Skip to main content
SpringerLink
Log in

Spatial and temporal variability in the relationship between cyanobacterial biomass and microcystins

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The increasing incidence of toxic cyanobacterial blooms, together with the difficulties to reliably predict cyanobacterial toxin (e.g. microcystins) concentration, has created the need to assess the predictive ability and variability of the cyanobacterial biomass–microcystin relationship, which is currently used to assess the risk to human and ecosystems health. To achieve this aim, we assessed the relationship between cyanobacterial biomass and microcystin concentration on a spatiotemporal scale by quantifying the concentration of cyanobacterial biomass and microcystin in eight lakes over 9 months. On both a temporal and spatial scale, the variability of microcystin concentration exceeded that of cyanobacterial biomass by up to four times. The relationship between cyanobacterial biomass and microcystin was weak and site specific. The variability of cyanobacterial biomass only explained 25 % of the variability in total microcystin concentration and 7 % of the variability of cellular microcystin concentration. Although a significant correlation does not always imply real cause, the results of multiple linear regression analysis suggest that the variability of cyanobacterial biomass and cellular microcystin concentration is influenced by salinity and total phosphorus, respectively. The weak cyanobacterial biomass–microcystin relationship, coupled with the fact that microcystin was present in concentrations exceeding the WHO drinking water guidelines (1 μg L−1) in most of the collected samples, emphasizes the high risk of error connected to the traditional indirect microcystin risk assessment method.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Al-Shehri, A. M. (2010). Toxin-producing blooms of the cyanobacterium Microcystis aeruginosa in rainwater ponds in Saudi Arabia. Oceanological and Hydrobiological Studies, 39(4), 171–187.

    Google Scholar 

  • ANZECC (2000). Australian and New Zealand guideline for fresh and marine water quality. Canberra: ANZECC

  • Baldia, S. F., Conaco, M. C. G., Nishijima, T., Imanishi, S., & Harada, K. (2003). Microcystin production during algal bloom occurrence in Laguna de Bay, the Philippines. Fisheries Science, 69(1), 110–116.

    CAS  Google Scholar 

  • Ballot, A., Pflugmacher, S., Wiegand, C., Kotut, K., & Krienitz, L. (2003). Cyanobacterial toxins in Lake Baringo, Kenya. Limnologica—Ecology and Management of Inland Waters, 33(1), 2–9.

    CAS  Google Scholar 

  • Barrington, D. J., & Ghadouani, A. (2008). Application of hydrogen peroxide for the removal of toxic cyanobacteria and other phytoplankton from wastewater. Environmental Science and Technology, 42(23), 8916–8921.

    CAS  Google Scholar 

  • Barrington, D. J., Ivey, G. N., & Ghadouani, A. (2011). Environmental factors and the application of hydrogen peroxide for the removal of toxic cyanobacteria from waste stabilization ponds. Journal of Environmental Engineering, 137(10).

  • Beutler, M., Wiltshire, K. H., Meyer, B., Moldaenke, C., Luring, C., Meyerhofer, M., et al. (2002). A fluorometric method for the differentiation of algal populations in vivo and in situ. Photosynthesis Research, 72(1), 39–53.

    CAS  Google Scholar 

  • Briand, E., Gugger, M., Francois, J. C., Bernard, C., Humbert, J. F., & Quiblier, C. (2008). Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (cyanobacterium) population. Applied and Environmental Microbiology, 74(12), 3839–3848.

    CAS  Google Scholar 

  • Briand, J. F., Jacquet, S., Flinois, C., Avois-Jacquet, C., Maisonnette, C., Leberre, B., et al. (2005). Variations in the microcystin production of Planktothrix rubescens (Cyanobacteria) assessed from a four-year survey of Lac du Bourget (France) and from laboratory experiments. Microbial Ecology, 50(3), 418–428.

    Google Scholar 

  • Carmichael, W. W., Azevedo, S. M. F. O., An, J. S., Molica, R. J. R., Jochimsen, E. M., Lau, S., et al. (2001). Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environmental and Health Perspective, 109(7), 663–668.

    CAS  Google Scholar 

  • Carrasco, D., Moreno, E., Sanchis, D., Wormer, L., Paniagua, T., Cueto, A. D., et al. (2006). Cyanobacterial abundance and microcystin occurrence in Mediterranean water reservoirs in Central Spain: microcystins in the Madrid area. Journal of Phycology, 41(3), 281–291.

    CAS  Google Scholar 

  • Chen, J., Han, F., Wang, F., Zhang, H. M., & Shi, Z. (2012). Accumulation and phytotoxicity of microcystin–LR in rice (Oryza sativa). Ecotoxicology and Environmental Safety, 76(2), 193–199.

    CAS  Google Scholar 

  • 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. Toxicological Sciences, 108(1), 81–89.

    CAS  Google Scholar 

  • Chorus, I., & Bartram, J. (1999). Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. London: E & FN Spon.

    Google Scholar 

  • Clesceri, L. S., Greenberg, A. E., & Eaton, A. D. (1998). Standard methods for the examination of water and wastewater, 20th Ed. Washington, DC: American Public Health Association

  • Davis, J. A., Rosich, R. S., Bradley, J. S., Growns, J. E., Schmidt, L. G., & Cheal, F. (1993). Wetland classification on the basis of water quality and invertebrate community data. Wetlands of the Swan Coastal Plain, 6, 242. Water Authority of Western Australia.

    Google Scholar 

  • Davis, T. W., Berry, D. L., Boyer, G. L., & Gobler, C. J. (2009). The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae, 8(5), 715–725.

    CAS  Google Scholar 

  • Dignum, M., Matthijs, H. C. P., Pel, R., Laanbroek, H. J., Mur, L. R., et al. (2005). Nutrient limitation of freshwater cyanobacteria—tools to monitor phosphorus limitation at the individual level. In J. Huisman, H. C. P. Matthijs, & P. M. Visser (Eds.), Harmful cyanobacteria. the Netherlands: Springer.

    Google Scholar 

  • Eisentraeger, A., Dott, W., Klein, J., & Hahn, S. (2003). Comparative studies on algal toxicity testing using fluorometric microplate and Erlenmeyer flask growth-inhibition assays. Ecotoxicology and Environmental Safety, 54(3), 346–354.

    CAS  Google Scholar 

  • Frank, C. A. P. (2002). Microcystin-producing cyanobacteria in recreational waters in southwestern Germany. Environmental Toxicology, 17(4), 361–366.

    CAS  Google Scholar 

  • Geis, S. W., Fleming, K. L., Korthals, E. T., Searle, G., Reynolds, L., & Karner, D. A. (2000). Modifications to the algal growth inhibition test for use as a regulatory assay. Environmental Toxicology and Chemistry, 19(1), 36–41.

    CAS  Google Scholar 

  • Ghadouani, A., & Coggins, L. X. (2011). Science, technology and policy for water pollution control at the watershed scale: current issues and future challenges. Physics and Chemistry of the Earth, Parts A/B/C, 36(9–11), 335–341.

    Google Scholar 

  • Ghadouani, A., Pinel-Alloul, B., Plath, K., Codd, G. A., & Lampert, W. (2004). Effects of Microcystis aeruginosa and purified microcystin–LR on the feeding behavior of Daphnia pulicaria. Limnology and Oceanography, 49(3), 666–679.

    Google Scholar 

  • Ghadouani, A., Pinel-Alloul, B., & Prepas, E. E. (2003). Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshwater Biology, 48(2), 363–381.

    Google Scholar 

  • Ghadouani, A., Pinel-Alloul, B., & Prepas, E. E. (2006). Could increased cyanobacterial biomass following forest harvesting cause a reduction in zooplankton body size structure? Canadian Journal of Fisheries and Aquatic Sciences, 63, 2308–2317.

    Google Scholar 

  • Ghadouani, A., & Smith, R. E. H. (2005). Phytoplankton distribution in Lake Erie as assessed by a new in situ spectrofluorometric technique. Journal of Great Lakes Research, 31(Supplement 2), 154–167.

    CAS  Google Scholar 

  • Graham, J. L., Jones, J. R., Jones, S. B., Downing, J. A., & Clevenger, T. E. (2004). Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. Water Research, 38(20), 4395–4404.

    CAS  Google Scholar 

  • Ha, J. H., Hidaka, T., & Tsuno, H. (2011). Analysis of factors affecting the ratio of microcystin to chlorophyll-a in cyanobacterial blooms using real-time polymerase chain reaction. Environmental Toxicology, 26(1), 21–28.

    CAS  Google Scholar 

  • Halstvedt, C. (2008). On the effect of abiotic environmental factors on production of bioactive oligopeptides in field populations of Planktothrix spp. (Cyanobacteria). Journal of Plankton Research, 30(5), 607–617.

    CAS  Google Scholar 

  • Harada, K., Kondo, F., & Lawton, L. A. (1999). Laboratory analysis of cyanotoxins. In I. Chorus & J. Bartram (Eds.), Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management (pp. 363–367). London: E & FN Spon on behalf of the World Health Organization.

    Google Scholar 

  • Havens, K. E. (2007). Chapter 33: Cyanobacteria blooms—effects on aquatic ecosystems. In: Cyanobacterial harmful algal blooms: state of the science and research needs (Vol. 619, pp. 733–747). New York: Springer.

  • HC (2010). Guidelines for Canadian drinking water quality: summary table. Ottawa: Health Canada.

  • Hillebrand, H., Durselen, C., Kirschtel, D., Pollingher, U., & Zohary, T. (1999). Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35(2), 403–424.

    Google Scholar 

  • Hobson, P., & Fallowfield, H. (2003). Effect of irradiance, temperature and salinity on growth and toxin production by Nodularia spumigena. Hydrobiologia, 493(1–3), 7–15.

    CAS  Google Scholar 

  • Hotto, A. M., Satchwell, M. F., Berry, D. L., Gobler, C. J., & Boyer, G. L. (2008). Spatial and temporal diversity of microcystins and microcystin-producing genotypes in Oneida Lake, NY. Harmful Algae, 7(5), 671–681.

    CAS  Google Scholar 

  • ISO (2005). Determination of microcystins: method using solid phase extraction (SPE) and high performance liquid chromatography (HPLC) with ultraviolet (UV) detection. Geneva: ISO

  • Izydorczyk, K., Jurczak, T., Wojtal-Frankiewicz, A., Skowron, A., Mankiewicz-Boczek, J., & Tarczynska, M. (2008). Influence of abiotic and biotic factors on microcystin content in Microcystis aeruginosa cells in a eutrophic temperate reservoir. Journal of Plankton Research, 30(4), 393–400.

    CAS  Google Scholar 

  • Jayatissa, L. P., Silva, E. I. L., McElhiney, J., & Lawton, L. A. (2006). Occurrence of toxigenic cyanobacterial blooms in freshwaters of Sri Lanka. Systematic and Applied Microbiology, 29(2), 156–164.

    CAS  Google Scholar 

  • Jean, M. J., Diane, C. C., Eugene, B. W., Hardy, F. J., & Michele, C. (2000). Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Canadian Journal of Fisheries and Aquatic Sciences, 57(1), 231–240.

    Google Scholar 

  • Joung, S.-H., Oh, H.-M., Ko, S.-R., & Ahn, C.-Y. (2010). Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae, 10(2), 188–193.

    Google Scholar 

  • Kann, J., & Smith, V. H. (1999). Estimating the probability of exceeding elevated pH values critical to fish populations in a hypereutrophic lake. Canadian Journal of Fisheries and Aquatic Sciences, 56(12), 2262–2270.

    Google Scholar 

  • Kardinaal, W. E. A., & Visser, P. M. (2005). Dynamics of cyanobacterial toxins—sources of variability in microcystin concentration. In J. Huisman, H. C. P. Matthijs, & P. M. Visser (Eds.), Harmful cyanobacteria (pp. 41–63). the Netherlands: Springer.

    Google Scholar 

  • Kemp, A. S. (2009). Freshwater cyanoprokaryota blooms in the Swan Coastal Plain wetlands: ecology, taxonomy and toxicology. Ph.D. thesis, Curtin University of Technology, Perth.

  • Komarek, J., & Hauer, T. (2011). CyanoDB.cz on-line database of cyanobacterial genera. Univ. of South Bohemia & Inst. of Botany AS CR. http://www.cyanodb.cz.

  • Kotak, B. G., Lam, A., Prepas, E. E., & Hrudey, S. E. (2000). Role of chemical and physical variables in regulating microcystin–LR concentration in phytoplankton of eutrophic lakes. Canadian Journal of Fisheries and Aquatic Sciences, 57(8), 1584–1593.

    CAS  Google Scholar 

  • Kotut, K., Ballot, A., Wiegand, C., & Krienitz, L. (2010). Toxic cyanobacteria at Nakuru sewage oxidation ponds—a potential threat to wildlife. Limnologica, 40(1), 47–53.

    CAS  Google Scholar 

  • 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(7), 1525–1530.

    CAS  Google Scholar 

  • Liu, Y. M., Chen, W., Li, D. H., Huang, Z. B., Shen, Y. W., & Liu, Y. D. (2011). Cyanobacteria–cyanotoxin-contaminations and eutrophication status before Wuxi Drinking Water Crisis in Lake Taihu, China. Journal of Environmental Sciences (China), 23(4), 575–581.

    CAS  Google Scholar 

  • Maske, S., Sangolkar, L., & Chakrabarti, T. (2010). Temporal variation in density and diversity of cyanobacteria and cyanotoxins in lakes at Nagpur (Maharashtra State), India. Environmental Monitoring and Assessment, 169(1–4), 299–308.

    CAS  Google Scholar 

  • Meriluoto, J., & Codd, G. (2005). Toxic—cyanobacterial monitoring and cyanotoxin analysis (Vol. 65, Acta Academiae Aboensis Ser. B, Mathematica et physica). Åbo: Åbo Akademi University Press.

    Google Scholar 

  • Mooney, K., Floyd, S., Foy, R., & Elliott, C. (2011). Initial studies on the occurrence of cyanobacteria and microcystins in Irish lakes. Environmental Toxicology, 26(5), 566–570.

    CAS  Google Scholar 

  • Naselli-Flores, L., Barone, R., Chorus, I., & Kurmayer, R. (2007). Toxic cyanobacterial blooms in reservoirs under a semiarid Mediterranean climate: the magnification of a problem. Environmental Toxicology, 22(4), 399–404.

    CAS  Google Scholar 

  • Nasri, H., Bouaicha, N., & Harche, M. K. (2007). A new morphospecies of Microcystis sp forming bloom in the Cheffia dam (Algeria): seasonal variation of microcystin concentrations in raw water and their removal in a full-scale treatment plant. Environmental Toxicology, 22(4), 347–356.

    CAS  Google Scholar 

  • NHMRC (2011). National water quality management strategy: Australian drinking water guidelines 6. (Vol. 1). Canberra: National Health and Medical Research Council.

  • Okello, W., Portmann, C., Erhard, M., Gademann, K., & Kurmayer, R. (2010). Occurrence of microcystin-producing cyanobacteria in Ugandan freshwater habitats. Environmental Toxicology, 25(4), 367–380.

    CAS  Google Scholar 

  • Orr, P. T., & Jones, G. J. (1998). Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnology and Oceanography, 43(7), 1604–1614.

    CAS  Google Scholar 

  • Orr, P. T., Jones, G. J., & Douglas, G. B. (2004). Response of cultured Microcystis aeruginosa from the Swan River, Australia, to elevated salt concentration and consequences for bloom and toxin management in estuaries. Marine and Freshwater Research, 55(3), 277–283.

    Google Scholar 

  • Palikova, M., Mares, J., Kopp, R., Hlavkova, J., Navratil, S., Adamovsky, O., et al. (2011). Accumulation of microcystins in Nile tilapia, Oreochromis niloticus L., and effects of a complex cyanobacterial bloom on the dietetic quality of muscles. Bulletin of Environmental Contamination and Toxicology, 87(1), 26–30.

    CAS  Google Scholar 

  • Pavlova, V., Babica, P., Todorova, D., Bratanova, Z., & Maršálek, B. (2006). Contamination of some reservoirs and lakes in Republic of Bulgaria by microcystins. Acta Hydrochimica et Hydrobiologica, 34(5), 437–441.

    CAS  Google Scholar 

  • Reichwaldt, E. S., & Ghadouani, A. (2012). Effects of rainfall patterns on toxic cyanobacterial blooms in a changing climate: between simplistic scenarios and complex dynamics. Water Research, 46(5), 1372–1393.

    CAS  Google Scholar 

  • Rinta-Kanto, J. M., Konopko, E. A., DeBruyn, J. M., Bourbonniere, R. A., Boyer, G. L., & Wilhelm, S. W. (2009). Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae, 8(5), 665–673.

    CAS  Google Scholar 

  • Sabart, M., Pobel, D., Briand, E., Combourieu, B., Salencon, M. J., Humbert, J. F., et al. (2010). Spatiotemporal variations in microcystin concentrations and in the proportions of microcystin-producing cells in several Microcystis aeruginosa populations. Applied and Environmental Microbiology, 76(14), 4750–4759.

    CAS  Google Scholar 

  • Srivastava, A., Choi, G.-G., Ahn, C.-Y., Oh, H.-M., Ravi, A., & Asthana, R. (2012). Dynamics of microcystin production and quantification of potentially toxigenic Microcystis sp. using real-time PCR. Water Research, 46(3), 817–827.

    CAS  Google Scholar 

  • Tonk, L. L., Bosch, L. K., Visser, L. P., & Huisman, L. J. (2007). Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquatic Microbial Ecology, 46(2), 117–123.

    Google Scholar 

  • Utermöhl, H. (1958). Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt. int. Verein. theor. angew. Limnology, 9, 1–38.

  • Vasconcelos, V., Martins, A., Vale, M., Antunes, A., Azevedo, J., Welker, M., et al. (2011). First report on the occurrence of microcystins in planktonic cyanobacteria from Central Mexico. Toxicon, 56(3), 425–431.

    Google Scholar 

  • Vezie, C., Rapala, J., Vaitomaa, J., Seitsonen, J., & Sivonen, K. (2002). Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microbial Ecology, 43(4), 443–454.

    CAS  Google Scholar 

  • Watzin, M. C., Miller, E. B., Shambaugh, A. D., & Kreider, M. A. (2006). Application of the WHO alert level framework to cyanobacterial monitoring of Lake Champlain, Vermont. Environmental Toxicology, 21(3), 278–288.

    CAS  Google Scholar 

  • WHO (1998). Cyanobacterial toxins: microcystin–LR. In: Guidelines for drinking water quality. (2nd Ed., Vol. 2, pp. 95–110). Geneva: World Health Organization.

  • WHO. (2003). Algae and cyanobacteria in freshwater: guidelines for safe recreational water environments (pp. 136–154). Geneva: World Health Organization.

    Google Scholar 

  • Wilhelm, S. W., Farnsley, S. E., LeCleir, G. R., Layton, A. C., Satchwell, M. F., DeBruyn, J. M., et al. (2011). The relationships between nutrients, cyanobacterial toxins and the microbial community in Taihu (Lake Tai), China. Harmful Algae, 10(2), 207–215.

    CAS  Google Scholar 

  • Wu, S., Wang, S., Yang, H., Xie, P., Ni, L., & Xu, J. (2008). Field studies on the environmental factors in controlling microcystin production in the subtropical shallow lakes of the Yangtze River. Bulletin of Environmental Contamination and Toxicology, 80(4), 329–334.

    CAS  Google Scholar 

  • Wu, S. K., Xie, P., Liang, G. D., Wang, S. B., & Liang, X. M. (2006). Relationships between microcystins and environmental parameters in 30 subtropical shallow lakes along the Yangtze River, China. Freshwater Biology, 51(12), 2309–2319.

    CAS  Google Scholar 

  • Yang, H., Xie, P., Xu, J., Zheng, L., Deng, D., Zhou, Q., et al. (2006). Seasonal variation of microcystin concentration in Lake Chaohu, a shallow subtropical lake in the People's Republic of China. Bulletin of Environmental Contamination and Toxicology, 77(3), 367–374.

    CAS  Google Scholar 

  • Znachor, P. P., Jurczak, P. T., Komarkova, P. J., Jezberova, P. J., Mankiewicz, P. J., Kastovska, P. K., et al. (2006). Summer changes in cyanobacterial bloom composition and microcystin concentration in eutrophic Czech reservoirs. Environmental Toxicology, 21(3), 236–243.

    CAS  Google Scholar 

  • Zurawell, R. W., Chen, H. R., Burke, J. M., & Prepas, E. E. (2005). Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. Journal of Toxicology and Environmental Health. Part B, Critical Reviews, 8(1), 1–37.

    CAS  Google Scholar 

Download references

Acknowledgments

This project was funded by the Australian Research Council’s Linkage Project funding scheme (LP0776571) and the Water Corporation of Western Australia. We wish to thank Matthew Timmins and Ricarda Fenske from Metabolomics Australia at The University of Western Australia for their assistance in the operation of LC-MS, Professor Pierre Legendre and Laura Firth for their valuable statistical advice and Liah Coggins for her help in the editing of the manuscript. During the study, S.C. Sinang was supported by a scholarship from Sultan Idris Education University (UPSI) and Malaysia Government.

Author information

Author notes

  1. Som Cit Sinang

    Present address: Faculty of Science and Mathematics, Sultan Idris Education University, 35900 Tanjong Malim, Perak, Malaysia

Authors and Affiliations

  1. Aquatic Ecology and Ecosystem Studies, School of Environmental Systems Engineering, The University of Western Australia, 35 Stirling Highway, M015, Crawley, WA, 6009, Australia

    Som Cit Sinang, Elke S. Reichwaldt & Anas Ghadouani

Authors
  1. Som Cit Sinang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elke S. Reichwaldt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anas Ghadouani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anas Ghadouani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sinang, S.C., Reichwaldt, E.S. & Ghadouani, A. Spatial and temporal variability in the relationship between cyanobacterial biomass and microcystins. Environ Monit Assess 185, 6379–6395 (2013). https://doi.org/10.1007/s10661-012-3031-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-012-3031-0

Keywords

Search

Navigation