Skip to main content

Advertisement

Log in

Massive fish mortality and Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

This paper presents a case study of a massive fish mortality during a Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake, Serbia in mid-December 2012. According to a preliminary investigation of the samples taken on November 6 before the fish mortalities and to extended analyses of samples taken on November 15, no values of significant physicochemical parameters emerged to explain the cause(s) of the fish mortality. No industrial pollutants were apparent at this location, and results excluded the likelihood of bacterial infections. Even after freezing, the dissolved oxygen concentration in the water was sufficient for fish survival. High concentrations of chlorophyll a and phaeophytin occurred in the lake, and phytoplankton bloom samples were lethal in Artemia salina bioassays. A bloom of the cyanobacterium C. raciborskii was recorded during November. Although the A. salina bioassays indicated the presence of toxic compounds in the cyanobacterial cells, the cyanotoxins, microcystins, cylindrospermopsin and saxitoxin were not detected.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ács A, Kovács AW, Csepregi JZs, Törő N, Kiss Gy, Győri J, Vehovszky Á, Kováts N, Farkas A (2013) The ecotoxicological evaluation of Cylindrospermopsis raciborskii from Lake Balaton (Hungary) employing a battery of bioassays and chemical screening. Toxicon 70:98–106

    Article  Google Scholar 

  • Allowed quantity of metals in foodstuffs (2002) Official Gazette of Republic of Serbia no. 32/2002. Belgrade

  • Andersen RJ, Luu HA, Chen DZ, Holmes CF, Kent ML, Le Blanc M, Taylor FJ, Williams DE (1993) Chemical and biological evidence links microcystins to salmon netpen liver disease. Toxicon 31:1315–1323

    Article  CAS  Google Scholar 

  • APHA (1992) Standard methods for the examination of water and wastewater, 18th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • APHA, AWWA, WEF (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Asocciation, Washington, DC

    Google Scholar 

  • Barica J (1984) Empirical models for prediction of algal blooms and collapses, winter oxygen depletion and a freeze-out effect in lakes: summary and verification. Verh Int Verein Limnol 22:309–319

    CAS  Google Scholar 

  • Barica J, Mathias JA (1979) Oxygen depletion and winterkill risk in small prairie lakes under extended ice cover. J Fish Res Board Can 36:980–986

    Article  Google Scholar 

  • Bury NR, Eddy FB, Codd GA (1995) The effects of the cyanobacterium Microcystis aeruginosa, the cyanobacterial hepatotoxin microcystin-LR and ammonia on growth rate and ionic regulation of brown trout. J Fish Biol 46(6):1042–1054

    CAS  Google Scholar 

  • Bury NR, Eddy FB, Codd GA (1996) Stress responses of brown trout, Salmo trutta L. to the cyanobacterium Microcystis aeruginosa. Environ Toxic Water 11:187–194

    Article  CAS  Google Scholar 

  • Bury NR, Codd GA, Wendelaar Bonga SF, Flik G (1998) Fatty acids from the cyanobacterium Microcystis aeruginosa with potent inhibitory effects on fish gill Na+/K+ -ATPase activity. J Exp Biol 201:81–89

    CAS  Google Scholar 

  • Ćirić M, Marković Z, Dulić Z, Subakov-Simić G (2010) First report of cyanobacterium Cylindrospermompsis raciborskii from carp ponds in Serbia. In: The 8th International Conference on Toxic Cyanobacteria (ICTC8); August 29-September 4 2010, Istanbul, Turkey, pp 14

  • Cvijan M, Fužinato S (2011) The first finding of Cylindrospermopsis raciborskii (Woloszińska) Seenayya et Subba Raju 1972 (Cyanoprokaryota) in Serbia. Arch Biol Sci 63:507–510

    Article  Google Scholar 

  • Diener M, Erler K, Hiller S, Christian B, Luckas B (2006) Determination of paralytic shellfish poisoning (PSP) toxins in dietary supplements by application of a new HPLC/FD method. Eur Food Res Technol 224:147–151

    Article  CAS  Google Scholar 

  • Đorđević NB, Simić SB (2014) Cyanobacterial blooms in oligosaline and alkaline microaccumulation before and after rehabilitation. Pol J Environ Stud 23(6):1975–1982

    Google Scholar 

  • Felföldy L (1980) A biològiai vizminösités. In: Vízügyi hidrobiológia, pp 1–263

  • Francy DS, Darner RA (1998) Factors affecting Escherichia coli concentrations at Lake Erie public bathing beaches: US Geological Survey Water-Resources Investigations. Report 98–4241

  • Francy DS, Bushon RN, Brady AMG, Kephart CM, Stoeckel DM (2005) Quality assurance/quality control manual, APPENDIX C6 Sediment Sample Collection, Processing, and Analysis Using Colilert Quanti-tray/2000® Method for Escherichia coli. USGS Ohio Water Science Center, Ohio Water Microbiology Laboratory, Columbus

    Google Scholar 

  • Haslouer SG (1979) Natural and pollution–caused fish kills in Kansas during 1978. Trans Kansas Acad Sci 82:197–204

    Article  CAS  Google Scholar 

  • Hautala H, Lamminmäki U, Spoof L, Nybom S, Meriluoto J, Vehniäinen M (2012) Quantitative PCR detection and improved sample preparation of microcystin-producing Anabaena, Microcystis and Planktothrix. Ecotoxicol Environ Safe 87:49–56

    Article  Google Scholar 

  • Hoff-Risseti C, Dorr FA, Schaker PDC, Pinto E, Werner VR, Fiore MF (2013) Cylindrospermopsin and saxitoxin synthetase genes in Cylindrospermopsis raciborskii strains from Brazilian freshwater. PLoS One 8(8):e74238

    Article  CAS  Google Scholar 

  • http://www.ribolov.co.rs/prijava-veternici-zbog-pomora-riba-u-aleksandrovackom-jezeru/. Accessed 10 March 2016

  • International Standard ISO 10260 E (1992) Water quality—measurement of biochemical parameters: Spectrometric determination of the chlorophyll-a concentration. 1st edn, Geneva

    Google Scholar 

  • Kann J, Smith VH (1999) Estimating the probability of exceeding elevated pH values critical to fish populations in a hypereutrophic lake. Can J Fish Aquat Sci 56(12):2262–2270

    Google Scholar 

  • Karadžić V, Simić GS, Natić D, Ržaničanin A, Ćirić M, Gačić Z (2013) Changes in the phytoplankton community and dominance of Cylindrospermopsis raciborskii (Wolosz.) Subba Raju in a temperate lowland river (Ponjavica, Serbia). Hydrobiologia 711(1):43–60

    Article  Google Scholar 

  • Kenefick SL, Hrudey SE, Peterson HG, Prepas EE (1993) Toxin release from Microcystis aeruginosa after chemical treatment. Water Sci Tech 27(3–4):433–440

    CAS  Google Scholar 

  • Kiss T, Vehovszky Á, Hiripi L, Kovács A, Vörös L (2002) Membrane effects of toxins isolated from a cyanobacterium, Cylindrospermopsis raciborskii, on identified molluscan neurons. Comp Biochem Physiol C 131:167–176

    CAS  Google Scholar 

  • Kiviranta JA, Sivonen K, Niemelä SI (1991) Detection of toxicity of cyanobacteria by A. salina bioassay. Environ Tox Water 6:423–436

    Article  CAS  Google Scholar 

  • Kokocinski M, Mankiewicz-Boczek J, Jurczak T, Spoof L, Meriluoto J, Rajmonczyk E, Hautala H, Vehniäinen M, Pawelczyk J, Soininen J (2013) Aphanizomenon gracile (Nostocales), a cylindrospermopsin-producing cyanobacterium in Polish lakes. Environ Sci Pollut R 20:5243–5264

    Article  CAS  Google Scholar 

  • Kramer DL (1987) Dissolved oxygen and fish behavior. Environ Biol Fish 18:81–92

    Article  Google Scholar 

  • La VT, Cooke SJ (2011) Advancing the science and practice of fish kill investigations. Rev Fish Sci 19(1):21–33

    Article  Google Scholar 

  • Lagos N, Onodera H, Zagatto PA, Andrinolo D, Azevedo SM, Oshima Y (1999) The first evidence of paralytic shellfish toxins in the fresh water cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37(10):1359–1373

    Article  CAS  Google Scholar 

  • Lam AKY, Prepas EE, Spink D, Hrudey SE (1995) Chemical control of hepatotoxic phytoplankton blooms: implications for human health. Water Res 29(8):1845–1854

    Article  CAS  Google Scholar 

  • LeGreslay M, McDermott G (2010) Counting chamber methods for quantitative phytoplankton analysis-Haemacytometer, Palmer-Maloney cell and Sedgewick-Rafter cell. In: Karlson B, Cusack C, Bresnan E (eds) Microscopic and molecular methods for quantitative phytoplancton analysis. Intergovernmental Oceanographic Commission, UNESCO, Paris, pp 25–30

    Google Scholar 

  • Magalhaes VF, Soares RM, Azevedo SMFO (2001) Microcystin contamination in fish from Jacarepagua Lagoon: ecological implication and human health risk. Toxicon 39:1077–1085

    Article  CAS  Google Scholar 

  • Metcalf JS, Codd GA (2012) Cyanotoxins. In: Whitton BA (ed) Ecology of cyanobacteria II. Their diversity in time and space. Springer, Dordrecht, pp 651–675

    Chapter  Google Scholar 

  • Meyer FP, Barclay LA (1990) Field manual for the investigation of fish kills. Resource publication 177. US Fish and Wildlife Service, Washington, DC, pp 1–120

    Google Scholar 

  • Meyer BN, Ferrigni NR, Putnam JE, Jacobson LB, Nichols DE, McLaughlin JL (1982) Brine shrimp: a convenient general bioassay for active plants constituents. Planta Med 45:31–34

    Article  CAS  Google Scholar 

  • Molica RJR, Onodera H, Garcia C, Andrinolo D, Nascimento S, Meguro H, Oshima Y, Azevedo SMFO, Lagos N (2002) Toxins in freshwater cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) isolated from Tabocas reservoir in Caruaru, Brazil, including demonstration of a new saxitoxin analogue. Phycologia 41:606–611

    Article  Google Scholar 

  • Molica RJR, Oliveira EJA, Carvalho PVVC, Costa APNSF, Cunha MCC, Melo GL, Azevedo SMFO (2005) Ocurrence of saxitoxins and anatoxin-a(s)-like anticholinesterase in Brazilian drinking water supply. Harmful Algae 4:743–753

    Article  CAS  Google Scholar 

  • Myers DN, Stoeckel DM, Bushon RN, Francy DS, Brady AMG (2007) Fecal indicator bacteria: US Geological Survey Techniques of Water-Resources Investigations, Book 9, chap. A7, section 7.1 (version 2.0). http://water.usgs.gov/owq/FieldManual/Chapter7/index.html

  • Natić D, Jovanović D, Knežević T, Karadžić V, Bulat Z, Matović V (2012) Microcystin-LR insurface water of Ponjavica River. Vojnosanit Pregl 69(9):753–758

    Article  Google Scholar 

  • Nováková K, Kohoutek J, Adamovsky O, Brack W, Krauss M, Bláha L (2013) Novel metabolites in cyanobacterium Cylindrospermopsis raciborskii with potencies to inhibit gap junctional intercellular communication. J Hazard Mat 262:571–579

    Article  Google Scholar 

  • Oshima Y (1995) Post-column derivatization liquid-chromatographic method for paralytic shellfish toxins. J AOAC Int 78(2):528–532

    CAS  Google Scholar 

  • Padisák J (1997) Cylindropsermopsis raciborskii (Woloszynska) Seenaya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv Hydrobiol Suppl 107(4):563–593

    Google Scholar 

  • Padisák J, Reynolds CS (1998) Selection of phytoplankton associations in Lake Balaton, Hungary, in response to eutrophication and restoration measures, with special reference to the cyanoprokaryotes. Hydrobiologia 384:41–53

    Article  Google Scholar 

  • Robarts RD, Waiser MJ, Arts MT, Evans MS (2005) Seasonal and diel changes of dissolved oxygen in a hypertrophic prairie lake. Lakes & Reservoirs: Res Manag 10:167–177

    Article  CAS  Google Scholar 

  • Rodger HD, Turnbull T, Edwards C, Codd GA (1994) Cyanobacteria (blue-green algae) bloom and associated pathology in brown trout, Salmo trutta L, in Loch Leven, Scotland. J Fish Dis 17:172–181

    Article  Google Scholar 

  • Rosen BH, Loftin KA, Smith CE, Lane RF, Keydel SP. (2010) Microphotographs of cyanobacteria documenting the effects of various cell-lysis techniques: U.S. Geological Survey Open-File Report 2010-1289. pp 203

  • Sayfritz SJ, Aasen JA, Aune T (2008) Determination of paralytic shellfish poisoning toxins in Norwegian shellfish by liquid chromatography with fluorescense and tandem mass spectrometry. Toxicon 52(2):330–340

    Article  CAS  Google Scholar 

  • Schrembri MA, Neilan BA, Saint CP (2001) Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ Toxicol 16(5):413–421

    Article  Google Scholar 

  • Simić S, Mišćević M, Đorđević N, Popović N (2011) Cyanobacteria in Aleksandrovac Lake- before and after revitalisation. In: Cyanobacteria and human health. 16th Academy of Studenica, July 1–3 2011, Novi Sad. Serbia, pp 42

  • Spoof L, Vesterkvist P, Lindholm T, Meriluoto J (2003) Screening for cyanobacterial hepatotoxins, microcystins and nodularin, in environmental water samples by reversed-phase liquid chromatography-electrospray ionisation mass spectrometry. J Chromatogr A 1020:105–119

    Article  CAS  Google Scholar 

  • Spoof L, Berg KA, Rapala J, Lahti K, Lepistö L, Metcalf JS, Codd GA, Meriluoto J (2006) First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environ Toxicol 21:552–560

    Article  CAS  Google Scholar 

  • Threshold limits of pollutants in surface and ground waters and sediments (2012) Official Gazette of Republic of Serbia no. 50/2012. Belgrade

  • Threshold limits for priority substances (2011) Official Gazette of Republic of Serbia no. 35/2011. Belgrade

  • Threshold limits of ecological, chemical and quantitative status of surface and groundwater (2011) Official Gazette of Republic of Serbia no. 74/2011. Belgrade

  • Thronson A, Quigg A (2008) Fifty-five years of fish kills in coastal Texas. Estuaries Coasts 31:802–813

    Article  CAS  Google Scholar 

  • van de Riet J, Gibbs RS, Muggah PM, RourkeWA MacNeil JD, Quilliam MA (2011) Liquid chromatography post-column oxidation (PCOX) method for the determination of paralytic shellfish toxins in mussels, clams, oysters and scallops: collaroborative study. J AOAC Int 94:1154–1176

    Google Scholar 

  • Vehovszky Á, Kovács AW, Szabó H, Győri J, Farkas A (2012) Neurotoxic effects evoked by cyanobacterial extracts suggest multiple receptors involved in electrophysiological responses of molluscan (CNS, heart) models. Acta Biol Hung 63:160–170

    Article  CAS  Google Scholar 

  • Vehovszky A, Kovács WA, Farkas A, Györi J, Szabó H, Vasas G (2015) Pharmacological studies confirm neurotoxic metabolite(s) produced by the bloom-forming Cylindrospermopsis raciborskii in Hungary. Environ Toxicol 30(5):501–512

    Article  CAS  Google Scholar 

  • Wohlsen T, Bates J, Vesey G, Robinson WA, Katouli M (2006) Evaluation of the methods for enumerating coliform bacteria from water samples using precise reference standards. Lett Appl Microbiol 42:350–356

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the funding of the Ministry of Education, Science and Technological Development of the Serbian Government (project number: 176020) and, also, COST Action ES1105 “CYANOCOST- Cyanobacterial blooms and toxins in water resources: Occurrence, impacts and management” for adding value to this study through networking and knowledge-sharing with European experts in the field.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Damjana Drobac.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Svirčev, Z., Obradović, V., Codd, G.A. et al. Massive fish mortality and Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake. Ecotoxicology 25, 1353–1363 (2016). https://doi.org/10.1007/s10646-016-1687-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-016-1687-x

Keywords

Navigation