, Volume 18, Issue 1, pp 34–46 | Cite as

The influence of a toxic cyanobacterial bloom and water hydrology on algal populations and macroinvertebrate abundance in the upper littoral zone of Lake Krugersdrift, South Africa

  • Paul J. Oberholster
  • Anna-Maria Botha
  • Peter J. Ashton


The biological interactions and the physical and chemical properties of the littoral zone of Lake Krugersdrift were studied for a 4-month period when a dense, toxic cyanobacterial bloom dominated by Microcystis aeruginosa was present in the main lake basin. The presence of a toxic strain of M. aeruginosa was confirmed through the use of ELISA and molecular markers that detect the presence of the mcyB and mcyD genes of the mcy gene cluster that synthesizes microcystin. An increase in Microcystis toxicity at sites dominated by the cyanobacterial scum was accompanied by an increase in total abundance of the macroinvertebrate families Hirudinae, Chironomidae, and Tubificidae. Sites located away from the cyanobacterial scum had a lower abundance but a higher diversity of macroinvertebrates. The water quality under the Microcystis scum was characterized by low pH values, low concentrations of dissolved oxygen, and lower total alkalinity values. The periphytic alga Ulothrix zonata was absent in areas dominated by the cyanobacterial scum, possibly as a result of overshadowing by the scum or direct toxic allelopathic effects on growth and photosynthesis. The diatom Diatoma vulgare dominated the benthic algal flora beneath the cyanobacterial scum.


Cyanobacterial scum Macroinvertebrates Littoral zone Functional feeding groups mcy gene cluster 


  1. Allanson BR, Hart RC, O’Keeffe JH, Robarts RD (1990) Inland waters of Southern Africa: an ecological perspective. Kluwer Academic Publishers, DordrechtGoogle Scholar
  2. Allen JD (1995) Stream ecology. Chapman and Hall, London, pp 1–338Google Scholar
  3. American Public Health Association (APHA), American Water Works Association (AWWA), and Water Pollution Control Federation (WPCF) (1980) Standard methods for the examination of water and wastewater, 15th edn. American Public Health Association, Washington, DCGoogle Scholar
  4. American Public Health Association (APHA) (1989) Standard methods for the examination of water and wastewater, 17th edn. American Public Health Association, Washington, DCGoogle Scholar
  5. Bagchi SN, Palod A, Chaunan VS (1990) Algicidal properties of a bloom forming blue-green alga, Oscillatoria sp. J Basic Microbiol 30:21–29. doi: 10.1002/jobm.3620300106 CrossRefGoogle Scholar
  6. Ball RC, Bahr TG (1975) Intensive survey: Red Cedar River, Michigan. In: Whitton BA (ed) River ecology. Blackwell, Oxford, pp 431–460Google Scholar
  7. Beattie KA, Kaya K, Codd GA (2000) The cyanobacterium Nodularia PCC 7804, of freshwater origin, produces [L-Har2] nodularin. Phytochemistry 54:57–61CrossRefGoogle Scholar
  8. Berger WH, Parker FL (1970) Diversity of planktonic Foraminifera in deep sea sediments. Science 168:1345–1347. doi: 10.1126/science.168.3937.1345 CrossRefGoogle Scholar
  9. Botha-Oberholster A-M, Oberholster PJ (2007) PCR based markers for detection and identification of toxic cyanobacteria. WRC Report No. 1502/1/07. Water Research Commission, Pretoria, pp 1–58Google Scholar
  10. Boyer GL, Satchwell MF, Shambaugh A, Watzin M, Mihuc TB, Rosen B (2004) The occurrence of cyanobacterial toxins in Lake Champlain Waters. In: Manley T, Manley P, Mihuc TB (eds) Lake Champlain: partnerships and research in the new millennium. Kluwer Academic Press, Dordrecht, pp 241–257Google Scholar
  11. Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 270:78–86CrossRefGoogle Scholar
  12. Carter-Lund H, Lund JWG (1995) Freshwater algae—their microscopic world explored. Biopress Ltd, pp 1–360Google Scholar
  13. Chong MWK, Wong PKS, Shaw GR, Seawright AA (2002) Toxicity and uptake mechanism of cylindrospermopsin and lophyrotomin in primary rat hepatocytes. Toxicon 40:205–211. doi: 10.1016/S0041-0101(01)00228-8 CrossRefGoogle Scholar
  14. Codd GA, Metcalf JS, Beattie KA (1999) Retention of Microcystis aeruginosa and microcystin by salad (Lactuca sativa) after spray irrigation with water containing cyanobacteria. Toxicon 37:1181–1185. doi: 10.1016/S0041-0101(98)00244-X CrossRefGoogle Scholar
  15. Figueredo CC, Giani A (2001) Seasonal variations in the diversity and species richness of phytoplankton in a tropical eutrophic reservoir. Hydrobiologia 445:165–174. doi: 10.1023/A:1017513731393 CrossRefGoogle Scholar
  16. Gausch H, Ivorra N, Lehmann V, Paulsson M, Real M, Sabater T (1998) Community composition and sensitivity of periphyton to atrazine in flowing waters: the role of environmental factors. J Appl Phycol 10:203–213. doi: 10.1023/A:1008035212208 CrossRefGoogle Scholar
  17. Grobbelaar JU (1985) Phytoplankton productivity in turbid waters. J Plankton Res 7:653–663. doi: 10.1093/plankt/7.5.653 CrossRefGoogle Scholar
  18. Grobbelaar JU (1992) Nutrient versus physical factors in determining the primary productivity of waters with high inorganic turbidity. Hydrobiologia 238:177–182. doi: 10.1007/BF00048786 CrossRefGoogle Scholar
  19. Grobbelaar JU, Botes E, Van den Heever JA, Botha A-M, Oberholster PJ (2004) Scope and dynamics of toxin produced by cyanophytes in the freshwaters of South Africa and the implications for human and other users. WRC Report No: 1029/1/04. Water Research Commission, Pretoria, pp 1–9Google Scholar
  20. Hellawell JM (1986) Biological indicators of freshwater pollution and environmental management. Elsevier Applied Science, LondonGoogle Scholar
  21. Hisbergues M, Christiansen G, Rouhiainen L, Sivonen K, Börner T (2003) PCR-based identification of microcystin-producing genotypes of different cyanobacterial genera. Arch Microbiol 180:402–410. doi: 10.1007/s00203-003-0605-9 CrossRefGoogle Scholar
  22. Ikawa M, Sasner JJ, Haney JF (2001) Activity of cyanobacterial and algal odor compounds found in lake waters on green alga Chlorella pyrenoidosa growth. Hydrobiologia 443:19–22. doi: 10.1023/A:1017535801766 CrossRefGoogle Scholar
  23. Kaebernick M, Dittman E, Börner T, Neilan BA (2000) Multiple alternate transcripts direct the biosynthesis of microcystin, a cyanobacterial non-ribosomal peptide. Appl Environ Microbiol 68:449–455. doi: 10.1128/AEM.68.2.449-455.2002 CrossRefGoogle Scholar
  24. Kahlert M, Andren CM (2005) Benthic diatoms as valuable indicators of acidity. Verh Int Verein Limnol 29:635–639Google Scholar
  25. Kiviranta J, Sivonen K, Lahti K, Luukkainen R (1991) Production and biodegradation of cyanobacterial toxins—a laboratory study. Arch Hydrobiol 121:281–294Google Scholar
  26. Lang C (1984) Eutrophication of Lake Leman and Neuchatel (Switzerland) indicated by oligochaete communities. Hydrobiologia 114:131–138. doi: 10.1007/BF00027907 CrossRefGoogle Scholar
  27. MacKintosh RW, Dalby KN, Campbell DG, Codd GA (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett 264:187–192. doi: 10.1016/0014-5793(90)80245-E CrossRefGoogle Scholar
  28. Meißner K, Dittmann E, Börmer T (1996) Toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa contain sequences homologous to peptide synthetase genes. FEMS Microbiol Lett 135:295–303. doi: 10.1016/0378-1097(95)00469-6 CrossRefGoogle Scholar
  29. Merrit RW, Cummins KW (1996) An introduction to the aquatic insects of North America, 3rd edn. Kendal/Hunt, Dubuque, Iowa, USAGoogle Scholar
  30. NIWR (National Institute for Water Research) (1985) The limnology of Hartbeespoort dam. South African National Scientific Programmes Report No. 110. Foundation for Research Development, PretoriaGoogle Scholar
  31. Niyogi DK, McKnight DM, Lewis WM (1999) Influences of water and substrate quality for periphyton in a Montana stream affected by acid mine drainage. Limnol Oceanogr 44:804–809Google Scholar
  32. Oberholster PJ (2004) Assessing genetic diversity and identification of Microcystis aeruginosa strains through AFLP and PCR-RFLP analysis. M.Sc. Thesis, University of the Free State, Bloemfontein, South Africa, pp 1–114Google Scholar
  33. Oberholster PJ, Botha A-M (2007) Use of PCR based technologies for risk assessment of a winter cyanobacterial bloom in Lake Midmar, South Africa. Afr J Biotechnol 6:1794–1805Google Scholar
  34. Oberholster PJ, Botha A-M, Cloete TE (2005a) An overview of toxic freshwater cyanobacteria in South Africa with special reference to risk, impact and detection by molecular marker tools. Biokem 17:57–71Google Scholar
  35. Oberholster PJ, Botha A-M, Cloete TE (2005b) Using a battery of bioassays, benthic phytoplankton and the AUSRIVAS method to monitor long-term coal tar contaminated sediment in the Cache la Poudre River, Colorado. Water Res 39:4913–4924. doi: 10.1016/j.watres.2005.08.029 CrossRefGoogle Scholar
  36. Patrick R, Reimer CW (1975) The diatoms of the United States exclusive of Alaska and Hawaii, vol 2. National Academy of Sciences, Philadelphia, USA Part 1. Monograph 13Google Scholar
  37. Pitois S, Jackson MH, Wood BJB (2001) Sources of the eutrophication problems associated with toxic algae: an overview. J Environ Health 64:25–32Google Scholar
  38. Poole HH, Atkins WRG (1929) Photo-electric measurements of submarine illumination throughout the year. J Mar Biol Assoc UK 16:297–324CrossRefGoogle Scholar
  39. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim Biophys Acta 975:384–394. doi: 10.1016/S0005-2728(89)80347-0 CrossRefGoogle Scholar
  40. Prat N, Ward JV (1994) The tamed river. In: Margalef R (ed) Limnology now: a paradigm of planetary problems. Elsevier Science B.V.,Amsterdam, The Netherlands, pp 219–236Google Scholar
  41. Republic of South Africa (1998) The National Water act (Act No. 36 of 1998) Government of the Republic of South Africa, Pretoria, South AfricaGoogle Scholar
  42. Rondel C, Arfi R, Corbn D, le Bihan F, Hadji Ndour E, Lazzaro X (2008) A cyanobacterial bloom prevents fish trophic cascades. Freshw Biol 53:637–651. doi: 10.1111/j.1365-2427.2007.01894.x CrossRefGoogle Scholar
  43. Shannon CE, Weaver W (1949) The mathematical theory of communications. University of Illinois Press, UrbanaGoogle Scholar
  44. Strayer D (1985) The benthic micrometazoans of Mirror Lake, New Hampshire. Arch Hydrobiol 72:287–426Google Scholar
  45. Sukenik A, Eshkol RL, Hadas O (2002) Inhibition of growth and photosynthesis of the Dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnol Oceanogr 47:1656–1663Google Scholar
  46. SYSTAT (1997) Systat® 7.0.1 for Windows®: Statistics. SPSS Inc, Chicago, USAGoogle Scholar
  47. Thorp JH, Covich AP (2001) Ecology and classification of North American freshwater invertebrates. Academic Press, San Diego, California, USA, pp 1–775CrossRefGoogle Scholar
  48. Tillett D, Parker DL, Neilan BA (2001) Detection of toxigenicity by a probe for the microcystin synthetase A gene (mcyA) of the cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies. Appl Environ Microbiol 67:2810–2818. doi: 10.1128/AEM.67.6.2810-2818.2001 CrossRefGoogle Scholar
  49. Ueno Y, Nagata S, Tsutsumi T, Hasegawa A, Yoshida F, Suttajit M et al (1996) Survey of microcystins in environmental water by a highly sensitive immunoassay based on monoclonal antibody. Nat Toxins 4:271–276Google Scholar
  50. Van Ginkel CE (2004) A national survey of the incidence of cyanobacterial blooms and toxin produced in major impoundments. Internal Report No. N/000/00/DEQ/0503. Resource Quality Services, Department of Water Affairs and Forestry, Pretoria, pp 1–44Google Scholar
  51. Van Ginkel CE, Hohls BC, Belcher E, Vermaak E, Gerber A (2001) Assessment of the Trophic Status Project. Internal report No. N/0000/00/DEQ/1799. Institute for Water Quality Studies, Department of Water Affairs and Forestry, Pretoria, pp 1–334Google Scholar
  52. Van Ginkel CE, Silberbauer MJ, Vermaak E (2000) The seasonal and spatial distribution of cyanobacteria in South African surface waters. Verh Int Verein Limnol 27:871–878Google Scholar
  53. Voelz NJ, Ward JV (1991) Biotic responses along the recovery gradient of a regulated stream. Can J Fish Aquat Sci 48:2477–2490. doi: 10.1139/f91-289 CrossRefGoogle Scholar
  54. Von Brand T (1944) Occurrence of anaerobiosis among invertebrates. Biodynamica 4:185–328Google Scholar
  55. Walmsley RD, Butty M, Van Der Piepen H, Grobler DC (1980) Light penetration and the interrelationships between optical parameters in a turbid subtropical impoundment. Hydrobiologia 70:145–157. doi: 10.1007/BF00015500 CrossRefGoogle Scholar
  56. Watson SB, Brownlee B, Satchwill T, Hargesheimer EE (2000) Quantitative analysis of trace levels of geosmin and MIB in source and drinking water using headspace SPME. Water Res 34:2818–2828. doi: 10.1016/S0043-1354(00)00027-0 CrossRefGoogle Scholar
  57. Wehr JD, Sheath RG (2001) Freshwater algae of North America, ecology and classification. Academic Press, San Diego, USA, pp 775–804Google Scholar
  58. White SH, Duivenvoorden LJ, Fabbro LD (2005) Impacts of a toxic Microcystis bloom on the macroinvertebrate fauna of Lake Elphinstone, Central Queensland, Australia. Hydrobiologia 548:117–126. doi: 10.1007/s10750-005-4756-3 CrossRefGoogle Scholar
  59. Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites—a short review. Toxicol Appl Pharmacol 203:201–218. doi: 10.1016/j.taap.2004.11.002 CrossRefGoogle Scholar
  60. Willen E (1976) A simplified method of phytoplankton counting. Br Phycol J 11:265–278. doi: 10.1080/00071617600650551 CrossRefGoogle Scholar
  61. Willen E (1991) Planktonic diatoms—an ecological review. Algol Stud 62:69–106 Stuttgart, Augustus 1991Google Scholar
  62. Winter JG, Dillon PJ, Paterson C, Reid RA, Somers KM (2003) Impacts of golf course construction and operation on headwater streams: bioassessment using benthic algae. Can J Bot 81:848–858. doi: 10.1139/b03-081 CrossRefGoogle Scholar
  63. Zohary T (1985) Hyperscum of the cyanobacterium Microcystis aeruginosa in a hypertrophic lake (Hartbeespoort Dam, South Africa). J Plankton Res 7:399–409. doi: 10.1093/plankt/7.3.399 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Paul J. Oberholster
    • 1
  • Anna-Maria Botha
    • 2
  • Peter J. Ashton
    • 1
  1. 1.CSIR Natural Resources and the EnvironmentPretoriaSouth Africa
  2. 2.Department of GeneticsUniversity of PretoriaPretoriaSouth Africa

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