Situation assessment, planning and management. In: I. Chorus, J. Bartram (Eds), Toxic cyanobacteria in water, Taylor and Francis, London, New York: 179-209.

Carbis, C.R., Rawlin, G.T., Mitchell, G.F., Anderson, J.W. and McCauley, I. 1996. The histopathology of carp, Cyprinus carpio L., exposed to microcystins by gavage, immersion and intraperitoneal administration. Journal of Fish Diseases, 19: 199207. doi: 10.1111/j.1365-2761.1996.tb00126.x

Carbis, C.R., Rawlin, G.T., Grant, P., Mitchell, G.F., Anderson, J.W. and McCauley, I. 1997. A study of feral carp, Cyprinus carpio L., exposed to Microcystis aeruginosa at Lake Mokoan, Australia, and possible implications for fish health. Journal of Fish Diseases, 20: 8191. doi: 10.1046/j.1365-2761.1997.d01-111.x

Carmichael, W.W., Azevedo, S.M.F.O., An, J.S., Molica, R.J., Jochimsen, E.M., Lau, S., Rinehart, K.L., Shaw, G.R. and Eaglesham, G.K. 2001. Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environmental Health Perspectives, 109: 663-668. doi: 10.1289/ehp.01109663

Chatzinikolaou, Y., Ioannou, A. and Lazaridou, M. 2010. Intrabasin spatial approach on pollution load estimation in a large Mediterranean river. Desalination, 250: 118129. doi: 10.1016/j.desal.2008.12.062.

Chorus, I. 2001. Cyanotoxin occurrence in freshwaters-a summary of survey results from different countries. In: I. Chorus (Ed.), Cyanotoxins: Occurrence, causes consequences, Spinger, Berlin: 75-78.

Codd, G.A. 1995. Cyanobacterial toxins: occurrence, properties and biological significance. Water Science and Technology, 32(4): 149-156. doi: 10.1016/0273- 1223(95)00692-3.

Codd, G.A., Chorus, I and Burch, M. 1999. Design of monitoring programmes. In: I. Chorus, J. Bartram (Eds), Toxic Cyanobacteria in water: a guide to their public health consequences, monitoring and management, E & FN Spon, London: 313-328.

Cooley, H.M., Evans, R.E. and Klaverkamp, J.F. 2000. Toxicology of dietary uranium in lake whitefish (Coregonus clupeaformis). Aquatic Toxicology, 48: 495515. doi: 10.1016/S0166-445X(99)00057-0.

Dietrich, D. and Hoeger, S. 2005. Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach? Toxicology and Applied Pharmacology, 203: 273289. doi: 10.1016/j.taap.2004.09.005.

Dos Santos, A.P.M.E. and Bracarense, A.P.F.R.L. 2008. Hepatotoxicity associated with microcystins. Semina:Ciencias Agrarias, 29: 417- 430. doi: 10.5433/1679-0359.2008v29n2p417

Ernst, B. 2008. Investigations of the impact of toxic cyanobacteria on fish. PhD thesis, Constance, Germany: Universität Konstanz. Dissertation, University of Kostanz.

Fisher, W., Dietrich, D. 2000a. Pathological and biochemical characterization of microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus carpio). Toxicology and Applied Pharmacology, 164: 7381. doi: 10.1006/taap.1999.8861.

Fischer, W. and Dietrich, D. 2000b. Toxicity of the cyanobacterial cyclic heptapeptide toxins microcystin LR and-RR in early life-stages of the African clawed frog (Xenopus laevis). Aquatic Toxicology, 49: 189 198. doi: 10.1016/S0166-445X(99)00079-X.

Fournie, J. W., Courtney, L.A. 2002. Histopathological evidence of regeneration following hepatotoxic effects of the cyanotoxin Microcystin-LR in the hardhead catfish and Gulf killifish. Journal of Aquatic Animal Health, 14: 273-80. doi: 10.1577/1548- 8667(2002)014_____0273:HEORFH>2.0.CO;2.

Hawkins, B.T. and Davis, T.P. 2005. The blood-brain barrier/neurovascular unit in health and disease. Pharmacological Reviews, 57: 173-85. doi: 10.1124/pr.57.2.4.

Huisman, J., Matthijs, H.C.P. and Visser, P.M. 2005. Harmful cyanobacteria. Springer, Berlin, 243 pp.

Kagalou, I., Kormas, K.A., Papadimitriou, T., Katsiapi, M., Genitsaris, S. and Moustaka-Gouni, M. 2012. Greece: occurrence, monitoring and risk management of cyanobacteria and cyanotoxins. In: I. Chorus (Ed), Current approaches to cyanotoxin risk assessment, risk management and regulations in different countries, Federal Environmental Agency (Umweltbundesamt), Berlin: 71-78.

Kagalou, I., Papadimitriou, T., Bacopoulos, V. and Leonardos, I. 2008. Assessment of microcystins in lake water and the omnivorous fish (Carassius gibelio, Bloch) in Lake Pamvotis (Greece) containing dense cyanobacterial bloom. Environmental Monitoring and Assessment, 137: 185-195. doi: 10.1007/s10661-007-9739-6.

Katsiapi, M., Moustaka-Gouni, M., Vardaka, E. and Kormas, K.A. 2013. Different phytoplankton descriptors show asynchronous changes in a shallow urban lake (L. Kastoria, Greece) after sewage diversion. Fundamental and Applied Limnology, 182:219-230. doi: 10.1127/1863-9135/2013/0362

Kolmakov, V. and Gladyshev, M. 2003. Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crusian carp. Aquatic Ecology, 37: 237-242. doi: 10.1023/A:1025801326088.

Kormas, K.A., Gkelis, S., Vardaka, E., Moustaka-Gouni, M. 2011. Morphologic and molecular analysis of bloom- forming Cyanobacteria in two eutrophic, shallow Mediterranean lakes. Limnologica, 41: 167-173. doi: 10.1016/j.limno.2010.10.003.

Kotak, B.J., Semalulu, S., Friytz, D.L., Prepas, E.E., Hrudey, S.E., Coppock, R.W. 1996. Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss). Toxicon, 34: 51725. doi: 10.1016/0041- 0101(96)00009-8.

Kottelat, M. and Freyhof, J. 2007. Handbook of European freshwater fishes. Publications Kottelat, Berlin, 646 pp.

Lang, T., Wosniok, W., Barsiene, J., Broeg, K., Kopecka, J. and Parkkonen, J. 2006. Liver histopathology in Baltic flounder (Platichthys flesus) as indicator of biological effects of contaminants. Marine Pollution Bulletin, 53: 488-496. doi: 10.1016/j.marpolbul.2005.11.008.

Li, L., Xie, P., Li, S., Qiu, T., Guo, L. 2007. Sequential ultrastructural and biochemical changes induced in vivo by the hepatotoxic microcystins in liver of the phytoplanktivorous silver carp Hypophthalmichthys molitrix. Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, 146: 357367. doi: 10.1016/j.cbpc.2007.04.008.

Malbrouck, C., Kestemont, P. 2006. Effects of Microcystins on fish. Environmental Toxicology and Chemistry, 25: 7286. doi: 10.1897/05-029R.1.

Mitsoura, A., Kagalou, I., Papaioannou, N., Berillis, P., Mente, E. and Papadimitriou T. 2013. The presence of microcystins in fish Cyprinus carpio tissues: an histopathological study. International Aquatic Research, 5: 8. doi:10.1186/2008-6970-5-8

Moutou, K., Tsikogias, S., Papadimitriou, T. and Kagalou, I. 2012. Oxidative stress in Cyprinus carpio to analyze microcystin impact in eutrophic shallow lakes: a preliminary study. Journal of Enviromental Monitoring, 14(8): 2195-2203. doi: 10.1039/c2em30129f.

Nübel, U., Garcia-Pichel, F. and Muyzer, G. 1997. PCR primers to amplify 16S rRNA genes from Cyanobacteria. Applied and Environmental Microbiology, 63: 3327-3332.

Oikonomou, A., Κatsiapi, M., Karayanni, H., Moustaka- Gouni, M. and Kormas, K. 2012. Plankton microorganisms coinciding with two consecutive mass fish kills in a newly reconstructed lake. The Scientific World Journal. doi:10.1100/2012/504135.

Papadimitriou, T., Kagalou, I., Stalikas, C., Pilidis, G. and Leonardos, I. 2012. Assessment of microcystins distribution and biomagnification in tissues of the aquatic food web compartments from a shallow lake and potential risks for public health. Ecotoxicology, 21: 1155-1166. doi: 10.1007/s10646-012-0870-y.

Papadimitriou, T., Katsiapi, M., Kormas, K.A., Moustaka- Gouni, M. and Kagalou, I. 2013. Artificially-born "killer" lake: phytoplankton based water quality and microcystin affected fish in a reconstructed lake. Science of the Total Environment, 452-453:116-124. doi: 10.1016/j.scitotenv.2013.02.035.

Råbergh, C.M.I., Bylund, G. and Eriksson, J.E. 1991. Histopathological effects of microcystin-LR, a cyclic peptide toxin from the cyanobacterium (blue-green algae) Microcystis aeruginosa, on common carp (Cyprinus carpio L.). Aquatic Toxicology, 20: 131 46. doi: 10.1016/0166-445X(91)90012-X.

Specziár, A., Tölg, L. and Biró, P. 1997. Feeding strategy and growth of cyprinids in the littoral zone of Lake Balaton. Journal of Fish Biology, 51: 1109-1124. doi: 10.1006/jfbi.1997.0514.

Specziár, A., Biro, P. and 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. doi: 10.1080/11250009809386842.

Vardaka, E., Moustaka-Gouni, M., Cook, C.M. and Lanaras, T. 2005. Cyanobacterial blooms and water quality in Greek waterbodies. Journal of Applied Phycology, 17: 391-401. doi: 10.1007/s10811-005- 8700-8.

Welker, M., Chorus, I. and Fastner, J. 2004. Occurrence of cyanobacterial toxins (microcystins) in surface waters of rural Bangladesh- pilot study. In W.H.O. Report, Bangladesh: 1-24.

WHO 1998. Blue-green algae in inland waters: Assessment and control of risks to public health. WHO Document, Annex G.

Xie, L.Q., Xie, P., Ozawa, K., Honma, T., Yokoyama, A., and Park, H.D. 2004. Dynamics of microcystins-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environmental Pollution, 127: 431439. doi: 10.1016/j.envpol.2003.08.011.

Zurawell, R.W., Chen, H., Burke, J.M. and Prepas, B.R. 2005. Hepatotoxic cyanobacteria: A review of the biological importance of microcystins in freshwater environment. Journal of Toxicology and Environmental Health, 8(B): 137. doi: 10.1080/10937400590889412.