Skip to main content
SpringerLink
Log in

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

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

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.

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

Similar content being viewed by others

References

  • 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 52:2233–2248

    Article  CAS  Google Scholar 

  • Agnihotri VK (2013) Anabaena flos-aquae. Crit Rev Environ Sci Technol 44:1995–2037

  • 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 327–472

  • 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 47:1355–1366

    Article  Google Scholar 

  • 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 49:98–115

    Article  Google Scholar 

  • 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 32:913–925

    Article  Google Scholar 

  • 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  

  • Bartram J, Chorus I (eds) (2002) Toxic Cyanobacteria in water: a guide to their public health consequences, monitoring and management. CRC Press

  • 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 69:98–105

    Article  CAS  Google Scholar 

  • Berger C (1975) Occurrence of Oscillatoria agardhii Gom. in some shallow eutrophic lakes. Verh Int Ver Theor Angew Limnol 19:2689–2697

  • Bormans M, Condie S (1998) Modelling the distribution of Anabaena and Melosira in a stratified river weir pool. Hydrobiologia 364:3–13

    Article  Google Scholar 

  • Bormans M, Sherman BS, Webster IT (1999) Is buoyancy regulation in cyanobacteria an adaptation to exploit separation of light and nutrients? Mar Freshw Res 50:897–906

    Article  Google Scholar 

  • 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 55:1–15

    Article  CAS  Google Scholar 

  • Bormans M, Ford PW, Fabbro L (2005) Spatial and temporal variability in cyanobacterial populations controlled by physical processes. J Plankton Res 27(1):61–70

    Article  Google Scholar 

  • 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 40:231–238

    Article  Google Scholar 

  • 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):3839–3848

    Article  CAS  PubMed  Google Scholar 

  • 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 50:291–300

    Article  Google Scholar 

  • Cardinale BJ et al (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592

    Article  PubMed  Google Scholar 

  • Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407

    Article  CAS  PubMed  Google Scholar 

  • Carmichael W (1997) The cyanotoxins. Adv Bot Res 27:211–256

    Article  CAS  Google Scholar 

  • Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum Ecol Risk Assess 7:1393–1407

    Article  Google Scholar 

  • 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 44:483–489

    Article  CAS  PubMed  Google Scholar 

  • 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 51:1–10

    Article  CAS  PubMed  Google Scholar 

  • Chislock MF, Sharp KL, Wilson AE (2014) Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Res 49:207–214

    Article  CAS  PubMed  Google Scholar 

  • 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 48:345–355

    Article  CAS  PubMed  Google Scholar 

  • Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Spon Press, New York

    Book  Google Scholar 

  • Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272

    Article  CAS  PubMed  Google Scholar 

  • 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 8:715–725

    Article  CAS  Google Scholar 

  • de Tezanos Pinto P, Litchman E (2010a) Eco-physiological responses of nitrogen-fixing cyanobacteria to light. Hydrobiologia 639:63–68

  • Dodds WK et al (2009) Eutrophication of US Freshwaters: analysis of Potential Economic Damages. Environ Sci Technol 43:12–19

    Article  CAS  PubMed  Google Scholar 

  • Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438(1–3):1–12

    Article  CAS  Google Scholar 

  • Dokulil MT, Teubner K (2012) Deep living Planktothrix rubescens modulated by environmental constraints and climate forcing. Hydrobiologia 698:29–46

    Article  CAS  Google Scholar 

  • 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 46:1364–1371

    Article  CAS  PubMed  Google Scholar 

  • 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 50:1404–1411

    Article  Google Scholar 

  • 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 8:329–342

    Article  CAS  Google Scholar 

  • 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):313–321

    Article  CAS  PubMed  Google Scholar 

  • 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):95–106

    Article  CAS  PubMed  Google Scholar 

  • 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 11:151–163

    Article  Google Scholar 

  • Fraisse et al (2013) Morphofunctional traits reflect differences in phytoplankton community between rivers of contrasting flow regime. Aquat Ecol 47:315–327

    Article  Google Scholar 

  • Gallina N, Anneville O, Beniston M (2011) Impacts of extreme air temperatures on cyanobacteria in five deep peri-Alpine lakes. Limnol Oceanogr 70:186–196

    Google Scholar 

  • Gallon JR, Chit KN, Brown EG (1990) Biosynthesis of the tropane-related cyanobacterial toxin anatoxin-a: role of ornithine decarboxylase. Phytochemistry 29:1107–1111

    Article  CAS  PubMed  Google Scholar 

  • 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 70:829–844

    Article  Google Scholar 

  • Gkelis S, Zaoutsos N (2014) Cyanotoxin occurrence and potentially toxin producing cyanobacteria in freshwaters of Greece: a multi-disciplinary approach. Toxicon 78:1–9

    Article  CAS  PubMed  Google Scholar 

  • Glazer AN (1984) Phycobilisome a macromolecular complex optimized for light energy transfer. Biochimica et Biophysica Acta (BBA)-Rev Bioenerg 768:29–51

    Article  CAS  Google Scholar 

  • 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):233–247

    Article  CAS  Google Scholar 

  • 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 733–747

  • Hillebrand H, Matthiessen B (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–1419

    Article  PubMed  Google Scholar 

  • 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 169:245–256

    Article  PubMed  Google Scholar 

  • 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 619:17–43

  • Huisman J, Matthijs HC, Visser PM (eds) (2006) Harmful cyanobacteria, vol 3. Springer

    Book  Google Scholar 

  • Humphries SE, Lyne VD (1988) Cyanophyte blooms: the role of cell buoyancy. Limnol Oceanogr 33:79–91

    Article  Google Scholar 

  • Ibelings BW, Chorus I (2007) Accumulation of cyanobacterial toxins in freshwater “seafood” and its consequences for public health: a review. Environ Pollut 150:177–192

    Article  CAS  PubMed  Google Scholar 

  • Ibelings BW, Maberly SC (1998) Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria. Limnol Oceanogr 43:408–419

    Article  CAS  Google Scholar 

  • 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 120:385–401

    Google Scholar 

  • 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 128:407–424

    Article  CAS  Google Scholar 

  • 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 10:171–181

    Article  Google Scholar 

  • 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 13:1456–1472

    Article  Google Scholar 

  • 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 10:4–16

    Article  CAS  Google Scholar 

  • Ibelings BW, Backer LC, Kardinaal WEA, Chorus I (2014) Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae 40:63–74

    Article  CAS  Google Scholar 

  • 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 Press

  • Istvanovics V, Shafik H, Presing M (2000) Growth and phosphate uptake kinetics of the cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshw Biol 43:257–275

    Article  Google Scholar 

  • 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 4:651–672

    Article  Google Scholar 

  • 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 48:127–148

    Google Scholar 

  • Jeppesen E et al (2005) Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshw Biol 50:1747–1771

    Article  CAS  Google Scholar 

  • Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Glob Change Biol 14:495–512

    Article  Google Scholar 

  • 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, 5–27

  • Kardinaal WEA et al. (2007) Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat Microb Ecol 48:1–12

  • 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 137:1171–1178

    Article  Google Scholar 

  • Komárek J, Mareš J (2012) An update to modern taxonomy (2011) of freshwater planktic heterocytous cyanobacteria. Hydrobiologia 698:327–351

    Article  CAS  Google Scholar 

  • Kosten S et al (2012) Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Change Biol 18:118–126

    Article  Google Scholar 

  • Kruk C et al (2010) A morphological classification capturing functional variation in phytoplankton. Freshw Biol 55:614–627

    Article  Google Scholar 

  • Kruk C et al (2011) Phytoplankton community composition can be predicted best in terms of morphological groups. Limnol Oceanogr 56:110–118

    Article  Google Scholar 

  • 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 43:107–118

    Article  CAS  PubMed  Google Scholar 

  • 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 177:233–244

    Article  Google Scholar 

  • 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 56:451–466

    Article  Google Scholar 

  • Lewis WM Jr, Wurtsbaugh WA (2008) Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. Int Rev Hydrobiol 93:446–465

    Article  CAS  Google Scholar 

  • Li R et al (2001) Isolation and identification of the cyanotoxin cylindrospermopsin and deoxy-cylindrospermopsin from a Thailand strain of Cylindrospermopsis raciborskii (Cyanobacteria). Toxicon 39:973–980

    Article  CAS  PubMed  Google Scholar 

  • Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639

    Article  Google Scholar 

  • Litchman E, Pinto PD, Klausmeier CA, Thomas MK, Yoshiyama K (2010) Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653:15–28

    Article  CAS  Google Scholar 

  • Livingstone DM (2003) Impact of secular climate change on the thermal structure of a large temperate central European lake. Clim Change 57:205–225

    Article  Google Scholar 

  • Lund JWG (1965) The ecology of the freshwater phytoplankton. Biol Rev 40(2):231–290

  • Lürling M, Eshetu F, Faassen EJ, Kosten S, Huszar VL (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559

    Article  Google Scholar 

  • Margalef R (1978) Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol Acta 1:493–509

    Google Scholar 

  • Moss B et al (2011) Allied attack: climate change and eutrophication. Inland Waters 1:101–105

    Article  Google Scholar 

  • 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 1:335–338

    Article  Google Scholar 

  • 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 111–121

  • 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 519:143–152

    Article  Google Scholar 

  • Oliver RL, Ganf GG (2000) Freshwater blooms. In: Whitton B and Malcolm P (eds) The Ecology of Cyanobacteria. Kluwer Academic Publishers, pp 149–186

  • 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 107:563–593

    Google Scholar 

  • Paerl HW, Huisman J (2008) Climate—blooms like it hot. SCIENCE-NEW YORK THEN WASHINGTON 320(5872):57

    Article  CAS  PubMed  Google Scholar 

  • Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37

    Article  CAS  PubMed  Google Scholar 

  • Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Total Environ 409:1739–1745

    Article  CAS  PubMed  Google Scholar 

  • Posch T, Koester O, Salcher MM, Pernthaler J (2012) Harmful filamentous cyanobacteria favoured by reduced water turnover with lake warming. Nat Clim Change 2:809–813

    Article  CAS  Google Scholar 

  • Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514

    Article  PubMed  Google Scholar 

  • Reynolds CS (1984) Phytoplankton periodicity—the interactions of form, function and environmental variability. Freshw Biol 14:111–142

    Article  Google Scholar 

  • Reynolds CS (1997) Excellence in ecology: vegetation processes in the pelagic: a model for ecosystem theory. Ecology Institute, Germany

    Google Scholar 

  • Reynolds CS (2006) The ecology of phytoplankton. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24:417–428

    Article  Google Scholar 

  • 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 59:99–114

    Article  Google Scholar 

  • Roozen FC et al (2003) Lake age and water level affect the turbidity of floodplain lakes along the lower Rhine. Freshw Biol 48(3):519–531

    Article  Google Scholar 

  • Ryan EF, Hamilton DP, Barnes GP (2004) Recent occurrence of Cylindrospermopsis raciborskii in Waikato lakes of New Zealand. NZ J Mar Freshw Res 37:829–836

    Article  Google Scholar 

  • Sas H, Ahlgren I (1989) Lake restoration by reduction of nutrient loading: expectations, experiences, and extrapolations. Academic Verlag, St. Augustin, p 497

  • Scheffer M, Rinaldi S, Gragnani A, Mur LR, vanNes EH (1997) On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78:272–282

    Article  Google Scholar 

  • Schindler D (1977) Evolution of phosphorus limitation in lakes. Science 195:260–262

    Article  CAS  PubMed  Google Scholar 

  • Schindler DW, Vallentyne JR (2008) The algal bowl, overfertilization of the world’s freshwaters and estuaries. University of Alberta Press

  • 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 105:11254–11258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott JT, McCarthy MJ (2010) Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnol Oceanogr 55:1265–1270

    Article  CAS  Google Scholar 

  • 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 46:1408–1419

    Article  CAS  PubMed  Google Scholar 

  • 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):2658–2666

    CAS  Google Scholar 

  • Smayda TJ (1971) Normal and accelerated sinking of phytoplankton in the sea. Mar Geol 11(2):105–122

  • 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 60:618–626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 619:855–865

  • 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):169–185

    Article  PubMed  Google Scholar 

  • 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 16:2844–2856

    Article  Google Scholar 

  • Stüken A et al (2006) Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45:696–703

    Article  Google Scholar 

  • Suding KN et al (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Glob Change Biol 14:1125–1140

    Article  Google Scholar 

  • 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 417–444

  • 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):5177–5181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tüxen R (1955) Das system der nordwestdeutschen. Pflanzengesellschaften. Mitt. Flor.-soz. Arbeitsgem. N.F. Stolzenau/Weser 5:155–176

  • 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 115:153–160

  • 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 9–45

  • Verspagen JM et al (2006) Water management strategies against toxic Microcystis blooms in the Dutch delta. Ecol Appl 16:313–327

    Article  PubMed  Google Scholar 

  • Verspagen JM et al (2014) Rising CO2 levels will intensify phytoplankton blooms in eutrophic and hypertrophic lakes. PLoS One 9(8):e104325

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 13:1–13

    Article  Google Scholar 

  • 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 36:435–450

    Article  Google Scholar 

  • 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 109–142

  • Vitousek PM et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45

    Article  Google Scholar 

  • 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 54:331–344

    Article  CAS  Google Scholar 

  • 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):59–64

    Article  Google Scholar 

  • Wagner C, Adrian R (2009) Cyanobacteria dominance: quantifying the effects of climate change. Limnol Oceanogr 54:2460–2468

    Article  Google Scholar 

  • Walsby AE (1991) The mechanical properties of the Microcystis gas vesicle. J Gen Microbiol 137:2401–2408

    Article  Google Scholar 

  • Walsby AE (1994) Gas vesicles. Microbiol Rev 58:94

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walsby AE (2005) Stratification by cyanobacteria in lakes: a dynamic buoyancy model indicates size limitations met by Planktothrix rubescens filaments. New Phytol 168:365–376

    Article  PubMed  Google Scholar 

  • 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 20:1357–1375

    Article  Google Scholar 

  • 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 162:133–145

    Article  Google Scholar 

  • WHO (1996) Guidelines for drinking water quality-health criteria and other supporting information, 2nd edn, vol 2. World Health Organization, Geneva

    Google Scholar 

  • Woodward G (2009) Biodiversity, ecosystem functioning and food webs in fresh waters: assembling the jigsaw puzzle. Freshw Biol 54:2171–2187

    Article  Google Scholar 

  • 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):130–139

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Institut F.A. Forel, University of Geneva, Geneva, Switzerland

    Evanthia Mantzouki & Bas W. Ibelings

  2. Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands

    Petra M. Visser

  3. UMR CNRS 6553 ECOBIO, Université de Rennes 1, Rennes, France

    Myriam Bormans

Authors
  1. Evanthia Mantzouki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Petra M. Visser
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Myriam Bormans
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bas W. Ibelings
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Evanthia Mantzouki.

Additional information

Guest editors: Petra M. Visser, Bas W. Ibelings, Jutta Fastner & Myriam Bormans/Cyanobacterial blooms. Ecology, prevention, mitigation and control.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mantzouki, E., Visser, P.M., Bormans, M. et al. Understanding the key ecological traits of cyanobacteria as a basis for their management and control in changing lakes. Aquat Ecol 50, 333–350 (2016). https://doi.org/10.1007/s10452-015-9526-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-015-9526-3

Keywords

Search

Navigation