Skip to main content
SpringerLink
Log in

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

  • Review Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

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.

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

  • 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 8:273–278

    CAS  Google Scholar 

  • Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277

    Google Scholar 

  • 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 6:117–146

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 53:289–299

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 167:547–559

    CAS  Google Scholar 

  • 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 62:4086–4094

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 16:523–534

    CAS  PubMed  Google Scholar 

  • 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 14:325–333

    CAS  PubMed  Google Scholar 

  • 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 49:885–893

    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

    CAS  PubMed  Google Scholar 

  • Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655

    Google Scholar 

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

    Google Scholar 

  • Carton AG (2005) The impact of light intensity and algal-induced turbidity on first-feeding Seriola lalandi larvae. Aquac Res 36:1588–1594

    Google Scholar 

  • 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 261:1026–1038

    CAS  Google Scholar 

  • 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 42:763–773

    CAS  PubMed  Google Scholar 

  • 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 44:1884–1892

    CAS  PubMed  Google Scholar 

  • Chislock MF, Sarnelle O, Olsen BK, Doster E, Wilson AE (2013) Large effects of consumer offense on ecosystem structure and function. Ecology 94:2375–2380

    PubMed  Google Scholar 

  • 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 14:155–161

    CAS  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

    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, London

    Google Scholar 

  • Christoffersen K, Lyck S, Winding A (2002) Microbial activity and bacterial community structure during degradation of microcystins. Aquat Microb Ecol 27:125–136

    Google Scholar 

  • 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 65:12–21

    PubMed  Google Scholar 

  • Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141

    Google Scholar 

  • 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 96:1–15

    CAS  PubMed  Google Scholar 

  • Cousins I, Bealing D, James H, Sutton A (1996) Biodegradation of microcystin-LR by indigenous mixed bacterial populations. Water Res 30:481–485

    CAS  Google Scholar 

  • Dao TS, Do-Hong L-C, Wiegand C (2010) Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring. Toxicon 55:1244–1254

    CAS  PubMed  Google Scholar 

  • 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 4:12

    Google Scholar 

  • De Bernardi R, Giussani G (1990) Are blue-green algae a suitable food for zooplankton? An overview. Hydrobiologia 200(201):29–41

    Google Scholar 

  • 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 15:1979–2003

    PubMed  Google Scholar 

  • 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 60:1517–1526

    Google Scholar 

  • De Senerpont Domis LN, Mooij WM, Huisman J (2007) Climate-induced shifts in an experimental phytoplankton community: a mechanistic approach. Hydrobiologia 584:403–413

    Google Scholar 

  • 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 46:2054–2060

    Google Scholar 

  • Dziallas C, Grossart HP (2011) Temperature and biotic factors influence bacterial communities associated with the cyanobacterium Microcystis sp. Environ Microbiol 13:1632–1641

    PubMed  Google Scholar 

  • 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 7:1669–1699

    CAS  Google Scholar 

  • 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 276:95–107

    Google Scholar 

  • 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 79:31–40

    CAS  PubMed  Google Scholar 

  • Ferrão-Filho AS, Kozlowsky-Suzuki B (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9:2729–2772

    PubMed Central  Google Scholar 

  • 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 33:223–229

    PubMed  Google Scholar 

  • Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (cyanobacteria) bloom occurrence and geographic expansion? J Phycol 43:256–265

    Google Scholar 

  • 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 31:143–152

    CAS  Google Scholar 

  • 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 845–886

    Google Scholar 

  • 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 72:127–142

    Google Scholar 

  • Ger KA, Hansson LA, Lürling M (2014) Understanding cyanobacteria–zooplankton interactions in a more eutrophic world. Freshw Biol 59:1783–1798

    Google Scholar 

  • 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 63:2308–2317

    Google Scholar 

  • 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 461–516

    Google Scholar 

  • Goudie AS (2014) Desert dust and human health disorders. Environ Int 63:101–113

    CAS  PubMed  Google Scholar 

  • Gray SM, Bieber FME, Mandrak NE (2014) Experimental evidence for species-specific response to turbidity in imperilled fishes. Aquat Conserv 24:546–560

    Google Scholar 

  • 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 70:1–8

    CAS  PubMed  Google Scholar 

  • 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 57:1214–1227

    CAS  Google Scholar 

  • Hairston N et al (2001) Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55:2203–2214

    PubMed  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. Springer, New York, pp 733–747

    Google Scholar 

  • Holst T, Jørgensen NO, Jørgensen C, Johansen A (2003) Degradation of microcystin in sediments at oxic and anoxic, denitrifying conditions. Water Res 37:4748–4760

    CAS  PubMed  Google Scholar 

  • 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 54:1113

    CAS  Google Scholar 

  • Humpage A (2008) Toxin types, toxicokinetics and toxicodynamics. Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 383–415

    Google Scholar 

  • Hyenstrand P, Blomqvist P, Pettersson A (1998) Factors determining cyanobacterial success in aquatic systems: a literature review. Arch Hydrobiol Spec Issues Adv Limnol 51:41–62

    Google Scholar 

  • 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 675–732

    Google Scholar 

  • Imanishi S, Kato H, Mizuno M, Tsuji K, K-i Harada (2005) Bacterial degradation of microcystins and nodularin. Chem Res Toxicol 18:591–598

    CAS  PubMed  Google Scholar 

  • Ishii H, Nishijima M, Abe T (2004) Characterization of degradation process of cyanobacterial hepatotoxins by a gram-negative aerobic bacterium. Water Res 38:2667–2676

    CAS  PubMed  Google Scholar 

  • Istvánovics V (2009) Eutrophication of lakes and reservoirs. In: Likens GE (ed) Encyclopedia of inland waters, vol 1. Elsevier, Oxford, pp 157–165

    Google Scholar 

  • 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 43:257–275

    Google Scholar 

  • 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 190:188–196

    CAS  PubMed  Google Scholar 

  • 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:e41222

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 107:9252–9257

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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, Gdynia

  • 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 3:138

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 14:219–224

    Google Scholar 

  • 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 18:47–55

    CAS  Google Scholar 

  • Kumagai M, Nakano S, Jiao C, Hayakawa K, Tsujimura S, Frenette JJ, Quesada A (2000) Effect of cyanobacterial blooms on thermal stratification. Limnology 1:191–195

    Google Scholar 

  • Kurmayer R (2001) Competitive ability of Daphnia under dominance of non-toxic filamentous cyanobacteria. Hydrobiologia 442:279–289

    Google Scholar 

  • Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282

    PubMed  Google Scholar 

  • Leão PN, Engene N, Antunes A, Gerwick WH, Vasconcelos V (2012) The chemical ecology of cyanobacteria. Nat Prod Rep 29:372–391

    PubMed Central  PubMed  Google Scholar 

  • 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 5:168–182

    PubMed Central  PubMed  Google Scholar 

  • 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 69:358–365

    CAS  PubMed  Google Scholar 

  • 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 29:505–513

    Google Scholar 

  • 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 23:481–486

    CAS  Google Scholar 

  • Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13:1560–1572

    PubMed  Google Scholar 

  • Liu L, Rein KS (2010) New peptides isolated from Lyngbya species: a review. Mar Drugs 8:1817–1837

    PubMed Central  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Malbrouck C, Kestemont P (2006) Effects of microcystins on fish. Environ Toxicol Chem 25:72

    CAS  PubMed  Google Scholar 

  • 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 263–291

    Google Scholar 

  • Manage PM, Edwards C, Singh BK, Lawton LA (2009) Isolation and identification of novel microcystin-degrading bacteria. Appl Environ Microbiol 75:6924–6928

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maršálek B, Bláha L (2004) Comparison of 17 biotests for detection of cyanobacterial toxicity. Environ Toxicol 19:310–317

    PubMed  Google Scholar 

  • Maruyama T et al (2006) Sphingosinicella microcystinivorans gen. nov., sp. nov., a microcystin-degrading bacterium. Int J Syst Evol Microbiol 56:85–89

    CAS  PubMed  Google Scholar 

  • Mazur-Marzec H, Plinski M (2009) Do toxic cyanobacteria blooms pose a threat to the Baltic ecosystem? Oceanologia 51:293–319

    Google Scholar 

  • 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 43:2801–2810

    CAS  PubMed  Google Scholar 

  • 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 32:1009–1021

    CAS  Google Scholar 

  • Méjean A, Paci G, Gautier V, Ploux O (2014) Biosynthesis of anatoxin-a and analogues (anatoxins) in cyanobacteria. Toxicon 91:15–22

    PubMed  Google Scholar 

  • Metcalf JS, Codd GA (2012) Cyanotoxins. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Dordrecht, pp 651–675

    Google Scholar 

  • 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 23:47–55

    Google Scholar 

  • Mohamed ZA, Alamri SA (2012) Biodegradation of cylindrospermopsin toxin by microcystin-degrading bacteria isolated from cyanobacterial blooms. Toxicon 60:1390–1395

    CAS  PubMed  Google Scholar 

  • Monserrat J, Pinho G, Yunes J (2003) Toxicological effects of hepatotoxins (microcystins) on aquatic organisms. Comments Toxicol 9:89–101

    CAS  Google Scholar 

  • Moreira C, Azevedo J, Antunes A, Vasconcelos V (2013) Cylindrospermopsin: occurrence, methods of detection and toxicology. J Appl Microbiol 114:605–620

    CAS  PubMed  Google Scholar 

  • 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 75:14–49

    PubMed Central  CAS  PubMed  Google Scholar 

  • Niu Y et al (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res 45:4169–4182

    CAS  PubMed  Google Scholar 

  • Nogueira IC, Saker ML, Pflugmacher S, Wiegand C, Vasconcelos VM (2004) Toxicity of the cyanobacterium Cylindrospermopsis raciborskii to Daphnia magna. Environ Toxicol 19:453–459

    CAS  PubMed  Google Scholar 

  • 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 14:313–334

    Google Scholar 

  • 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 14:77–88

    CAS  Google Scholar 

  • Oliver RL, Hamilton DP, Brookes JD, Ganf GG (2012) Physiology, blooms and prediction of planktonic cyanobacteria. In: Ecology of cyanobacteria II. Springer, Dordrecht, pp 155–194

  • Osborne NJ, Webb PM, Moore MR, Shaw GR (2001) Environmental toxicology of the cyanobacterium Lyngbya spp. Toxicology 164:203

    Google Scholar 

  • 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 72:473–478

    CAS  PubMed  Google Scholar 

  • O’Sullivan P, Reynolds C (2005) The lakes handbook: Vol. 2: Lake restoration and rehabilitation. Blackwell Publishing, Malden

    Google Scholar 

  • 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 4:131–138

    CAS  Google Scholar 

  • Padisák J (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol 107:563–593

    Google Scholar 

  • Paerl H, Fulton III R (2006) Ecology of harmful cyanobacteria. In: Ecology of harmful algae. Springer, Dordrecht, pp 95–109

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

    CAS  PubMed  Google Scholar 

  • Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010

    CAS  PubMed  Google Scholar 

  • Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363

    CAS  PubMed  Google Scholar 

  • 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 45:1973–1983

    CAS  PubMed  Google Scholar 

  • Pimentel D et al (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20

    Google Scholar 

  • Ploug H et al (2010) Carbon and nitrogen fluxes associated with the cyanobacterium Aphanizomenon sp. in the Baltic Sea. ISME J 4:1215–1223

    CAS  PubMed  Google Scholar 

  • 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 59:1441–1461

    CAS  PubMed  Google Scholar 

  • 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 20:1852–1860

    CAS  PubMed  Google Scholar 

  • 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 10:67–70

    CAS  PubMed  Google Scholar 

  • 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 41:39–45

    CAS  Google Scholar 

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

    Google Scholar 

  • 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 147–152

    Google Scholar 

  • Ricciardi A, Cohen J (2007) The invasiveness of an introduced species does not predict its impact. Biol Invasions 9:309–315

    Google Scholar 

  • Richards GR, Farrell AP (eds) (2009) Fish physiology: hypoxia. Elsevier, Amsterdam

    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

    Google Scholar 

  • 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 6:1062–1079

    PubMed Central  PubMed  Google Scholar 

  • 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–S142

    Google Scholar 

  • 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 50:440–448

    CAS  Google Scholar 

  • 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 58:149–155

    Google Scholar 

  • Sadler T, von Elert E (2014) Physiological interaction of Daphnia and Microcystis with regard to cyanobacterial secondary metabolites. Aquat Toxicol 156:96–105

    CAS  PubMed  Google Scholar 

  • 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 229:271–276

    CAS  PubMed  Google Scholar 

  • 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 VI

  • Salmaso N, Naselli-Flores L, Padisák J (2015) Functional classifications and their application in phytoplankton ecology. Freshw Biol. doi:10.1111/fwb.12520

  • Sarma TA (2013) Handbook of cyanobacteria. CRC Press, Taylor and Francis, Boca Raton

    Google Scholar 

  • Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50:1565–1570

    Google Scholar 

  • Scavia D et al (2014) Assessing and addressing the re-eutrophication of Lake Erie: central basin hypoxia. J Gt Lakes Res 40:226–246

    CAS  Google Scholar 

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

    Google Scholar 

  • 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 1–14

  • 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 148:9–15

    CAS  PubMed  Google Scholar 

  • 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 25:1567–1573

    Google Scholar 

  • 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 98:11789–11794

    PubMed Central  CAS  PubMed  Google Scholar 

  • Smith MJ (2005) Biodegradation of the cyanotoxin cylindrospermopsin. The University of Queensland, Brisbane

    Google Scholar 

  • 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 23:413–421

    CAS  PubMed  Google Scholar 

  • Smith DJ, Griffin DW, Jaffe DA (2011) The high life: transport of microbes in the atmosphere. EOS Trans Am Geophys Union 92:249–250

    Google Scholar 

  • 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 159:2367–2377

    Google Scholar 

  • 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:e52243

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • 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 466–467:152–163

    PubMed  Google Scholar 

  • Stevenson BS, Waterbury JB (2006) Isolation and identification of an epibiotic bacterium associated with heterocystous Anabaena cells. Biol Bull 210:73–77

    PubMed  Google Scholar 

  • 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 613–637

    Google Scholar 

  • 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 47:1656–1663

    Google Scholar 

  • 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 3:86

    Google Scholar 

  • 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 27:36–55

    Google Scholar 

  • 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 171:285–295

    Google Scholar 

  • 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 167:533–546

    CAS  Google Scholar 

  • Urrutia-Cordero P et al (2013) Effects of harmful cyanobacteria on the fershwater pathogenic free-living amoeba Acanthoamoeba castellanii. Aquat Toxicol 130:9–17

    PubMed  Google Scholar 

  • 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 698:263–272

    Google Scholar 

  • 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–S107

    Google Scholar 

  • 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:e104325

    PubMed Central  PubMed  Google Scholar 

  • 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 111:1909–1917

    Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    CAS  Google Scholar 

  • 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 152:473–484

    PubMed  Google Scholar 

  • 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 51:1915–1924

    Google Scholar 

  • Wolf HU, Frank C (2002) Toxicity assessment of cyanobacterial toxin mixtures. Environ Toxicol 17:395–399

    CAS  PubMed  Google Scholar 

  • 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 7:206–213

    Google Scholar 

  • 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 61:85–96

    CAS  PubMed  Google Scholar 

  • Wu Z, Zeng B, Li R, Song L (2011) Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation. Harmful Algae 15:53–58

    Google Scholar 

  • 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. 464

  • 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 20:293–300

    CAS  PubMed  Google Scholar 

  • 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:e32285

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yokoyama A, Park HD (2003) Depuration kinetics and persistence of the cyanobacterial toxin microcystin-LR in the freshwater bivalve Unio douglasiae. Environ Toxicol 18:61–67

    CAS  PubMed  Google Scholar 

  • Żak A, Musiewicz K, Kosakowska A (2012) Allelopathic activity of the Baltic cyanobacteria against microalgae. Estuar Coast Shelf Sci 112:4–10

    Google Scholar 

  • Zohary T, Padisák J, Naselli-Flores L (2010) Phytoplankton in the physical environment: beyond nutrients, at the end, there is some light. Hydrobiologia 639:261–269

    CAS  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. Kinneret Limnological Laboratory, Israel Oceanographic & Limnological Research, 14950, Migdal, Israel

    Assaf Sukenik

  2. Dpt. Biologia, Universidad Autónoma de Madrid, 28049, Madrid, Spain

    A. Quesada

  3. IASMA Research and Innovation Centre, Istituto Agrario di S. Michele all’Adige - Fondazione E. Mach, Via E. Mach 1, 38010, S. Michele all’Adige, Trento, Italy

    N. Salmaso

Authors
  1. Assaf Sukenik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Quesada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Salmaso
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Assaf Sukenik.

Additional information

Communicated by Anurag chaurasia.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sukenik, A., Quesada, A. & Salmaso, N. Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning. Biodivers Conserv 24, 889–908 (2015). https://doi.org/10.1007/s10531-015-0905-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-015-0905-9

Keywords

Search

Navigation