Advertisement

Aquatic Ecology

, Volume 50, Issue 3, pp 333–350 | Cite as

Understanding the key ecological traits of cyanobacteria as a basis for their management and control in changing lakes

  • Evanthia MantzoukiEmail author
  • Petra M. Visser
  • Myriam Bormans
  • Bas W. Ibelings
Article

Abstract

Anticipated climatic changes combined with eutrophication are predicted to enhance the dominance of several notorious cyanobacterial taxa. Cyanobacteria have many key ecological traits that may allow them to thrive under foreseen scenarios of environmental change. Understanding the ecophysiological traits of harmful species has proven important for their successful control and management. Indeed, if the links between key cyanobacterial traits and the specific environmental conditions that allow expression of these traits can be disrupted, we could identify (novel) means for operational control and mitigate or prevent water quality problems. A good example is artificial mixing of a lake that breaks down the water column stability on which fast floating, buoyant cyanobacteria depend. Based upon Reynolds’ functional phytoplankton classification, we focused on five groups of cyanobacteria that from a management point of view can be seen as homogeneous and have comparable environmental sensitivities. For each group, we present (1) its key traits, (2) how these characteristics will maintain their function under future environmental change, (3) explanation of how understanding the function of these traits can reveal the “Achilles heel” of the particular functional group and (4) which (combination of) control measures is most likely to be successful. Despite looking for specific environmental sensitivities of individual groups, we maintain that controlling nutrients remains the basis for managing blooms, no matter which functional type dominates. Providing further ecological knowledge to lake management could be the key to effective bloom control and healthier, sustainable freshwater ecosystems even in a warmer future.

Keywords

Climate change Cyanobacterial blooms Eutrophication Functional traits Lake management Microcystins 

Notes

Acknowledgments

We would like to acknowledge two EU COST Actions; ES 1105 “CYANOCOST—Cyanobacterial blooms and toxins in water resources: Occurrence, impacts and management” and ES1201 “NETLAKE—Networking Lake Observatories in Europe” that offer us the possibility to develop the idea of this manuscript through numerous discussions with experts and researchers on cyanobacterial blooms. We would also like to thank all the anonymous reviewers for helping us improve our manuscript with all their constructive comments.

References

  1. Agawin N, Rabouille S, Veldhuis M, Servatius L, Hol S, van Overzee HM, Huisman J (2007) Competition and facilitation between unicellular nitrogen-fixing cyanobacteria and non-nitrogen-fixing phytoplankton species. Limnol Oceanogr 52:2233–2248CrossRefGoogle Scholar
  2. Agnihotri VK (2013) Anabaena flos-aquae. Crit Rev Environ Sci Technol 44:1995–2037Google Scholar
  3. Anagnostidis K, Komárek J (1988) Modern approach to the classification system of cyanophytes. 3-Oscillatoriales. Algol Stud/Archiv für Hydrobiologie, Supplement Volumes 50–53, pp 327–472Google Scholar
  4. Anneville O, Souissi S, Ibanez F, Ginot V, Druart JC, Angeli N (2002) Temporal mapping of phytoplankton assemblages in Lake Geneva: annual and interannual changes in their patterns of succession. Limnol Oceanogr 47:1355–1366CrossRefGoogle Scholar
  5. Anneville O, Souissi S, Gammeter S, Straile D (2004) Seasonal and inter-annual scales of variability in phytoplankton assemblages: comparison of phytoplankton dynamics in three peri-alpine lakes over a period of 28 years. Freshw Biol 49:98–115CrossRefGoogle Scholar
  6. Anneville O, Molinero JC, Souissi S, Gerdeaux D (2010) Seasonal and interannual variability of cladoceran communities in two peri-alpine lakes: uncoupled response to the 2003 heat wave. J Plankton Res 32:913–925CrossRefGoogle Scholar
  7. Anneville O, Domaizon I, Kerimoglu O, Rimet F, Jacquet S (2015) Blue-green algae in a “greenhouse century”? New insights from field data on climate change impacts on cyanobacteria abundance. Ecosystems 18(3):441–458  Google Scholar
  8. Bartram J, Chorus I (eds) (2002) Toxic Cyanobacteria in water: a guide to their public health consequences, monitoring and management. CRC PressGoogle Scholar
  9. Bauersachs T, Stal LJ, Grego M, Schwark L (2014) Temperature induced changes in the heterocyst glycolipid composition of N-2 fixing heterocystous cyanobacteria. Org Geochem 69:98–105CrossRefGoogle Scholar
  10. Berger C (1975) Occurrence of Oscillatoria agardhii Gom. in some shallow eutrophic lakes. Verh Int Ver Theor Angew Limnol 19:2689–2697Google Scholar
  11. Bormans M, Condie S (1998) Modelling the distribution of Anabaena and Melosira in a stratified river weir pool. Hydrobiologia 364:3–13CrossRefGoogle Scholar
  12. Bormans M, Sherman BS, Webster IT (1999) Is buoyancy regulation in cyanobacteria an adaptation to exploit separation of light and nutrients? Mar Freshw Res 50:897–906CrossRefGoogle Scholar
  13. Bormans M, Ford PW, Fabbro L, Hancock G (2004) Onset and persistence of cyanobacterial blooms in a large impounded tropical river, Australia. Mar Freshw Res 55:1–15CrossRefGoogle Scholar
  14. Bormans M, Ford PW, Fabbro L (2005) Spatial and temporal variability in cyanobacterial populations controlled by physical processes. J Plankton Res 27(1):61–70CrossRefGoogle Scholar
  15. Briand JF, Leboulanger C, Humbert JF, Bernard C, Dufour P (2004) Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? J Phycol 40:231–238CrossRefGoogle Scholar
  16. Briand E et al (2008) Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (Cyanobacterium) population. Appl Environ Microbiol 74(12):3839–3848PubMedCrossRefGoogle Scholar
  17. Butterwick C, Heaney SI, Talling JF (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw Biol 50:291–300CrossRefGoogle Scholar
  18. Cardinale BJ et al (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592PubMedCrossRefGoogle Scholar
  19. Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407PubMedCrossRefGoogle Scholar
  20. Carmichael W (1997) The cyanotoxins. Adv Bot Res 27:211–256CrossRefGoogle Scholar
  21. Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum Ecol Risk Assess 7:1393–1407CrossRefGoogle Scholar
  22. Castro D, Vera D, Lagos N, García C, Vásquez M (2004) The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii. Toxicon 44:483–489PubMedCrossRefGoogle Scholar
  23. Cheung MY, Liang S, Lee J (2013) Toxin-producing cyanobacteria in freshwater: a review of the problems, impact on drinking water safety, and efforts for protecting public health. J Microbiol 51:1–10PubMedCrossRefGoogle Scholar
  24. Chislock MF, Sharp KL, Wilson AE (2014) Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Res 49:207–214PubMedCrossRefGoogle Scholar
  25. Chonudomkul D, Yongmanitchai W, Theeragool G, Kawachi M, Kasai F, Kaya K, Watanabe MM (2004) Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiol Ecol 48:345–355PubMedCrossRefGoogle Scholar
  26. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Spon Press, New YorkCrossRefGoogle Scholar
  27. Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272PubMedCrossRefGoogle Scholar
  28. Davis TW, Berry DL, Boyer GL, Gobler CJ (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 8:715–725CrossRefGoogle Scholar
  29. de Tezanos Pinto P, Litchman E (2010a) Eco-physiological responses of nitrogen-fixing cyanobacteria to light. Hydrobiologia 639:63–68Google Scholar
  30. Dodds WK et al (2009) Eutrophication of US Freshwaters: analysis of Potential Economic Damages. Environ Sci Technol 43:12–19PubMedCrossRefGoogle Scholar
  31. Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438(1–3):1–12CrossRefGoogle Scholar
  32. Dokulil MT, Teubner K (2012) Deep living Planktothrix rubescens modulated by environmental constraints and climate forcing. Hydrobiologia 698:29–46CrossRefGoogle Scholar
  33. Elliott JA (2012) Is the future blue-green? A review of the current model predictions of how climate change could affect pelagic freshwater cyanobacteria. Water Res 46:1364–1371PubMedCrossRefGoogle Scholar
  34. Elliott JA, Thackeray SJ, Huntingford C, Jones RG (2005) Combining a regional climate model with a phytoplankton community model to predict future changes in phytoplankton in lakes. Freshw Biol 50:1404–1411CrossRefGoogle Scholar
  35. Ernst B, Hoeger SJ, O’Brien E, Dietrich DR (2009) Abundance and toxicity of Planktothrix rubescens in the pre-alpine Lake Ammersee, Germany. Harmful Algae 8:329–342CrossRefGoogle Scholar
  36. Fastner J et al (2003) Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii Cyanobacteria) isolates. Toxicon 42(3):313–321PubMedCrossRefGoogle Scholar
  37. Fietz S, Nicklish A (2002) Acclimation of the diatom Stephanodiscus neoastraea and the cyanobacterium Planktothrix agardhii to simulated natural light fluctuations. Photosynth Res 72(1):95–106PubMedCrossRefGoogle Scholar
  38. Foy RH, Gibson CE, Smith RV (1976) The influence of day length, light intensity and temperature on the growth rates of planktonic blue-green algae. Br Phycol J 11:151–163CrossRefGoogle Scholar
  39. Fraisse et al (2013) Morphofunctional traits reflect differences in phytoplankton community between rivers of contrasting flow regime. Aquat Ecol 47:315–327CrossRefGoogle Scholar
  40. Gallina N, Anneville O, Beniston M (2011) Impacts of extreme air temperatures on cyanobacteria in five deep peri-Alpine lakes. Limnol Oceanogr 70:186–196Google Scholar
  41. Gallon JR, Chit KN, Brown EG (1990) Biosynthesis of the tropane-related cyanobacterial toxin anatoxin-a: role of ornithine decarboxylase. Phytochemistry 29:1107–1111PubMedCrossRefGoogle Scholar
  42. Ganf GG, Oliver RL (1982) Vertical separation of light and available nutrients as a factor causing replacement of green-algae by blue-green-algae in the plankton of a stratified lake. J Ecol 70:829–844CrossRefGoogle Scholar
  43. Gkelis S, Zaoutsos N (2014) Cyanotoxin occurrence and potentially toxin producing cyanobacteria in freshwaters of Greece: a multi-disciplinary approach. Toxicon 78:1–9PubMedCrossRefGoogle Scholar
  44. Glazer AN (1984) Phycobilisome a macromolecular complex optimized for light energy transfer. Biochimica et Biophysica Acta (BBA)-Rev Bioenerg 768:29–51CrossRefGoogle Scholar
  45. Gulati RD, Pires LMD, Van Donk E (2008) Lake restoration studies: failures, bottlenecks and prospects of new ecotechnological measures. Limnol Ecol Manag Inland Waters 38(3):233–247CrossRefGoogle Scholar
  46. Havens KE (2008) Cyanobacteria blooms: effects on aquatic ecosystems. In: Hudnell HK (ed) Cyanobacterial harmful algal blooms: state of the science and research needs, vol 619. Advances in experimental medicine and biology pp 733–747Google Scholar
  47. Hillebrand H, Matthiessen B (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–1419PubMedCrossRefGoogle Scholar
  48. Huber V, Wagner C, Gerten D, Adrian R (2012) To bloom or not to bloom: contrasting responses of cyanobacteria to recent heat waves explained by critical thresholds of abiotic drivers. Oecologia 169:245–256PubMedCrossRefGoogle Scholar
  49. Hudnell HK, Dortch Q (2008) Chapter 2: a synopsis of research needs identified at the interagency, international symposium on cyanobacterial harmful algal blooms (ISOC-HAB). In: Hudnell HK (ed) Cyanobacterial harmful algal blooms: state of the science and research needs advances in experimental medicine and biology 619:17–43Google Scholar
  50. Huisman J, Matthijs HC, Visser PM (eds) (2006) Harmful cyanobacteria, vol 3. SpringerCrossRefGoogle Scholar
  51. Humphries SE, Lyne VD (1988) Cyanophyte blooms: the role of cell buoyancy. Limnol Oceanogr 33:79–91CrossRefGoogle Scholar
  52. Ibelings BW, Chorus I (2007) Accumulation of cyanobacterial toxins in freshwater “seafood” and its consequences for public health: a review. Environ Pollut 150:177–192PubMedCrossRefGoogle Scholar
  53. Ibelings BW, Maberly SC (1998) Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria. Limnol Oceanogr 43:408–419CrossRefGoogle Scholar
  54. Ibelings BW, Mur LR, Kinsman R, Walsby A (1991) Microcystis changes its buoyancy in response to the average irradiance in the surface mixed layer. Archiv für Hydrobiologie 120:385–401Google Scholar
  55. Ibelings BW, Kroon BMA, Mur LR (1994) Acclimation Of Photosystem-Ii in a cyanobacterium and a eukaryotic green-alga to high and fluctuating photosynthetic photon flux densities, simulating light regimes induced by mixing in lakes. New Phytol 128:407–424CrossRefGoogle Scholar
  56. Ibelings B, Admiraal W, Bijkerk R, Ietswaart T, Prins H (1998) Monitoring of algae in Dutch rivers: does it meet its goals? J Appl Phycol 10:171–181CrossRefGoogle Scholar
  57. Ibelings BW, Vonk M, Los HFJ, van der Molen DT, Mooij WM (2003) Fuzzy modeling of cyanobacterial surface waterblooms: validation with NOAA–AVHRR satellite images. Ecol Appl 13:1456–1472CrossRefGoogle Scholar
  58. Ibelings BW, Portielje R, Lammens EH, Noordhuis R, van den Berg MS, Joosse W, Meijer ML (2007) Resilience of alternative stable states during the recovery of shallow lakes from eutrophication: lake Veluwe as a case study. Ecosystems 10:4–16CrossRefGoogle Scholar
  59. Ibelings BW, Backer LC, Kardinaal WEA, Chorus I (2014) Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae 40:63–74CrossRefGoogle Scholar
  60. IPCC Climate Change (2007) Impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University PressGoogle Scholar
  61. Istvanovics V, Shafik H, Presing M (2000) Growth and phosphate uptake kinetics of the cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshw Biol 43:257–275CrossRefGoogle Scholar
  62. Jacquet S et al (2005) The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural French lake (Lac du Bourget). Harmful Algae 4:651–672CrossRefGoogle Scholar
  63. Jeppesen E, Kristensen P, Jensen JP, Søndergaard M, Mortensen E, Lauridsen T (1991) Recovery resilience following a reduction in external phosphorus loading of shallow, eutrophic Danish lakes: duration, regulating factors and methods for overcoming resilience. Mem Ist Ital Idrobiol 48:127–148Google Scholar
  64. Jeppesen E et al (2005) Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771CrossRefGoogle Scholar
  65. Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Glob Change Biol 14:495–512CrossRefGoogle Scholar
  66. Kaplan-Levy RN, Hadas O, Summers ML, Rücker J, Sukenik A (2010) Akinetes: dormant cells of cyanobacteria. In: Lubzens E, Cerda J, Clark M (eds) Dormancy and resistance in harsh environments. Springer, Berlin, 5–27Google Scholar
  67. Kardinaal WEA et al. (2007) Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat Microb Ecol 48:1–12Google Scholar
  68. Kinsman R, Ibelings BW, Walsby A (1991) Gas vesicle collapse by turgor pressure and its role in buoyancy regulation by Anabaena flos-aquae. J Gen Microbiol 137:1171–1178CrossRefGoogle Scholar
  69. Komárek J, Mareš J (2012) An update to modern taxonomy (2011) of freshwater planktic heterocytous cyanobacteria. Hydrobiologia 698:327–351CrossRefGoogle Scholar
  70. Kosten S et al (2012) Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Change Biol 18:118–126CrossRefGoogle Scholar
  71. Kruk C et al (2010) A morphological classification capturing functional variation in phytoplankton. Freshw Biol 55:614–627CrossRefGoogle Scholar
  72. Kruk C et al (2011) Phytoplankton community composition can be predicted best in terms of morphological groups. Limnol Oceanogr 56:110–118CrossRefGoogle Scholar
  73. Kurmayer R, Dittmann E, Fastner J, Chorus I (2002) Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany). Microb Ecol 43:107–118PubMedCrossRefGoogle Scholar
  74. Lammens EH, van Nes EH, Meijer M-L, van den Berg MS (2004) Effects of commercial fishery on the bream population and the expansion of Chara aspera in Lake Veluwe. Ecol Model 177:233–244CrossRefGoogle Scholar
  75. Levine S, Schindler D (1999) Influence of nitrogen to phosphorus supply ratios and physicochemical conditions on cyanobacteria and phytoplankton species composition in the Experimental Lakes Area, Canada. Can J Fish Aquat Sci 56:451–466CrossRefGoogle Scholar
  76. Lewis WM Jr, Wurtsbaugh WA (2008) Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. Int Rev Hydrobiol 93:446–465CrossRefGoogle Scholar
  77. Li R et al (2001) Isolation and identification of the cyanotoxin cylindrospermopsin and deoxy-cylindrospermopsin from a Thailand strain of Cylindrospermopsis raciborskii (Cyanobacteria). Toxicon 39:973–980PubMedCrossRefGoogle Scholar
  78. Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639CrossRefGoogle Scholar
  79. Litchman E, Pinto PD, Klausmeier CA, Thomas MK, Yoshiyama K (2010) Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653:15–28CrossRefGoogle Scholar
  80. Livingstone DM (2003) Impact of secular climate change on the thermal structure of a large temperate central European lake. Clim Change 57:205–225CrossRefGoogle Scholar
  81. Lund JWG (1965) The ecology of the freshwater phytoplankton. Biol Rev 40(2):231–290Google Scholar
  82. Lürling M, Eshetu F, Faassen EJ, Kosten S, Huszar VL (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559CrossRefGoogle Scholar
  83. Margalef R (1978) Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol Acta 1:493–509Google Scholar
  84. Moss B et al (2011) Allied attack: climate change and eutrophication. Inland Waters 1:101–105CrossRefGoogle Scholar
  85. Mur LR, Gons H, Van Liere L (1977) Some experiments on the competition between green algae and blue-green bacteria in light-limited environments. FEMS Microbiol Lett 1:335–338CrossRefGoogle Scholar
  86. Nixdorf B, Mischke U, Rücker J (2003) Phytoplankton assemblages and steady state in deep and shallow eutrophic lakes—an approach to differentiate the habitat properties of Oscillatoriales. In: Naselli-Flores L, Padisák J, Dokulil MT (eds) Phytoplankton and equilibrium concept: the ecology of steady-state assemblages. Springer, Netherlands, pp 111–121Google Scholar
  87. O’Brien KR, Meyer DL, Waite AM, Ivey GN, Hamilton DP (2004) Disaggregation of Microcystis aeruginosa colonies under turbulent mixing: laboratory experiments in a grid-stirred tank. Hydrobiologia 519:143–152CrossRefGoogle Scholar
  88. Oliver RL, Ganf GG (2000) Freshwater blooms. In: Whitton B and Malcolm P (eds) The Ecology of Cyanobacteria. Kluwer Academic Publishers, pp 149–186Google Scholar
  89. Padisák J (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv Für Hydrobiologie Supplementband Monographische Beitrage 107:563–593Google Scholar
  90. Paerl HW, Huisman J (2008) Climate—blooms like it hot. SCIENCE-NEW YORK THEN WASHINGTON 320(5872):57PubMedCrossRefGoogle Scholar
  91. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37PubMedCrossRefGoogle Scholar
  92. Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Total Environ 409:1739–1745PubMedCrossRefGoogle Scholar
  93. Posch T, Koester O, Salcher MM, Pernthaler J (2012) Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nat Clim Change 2:809–813CrossRefGoogle Scholar
  94. Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514PubMedCrossRefGoogle Scholar
  95. Reynolds CS (1984) Phytoplankton periodicity—the interactions of form, function and environmental variability. Freshw Biol 14:111–142CrossRefGoogle Scholar
  96. Reynolds CS (1997) Excellence in ecology: vegetation processes in the pelagic: a model for ecosystem theory. Ecology Institute, GermanyGoogle Scholar
  97. Reynolds CS (2006) The ecology of phytoplankton. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  98. Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24:417–428CrossRefGoogle Scholar
  99. Rigosi A, Carey CC, Ibelings BW, Brookes JD (2014) The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnol Oceanogr 59:99–114CrossRefGoogle Scholar
  100. Roozen FC et al (2003) Lake age and water level affect the turbidity of floodplain lakes along the lower Rhine. Freshw Biol 48(3):519–531CrossRefGoogle Scholar
  101. Ryan EF, Hamilton DP, Barnes GP (2004) Recent occurrence of Cylindrospermopsis raciborskii in Waikato lakes of New Zealand. NZ J Mar Freshw Res 37:829–836CrossRefGoogle Scholar
  102. Sas H, Ahlgren I (1989) Lake restoration by reduction of nutrient loading: expectations, experiences, and extrapolations. Academic Verlag, St. Augustin, p 497Google Scholar
  103. Scheffer M, Rinaldi S, Gragnani A, Mur LR, vanNes EH (1997) On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78:272–282CrossRefGoogle Scholar
  104. Schindler D (1977) Evolution of phosphorus limitation in lakes. Science 195:260–262PubMedCrossRefGoogle Scholar
  105. Schindler DW, Vallentyne JR (2008) The algal bowl, overfertilization of the world’s freshwaters and estuaries. University of Alberta PressGoogle Scholar
  106. Schindler DW et al (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci USA 105:11254–11258PubMedPubMedCentralCrossRefGoogle Scholar
  107. Scott JT, McCarthy MJ (2010) Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnol Oceanogr 55:1265–1270CrossRefGoogle Scholar
  108. Sinha R, Pearson LA, Davis TW, Burford MA, Orr PT, Neilan BA (2012) Increased incidence of Cylindrospermopsis raciborskii in temperate zones—is climate change responsible? Water Res 46:1408–1419PubMedCrossRefGoogle Scholar
  109. Sivonen K (1990) Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Appl Environ Micorbiol 56(9):2658–2666Google Scholar
  110. Smayda TJ (1971) Normal and accelerated sinking of phytoplankton in the sea. Mar Geol 11(2):105–122Google Scholar
  111. Staal J, Hlobil H, Van Tulder M, Waddell G, Burton AK, Koes B, Van Mechelen W (2003) Occupational health guidelines for the management of low back pain: an international comparison. Occup Environ Med 60:618–626PubMedPubMedCentralCrossRefGoogle Scholar
  112. Steffensen DA (2008) Economic cost of cyanobacterial blooms. In: Cyanobacterial harmful algal blooms: state of the science and research needs advances in experimental medicine and biology 619:855–865Google Scholar
  113. Stomp M, van Dijk MA, van Overzee HMJ, Wortel MT, Sigon CAM, Egas M, Hoogvelt H, Gons HJ, Huisman J (2008) The timescale of phenotypic plasticity and its impact on competition in fluctuating environments. Am Nat 172(5):169–185PubMedCrossRefGoogle Scholar
  114. Straile D, Kerimoglu O, Peeters F, Jochimsen MC, Kümmerlin R, Rinke K, Rothhaupt KO (2010) Effects of a half a millennium winter on a deep lake—a shape of things to come? Glob Change Biol 16:2844–2856CrossRefGoogle Scholar
  115. Stüken A et al (2006) Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45:696–703CrossRefGoogle Scholar
  116. Suding KN et al (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Glob Change Biol 14:1125–1140CrossRefGoogle Scholar
  117. Tandeau de Marsac N (1991) Chromatic adaptation by cyanobacteria. In: Bogorad L, Vasil IK (eds) The photosynthetic apparatus: molecular biology and operation. Academic Press, San Diego, pp 417–444Google Scholar
  118. Tonk L et al (2005) The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Appl Environ Microbiol 71(9):5177–5181PubMedPubMedCentralCrossRefGoogle Scholar
  119. Tüxen R (1955) Das system der nordwestdeutschen. Pflanzengesellschaften. Mitt. Flor.-soz. Arbeitsgem. N.F. Stolzenau/Weser 5:155–176Google Scholar
  120. Van Liere L, Mur LR (1979) Growth-kinetics of Oscillatoria agardhii Gomont in continuous culture, limited in its growth by the light energy supply. J Gen Microbiol 115:153–160Google Scholar
  121. Van Liere L, Walsby AE (1982) Interactions of cyanobacteria with light. In: Carr NG, Whitton BA (eds) The Biology of Cyanobacteria. Blackwell Scientific Publications, Oxford, pp 9–45Google Scholar
  122. Verspagen JM et al (2006) Water management strategies against toxic Microcystis blooms in the Dutch delta. Ecol Appl 16:313–327PubMedCrossRefGoogle Scholar
  123. Verspagen JM et al (2014) Rising CO2 levels will intensify phytoplankton blooms in eutrophic and hypertrophic lakes. PLoS One 9(8):e104325PubMedPubMedCentralCrossRefGoogle Scholar
  124. Viney NR et al (2007) Modelling adaptive management strategies for coping with the impacts of climate variability and change on riverine algal blooms. Glob Change Biol 13:1–13CrossRefGoogle Scholar
  125. Visser P, Ibelings B, van der Veer B, Koedood J, Mur R (1996) Artificial mixing prevents nuisance blooms of the cyanobacterium Microcystis in Lake Nieuwe Meer, the Netherlands. Freshw Biol 36:435–450CrossRefGoogle Scholar
  126. Visser PM, Ibelings BW, Mur LR, Walsby AE (2005) The ecophysiology of the harmful cyanobacterium Microcystis In: Huisman J, Matthijs HCP, Visser PM (eds) Harmful cyanobacteria. Springer, Netherlands, pp 109–142Google Scholar
  127. Vitousek PM et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45CrossRefGoogle Scholar
  128. Vrede T, Ballantyne A, Mille-Lindblom C, Algesten G, Gudasz C, Lindahl S, Brunberg AK (2009) Effects of N:P loading ratios on phytoplankton community composition, primary production and N fixation in a eutrophic lake. Freshw Biol 54:331–344CrossRefGoogle Scholar
  129. Wacklin P, Hoffmann L, Komárek J (2009) Nomenclatural validation of the genetically revised cyanobacterial genus Dolichospermum (Ralfs ex Bornet et Flahault) comb. nova. Fottea 9(1):59–64CrossRefGoogle Scholar
  130. Wagner C, Adrian R (2009) Cyanobacteria dominance: quantifying the effects of climate change. Limnol Oceanogr 54:2460–2468CrossRefGoogle Scholar
  131. Walsby AE (1991) The mechanical properties of the Microcystis gas vesicle. J Gen Microbiol 137:2401–2408CrossRefGoogle Scholar
  132. Walsby AE (1994) Gas vesicles. Microbiol Rev 58:94PubMedPubMedCentralGoogle Scholar
  133. Walsby AE (2005) Stratification by cyanobacteria in lakes: a dynamic buoyancy model indicates size limitations met by Planktothrix rubescens filaments. New Phytol 168:365–376PubMedCrossRefGoogle Scholar
  134. Walsby AE, Avery A, Schanz F (1998) The critical pressures of gas vesicles in Planktorhrix rubescens in relation tothe depth of winter mixing in Lake Zürich, Switzerland. J Plankton Res 20:1357–1375CrossRefGoogle Scholar
  135. Walsby AE, Ng G, Dunn C, Davis PA (2004) Comparison of the depth where Planktothrix rubescens stratifies and the depth where the daily insolation supports its neutral buoyancy. New Phytol 162:133–145CrossRefGoogle Scholar
  136. WHO (1996) Guidelines for drinking water quality-health criteria and other supporting information, 2nd edn, vol 2. World Health Organization, GenevaGoogle Scholar
  137. Woodward G (2009) Biodiversity, ecosystem functioning and food webs in fresh waters: assembling the jigsaw puzzle. Freshw Biol 54:2171–2187CrossRefGoogle Scholar
  138. Yılmaz M, Phlips EJ, Szabo NJ, Badylak S (2008) A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon for cylindrospermopsin production. Toxicon 51(1):130–139PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Evanthia Mantzouki
    • 1
    Email author
  • Petra M. Visser
    • 2
  • Myriam Bormans
    • 3
  • Bas W. Ibelings
    • 1
  1. 1.Institut F.A. ForelUniversity of GenevaGenevaSwitzerland
  2. 2.Institute for Biodiversity and Ecosystem DynamicsUniversity of AmsterdamAmsterdamThe Netherlands
  3. 3.UMR CNRS 6553 ECOBIOUniversité de Rennes 1RennesFrance

Personalised recommendations