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

Biodiversity and Conservation

Volumn 24, Issue 4, 2015, Pages 889-908

  Sukenik, Assaf ^a   Quesada, A ^b   Salmaso, N ^c  

^a ISRAEL OCEANOGRAPHIC AND LIMNOLOGICAL RESEARCH   (Israel)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

Aquatic ecosystems; Chroococcales; Cyanobacteria; Cyanotoxins; Invasive species; Nostocales

Indexed keywords

EID: 84939976328     PISSN: 09603115     EISSN: 15729710     Source Type: Journal    
DOI: 10.1007/s10531-015-0905-9     Document Type: Review

References (168)

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 8:273–278
2. Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684
3. Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277
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 6:117–146
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 53:289–299
6. 7] microcystin-RR. Arch Hydrobiol 167:547–559
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 62:4086–4094
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 16:523–534
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 14:325–333
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 49:885–893
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 46:1394–1407
12. Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655
13. Carmichael WW (2001) Health effects of toxin-producing cyanobacteria: “The CyanoHABs”. Hum Ecol Risk Assess 7:1393–1407
14. Carton AG (2005) The impact of light intensity and algal-induced turbidity on first-feeding Seriola lalandi larvae. Aquac Res 36:1588–1594
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 261:1026–1038
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 42:763–773
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 44:1884–1892
18. Chislock MF, Sarnelle O, Olsen BK, Doster E, Wilson AE (2013) Large effects of consumer offense on ecosystem structure and function. Ecology 94:2375–2380
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 14:155–161
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 48:345–355
21. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. Spon Press, London
22. Christoffersen K, Lyck S, Winding A (2002) Microbial activity and bacterial community structure during degradation of microcystins. Aquat Microb Ecol 27:125–136
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 65:12–21
24. Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141
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 96:1–15
26. Cousins I, Bealing D, James H, Sutton A (1996) Biodegradation of microcystin-LR by indigenous mixed bacterial populations. Water Res 30:481–485
27. Dao TS, Do-Hong L-C, Wiegand C (2010) Chronic effects of cyanobacterial toxins on Daphnia magna and their offspring. Toxicon 55:1244–1254
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 4:12
29. De Bernardi R, Giussani G (1990) Are blue-green algae a suitable food for zooplankton? An overview. Hydrobiologia 200(201):29–41
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 15:1979–2003
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 60:1517–1526
32. De Senerpont Domis LN, Mooij WM, Huisman J (2007) Climate-induced shifts in an experimental phytoplankton community: a mechanistic approach. Hydrobiologia 584:403–413
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 46:2054–2060
34. Dziallas C, Grossart HP (2011) Temperature and biotic factors influence bacterial communities associated with the cyanobacterium Microcystis sp. Environ Microbiol 13:1632–1641
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 7:1669–1699
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 276:95–107
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 79:31–40
38. Ferrão-Filho AS, Kozlowsky-Suzuki B (2011) Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar Drugs 9:2729–2772
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 33:223–229
40. Figueredo CC, Giani A, Bird DF (2007) Does allelopathy contribute to Cylindrospermopsis raciborskii (cyanobacteria) bloom occurrence and geographic expansion? J Phycol 43:256–265
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 31:143–152
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 845–886
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 72:127–142
44. Ger KA, Hansson LA, Lürling M (2014) Understanding cyanobacteria–zooplankton interactions in a more eutrophic world. Freshw Biol 59:1783–1798
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 63:2308–2317
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 461–516
47. Goudie AS (2014) Desert dust and human health disorders. Environ Int 63:101–113
48. Gray SM, Bieber FME, Mandrak NE (2014) Experimental evidence for species-specific response to turbidity in imperilled fishes. Aquat Conserv 24:546–560
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 70:1–8
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 57:1214–1227
51. Hairston N et al (2001) Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55:2203–2214
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 733–747
53. Holst T, Jørgensen NO, Jørgensen C, Johansen A (2003) Degradation of microcystin in sediments at oxic and anoxic, denitrifying conditions. Water Res 37:4748–4760
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 54:1113
55. Humpage A (2008) Toxin types, toxicokinetics and toxicodynamics. Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York, pp 383–415
56. Hyenstrand P, Blomqvist P, Pettersson A (1998) Factors determining cyanobacterial success in aquatic systems: a literature review. Arch Hydrobiol Spec Issues Adv Limnol 51:41–62
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 675–732
58. Imanishi S, Kato H, Mizuno M, Tsuji K, K-i Harada (2005) Bacterial degradation of microcystins and nodularin. Chem Res Toxicol 18:591–598
59. Ishii H, Nishijima M, Abe T (2004) Characterization of degradation process of cyanobacterial hepatotoxins by a gram-negative aerobic bacterium. Water Res 38:2667–2676
60. Istvánovics V (2009) Eutrophication of lakes and reservoirs. In: Likens GE (ed) Encyclopedia of inland waters, vol 1. Elsevier, Oxford, pp 157–165
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 43:257–275
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 190:188–196
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:e41222
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 107:9252–9257
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, Gdynia
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 3:138
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 14:219–224
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 18:47–55
69. Kumagai M, Nakano S, Jiao C, Hayakawa K, Tsujimura S, Frenette JJ, Quesada A (2000) Effect of cyanobacterial blooms on thermal stratification. Limnology 1:191–195
70. Kurmayer R (2001) Competitive ability of Daphnia under dominance of non-toxic filamentous cyanobacteria. Hydrobiologia 442:279–289
71. Leão PN, Vasconcelos MTSD, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282
72. Leão PN, Engene N, Antunes A, Gerwick WH, Vasconcelos V (2012) The chemical ecology of cyanobacteria. Nat Prod Rep 29:372–391
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 5:168–182
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 69:358–365
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 29:505–513
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 23:481–486
77. Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13:1560–1572
78. Liu L, Rein KS (2010) New peptides isolated from Lyngbya species: a review. Mar Drugs 8:1817–1837
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 58:552–559
80. Malbrouck C, Kestemont P (2006) Effects of microcystins on fish. Environ Toxicol Chem 25:72
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 263–291
82. Manage PM, Edwards C, Singh BK, Lawton LA (2009) Isolation and identification of novel microcystin-degrading bacteria. Appl Environ Microbiol 75:6924–6928
83. Maršálek B, Bláha L (2004) Comparison of 17 biotests for detection of cyanobacterial toxicity. Environ Toxicol 19:310–317
84. Maruyama T et al (2006) Sphingosinicella microcystinivorans gen. nov., sp. nov., a microcystin-degrading bacterium. Int J Syst Evol Microbiol 56:85–89
85. Mazur-Marzec H, Plinski M (2009) Do toxic cyanobacteria blooms pose a threat to the Baltic ecosystem? Oceanologia 51:293–319
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 43:2801–2810
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 32:1009–1021
88. Méjean A, Paci G, Gautier V, Ploux O (2014) Biosynthesis of anatoxin-a and analogues (anatoxins) in cyanobacteria. Toxicon 91:15–22
89. Metcalf JS, Codd GA (2012) Cyanotoxins. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Dordrecht, pp 651–675
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 23:47–55
91. Mohamed ZA, Alamri SA (2012) Biodegradation of cylindrospermopsin toxin by microcystin-degrading bacteria isolated from cyanobacterial blooms. Toxicon 60:1390–1395
92. Monserrat J, Pinho G, Yunes J (2003) Toxicological effects of hepatotoxins (microcystins) on aquatic organisms. Comments Toxicol 9:89–101
93. Moreira C, Azevedo J, Antunes A, Vasconcelos V (2013) Cylindrospermopsin: occurrence, methods of detection and toxicology. J Appl Microbiol 114:605–620
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 75:14–49
95. Niu Y et al (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res 45:4169–4182
96. Nogueira IC, Saker ML, Pflugmacher S, Wiegand C, Vasconcelos VM (2004) Toxicity of the cyanobacterium Cylindrospermopsis raciborskii to Daphnia magna. Environ Toxicol 19:453–459
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 14:313–334
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 14:77–88
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 155–194
100. Osborne NJ, Webb PM, Moore MR, Shaw GR (2001) Environmental toxicology of the cyanobacterium Lyngbya spp. Toxicology 164:203
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 72:473–478
102. O’Sullivan P, Reynolds C (2005) The lakes handbook: Vol. 2: Lake restoration and rehabilitation. Blackwell Publishing, Malden
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 4:131–138
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 107:563–593
105. Paerl H, Fulton III R (2006) Ecology of harmful cyanobacteria. In: Ecology of harmful algae. Springer, Dordrecht, pp 95–109
106. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37
107. Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010
108. Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363
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 45:1973–1983
110. Pimentel D et al (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20
111. Ploug H et al (2010) Carbon and nitrogen fluxes associated with the cyanobacterium Aphanizomenon sp. in the Baltic Sea. ISME J 4:1215–1223
112. 2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59:1441–1461
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 20:1852–1860
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 10:67–70
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 41:39–45
116. Reynolds C (2006) The ecology of phytoplankton. Cambridge University Press, Cambridge
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 147–152
118. Ricciardi A, Cohen J (2007) The invasiveness of an introduced species does not predict its impact. Biol Invasions 9:309–315
119. Richards GR, Farrell AP (eds) (2009) Fish physiology: hypoxia. Elsevier, Amsterdam
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 59:99–114
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 6:1062–1079
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–S142
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 50:440–448
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 58:149–155
125. Sadler T, von Elert E (2014) Physiological interaction of Daphnia and Microcystis with regard to cyanobacterial secondary metabolites. Aquat Toxicol 156:96–105
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 229:271–276
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 VI
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 Raton
130. Sarnelle O, Wilson AE (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol Oceanogr 50:1565–1570
131. Scavia D et al (2014) Assessing and addressing the re-eutrophication of Lake Erie: central basin hypoxia. J Gt Lakes Res 40:226–246
132. Scheffer M, Rinaldi S, Gragnani A, Mur LR, van Nes EH (1997) On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78:272–282
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 1–14
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 148:9–15
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 25:1567–1573
136. 2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98:11789–11794
137. Smith MJ (2005) Biodegradation of the cyanotoxin cylindrospermopsin. The University of Queensland, Brisbane
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 23:413–421
139. Smith DJ, Griffin DW, Jaffe DA (2011) The high life: transport of microbes in the atmosphere. EOS Trans Am Geophys Union 92:249–250
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 159:2367–2377
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:e52243
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
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 466–467:152–163
144. Stevenson BS, Waterbury JB (2006) Isolation and identification of an epibiotic bacterium associated with heterocystous Anabaena cells. Biol Bull 210:73–77
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 613–637
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 47:1656–1663
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 3:86
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 27:36–55
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 171:285–295
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 167:533–546
151. Urrutia-Cordero P et al (2013) Effects of harmful cyanobacteria on the fershwater pathogenic free-living amoeba Acanthoamoeba castellanii. Aquat Toxicol 130:9–17
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 698:263–272
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–S107
154. 2 levels will intensify phytoplankton blooms in eutrophic and hypertrophic lakes. PLoS One 9:e104325
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 111:1909–1917
156. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499
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 152:473–484
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 51:1915–1924
159. Wolf HU, Frank C (2002) Toxicity assessment of cyanobacterial toxin mixtures. Environ Toxicol 17:395–399
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 7:206–213
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 61:85–96
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 15:53–58
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. 464
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 20:293–300
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:e32285
166. Yokoyama A, Park HD (2003) Depuration kinetics and persistence of the cyanobacterial toxin microcystin-LR in the freshwater bivalve Unio douglasiae. Environ Toxicol 18:61–67
167. Żak A, Musiewicz K, Kosakowska A (2012) Allelopathic activity of the Baltic cyanobacteria against microalgae. Estuar Coast Shelf Sci 112:4–10
168. Zohary T, Padisák J, Naselli-Flores L (2010) Phytoplankton in the physical environment: beyond nutrients, at the end, there is some light. Hydrobiologia 639:261–269