Have a personal or library account? Click to login
Simultaneous accumulation of anatoxin-a and microcystins in three fish species indigenous to lakes affected by cyanobacterial blooms Cover

Simultaneous accumulation of anatoxin-a and microcystins in three fish species indigenous to lakes affected by cyanobacterial blooms

Oceanological and Hydrobiological Studies
Volume 41 (2012): Issue 4 (December 2012)
By: Barbara Pawlik-Skowrońska,  Magdalena Toporowska and  Jacek Rechulicz  
Open Access
|Nov 2012

References

  1. [1] Adamovsky O., Kopp R., Hilscherova K., Babica P., Palikova M., Paskova V., Navratil S., Marsalek B., Blaha L., 2007, Microcystin kinetics ( bioaccumulation and elimination) and biochemical responses in common carp (Cyprinus carpio) and silver carp (Hypophthalmichthys molitrix) exposed to toxic cyanobacterial blooms. Environ. Toxicol. Chem. 26: 2687–2693. http://dx.doi.org/10.1897/07-213.110.1897/07-213.1
    Search in Google Scholar
  2. [2] Ballot A., Fastner J., Lantz M., Wiedner C., 2010, First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatchenkoi in northeastern Germany. Toxicon, 56: 964–971 http://dx.doi.org/10.1016/j.toxicon.2010.06.02110.1016/j.toxicon.2010.06.021
    Search in Google Scholar
  3. [3] Becker V., de Cardoso L., Motta Marques D., 2004, Development of Anabaena Bory ex Bornet & Flahault (Cyanobacteria) blooms in a shallow, subtropical lake in southern Brazil, Acta Limnol. Bras., 16: 306–317
    Search in Google Scholar
  4. [4] Berry J.P., Gantar M., Gibbs P.D., Schmale M.C. 2007, The zebrafish (Danio rerio) embryo as a model system for identification and characterization of developmental toxins from marine and freshwater microalgae, Comp. Bioch. Physiol. Part C, 145: 61–72 10.1016/j.cbpc.2006.07.011
    Search in Google Scholar
  5. [5] Bogialli S., Bruno M., Curini R., Di Corcia A., Lagana A., 2006, Simple and rapid determination of anatoxin-a in Lake water and Fish muscle tissue by liquid chromatography-tandem mass spectrometry, J. Chromatogr.A., 1122:180–185 http://dx.doi.org/10.1016/j.chroma.2006.04.06410.1016/j.chroma.2006.04.064
    Search in Google Scholar
  6. [6] Bradburn M., Lewis Jr W.M., McCutchan Jr J.H., 2012, Comparative adaptations of Aphanizpmenon and Anabaena for nitrogen fixation under weak irradiance. Freshwat. Biol., 57: 1042–1049. http://dx.doi.org/10.1111/j.1365-2427.2012.02765.x10.1111/j.1365-2427.2012.02765.x
    Search in Google Scholar
  7. [7] Briand J.F., Robillot C., Quiblier-Lloberas C., Bernard C., 2002, A perennial bloom of Planktothrix agardhii (Cyanobacteria) in a shallow eutrophic French lake: limnological and microcystin production studies Arch. Hydrobiol., 153: 605–622 10.1127/archiv-hydrobiol/153/2002/605
    Search in Google Scholar
  8. [8] Bumke-Vogt C., Mailahn W., Chorus I., 1999, Anatoxin-a and neurotoxic Cyanobacteria in German lakes and reservoirs., Environ. Toxicol., 14: 117–125 http://dx.doi.org/10.1002/(SICI)1522-7278(199902)14:1<;117::AID-TOX15>3.0.CO;2-V10.1002/(SICI)1522-7278(199902)14:1<;117::AID-TOX15>3.0.CO;2-V
    Search in Google Scholar
  9. [9] Carmichael W.W., 1992, Cyanobacteria secondary metabolites — the cyanotoxins. J. Appl. Bacteriol., 72: 445–459 http://dx.doi.org/10.1111/j.1365-2672.1992.tb01858.x10.1111/j.1365-2672.1992.tb01858.x
    Search in Google Scholar
  10. [10] Carlson R.E., 1977, A trophic state index for lakes, Limnol. Oceanogr., 22: 361–369 http://dx.doi.org/10.4319/lo.1977.22.2.036110.4319/lo.1977.22.2.0361
    Search in Google Scholar
  11. [11] Cazenave J., Bistoni M.A., Pesce S.F., Wunderlin D.A., 2006, Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus experimentally exposed to microcystin-RR, Aquat. Toxicol., 76: 1–12 http://dx.doi.org/10.1016/j.aquatox.2005.08.01110.1016/j.aquatox.2005.08.011
    Search in Google Scholar
  12. [12] Chen J., Xie P., Li L., Xu J., 2009, First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage, Toxicol. Sci., 108: 81–89 http://dx.doi.org/10.1093/toxsci/kfp00910.1093/toxsci/kfp009
    Search in Google Scholar
  13. [13] Codd, G., 2000, Cyanobacterial toxins, the parception of water quality, and the prioritisation of eutrophication control, Ecol. Eng., 16: 51–60 http://dx.doi.org/10.1016/S0925-8574(00)00089-610.1016/S0925-8574(00)00089-6
    Search in Google Scholar
  14. [14] Dikkeboom R., Van der Knaap W.P.W., Meuleman E.A., Sminia T., 1985, A comparative study on the internal defence system of juvenile and adult Lymnaea stagnalis, Immunology, 55: 547–553
    Search in Google Scholar
  15. [15] El Ghazali I., Saqrane S., Carvalho A.P., Ouahid Y., Del Campo F., Oudra B., Vasconcelos V., 2010, Effect of different microcystin profiles on toxin bioaccumulation in common carp (Cyprinus carpio) larvae via Artemia nauplii, Ecotox. Environ. Safety, 73: 762–770 http://dx.doi.org/10.1016/j.ecoenv.2009.12.01510.1016/j.ecoenv.2009.12.015
    Search in Google Scholar
  16. [16] Furey A., Crowley J., Hamilton B., Lehane M., James K.J., 2005, Strategies to avoid the mis-identification of anatoxin-a using mass spectrometry in the forensic investigation of acute neurotoxic poisoning, J. Chromat. A., 1082: 91–97 http://dx.doi.org/10.1016/j.chroma.2005.05.04010.1016/j.chroma.2005.05.040
    Search in Google Scholar
  17. [17] Golterman H.L., 1971, Methods for chemical analysis of fresh waters. Blackwell, IBP Handbook, Oxford, -, Edinburgh, pp. 166
    Search in Google Scholar
  18. [18] Grabowska M., Mazur-Marzec H., 2010, The effect of cyanobacterial blooms in the Siemianówka dam reservoir on the phytoplankton structure in the Narew river, Hydrobiol. Oceanol. Stud., 40:19–26 http://dx.doi.org/10.2478/s13545-011-0003-x10.2478/s13545-011-0003-x
    Search in Google Scholar
  19. [19] Harada K.I., Tsuji K., Watanabe M.F., Kondo F., 1996, Stability of microcystins from cyanobacteria. III. Effect of pH and temperature, Phycologia, 35: 83–88 http://dx.doi.org/10.2216/i0031-8884-35-6S-83.110.2216/i0031-8884-35-6S-83.1
    Search in Google Scholar
  20. [20] Hardy J., 2008, Final Report. Washington State Recreational Guidance for Microcystins (Provisional) and Anatoxin-a (Interim/Provisional), Washington State Department of Health, Olympia, Washington, pp 19
    Search in Google Scholar
  21. [21] Ibelings B.W., Bruning K., de Jonge J., Wolfstein K., Dionisio Pires L., Postma J., Burger T., 2005, Distribution of microcystins in a lake foodweb: no evidence for biomagnification, Microbial. Ecol., 49: 487–500 http://dx.doi.org/10.1007/s00248-004-0014-x10.1007/s00248-004-0014-x
    Search in Google Scholar
  22. [22] James K.J., Furey A., Sherlock I.R., Stack M.A., Twohing M., 1998, Sensitive determination of anatoxin-a, homoanatoxin-a and their degradation products by liquid chromatography with fluorometric detection, J. Chromatogr. A., 798: 147–157 http://dx.doi.org/10.1016/S0021-9673(97)01207-710.1016/S0021-9673(97)01207-7
    Search in Google Scholar
  23. [23] Kaya K., Sano T., 1999, Total microcystin determination using erythro-2-methyl-3-(methoxy-d3)-4-phenylbutyric acid (MMPB-d3) as the internal standard, Anal. Chim. Acta., 386: 107–112 http://dx.doi.org/10.1016/S0003-2670(99)00012-410.1016/S0003-2670(99)00012-4
    Search in Google Scholar
  24. [24] Kopp R., Mareš J., Palíková M., Navrátil S., Kubíček Z., Ziková A., Klávková J., Bláha L., 2009, Biochemical parameters of blood plasma and content of microcystins in tissues of common carp (Cyprinus carpio L.) from a hypertrophic pond with cyanobacterial water bloom, Aquacult. Res., 40: 1683–1693 http://dx.doi.org/10.1111/j.1365-2109.2009.02285.x10.1111/j.1365-2109.2009.02285.x
    Search in Google Scholar
  25. [25] Kamjunke N., Schmidt K., Pfchlugmacher S., Mehner T., 2002, Consumption of cyanobacteria by roach (Rutilus rutilus): useful or harmful to the fish?, Freshwat. Biol., 47: 243–250 http://dx.doi.org/10.1046/j.1365-2427.2002.00800.x10.1046/j.1365-2427.2002.00800.x
    Search in Google Scholar
  26. [26] Kolmakov V.I., Gladyshev M.I., 2003, Growth and potential photosynthesis of cyanobacteria are stimulated by viable gut passage in crucian carp, Aquat. Ecol., 37: 237–242 http://dx.doi.org/10.1023/A:102580132608810.1023/A:1025801326088
    Search in Google Scholar
  27. [27] Kotak B.G., Zurawell R.W., Prepas E.E., Holmes C.F.B., 1996, Microcystin-LR concentration in aquatic food web compartments from lakes of varying trophic status, Can. J. Fish. Aquat. Sci., 53: 1974–1985 http://dx.doi.org/10.1139/cjfas-53-9-197410.1139/cjfas-53-9-1974
    Search in Google Scholar
  28. [28] Kurmayer R., Christiansen G., Fastner.J, Borner T., 2004, Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium Planktothrix spp, Environ. Microbiol., 6: 831–841 http://dx.doi.org/10.1111/j.1462-2920.2004.00626.x10.1111/j.1462-2920.2004.00626.x
    Search in Google Scholar
  29. [29] 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: 140–148 http://dx.doi.org/10.1016/j.aquatox.2006.06.00410.1016/j.aquatox.2006.06.004
    Search in Google Scholar
  30. [30] Lawton L.A., Edwards C., Codd G.A., 1994, Extraction and high performance liquid chromatographic method for the determination of microcystins in raw and treated waters, Analyst, 119: 1525–1530 http://dx.doi.org/10.1039/an994190152510.1039/an9941901525
    Search in Google Scholar
  31. [31] Li X.Y., Chung I.K., Kim J.I., Lee J.A., 2004, Subchronic oral toxicity of microcystin in common carp (Cyprinus carpio L.) exposed to Microcystis under laboratory conditions, Toxicon 44: 821–827 http://dx.doi.org/10.1016/j.toxicon.2004.06.01010.1016/j.toxicon.2004.06.010
    Search in Google Scholar
  32. [32] Malbrouck C., Kestemont P., 2006, Effects of microcystins on fish, Environ. Toxicol. Chem., 25: 72–86 http://dx.doi.org/10.1897/05-029R.110.1897/05-029R.1
    Search in Google Scholar
  33. [33] Mazur-Marzec H., 2006, Characterization of phycotoxins produced by Cyanobacteria, Oceanol. Hydrobiol. Stud., 35: 85–109
    Search in Google Scholar
  34. [34] Oberemm A., Fastner J., Steinberg C.E.W., 1997. Effects of microcystin-LR and cyanobacterial crude extracts on embryo-larval development of zebrafish (Danio rerio), Wat. Res., 11: 2918–2921 http://dx.doi.org/10.1016/S0043-1354(97)00120-610.1016/S0043-1354(97)00120-6
    Search in Google Scholar
  35. [35] Osswald J., Azevedo J., Vasconcelos V., Guilhermino L., 2011, Experimental determination of the bioconcentration factors for anatoxin-a in juvenile rainbow trout (Oncorhynchus mykiss). Proc. Intern.Ac. Ecol. Environ. Sci., 1(2): 77–86
    Search in Google Scholar
  36. [36] Osswald J, Carvalho A, Claro J., Vasconcelos V., 2009a, Effects of cyanobacterial extracts containing anatoxin-a and of pure anatoxin-a on early developmental stages of carp. Ecotoxicology and Environmental Safety, 72: 473–478 http://dx.doi.org/10.1016/j.ecoenv.2008.05.01110.1016/j.ecoenv.2008.05.01118640721
    Search in Google Scholar
  37. [37] Osswald J., Rellan S., Gago-Martinez A., Vasconcelos V., 2009b, Production of anatoxin-a by cyanobacterial strains isolated from Portugese fresh water systems, Ecotoxicology, 18: 1100–1115 http://dx.doi.org/10.1007/s10646-009-0375-510.1007/s10646-009-0375-5
    Search in Google Scholar
  38. [38] Osswald J., Rellán S., Carvalho A.P., Gago A., Vasconcelos V., 2007, Acute effects of an anatoxin-a producing cyanobacterium on juvenile fish — Cyprinus carpio L, Toxicon, 49: 693–698 http://dx.doi.org/10.1016/j.toxicon.2006.11.01010.1016/j.toxicon.2006.11.010
    Search in Google Scholar
  39. [39] Ozawa K., Yokoyama A., Ishikawa K., Kumagai M., Watanabe M.F., Park H.D., 2003, Accumulation and depuration of microcystin produced by the cyanobacterium Microcystis in a freshwater snail, Limnology, 4: 131–138 http://dx.doi.org/10.1007/s10201-003-0106-110.1007/s10201-003-0106-1
    Search in Google Scholar
  40. [40] Papadimitriou O., 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: 418–427 http://dx.doi.org/10.1002/tox.2051310.1002/tox.20513
    Search in Google Scholar
  41. [41] Pawlik-Skowrońska B., Pirszel J., Kornijów R., 2008, Spatial and temporal variation in microcystin concentrations during perennial bloom of Planktothrix agardhiii in a hypertrophic lake, Ann. Limnol. — Int. J. Lim., 44: 63–68 http://dx.doi.org/10.1051/limn:200802310.1051/limn:2008023
    Search in Google Scholar
  42. [42] Pawlik-Skowrońska B., Skowroński T., Pirszel J., Adamczyk A., 2004, Relationship between cyanobacterial bloom and anatoxin-a and microcystin occurrence in the eutrophic dam reservoir (SE Poland), Pol. J. Ecol., 52: 479–490
    Search in Google Scholar
  43. [43] Pawlik-Skowrońska B., Toporowska M., 2011, Blooms of toxin-producing Cyanobacteria — a real threat in small dam reservoirs at the beginning of their operation, Hydrobiol. Oceanol. Stud., 40(4): 30–37 http://dx.doi.org/10.2478/s13545-011-0038-z10.2478/s13545-011-0038-z
    Search in Google Scholar
  44. [44] Pflugmacher S., Wiegand C., Oberemm A., Beattie K.A., Krause E., Codd G.A., 1998, Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxification, Biochim. Biophys. Acta., 142: 527–533 http://dx.doi.org/10.1016/S0304-4165(98)00107-X10.1016/S0304-4165(98)00107-X
    Search in Google Scholar
  45. [45] Rücker J., Wiedner C., Zippel P., 1997, Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes, Hydrobiologia, 342/343: 107–115 http://dx.doi.org/10.1023/A:101701320803910.1023/A:1017013208039
    Search in Google Scholar
  46. [46] Rantala-Ylinen A., Kana S., Wang H, Rouhiainen L., Wahlsten M., Rizzi E., Berg K., Gugger M., Sivonen K., 2011, Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. Strain 37 and molecular methods to detect potential producers. Appl. Environ. Microbiol., 77: 7271–7278 http://dx.doi.org/10.1128/AEM.06022-1110.1128/AEM.06022-11319486621873484
    Search in Google Scholar
  47. [47] Rymuszka A., Sierosławska A., 2010, Study on apoptotic effects of neurotoxin anatoxin-a on fish immune cells, Neuro. Endocrinol. Lett., 31Suppl. 2: 11–15
    Search in Google Scholar
  48. [48] Sivonen K., Himberg K., Luukkainen R., Niemela S.I., Poon G.K., Codd G.A., 1989, Preliminary Characterization of neurotoxic cyanobacteria blooms and strains from Finland, Toxicol. Assess., 4: 339–352 http://dx.doi.org/10.1002/tox.254004031010.1002/tox.2540040310
    Search in Google Scholar
  49. [49] Sivonen K., Niemelä S.I., Niemi R.M., Lepistö L., Luoma T.H., Räsänen L.A., 1990, Toxic cyanobacteria (blue-green algae) in Finnish fresh and coastal waters, Hydrobiologia, 190: 267–275 http://dx.doi.org/10.1007/BF0000819510.1007/BF00008195
    Search in Google Scholar
  50. [50] Smith et al. 2008
    Search in Google Scholar
  51. [51] Sotero-Santos R.B., Dellamano-Oliveira M.J., Carvalho E.G., Rocha O., 2008, Composition and toxicity of cyanobacterial bloom in a tropical reservoir. Harmful Algae, 7/5: 590–598 http://dx.doi.org/10.1016/j.hal.2007.12.01710.1016/j.hal.2007.12.017
    Search in Google Scholar
  52. [52] Toporowska M., Pawlik-Skowrońska B., Krupa D., Kornijów R., 2010, Winter versus summer blooming of phytoplankton in a shallow lake: effect of hypertrophic conditions, Pol. J. Ecol., 58: 159–168
    Search in Google Scholar
  53. [53] Utermöhl H., 1958, Zur Vervollkommung der quantitative Phytoplanktonmethodik, Mitt. Internat. Verein. Limnol., 2: 1–38 10.1080/05384680.1958.11904091
    Search in Google Scholar
  54. [54] Van Apeldoorn M.E., van Egmond H.P., Speijers G.J.A., Bakker G.J.I., 2007, Toxins of cyanobacteria. A review, Mol. Nutr. Food Res., 51: 7–60 http://dx.doi.org/10.1002/mnfr.20060018510.1002/mnfr.20060018517195276
    Search in Google Scholar
  55. [55] Welker M., Döhren H., 2006, Cyanobacterial peptides — nature’s own combinatorial biosynthesis, FEMS Microbiol. Rev., 30: 530–563 http://dx.doi.org/10.1111/j.1574-6976.2006.00022.x10.1111/j.1574-6976.2006.00022.x16774586
    Search in Google Scholar
  56. [56] WHO, 1999, Toxic Cyanobacteria in Water: A guide to their public health consequences, monitoring and management, Routledge London and New York
    Search in Google Scholar
  57. [57] Wilson A.E., Sarnelle O., Tillmanns A.R., 2006, Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments, Limnol. Oceanogr., 51: 1915–1924 http://dx.doi.org/10.4319/lo.2006.51.4.191510.4319/lo.2006.51.4.1915
    Search in Google Scholar
  58. [58] Zhang D., Xie P., Chen Y., Dai M., Qiu T., Liu Y., Liang G., 2009, Determination of microcystin-LR and its metabolites in snail (Bellemya aeruginosa), shrimp (Macrobrachium nipponensis) and silver carp (Hypophthalmichthys molitrix) from lake Taihu, China, Chemosphere, 76: 974–981 http://dx.doi.org/10.1016/j.chemosphere.2009.04.03410.1016/j.chemosphere.2009.04.03419473685
    Search in Google Scholar
  59. [59] Xie L.Q., Xie P., Guo L.G., 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, Environ. Toxicol., 20: 293–300 http://dx.doi.org/10.1002/tox.2012010.1002/tox.2012015892067
    Search in Google Scholar
  60. [60] Xie L., Xie P., Ozawa K., Honma T., Yokoyama A., Park H-D., 2004, Dynamics of microcystins-LR and _RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment. Environ. Pollut. 127: 431–439 http://dx.doi.org/10.1016/j.envpol.2003.08.01110.1016/j.envpol.2003.08.01114638304
    Search in Google Scholar
DOI: https://doi.org/10.2478/s13545-012-0039-6 | Journal eISSN: 1897-3191 | Journal ISSN: 1730-413X
Journal RSS Feed
Language: English
Page range: 53 - 65
Published on: Nov 6, 2012
Published by: University of Gdańsk
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year
Keywords:
anatoxin-a,
cyanobacteria,
fish,
microcystins,
risk assessment
Related subjects:
Chemistry,
Chemistry, other,
Geosciences,
Geosciences, other,
Life sciences,
Life sciences, other

© 2012 Barbara Pawlik-Skowrońska, Magdalena Toporowska, Jacek Rechulicz, published by University of Gdańsk
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Previous articleVolume 41 (2012): Issue 4 (December 2012)Next article