Biodiversity and Conservation

, Volume 24, Issue 4, pp 889–908 | Cite as

Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning

  • Assaf Sukenik
  • A. Quesada
  • N. Salmaso
Review Paper


The recent invasion and proliferation of toxic cyanobacteria in diverse aquatic habitats is a well-known worldwide phenomenon. The expansion of cyanobacterial blooms have the potential to significantly alter the structure of the native community and to modify ecosystem functioning. Public and scientific attention was primarily given to the effect on the water quality due to a variety of toxic compounds that some species produce. However, the expansion of toxic and non-toxic cyanobacteria to a wide geographic range may have an impact on the ecosystems, trophic cascades and geochemical cycles. Here we briefly summarize the geographic expansion of cyanobacteria species. We further deliberate the physiological advantages of the invading cyanobacterial species and the ecological effect of cyanotoxins. We discuss recent studies on the contribution of cyanotoxins to the invasion process and the impact toxin producing cyanobacteria have on their newly invaded habitats, the effect of alien cyanobacteria on zooplankton and fish and on the diversity and complexity of the microbial community.


Cyanobacteria Cyanotoxins Aquatic ecosystems Nostocales Chroococcales Invasive species 



We deeply appreciate knowledge sharing with European experts and researchers via the European Cooperation in Science and Technology, COST Action ES 1105. AS was supported by Israel Water Authority and research grants awarded by the Israel Science Foundation (ISF Grant No. 319/12), Israel Ministry of Science Technology and Space (MOST) and German Ministry of Research and Technology (BMBF).


  1. Akcaalan R, Mazur-Marzec H, Zalewska A, Albay M (2009) Phenotypic and toxicological characterization of toxic Nodularia spumigena from a freshwater lake in Turkey. Harmful Algae 8:273–278Google Scholar
  2. Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684PubMedCentralPubMedGoogle Scholar
  3. Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277Google Scholar
  4. Berry JP, Gantar M, Perez MH, Berry G, Noriega FG (2008) Cyanobacterial toxins as allelochemicals with potential applications as algaecides, herbicides and insecticides. Mar Drugs 6:117–146PubMedCentralPubMedGoogle Scholar
  5. Berry JP, Gibbs PD, Schmale MC, Saker ML (2009) Toxicity of cylindrospermopsin, and other apparent metabolites from Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum, to the zebrafish (Danio rerio) embryo. Toxicon 53:289–299PubMedCentralPubMedGoogle Scholar
  6. Blom JF, Baumann HI, Codd GA, Jüttner F (2006) Sensitivity and adaptation of aquatic organisms to oscillapeptin J and [D-Asp3, (E)-Dhb7] microcystin-RR. Arch Hydrobiol 167:547–559Google Scholar
  7. Bourne DG, Jones GJ, Blakeley RL, Jones A, Negri AP, Riddles P (1996) Enzymatic pathway for the bacterial degradation of the cyanobacterial cyclic peptide toxin microcystin LR. Appl Environ Microbiol 62:4086–4094PubMedCentralPubMedGoogle Scholar
  8. Bourne DG, Riddles P, Jones GJ, Smith W, Blakeley RL (2001) Characterisation of a gene cluster involved in bacterial degradation of the cyanobacterial toxin microcystin LR. Environ Toxicol 16:523–534PubMedGoogle Scholar
  9. Bradley WG, Borenstein AR, Nelson LM, Codd GA, Rosen BH, Stommel EW, Cox PA (2013) Is exposure to cyanobacteria an environmental risk factor for amyotrophic lateral sclerosis and other neurodegenerative diseases? Amyotroph Lateral Scler Frontotemporal Degener 14:325–333PubMedGoogle Scholar
  10. Buijse AD, Schaap LA, Bust TP (1992) Influence of water clarity on the catchability of six freshwater fish species in bottom trawls. Can J Fish Aquat Sci 49:885–893Google Scholar
  11. Carey CC, Ibelings BW, Hoffmann EP, Hamilton DP, Brookes JD (2012) Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Res 46:1394–1407PubMedGoogle Scholar
  12. Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655Google Scholar
  13. Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum Ecol Risk Assess 7:1393–1407Google Scholar
  14. Carton AG (2005) The impact of light intensity and algal-induced turbidity on first-feeding Seriola lalandi larvae. Aquac Res 36:1588–1594Google Scholar
  15. Chen J, Xie P, Zhang D, Ke Z, Yang H (2006) In situ studies on the bioaccumulation of microcystins in the phytoplanktivorous silver carp (Hypophthalmichthys molitrix) stocked in Lake Taihu with dense toxic Microcystis blooms. Aquaculture 261:1026–1038Google Scholar
  16. Chen W, Song L, Peng L, Wan N, Zhang X, Gan N (2008) Reduction in microcystin concentrations in large and shallow lakes: water and sediment-interface contributions. Water Res 42:763–773PubMedGoogle Scholar
  17. Chen X, Yang X, Yang L, Xiao B, Wu X, Wang J, Wan H (2010) An effective pathway for the removal of microcystin LR via anoxic biodegradation in lake sediments. Water Res 44:1884–1892PubMedGoogle Scholar
  18. Chislock MF, Sarnelle O, Olsen BK, Doster E, Wilson AE (2013) Large effects of consumer offense on ecosystem structure and function. Ecology 94:2375–2380PubMedGoogle Scholar
  19. Chiswell RK, Shaw GR, Eaglesham G, Smith MJ, Norris RL, Seawright AA, Moore MR (1999) Stability of cylindrospermopsin, the toxin from the cyanobacterium, Cylindrospermopsis raciborskii: effect of pH, temperature, and sunlight on decomposition. Environ Toxicol 14:155–161Google Scholar
  20. 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 48:345–355PubMedGoogle Scholar
  21. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Spon Press, LondonGoogle Scholar
  22. Christoffersen K, Lyck S, Winding A (2002) Microbial activity and bacterial community structure during degradation of microcystins. Aquat Microb Ecol 27:125–136Google Scholar
  23. Cirés S, Wörmer L, Wiedner C, Quesada A (2013) Temperature-dependent dispersal strategies of Aphanizomenon ovalisporum (Nostocales, Cyanobacteria): implications for the annual life cycle. Microb Ecol 65:12–21PubMedGoogle Scholar
  24. Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141Google Scholar
  25. Corbel S, Mougin C, Bouaïcha N (2014) Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 96:1–15PubMedGoogle Scholar
  26. Cousins I, Bealing D, James H, Sutton A (1996) Biodegradation of microcystin-LR by indigenous mixed bacterial populations. Water Res 30:481–485Google Scholar
  27. Dao TS, Do-Hong L-C, Wiegand C (2010) Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring. Toxicon 55:1244–1254PubMedGoogle Scholar
  28. de Abreu FQ, Ferrão-Filho AdS (2013) Effects of an Anatoxin-a (s)-producing strain of Anabaena spiroides (Cyanobacteria) on the survivorship and somatic growth of two Daphnia similis clones. J Environ Prot 4:12Google Scholar
  29. De Bernardi R, Giussani G (1990) Are blue-green algae a suitable food for zooplankton? An overview. Hydrobiologia 200(201):29–41Google Scholar
  30. de la Cruz AA et al (2013) A review on cylindrospermopsin: the global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environ Sci Process Impacts 15:1979–2003PubMedGoogle Scholar
  31. De Robertis A, Ryer CH, Veloza A, Brodeur RD (2003) Differential effects of turbidity on prey consumption of piscivorous and planktivorous fish. Can J Fish Aquat Sci 60:1517–1526Google Scholar
  32. De Senerpont Domis LN, Mooij WM, Huisman J (2007) Climate-induced shifts in an experimental phytoplankton community: a mechanistic approach. Hydrobiologia 584:403–413Google Scholar
  33. DeMott WR, Gulati RD, Van Donk E (2001) Daphnia food limitation in three hypereutrophic Dutch lakes: evidence for exclusion of large-bodied species by interfering filaments of cyanobacteria. Limnol Oceanogr 46:2054–2060Google Scholar
  34. Dziallas C, Grossart HP (2011) Temperature and biotic factors influence bacterial communities associated with the cyanobacterium Microcystis sp. Environ Microbiol 13:1632–1641PubMedGoogle Scholar
  35. Ekau W, Auel H, Pörtner H-O, Gilbert D (2010) Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish). Biogeosciences 7:1669–1699Google Scholar
  36. Engström-Öst J, Lehtiniemi M, Green S, Kozlowsky-Suzuki B, Viitasalo M (2002) Does cyanobacterial toxin accumulate in mysid shrimps and fish via copepods? J Exp Mar Biol Ecol 276:95–107Google Scholar
  37. Ernst B, Hoeger SJ, O’Brien E, Dietrich DR (2006) Oral toxicity of the microcystin-containing cyanobacterium Planktothrix rubescens in European whitefish (Coregonus lavaretus). Aquat Toxicol 79:31–40PubMedGoogle Scholar
  38. Ferrão-Filho AS, Kozlowsky-Suzuki B (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9:2729–2772PubMedCentralGoogle Scholar
  39. Ferrão-Filho AS, Soares MCS, Lima RS, Magalhães VF (2014) Effects of Cylindrospermopsis raciborskii (cyanobacteria) on the swimming behavior of Daphnia (cladocera). Environ Toxicol Chem 33:223–229PubMedGoogle Scholar
  40. Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (cyanobacteria) bloom occurrence and geographic expansion? J Phycol 43:256–265Google Scholar
  41. Freitas EC, Pinheiro C, Rocha O, Loureiro S (2014) Can mixtures of cyanotoxins represent a risk to the zooplankton? The case study of Daphnia magna Straus exposed to hepatotoxic and neurotoxic cyanobacterial extracts. Harmful Algae 31:143–152Google Scholar
  42. Furey A, Allis O, Ortea P, Lehane M, James K (2008) Hepatotoxins: context and chemical determination. In: Botana LM (ed) Seafood and freshwater toxins: pharmacology, physiology and detection, vol 173, 2nd edn. Taylor and Francis, Boca Raton, pp 845–886Google Scholar
  43. Gao Y, O’Neil J, Stoecker D, Cornwell J (2014) Photosynthesis and nitrogen fixation during cyanobacteria blooms in an oligohaline and tidal freshwater estuary. Aquat Microb Ecol 72:127–142Google Scholar
  44. Ger KA, Hansson LA, Lürling M (2014) Understanding cyanobacteria–zooplankton interactions in a more eutrophic world. Freshw Biol 59:1783–1798Google Scholar
  45. Ghadouani A, Pinel-Alloul B, Prepas EE (2006) Could increased cyanobacterial biomass following forest harvesting cause a reduction in zooplankton body size structure? Can J Fish Aquat Sci 63:2308–2317Google Scholar
  46. Gliwicz ZM (2004) Zooplankton. In: O’Sullivan P, Reynolds C (eds) The lakes handbook. Volume 1. Limnology and Limnetic Ecology, vol 5. Blackwell Publishing, Malden, pp 461–516Google Scholar
  47. Goudie AS (2014) Desert dust and human health disorders. Environ Int 63:101–113PubMedGoogle Scholar
  48. Gray SM, Bieber FME, Mandrak NE (2014) Experimental evidence for species-specific response to turbidity in imperilled fishes. Aquat Conserv 24:546–560Google Scholar
  49. Ha M-H, Pflugmacher S (2013) Phytotoxic effects of the cyanobacterial neurotoxin anatoxin-a: morphological, physiological and biochemical responses in aquatic macrophyte, Ceratophyllum demersum. Toxicon 70:1–8PubMedGoogle Scholar
  50. Hadas O, Pinkas R, Malinsky-Rushansky N, Nishri A, Kaplan A, Rimmer A, Sukenik A (2012) Appearance and establishment of diazotrophic cyanobacteria in Lake Kinneret, Israel. Freshw Biol 57:1214–1227Google Scholar
  51. Hairston N et al (2001) Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55:2203–2214PubMedGoogle Scholar
  52. Havens KE (2008) Cyanobacteria blooms: effects on aquatic ecosystems. In: Hudnell HK (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 733–747Google Scholar
  53. Holst T, Jørgensen NO, Jørgensen C, Johansen A (2003) Degradation of microcystin in sediments at oxic and anoxic, denitrifying conditions. Water Res 37:4748–4760PubMedGoogle Scholar
  54. Holzner C, Aeschbach-Hertig W, Simona M, Veronesi M, Imboden D, Kipfer R (2009) Exceptional mixing events in meromictic Lake Lugano (Switzerland/Italy), studied using environmental tracers. Limnol Oceanogr 54:1113Google Scholar
  55. Humpage A (2008) Toxin types, toxicokinetics and toxicodynamics. Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 383–415Google Scholar
  56. Hyenstrand P, Blomqvist P, Pettersson A (1998) Factors determining cyanobacterial success in aquatic systems: a literature review. Arch Hydrobiol Spec Issues Adv Limnol 51:41–62Google Scholar
  57. Ibelings BW, Havens KE (2008) Cyanobacterial toxins: a qualitative meta-analysis of concentrations, dosage and effects in freshwater, estuarine and marine biota. In: Hudnell H (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 675–732Google Scholar
  58. Imanishi S, Kato H, Mizuno M, Tsuji K, K-i Harada (2005) Bacterial degradation of microcystins and nodularin. Chem Res Toxicol 18:591–598PubMedGoogle Scholar
  59. Ishii H, Nishijima M, Abe T (2004) Characterization of degradation process of cyanobacterial hepatotoxins by a gram-negative aerobic bacterium. Water Res 38:2667–2676PubMedGoogle Scholar
  60. Istvánovics V (2009) Eutrophication of lakes and reservoirs. In: Likens GE (ed) Encyclopedia of inland waters, vol 1. Elsevier, Oxford, pp 157–165Google Scholar
  61. Istvánovics V, Shafik HM, Présing M, Juhos S (2000) Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshw Biol 43:257–275Google Scholar
  62. Jiang J, Gu X, Song R, Wang X, Yang L (2011) Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara. J Hazard Mater 190:188–196PubMedGoogle Scholar
  63. Jokela J, Oftedal L, Herfindal L, Permi P, Wahlsten M, Døskeland SO, Sivonen K (2012) Anabaenolysins, novel cytolytic lipopeptides from benthic Anabaena cyanobacteria. PLoS One 7:e41222PubMedCentralPubMedGoogle Scholar
  64. Jonasson S et al (2010) Transfer of a cyanobacterial neurotoxin within a temperate aquatic ecosystem suggests pathways for human exposure. Proc Natl Acad Sci USA 107:9252–9257PubMedCentralPubMedGoogle Scholar
  65. Jones E, Fryer R, Kynoch R, Summerbell K (2004) Working document: the influence of twine colour and contrast on the effectiveness of square mesh panels in a demersal whitefish trawl. ICES WGFTFB Working Paper, 20–23 April 2004, GdyniaGoogle Scholar
  66. Kaplan A, Harel M, Kaplan-Levy RN, Hadas O, Sukenik A, Dittmann E (2012) The languages spoken in the water body (or the biological role of cyanobacterial toxins). Front Microbiol 3:138PubMedCentralPubMedGoogle Scholar
  67. Kling HJ, Watson SB, McCullough GK, Stainton MP (2011) Bloom development and phytoplankton succession in Lake Winnipeg: a comparison of historical records with recent data. Aquat Ecosyst Health Manage 14:219–224Google Scholar
  68. Kozlowsky-Suzuki B, Wilson AE, Ferrão-Filho AdS (2012) Biomagnification or biodilution of microcystins in aquatic foodwebs? Meta-analyses of laboratory and field studies. Harmful Algae 18:47–55Google Scholar
  69. Kumagai M, Nakano S, Jiao C, Hayakawa K, Tsujimura S, Frenette JJ, Quesada A (2000) Effect of cyanobacterial blooms on thermal stratification. Limnology 1:191–195Google Scholar
  70. Kurmayer R (2001) Competitive ability of Daphnia under dominance of non-toxic filamentous cyanobacteria. Hydrobiologia 442:279–289Google Scholar
  71. Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282PubMedGoogle Scholar
  72. Leão PN, Engene N, Antunes A, Gerwick WH, Vasconcelos V (2012) The chemical ecology of cyanobacteria. Nat Prod Rep 29:372–391PubMedCentralPubMedGoogle Scholar
  73. Lemaire V, Brusciotti S, van Gremberghe I, Vyverman W, Vanoverbeke J, De Meester L (2012) Genotype × genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea Daphnia. Evol Appl 5:168–182PubMedCentralPubMedGoogle Scholar
  74. Lemes GA, Kersanach R, Pinto Lda S, Dellagostin OA, Yunes JS, Matthiensen A (2008) Biodegradation of microcystins by aquatic Burkholderia sp. from a South Brazilian coastal lagoon. Ecotoxicol Environ Saf 69:358–365PubMedGoogle Scholar
  75. Li N et al (2011) Metagenome of microorganisms associated with the toxic Cyanobacteria Microcystis aeruginosa analyzed using the 454 sequencing platform. Chin J Oceanol Limnol 29:505–513Google Scholar
  76. Lindholm T, Eriksson JE, Meriluoto JA (1989) Toxic cyanobacteria and water quality problems—examples from a eutrophic lake on Åland, south west Finland. Water Res 23:481–486Google Scholar
  77. Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13:1560–1572PubMedGoogle Scholar
  78. Liu L, Rein KS (2010) New peptides isolated from Lyngbya species: a review. Mar Drugs 8:1817–1837PubMedCentralPubMedGoogle Scholar
  79. Lurling M, Eshetu F, Faassen EJ, Kosten S, Huszar VL (2013) Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshw Biol 58:552–559Google Scholar
  80. Malbrouck C, Kestemont P (2006) Effects of microcystins on fish. Environ Toxicol Chem 25:72PubMedGoogle Scholar
  81. Maldener I, Summers ML, Sukenik A (2014) Cellular differentiation in filamentous cyanobacteria. In: Flores E, Herrero A (eds) The cell biology of cyanobacteria. Caister Academic Press, Norfolk, pp 263–291Google Scholar
  82. Manage PM, Edwards C, Singh BK, Lawton LA (2009) Isolation and identification of novel microcystin-degrading bacteria. Appl Environ Microbiol 75:6924–6928PubMedCentralPubMedGoogle Scholar
  83. Maršálek B, Bláha L (2004) Comparison of 17 biotests for detection of cyanobacterial toxicity. Environ Toxicol 19:310–317PubMedGoogle Scholar
  84. Maruyama T et al (2006) Sphingosinicella microcystinivorans gen. nov., sp. nov., a microcystin-degrading bacterium. Int J Syst Evol Microbiol 56:85–89PubMedGoogle Scholar
  85. Mazur-Marzec H, Plinski M (2009) Do toxic cyanobacteria blooms pose a threat to the Baltic ecosystem? Oceanologia 51:293–319Google Scholar
  86. Mazur-Marzec H, Toruńska A, Błońska MJ, Moskot M, Pliński M, Jakóbkiewicz-Banecka J, Węgrzyn G (2009) Biodegradation of nodularin and effects of the toxin on bacterial isolates from the Gulf of Gdańsk. Water Res 43:2801–2810PubMedGoogle Scholar
  87. Mehnert G, Leunert F, Cirés S, Jöhnk KD, Rücker J, Nixdorf B, Wiedner C (2010) Competitiveness of invasive and native cyanobacteria from temperate freshwaters under various light and temperature conditions. J Plankton Res 32:1009–1021Google Scholar
  88. Méjean A, Paci G, Gautier V, Ploux O (2014) Biosynthesis of anatoxin-a and analogues (anatoxins) in cyanobacteria. Toxicon 91:15–22PubMedGoogle Scholar
  89. Metcalf JS, Codd GA (2012) Cyanotoxins. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Dordrecht, pp 651–675Google Scholar
  90. Mitrovic SM, Bowling LC, Buckney RT (2001) Vertical disentrainment of Anabaena circinalis in the turbid, freshwater Darling River, Australia: quantifying potential benefits from buoyancy. J Plankton Res 23:47–55Google Scholar
  91. Mohamed ZA, Alamri SA (2012) Biodegradation of cylindrospermopsin toxin by microcystin-degrading bacteria isolated from cyanobacterial blooms. Toxicon 60:1390–1395PubMedGoogle Scholar
  92. Monserrat J, Pinho G, Yunes J (2003) Toxicological effects of hepatotoxins (microcystins) on aquatic organisms. Comments Toxicol 9:89–101Google Scholar
  93. Moreira C, Azevedo J, Antunes A, Vasconcelos V (2013) Cylindrospermopsin: occurrence, methods of detection and toxicology. J Appl Microbiol 114:605–620PubMedGoogle Scholar
  94. Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49PubMedCentralPubMedGoogle Scholar
  95. Niu Y et al (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res 45:4169–4182PubMedGoogle Scholar
  96. Nogueira IC, Saker ML, Pflugmacher S, Wiegand C, Vasconcelos VM (2004) Toxicity of the cyanobacterium Cylindrospermopsis raciborskii to Daphnia magna. Environ Toxicol 19:453–459PubMedGoogle Scholar
  97. O’Neil J, Davis TW, Burford MA, Gobler C (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334Google Scholar
  98. Oberemm A, Becker J, Codd GA, Steinberg C (1999) Effects of cyanobacterial toxins and aqueous crude extracts of cyanobacteria on the development of fish and amphibians. Environ Toxicol 14:77–88Google Scholar
  99. Oliver RL, Hamilton DP, Brookes JD, Ganf GG (2012) Physiology, blooms and prediction of planktonic cyanobacteria. In: Ecology of cyanobacteria II. Springer, Dordrecht, pp 155–194Google Scholar
  100. Osborne NJ, Webb PM, Moore MR, Shaw GR (2001) Environmental toxicology of the cyanobacterium Lyngbya spp. Toxicology 164:203Google Scholar
  101. Osswald J, Carvalho AP, Claro J, Vasconcelos V (2009) Effects of cyanobacterial extracts containing anatoxin-a and of pure anatoxin-a on early developmental stages of carp. Ecotoxicol Environ Saf 72:473–478PubMedGoogle Scholar
  102. O’Sullivan P, Reynolds C (2005) The lakes handbook: Vol. 2: Lake restoration and rehabilitation. Blackwell Publishing, MaldenGoogle Scholar
  103. Ozawa K, Yokoyama A, Ishikawa K, Kumagai M, Watanabe MF, Park H-D (2003) Accumulation and depuration of microcystin produced by the cyanobacterium Microcystis in a freshwater snail. Limnology 4:131–138Google Scholar
  104. Padisák J (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol 107:563–593Google Scholar
  105. Paerl H, Fulton III R (2006) Ecology of harmful cyanobacteria. In: Ecology of harmful algae. Springer, Dordrecht, pp 95–109Google Scholar
  106. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37PubMedGoogle Scholar
  107. Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010PubMedGoogle Scholar
  108. Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363PubMedGoogle Scholar
  109. Paerl HW, Xu H, McCarthy MJ, Zhu G, Qin B, Li Y, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45:1973–1983PubMedGoogle Scholar
  110. Pimentel D et al (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20Google Scholar
  111. Ploug H et al (2010) Carbon and nitrogen fluxes associated with the cyanobacterium Aphanizomenon sp. in the Baltic Sea. ISME J 4:1215–1223PubMedGoogle Scholar
  112. Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461PubMedGoogle Scholar
  113. Puerto M, Jos A, Pichardo S, Gutiérrez-Praena D, Cameán A (2011) Acute effects of pure cylindrospermopsin on the activity and transcription of antioxidant enzymes in tilapia (Oreochromis niloticus) exposed by gavage. Ecotoxicology 20:1852–1860PubMedGoogle Scholar
  114. Purdie EL, Metcalf JS, Kashmiri S, Codd GA (2009) Toxicity of the cyanobacterial neurotoxin β-N-methylamino-l-alanine to three aquatic animal species. Amyotroph Lateral Scler 10:67–70PubMedGoogle Scholar
  115. Quesada A, Moreno E, Carrasco D, Paniagua T, Wormer L, De Hoyos C, Sukenik A (2006) Toxicity of Aphanizomenon ovalisporum (Cyanobacteria) in a Spanish water reservoir. Eur J Phycol 41:39–45Google Scholar
  116. Reynolds C (2006) The ecology of phytoplankton. Cambridge University Press, CambridgeGoogle Scholar
  117. Reynolds C, Dokulil M, Padisák J (2000) Understanding the assembly of phytoplankton in relation to the trophic spectrum: where are we now? In: Reynolds C, Dokulil M, Padisák J (eds) The trophic spectrum revisited—Proceedings of the 11th workshop of the international association of phytoplankton taxonomy and ecology (IAP). Springer, Dordrecht, pp 147–152Google Scholar
  118. Ricciardi A, Cohen J (2007) The invasiveness of an introduced species does not predict its impact. Biol Invasions 9:309–315Google Scholar
  119. Richards GR, Farrell AP (eds) (2009) Fish physiology: hypoxia. Elsevier, AmsterdamGoogle Scholar
  120. 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 59:99–114Google Scholar
  121. Ríos V, Guzmán-Guillén R, Moreno IM, Prieto AI, Puerto M, Jos A, Cameán AM (2014) Influence of two depuration periods on the activity and transcription of antioxidant enzymes in Tilapia exposed to repeated doses of cylindrospermopsin under laboratory conditions. Toxins 6:1062–1079PubMedCentralPubMedGoogle Scholar
  122. Roberts JJ, Höök TO, Ludsin SA, Pothoven SA, Vanderploeg HA, Brandt SB (2009) Effects of hypolimnetic hypoxia on foraging and distributions of Lake Erie yellow perch. J Exp Mar Biol Ecol 381:S132–S142Google Scholar
  123. Rohrlack T, Christoffersen K, Dittmann E, Nogueira I, Vasconcelos V, Börner T (2005) Ingestion of microcystins by Daphnia: intestinal uptake and toxic effects. Limnol Oceanogr 50:440–448Google Scholar
  124. Rojo C, Segura M, Rodrigo MA (2013) The allelopathic capacity of submerged macrophytes shapes the microalgal assemblages from a recently restored coastal wetland. Ecol Eng 58:149–155Google Scholar
  125. Sadler T, von Elert E (2014) Physiological interaction of Daphnia and Microcystis with regard to cyanobacterial secondary metabolites. Aquat Toxicol 156:96–105PubMedGoogle Scholar
  126. Saito T et al (2003) Detection and sequencing of the microcystin LR-degrading gene, mlrA, from new bacteria isolated from Japanese lakes. FEMS Microbiol Lett 229:271–276PubMedGoogle Scholar
  127. Salmaso N, Cerasino L, Flaim G, Tolotti M (eds) (2012) Phytoplankton responses to human impacts at different scales. Developments in Hydrobiology, vol 221. Springer, Dordrecht, p VIGoogle Scholar
  128. Salmaso N, Naselli-Flores L, Padisák J (2015) Functional classifications and their application in phytoplankton ecology. Freshw Biol. doi: 10.1111/fwb.12520
  129. Sarma TA (2013) Handbook of cyanobacteria. CRC Press, Taylor and Francis, Boca RatonGoogle Scholar
  130. Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50:1565–1570Google Scholar
  131. Scavia D et al (2014) Assessing and addressing the re-eutrophication of Lake Erie: central basin hypoxia. J Gt Lakes Res 40:226–246Google Scholar
  132. Scheffer M, Rinaldi S, Gragnani A, Mur LR, van Nes EH (1997) On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78:272–282Google Scholar
  133. Senogles P, Smith M (2002) Physical, chemical and biological methods for the degradation of the cyanobacterial toxin, cylindrospermopsin. In: AWWA water quality technology conference & exhibition. American Water Works Association, pp 1–14Google Scholar
  134. Shams S, Cerasino L, Salmaso N, Dietrich DR (2014) Experimental models of microcystin accumulation in Daphnia magna grazing on Planktothrix rubescen: implications for water management. Aquat Toxicol 148:9–15PubMedGoogle Scholar
  135. Shao J, Peng L, Luo S, Yu G, J-d Gu, Lin S, Li R (2013) First report on the allelopathic effect of Tychonema bourrellyi (Cyanobacteria) against Microcystis aeruginosa (Cyanobacteria). J Appl Phycol 25:1567–1573Google Scholar
  136. Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, Ogawa T (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98:11789–11794PubMedCentralPubMedGoogle Scholar
  137. Smith MJ (2005) Biodegradation of the cyanotoxin cylindrospermopsin. The University of Queensland, BrisbaneGoogle Scholar
  138. Smith MJ, Shaw GR, Eaglesham GK, Ho L, Brookes JD (2008) Elucidating the factors influencing the biodegradation of cylindrospermopsin in drinking water sources. Environ Toxicol 23:413–421PubMedGoogle Scholar
  139. Smith DJ, Griffin DW, Jaffe DA (2011) The high life: transport of microbes in the atmosphere. EOS Trans Am Geophys Union 92:249–250Google Scholar
  140. Sommer U, Adrian R, Bauer B, Winder M (2012) The response of temperate aquatic ecosystems to global warming: novel insights from a multidisciplinary project. Mar Biol 159:2367–2377Google Scholar
  141. Sotton B et al (2012) Impact of toxic cyanobacterial blooms on Eurasian perch (Perca fluviatilis): experimental study and in situ observations in a peri-alpine lake. PLoS One 7:e52243PubMedCentralPubMedGoogle Scholar
  142. Sotton B, Domaizon I, Anneville O, Cattanéo F, Guillard J (2014a) Nodularin and cylindrospermopsin: a review of their effects on fish. Rev Fish Biol Fish. doi: 10.1007/s11160-014-9366-6 Google Scholar
  143. Sotton B, Guillard J, Anneville O, Maréchal M, Savichtcheva O, Domaizon I (2014b) Trophic transfer of microcystins through the lake pelagic food web: evidence for the role of zooplankton as a vector in fish contamination. Sci Total Environ 466–467:152–163PubMedGoogle Scholar
  144. Stevenson BS, Waterbury JB (2006) Isolation and identification of an epibiotic bacterium associated with heterocystous Anabaena cells. Biol Bull 210:73–77PubMedGoogle Scholar
  145. Stewart I, Seawright AA, Shaw GR (2008) Cyanobacterial poisoning in livestock, wild mammals and birds—an overview. In: Hudnell H (ed) Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 613–637Google Scholar
  146. Sukenik A et al (2002) Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatunense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnol Oceanogr 47:1656–1663Google Scholar
  147. Sukenik A, Hadas O, Kaplan A, Quesada A (2012) Invasion of Nostocales (cyanobacteria) to subtropical and temperate freshwater lakes–physiological, regional, and global driving forces. Front Aquat Microbiol 3:86Google Scholar
  148. Svirčev Z, Krstič S, Miladinov-Mikov M, Baltič V, Vidovič M (2009) Freshwater cyanobacterial blooms and primary liver cancer epidemiological studies in Serbia. J Environ Sci Health C 27:36–55Google Scholar
  149. Tillmanns AR, Wilson AE, Pick FR, Sarnelle O (2008) Meta-analysis of cyanobacterial effects on zooplankton population growth rate: species-specific responses. Fundam Appl Limnol/Arch Hydrobiol 171:285–295Google Scholar
  150. Trubetskova IL, Haney JF (2006) Effects of differing concentrations of microcystin-producing Microcystis aeruginosa on growth, reproduction, survivorship and offspring of Daphnia magna. Arch Hydrobiol 167:533–546Google Scholar
  151. Urrutia-Cordero P et al (2013) Effects of harmful cyanobacteria on the fershwater pathogenic free-living amoeba Acanthoamoeba castellanii. Aquat Toxicol 130:9–17PubMedGoogle Scholar
  152. Üveges V, Tapolczai K, Krienitz L, Padisák J (2012) Photosynthetic characteristics and physiological plasticity of an Aphanizomenon flos-aquae (Cyanobacteria, Nostocaceae) winter bloom in a deep oligo-mesotrophic lake (Lake Stechlin, Germany). Hydrobiologia 698:263–272Google Scholar
  153. Vanderploeg HA et al (2009) Hypoxia affects spatial distributions and overlap of pelagic fish, zooplankton, and phytoplankton in Lake Erie. J Exp Mar Biol Ecol 381:S92–S107Google Scholar
  154. Verspagen JM, Van de Waal DB, Finke JF, Visser PM, Van Donk E, Huisman J (2014) Rising CO2 levels will intensify phytoplankton blooms in eutrophic and hypertrophic lakes. PLoS One 9:e104325PubMedCentralPubMedGoogle Scholar
  155. Vestola J et al (2014) Hassallidins, antifungal glycolipopeptides, are widespread among cyanobacteria and are the end-product of a nonribosomal pathway. Proc Natl Acad Sci USA 111:1909–1917Google Scholar
  156. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499Google Scholar
  157. Wiedner C, Rücker J, Brüggemann R, Nixdorf B (2007) Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia 152:473–484PubMedGoogle Scholar
  158. Wilson AE, Sarnelle O, Tillmanns AR (2006) Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnol Oceanogr 51:1915–1924Google Scholar
  159. Wolf HU, Frank C (2002) Toxicity assessment of cyanobacterial toxin mixtures. Environ Toxicol 17:395–399PubMedGoogle Scholar
  160. Wormer L, Cirés S, Carrasco D, Quesada A (2008) Cylindrospermopsin is not degraded by co-occurring natural bacterial communities during a 40-day study. Harmful Algae 7:206–213Google Scholar
  161. Wu X, Xi W, Ye W, Yang H (2007) Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiol Ecol 61:85–96PubMedGoogle Scholar
  162. Wu Z, Zeng B, Li R, Song L (2011) Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation. Harmful Algae 15:53–58Google Scholar
  163. Wurts WA, Durborow RM (1992) Interactions of pH, carbon dioxide, alkalinity and hardness in fish ponds. Southern Regional Aquaculture Center Stoneville, Mississipi State University No. 464Google Scholar
  164. Xie L, Xie P, Guo L, Li L, Miyabara Y, Park H-D (2005) Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environ Toxicol 20:293–300PubMedGoogle Scholar
  165. Yang Z, Lü K, Chen Y, Montagnes DJS (2012) The interactive effects of ammonia and microcystin on life-history traits of the cladoceran Daphnia magna: synergistic or antagonistic? PLoS One 7:e32285PubMedCentralPubMedGoogle Scholar
  166. Yokoyama A, Park HD (2003) Depuration kinetics and persistence of the cyanobacterial toxin microcystin-LR in the freshwater bivalve Unio douglasiae. Environ Toxicol 18:61–67PubMedGoogle Scholar
  167. Żak A, Musiewicz K, Kosakowska A (2012) Allelopathic activity of the Baltic cyanobacteria against microalgae. Estuar Coast Shelf Sci 112:4–10Google Scholar
  168. Zohary T, Padisák J, Naselli-Flores L (2010) Phytoplankton in the physical environment: beyond nutrients, at the end, there is some light. Hydrobiologia 639:261–269Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Kinneret Limnological LaboratoryIsrael Oceanographic & Limnological ResearchMigdalIsrael
  2. 2.Dpt. BiologiaUniversidad Autónoma de MadridMadridSpain
  3. 3.IASMA Research and Innovation CentreIstituto Agrario di S. Michele all’Adige - Fondazione E. MachS. Michele all’AdigeItaly

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