Skip to main content

Advertisement

Log in

Contrasting cyanobacterial communities and microcystin concentrations in summers with extreme weather events: insights into potential effects of climate change

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Current climate change scenarios predict that aquatic systems will experience increases in temperature, thermal stratification, water column stability and in some regions, greater precipitation. These factors have been associated with promoting cyanobacterial blooms. However, limited data exist on how cyanobacterial composition and toxin production will be affected. Using a shallow eutrophic lake, we investigated how precipitation intensity and extended droughts influenced: (i) physical and chemical conditions, (ii) cyanobacterial community succession, and (iii) toxin production by Microcystis. Moderate levels of nitrate related to intermittent high rainfall during the summer of 2013–2014, lead to the dominance of Aphanizomenon gracile and Dolichospermum crassum (without heterocytes). Microcystis aeruginosa blooms occurred when ammonium concentrations and water temperature increased, and total nitrogen:total phosphorus ratios were low. In contrast, an extended drought (2014–2015 summer) resulted in prolonged stratification, increased dissolved reactive phosphorus, and low dissolved inorganic nitrogen concentrations. All A. gracile and D. crassum filaments contained heterocytes, M. aeruginosa density remained low, and the picocyanobacteria Aphanocapsa was abundant. A positive relationship (P < 0.001) was identified between microcystin quotas and surface water temperature. These results highlight the complex successional interplay of cyanobacteria species and demonstrated the importance of climate through its effect on nutrient concentrations, water temperature, and stratification.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahn, C. Y., H. M. Oh & Y. S. Park, 2011. Evaluation of environmental factors on cyanobacterial bloom in eutrophic reservoir using artificial neural networks. Journal of Phycology 47: 495–504.

    Article  CAS  PubMed  Google Scholar 

  • Amé, M. & D. Wunderlin, 2005. Effects of iron, ammonium and temperature on microcystin content by a natural concentrated Microcystis aeruginosa population. Water, Air, and Soil Pollution 168: 235–248.

    Article  CAS  Google Scholar 

  • Anderson, M., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth: 214 pp.

    Google Scholar 

  • APHA, 2005. Standard Methods for the Examination of Water and Wastewater, 21st edn. American Public Health Association (APHA), American Water Works Association (AWWA) and Water Environment Federation (WEF): 541 pp.

  • Baker, P. D. & L. D. Fabbro, 2002. A Guide to the Identification of Common Blue-Green Algae (Cyanoprokaryotes) in Australian Freshwaters, 2nd edn. Cooperative Research Centre for Freshwater Ecology, Australia: 56 pp.

  • Beversdorf, L. J., T. R. Miller & K. D. McMahon, 2013. The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake. PLoS One 8: e56103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blomqvist, P., A. Petterson & P. Hyenstrand, 1994. Ammonium–nitrogen: a key regulatory factor causing dominance of non-nitrogen-fixing cyanobacteria in aquatic systems. Archiv für Hydrobiologie 132: 141–164.

    CAS  Google Scholar 

  • Bolch, C. J. S. & S. I. Blackburn, 1996. Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kütz. Journal of Applied Phycology 8: 5–13.

    Article  Google Scholar 

  • Borges, H., S. A. Wood, J. Puddick, E. Blaney, I. Hawes, D. R. Dietrich & D. P. Hamilton, 2016. Intracellular, environmental and biotic interactions influence recruitment of benthic Microcystis (Cyanophyceae) in a shallow eutrophic lake. Journal of Plankton Research. doi:10.1093/plankt/fbw046.

  • Bormans, M., P. W. Ford & L. Fabbro, 2005. Spatial and temporal variability in cyanobacterial populations controlled by physical processes. Journal of Plankton Research 27: 61–70.

    Article  Google Scholar 

  • Brookes, J. D. & C. C. Carey, 2011. Resilience to blooms. Science 334: 46–47.

    Article  CAS  PubMed  Google Scholar 

  • Cai, Y. & F. Kong, 2013. Diversity and dynamics of picocyanobacteria and the bloom-forming cyanobacteria in a large shallow eutrophic lake (Lake Chaohu, China). Journal of Limnology 72: 473–484.

    Article  Google Scholar 

  • Carey, C. C., B. W. Ibelings, E. P. Hoffmann, D. P. Hamilton & J. D. Brookes, 2012. Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Research 46: 1394–1407.

    Article  CAS  PubMed  Google Scholar 

  • Chorus, I., 2001. Cyanotoxins – Occurrence, Causes, Consequences. Springer Berlin Heidelberg, Berlin: 357 pp.

    Google Scholar 

  • Chorus, I. & L. Mur, 1999. Preventive measures. In Chorus, I. & J. Bartram (eds), Toxic Cyanobacteria in Water – A Guide to their Public Health Consequences, Monitoring and Management. E and FN Spon, London: 235–273.

    Chapter  Google Scholar 

  • Chu, Z., X. Jin, N. Iwami & Y. Inamori, 2007. The effect of temperature on growth characteristics and competitions of Microcystis aeruginosa and Oscillatoria mougeotii in a shallow, eutrophic lake simulator system. In Qin, B., Z. Liu & K. Havens (eds), Eutrophication of Shallow Lakes with Special Reference to Lake Taihu, China. Springer, Dordrecht: 217–223.

    Chapter  Google Scholar 

  • Clearwater, S. J., S. A. Wood, N. R. Phillips, S. M. Parkyn, R. van Ginkel & K. J. Thompson, 2014. Toxicity thresholds for juvenile freshwater mussels Echyridella menziesii and crayfish Paranephrops planifrons, after acute or chronic exposure to Microcystis sp. Environmental Toxicology 29: 487–502.

    Article  CAS  PubMed  Google Scholar 

  • Codd, G., L. Morrison & J. Metcalf, 2005. Cyanobacterial toxins: risk management for health protection. Toxicology and Applied Pharmacology 203: 264–272.

    Article  CAS  PubMed  Google Scholar 

  • Conley, D. J., H. W. Paerl, R. W. Howarth, D. F. Boesch, S. P. Seitzinger, K. E. Havens, C. Lancelot & G. E. Likens, 2009. Controlling eutrophication: nitrogen and phosphorus. Science 323: 1014–1015.

    Article  CAS  PubMed  Google Scholar 

  • Conradie, K. R. & S. Barnard, 2012. The dynamics of toxic Microcystis strains and microcystin production in two hypertrophic South African reservoirs. Harmful Algae 20: 1–10.

    Article  CAS  Google Scholar 

  • Dai, G. Z., J.-L. Shang & B. S. Qiu, 2012. Ammonia may play an important role in the succession of cyanobacterial blooms and the distribution of common algal species in shallow freshwater lakes. Global Change Biology 18: 1571–1581.

    Article  Google Scholar 

  • Davis, T. W., D. L. Berry, G. L. Boyer & C. J. Gobler, 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: 715–725.

    Article  CAS  Google Scholar 

  • Dolman, A. M., J. Rucker, F. R. Pick, J. Fastner, T. Rohrlack, U. Mischke & C. Wiedner, 2012. Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus. PLoS One 7: e38757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dziallas, C. & H. P. Grossart, 2011. Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS One 6: e25569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández, C., V. Estrada & E. Parodi, 2015. Factors triggering cyanobacteria dominance and succession during blooms in a hypereutrophic drinking water supply reservoir. Water, Air, Soil and Pollution 226: 1–13.

    Article  CAS  Google Scholar 

  • Flint, E., 1975. Phytoplankton in some New Zealand lakes. In Jolly, V. H. & J. M. Brown (eds), New Zealand Lakes. Auckland University Press, Auckland: 63–192.

    Google Scholar 

  • Garcia-Pichel, F., J. Belnap, S. Neuer & F. Schanz, 2003. Estimates of global cyanobacterial biomass and its distribution. Algological Studies 109: 213–227.

    Article  Google Scholar 

  • Hamilton, D. P., S. A. Wood, D. R. Dietrich & J. Puddick, 2014. Costs of harmful blooms of freshwater cyanobacteria. In Sharma, N. K., A. K. Rai & S. J. Lucas (eds), Cyanobacteria: An Economic Perspective. Wiley, New York: 245–256.

    Google Scholar 

  • Harke, M. J. & C. J. Gobler, 2013. Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS One 8: e69834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harke, M. J., M. M. Steffen, C. J. Gobler, T. G. Otten, S. W. Wilhelm, S. A. Wood & H. W. Paerl, 2016. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54: 4–20.

    Article  Google Scholar 

  • Haugland, R. A., S. C. Siefring, L. J. Wymer, K. P. Brenner & A. P. Dufour, 2005. Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase chain reaction and membrane filter culture analysis. Water Research 39: 559–568.

    Article  CAS  PubMed  Google Scholar 

  • Havens, K., H. Paerl, E. Phlips, M. Zhu, J. Beaver & A. Srifa, 2016. Extreme weather events and climate variability provide a lens to how shallow lakes may respond to climate change. Water 8: 229.

    Article  Google Scholar 

  • Horst, G. P., O. Sarnelle, J. D. White, S. K. Hamilton, R. B. Kaul & J. D. Bressie, 2014. Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa. Water Research 54: 188–198.

    Article  CAS  PubMed  Google Scholar 

  • IPCC, 2007. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller (eds), Climate Change 2007: The Physical Science Basis. Cambridge University Press, Cambridge.

    Google Scholar 

  • Jacobsen, B. & P. Simonsen, 1993. Disturbance events affecting phytoplankton biomass, composition and species diversity in a shallow, eutrophic, temperate lake. In Padisák, J., C. S. Reynolds & U. Sommer (eds), Intermediate Disturbance Hypothesis in Phytoplankton Ecology. Springer, Dordrecht: 9–14.

    Chapter  Google Scholar 

  • Jöhnk, K. D., J. E. F. Huisman, J. Sharples, B. E. N. Sommeijer, P. M. Visser & J. M. Stroom, 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology 14: 495–512.

    Article  Google Scholar 

  • Jones, G. J. & W. Poplawski, 1998. Understanding and management of cyanobacterial blooms in sub-tropical reservoirs of Queensland, Australia. Water Science and Technology 37: 161–168.

    Article  CAS  Google Scholar 

  • Kleinteich, J., S. A. Wood, F. C. Kupper, A. Camacho, A. Quesada, T. Frickey & D. R. Dietrich, 2012. Temperature-related changes in polar cyanobacterial mat diversity and toxin production. Nature Climate Change 2: 356–360.

    Article  CAS  Google Scholar 

  • Komárek, J. & K. Anagnostidis, 1999. Süßwasserflora von Mitteleuropa: Cyanoprokaryota 19/1. Teil: Chroococcales. Springer Spektrum, Berlin.

    Google Scholar 

  • Kosten, S., V. L. M. Huszar, E. Bécares, L. S. Costa, E. van Donk, L. A. Hansson, E. Jeppesen, C. Kruk, G. Lacerot, N. Mazzeo, L. De Meester, B. Moss, M. Lürling, T. Nõges, S. Romo & M. Scheffer, 2012. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118–126.

    Article  Google Scholar 

  • Kouzminov, A., J. Ruck & S. A. Wood, 2007. New Zealand risk management approach for toxic cyanobacteria in drinking water. Australian and New Zealand Journal of Public Health 31: 275–281.

    Article  PubMed  Google Scholar 

  • Krüger, T., C. Wiegand, L. Kun, B. Luckas & S. Pflugmacher, 2010. More and more toxins around-analysis of cyanobacterial strains isolated from Lake Chao (Anhui Province, China). Toxicon 56: 1520–1524.

    Article  CAS  PubMed  Google Scholar 

  • Kurmayer, R. & T. Kutzenberger, 2003. Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Applied and Environmental Microbiology 69: 6723–6730.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laamanen, M. & H. Kuosa, 2005. Annual variability of biomass and heterocysts of the N2-fixing cyanobacterium Aphanizomenon flos-aquae in the Baltic Sea with reference to Anabaena spp. and Nodularia spumigena. Boreal Environment Research 10: 19–30.

    Google Scholar 

  • Legendre, L. & F. Rassoulzadegan, 1995. Plankton and nutrient dynamics in marine waters. Ophelia 41: 153–172.

    Article  Google Scholar 

  • Lehman, P. W., G. Boyer, M. Satchwell & S. Waller, 2008. The influence of environmental conditions on the seasonal variation of Microcystis cell density and microcystins concentration in San Francisco Estuary. Hydrobiologia 600: 187–204.

    Article  CAS  Google Scholar 

  • Lewis, W. M. & W. A. Wurtsbaugh, 2008. Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. International Review of Hydrobiology 93: 446–465.

    Article  CAS  Google Scholar 

  • Marinho, M. & S. M. F. de Oliveira e Azevedo, 2007. Influence of N/P ratio on competitive abilities for nitrogen and phosphorus by Microcystis aeruginosa and Aulacoseira distans. Aquatic Ecology 41: 525–533.

    Article  CAS  Google Scholar 

  • McArdle, B. H. & M. J. Anderson, 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290–297.

    Article  Google Scholar 

  • McGregor, G. & L. D. Fabbro, 2001. A Guide to the Identification of Australian Freshwater Planktonic Chroococcales (Cyanoprokaryota/Cyanobacteria). Cooperative Research Centre for Freshwater Ecology, Australia: 61 pp.

  • Mur, L. R., O. M. Skulberg & H. Utkilen, 1999. Cyanobacteria in the environment. In Chorus, I. & J. Bartram (eds), Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. Published on Behalf of the World Health Organisation by E and FN Spon, London: 15–40.

    Google Scholar 

  • NHMRC, 2008. Guidelines for Managing Risks in Recreational Water. National Health and Medical Research Council, Canberra.

    Google Scholar 

  • Ni, W. M., J. Y. Zhang, T. D. Ding, R. J. Stevenson & Y. M. Zhu, 2012. Environmental factors regulating cyanobacteria dominance and microcystin production in a subtropical lake within the Taihu watershed, China. Journal of Zhejiang University, SCIENCE A 13: 311–322.

    Article  CAS  Google Scholar 

  • O’Neil, J. M., T. W. Davis, M. A. Burford & C. J. Gobler, 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313–334.

    Article  CAS  Google Scholar 

  • Oliver, R. L., D. P. Hamilton, J. D. Brookes & G. G. Ganf, 2012. Physiology, blooms and prediction of planktonic cyanobacteria. In Whitton, B. A. (ed.), Ecology of Cyanobacteria II: Their Diversity in Space and Time. Springer, Dordrecht: 155–194.

    Chapter  Google Scholar 

  • Paerl, H. W., 2014. Mitigating harmful cyanobacterial blooms in a human- and climatically-impacted world. Life 4: 988–1012.

    Article  PubMed  PubMed Central  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2008. Blooms like it hot. Science 320: 57–58.

    Article  CAS  PubMed  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.

    Article  CAS  PubMed  Google Scholar 

  • Paerl, H. & T. Otten, 2013. Harmful cyanobacterial blooms: causes, consequences, and controls. Microbial Ecology 65: 995–1010.

    Article  CAS  PubMed  Google Scholar 

  • Paerl, H. W. & V. J. Paul, 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.

    Article  CAS  PubMed  Google Scholar 

  • Paerl, H., L. Valdes, A. Joyner, B. Peierls, M. Piehler, S. Riggs, R. Christian, L. Eby, L. Crowder, J. Ramus, E. Clesceri, C. Buzzelli & R. Luettich, 2006. Ecological response to hurricane events in the Pamlico Sound system, North Carolina, and implications for assessment and management in a regime of increased frequency. Estuaries and Coasts 29: 1033–1045.

    Article  Google Scholar 

  • Pinheiro, J. & D. Bates, 2000. Mixed-Effects Models in S and S-PLUS. Springer, New York.

    Book  Google Scholar 

  • R Development Core Team, 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.R-project.org/].

  • Rajaniemi-Wacklin, P., A. Rantala, P. Kuuppo, K. Haukka & K. Sivonen, 2008. Cyanobacterial community composition in shallow, eutrophic Lake Tuusulanjärvi studied by microscopy, strain isolation, DGGE and cloning. Algological Studies 126: 137–157.

    Article  CAS  Google Scholar 

  • Raven, J. A., 1998. The twelfth Tansley Lecture. Small is beautiful: the picophytoplankton. Functional Ecology 12: 503–513.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Reynolds, C. S., 1989. Physical determinants of phytoplankton succession. In Sommer, U. (ed.), Plankton Ecology. Springer Berlin Heidelberg, Berlin: 9–56.

    Chapter  Google Scholar 

  • Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rogers, S., 2014. Investigation of microcystin processing, production and export by Microcystis sp. Masters of Science Thesis, University of Waikato, Hamilton.

  • Rueckert, A. & S. C. Cary, 2009. Use of an armored RNA standard to measure microcystin synthetase E gene expression in toxic Microcystis sp. by reverse-transcription QPCR. Limnology and Oceanography: Methods 7: 509–520.

    Article  CAS  Google Scholar 

  • Saker, M. L., J. Fastner, E. Dittmann, G. Christiansen & V. M. Vasconcelos, 2005. Variation between strains of the cyanobacterium Microcystis aeruginosa isolated from a Portuguese river. Journal of Applied Microbiology 99: 749–757.

    Article  CAS  PubMed  Google Scholar 

  • Schindler, D. W., R. E. Hecky, D. L. Findlay, M. P. Stainton, B. R. Parker, M. J. Paterson, K. G. Beaty, M. Lyng & S. E. M. Kasian, 2008. Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proceedings of the National Academy of Sciences of USA 105: 11254–11258.

    Article  CAS  Google Scholar 

  • Smith, V. H., 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221: 669–671.

    Article  CAS  PubMed  Google Scholar 

  • Smith, V. H., 2003. Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science and Pollution Research 10: 126–139.

    Article  CAS  PubMed  Google Scholar 

  • Smith, V. H., S. A. Wood, C. G. McBride, J. Atalah, D. P. Hamilton & J. Abell, 2016. Phosphorus and nitrogen loading restraints are essential for successful eutrophication control of Lake Rotorua, New Zealand. Inland Waters 6: 273–283.

    Article  Google Scholar 

  • Steffensen, D. A., 2008. Economic cost of cyanobacterial blooms. Advances in Experimental Medicine and Biology 619: 855–865.

    Article  PubMed  Google Scholar 

  • Suikkanen, S., G. O. Fistarol & E. Granéli, 2004. Allelopathic effects of the Baltic cyanobacteria Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lemmermannii on algal monocultures. Journal of Experimental Marine Biology and Ecology 308: 85–101.

    Article  Google Scholar 

  • Sun, J. & D. Liu, 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research 25: 1331–1346.

    Article  Google Scholar 

  • Takamura, N., T. Iwakuma & M. Yasuno, 1987. Uptake of 13C and 15N (ammonium, nitrate and urea) by Microcystis in Lake Kasumigaura. Journal of Plankton Research 9: 151–165.

    Article  Google Scholar 

  • Takamura, N., A. Otsuki, M. Aizaki & Y. Nojiri, 1992. Phytoplankton species shift accompanied by transition from nitrogen dependence to phosphorus dependence of primary production in Lake Kasumigaura, Japan. Archiv für Hydrobiologie 124: 129–148.

    Google Scholar 

  • Tóth, L. G. & J. Padisák, 1986. Meteorological factors affecting the bloom of Anabaenopsis raciborskii Wolosz. (Cyanophyta: Hormogonales) in the shallow Lake Balaton, Hungary. Journal of Plankton Research 8: 353–363.

    Article  Google Scholar 

  • Trolle, D., D. P. Hamilton, C. A. Pilditch, I. C. Duggan & E. Jeppesen, 2010. Predicting the effects of climate change on trophic status of three morphologically varying lakes: implications for lake restoration and management. Environmental Modelling and Software 26: 354–370.

    Article  Google Scholar 

  • Utermöhl, H., 1958. Towards a perfection of quantitative phytoplankton methodology. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Vaitomaa, J., A. Rantala, K. Halinen, L. Rouhiainen, P. Tallberg, L. Mokelke & K. Sivonen, 2003. Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes. Applied and Environmental Microbiology 69: 7289–7297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van de Waal, D. B., J. M. Verspagen, J. F. Finke, V. Vournazou, A. K. Immers, W. E. Kardinaal, L. Tonk, S. Becker, E. Van Donk, P. M. Visser & J. Huisman, 2011. Reversal in competitive dominance of a toxic versus non-toxic cyanobacterium in response to rising CO2. The ISME Journal 5: 1438–1450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Westhuizen, A. J. & J. N. Eloff, 1985. Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006). Planta 163: 55–59.

    Article  PubMed  Google Scholar 

  • van der Westhuizen, A. J., J. N. Eloff & G. H. J. Krüger, 1986. Effect of temperature and light (fluence rate) on the composition of the toxin of the cyanobacterium Microcystis aeruginosa (UV-006). Archiv für Hydrobiologie 108: 145–154.

    Google Scholar 

  • Vrede, T., A. Ballantyne, C. Mille-Lindblom, G. Algesten, C. Gudasz, S. Lindahl & A. K. Brunberg, 2009. Effects of N:P loading ratios on phytoplankton community composition, primary production and N fixation in a eutrophic lake. Freshwater Biology 54: 331–344.

    Article  CAS  Google Scholar 

  • Wagner, C. & R. Adrian, 2009. Cyanobacteria dominance: quantifying the effects of climate change. Limnology and Oceanography 54: 2460–2468.

    Article  Google Scholar 

  • Walve, J. & U. Larsson, 2007. Blooms of Baltic Sea Aphanizomenon sp. (Cyanobacteria) collapse after internal phosphorus depletion. Aquatic Microbial Ecology 49: 57–69.

    Article  Google Scholar 

  • Watanabe, M. F. & S. Oishi, 1985. Effects of environmental factors on toxicity of a cyanobacterium (Microcystis aeruginosa) under culture conditions. Applied and Environmental Microbiology 49: 1342–1344.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watson, S. B., E. McCauley & J. A. Downing, 1997. Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnology and Oceanography 42: 487–495.

    Article  Google Scholar 

  • WHO, 2003. Guidelines for Safe Recreational Water Environments: Coastal and Fresh Waters. World Health Organization, Geneva.

    Google Scholar 

  • Wood, S. A., A. L. M. Crowe, J. G. Ruck & R. G. Wear, 2005. New records of planktonic cyanobacteria in New Zealand freshwaters. New Zealand Journal of Botany 43: 479–492.

    Article  Google Scholar 

  • Wood, S. A., D. P. Hamilton, W. J. Paul, K. A. Safi & W. M. Williamson, 2009. New Zealand Guidelines for Cyanobacteria in Recreational Fresh Waters. Ministry for the Environment and the Ministry of Health, Wellington.

    Google Scholar 

  • Wood, S. A., M. J. Prentice, K. Smith & D. P. Hamilton, 2010. Low dissolved inorganic nitrogen and increased heterocyte frequency: precursors to Anabaena planktonica blooms in a temperate, eutrophic reservoir. Journal of Plankton Research 32: 1315–1325.

    Article  CAS  Google Scholar 

  • Wood, S. A., A. Rueckert, D. P. Hamilton, S. C. Cary & D. R. Dietrich, 2011. Switching toxin production on and off: intermittent microcystin synthesis in a Microcystis bloom. Environmental Microbiology Reports 3: 118–124.

    Article  CAS  PubMed  Google Scholar 

  • Wood, S. A., D. R. Dietrich, C. S. Cary & D. P. Hamilton, 2012a. Increasing Microcystis cell density enhances microcystin synthesis: a mesocosm study. Inland Waters 2: 17–22.

    Article  CAS  Google Scholar 

  • Wood, S. A., N. R. Phillips, M. de Winton & M. Gibbs, 2012b. Consumption of benthic cyanobacterial mats and nodularin-R accumulation in freshwater crayfish (Paranephrops planifrons) in Lake Tikitapu (Rotorua, New Zealand). Harmful Algae 20: 175–179.

    Article  CAS  Google Scholar 

  • Wood, S. A., J. Puddick, H. Borges, D. R. Dietrich & D. P. Hamilton, 2015. Potential effects of climate change on cyanobacterial toxin production. In Botana, L. M., C. Louzao & N. Vilariño (eds), Climate Change and Marine and Freshwater Toxins. De Gruyter, Berlin: 155–180.

    Google Scholar 

  • Xie, L., P. Xie, S. Li, H. Tang & H. Liu, 2003. The low TN:TP ratio, a cause or a result of Microcystis blooms? Water Research 37: 2073–2080.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, M., T. Yoshida, Y. Takashima, N. Hosoda & S. Hiroishi, 2007. Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiology Letters 266: 49–53.

    Article  CAS  PubMed  Google Scholar 

  • Yu, L., F. Kong, M. Zhang, Z. Yang, X. Shi & M. Du, 2014. The dynamics of Microcystis genotypes and microcystin production and associations with environmental factors during blooms in Lake Chaohu, China. Toxins 6: 3238–3257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zapomělová, E., P. Hrouzek, K. Řeháková, M. Šabacká, M. Stibal, L. Caisová, J. Komárková & A. Lukešová, 2008. Morphological variability in selected heterocystous cyanobacterial strains as a response to varied temperature, light intensity and medium composition. Folia Microbiology 53: 333–341.

    Article  CAS  Google Scholar 

  • Zuur, A. F., E. N. Ieno & C. S. Elphick, 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecology and Evolution 1: 3–14.

    Article  Google Scholar 

  • Zuur, A. F., J. M. Hilbe & E. N. Ieno, 2013. A Beginner’s Guide to GLM and GLMM with R: A Frequentist and Bayesian perspective for Ecologists. Highland Statistics, Newburgh.

    Google Scholar 

Download references

Acknowledgments

This research was supported by the Marsden Fund of the Royal Society of New Zealand (12-UOW-087; Toxic in Crowds), the New Zealand Ministry of Business, Innovation and Employment (UOWX1503; Enhancing the Health and Resilience of New Zealand Lakes), the Royal Society of New Zealand International Research Staff Exchange Scheme Fellowship (MEAT Agreement 295223) and the Marie Curie International Research Staff Exchange Scheme Fellowship (PIRSES-GA-2011-295223). We thank Spencer and Thomas Kahu for sample collection, and the Kahu family, Ngāi Tahu and Environment Canterbury for allowing access to Lake Rotorua. We acknowledge Kati Doehring and Weimin Jiang (Cawthron) for assistance with Figs. 1 and 2, respectively.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susanna A. Wood.

Additional information

Handling editor: Judit Padisák

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wood, S.A., Borges, H., Puddick, J. et al. Contrasting cyanobacterial communities and microcystin concentrations in summers with extreme weather events: insights into potential effects of climate change. Hydrobiologia 785, 71–89 (2017). https://doi.org/10.1007/s10750-016-2904-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2904-6

Keywords

Navigation