Log in

Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings

  • Review Article
  • Published:
Archives of Toxicology Aims and scope Submit manuscript

Abstract

Cyanobacteria are photoautotrophic organisms which occur in aquatic and terrestrial environments. They have the potential to produce toxins which pose a threat to human and animal health. This review covers the global distribution of the common cyanotoxins and related poisoning cases. A total of 468 selected articles on toxic cyanobacteria, dating from the earliest records until 2018, were reviewed. Most of the articles were published after 2000 (72%; 337 out of 468), which is consistent with the recent growth in interest in the analysis, toxinology and ecotoxicology of cyanotoxins. Animal and/or human poisoning cases were described in more than a third of the overall publications (38%; 177 out of 468). The reviewed publications showed that there were 1118 recorded identifications of major cyanotoxins in 869 freshwater ecosystems from 66 countries throughout the world. Microcystins were the most often recorded cyanotoxins worldwide (63%; 699 out of 1118), followed by cylindrospermopsin (10%; 107 out of 1118), anatoxins (9%; 100 out of 1118), and saxitoxins (8%; 93 out of 1118). Nodularins were the most rarely recorded cyanotoxins (2%; 19 out of 1118); however, there were also reports where cyanotoxins were not analysed or specified (9%; 100 out of 1118). The most commonly found toxic cyanobacterial genera were Microcystis spp. (669 reports), Anabaena spp. (397 reports), Aphanizomenon spp. (100 reports), Planktothrix spp. (98 reports), and Oscillatoria spp. (75 reports). Furthermore, there were 183 recorded cyanotoxin poisonings of humans and/or animals. Out of all toxic cyanobacterial blooms reviewed in this paper, the highest percentage of associated poisonings was found in North and Central America (39%; 69 cases out of 179), then Europe (20%; 35 out of 179), Australia including New Zealand (15%; 27 out of 179), and Africa (11%; 20 out of 179), while the lowest percentage was related to Asia (8%; 14 cases out of 179) and South America (8%; 14 cases out of 179). Events where only animals were known to have been affected were 63% (114 out of 182), whereas 32% (58 out of 182) of the investigated events involved only humans. A historical overview of human and animal poisoning episodes associated with cyanobacterial blooms is presented. Further, geographical data on the occurrence of cyanotoxins and related poisonings based on the available literature are shown. Some countries (mainly European) have done very intensive research on the occurrence of toxic cyanobacteria and cyanotoxins, and reported related ecotoxicological observations, while in some countries the lack of data is apparent. The true global extent of cyanotoxins and associated poisonings is likely to be greater than found in the available literature, and it can be assumed that ecotoxicological and hygienic problems caused by toxic cyanobacteria may occur in more environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

ATX-a:

Anatoxin-a

ATX-a(S):

Anatoxin-a(S)

BMAA:

β-N-Methylamino-l-alanine

CYN:

Cylindrospermopsin

HomoATXa:

Homoanatoxin-a

MC:

Microcystin

MC-LR:

Microcystin-LR

NOD:

Nodularin

NSTX:

Neosaxitoxin

PLC:

Primary liver cancer

STX:

Saxitoxin

LC–MS/MS:

Liquid chromatography with tandem mass spectrometric detection methods

LPS:

Lipopolysaccharides

WHO:

World Health Organization

N/A:

Toxic cyanobacterial metabolites not analysed

ND:

Not determined

N/S:

Not stated

UR:

Unknown reasons (group of cyanotoxins was not specified)

References

  • Affan A, Khomayis HS, Harbi SMA, Haque M, Khan S (2015) Effect of environmental factors on cyanobacterial abundance and cyanotoxins production in natural and drinking water, Bangladesh. Pak J Biol Sci 18:50–58. https://doi.org/10.3923/pjbs.2015.50.58

    Article  CAS  PubMed  Google Scholar 

  • Albay M (1996) The investigation of pollution levels from the point of view of biology of Lake Iznik. Doctorate Thesis, Istanbul University, Institute of Science, Istanbul. In Turkish

  • Albay M, Akcaalan R, Aykulu G, Tufekci H, Beattie KA, Codd GA (2003a) Occurrence of toxic cyanobacteria before and after copper sulphate treatment in a water reservoir, Istanbul, Turkey. Algol Stud 109(1):67–78. https://doi.org/10.1127/1864-1318/2003/0109-0067

    Article  Google Scholar 

  • Albay M, Akcaalan R, Tufekci H, Metcalf JS, Beattie KA, Codd GA (2003b) Depth profiles of cyanobacterial hepatotoxins (microcystins) in three Turkish freshwater lakes. Hydrobiologia 505(1–3):89–95

    Google Scholar 

  • Alonso-Andicoberry C, García-Villada L, Lopez-Rodas V, Costas E (2002) Catastrophic mortality of flamingos in a Spanish national park caused by cyanobacteria. Vet Rec 151:706–707

    CAS  PubMed  Google Scholar 

  • Annadotter H, Cronberg G, Lawton LA, Hanson H-B (1996) An outbreak of gastro-enteritis associated with consumption of cyanobacteria. In: Kaas H, Moestrup Ø, Henriksen P (eds) Abstracts of the First International Congress on Toxic Cyanobacteria

  • Annadotter H, Cronberg G, Lawton LA, Hansson HB, Göthe U, Skulberg OM (2001) An extensive outbreak of gastroenteritis associated with the toxic cyanobacterium Planktothrix agardhii (Oscillatoriales, Cyanophyceae) in Scania, South Sweden. In: Chorus I (ed) Cyanotoxins—occurence, causes, consequences. Springer, Berlin, pp 200–208

    Google Scholar 

  • Apesteguia C, Marta JM, García de Emiliani MO (1974) Aquatic bloom of blue-green algae in the waters of Lake Parque Belgrano (Floración acuática de algas verde-azules en las aguas del Lago del Parque Belgrano (Santa Fe)). Temas Salud 1:29–49

  • Aráoz R, Molgó J, Tandeau de Marsac N (2010) Neurotoxic cyanobacterial toxins. Toxicon 56:813–828

    PubMed  Google Scholar 

  • Arnold DE (1971) Ingestion, assimilation, survival and reproduction by Daphnia pulex fed seven species of blue-green algae. Limnol Oceanogr 16(6):906–920

    Google Scholar 

  • Azevedo SM, Carmichael WW, Jochimsen EM, Rinehart KL, Lau S, Shaw GR, Eaglesham GK (2002) Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology 181–182:441–446

    PubMed  Google Scholar 

  • Backer LC, Carmichael W, Kirkpatrick B, Williams C, Irvin M, Zhou Y, Johnson TB, Nierenberg K, Hill VR, Kieszak SM, Cheng Y-S (2008) Recreational exposure to low concentrations of microcystins during an algal bloom in a small lake. Mar Drugs 6(2):389–406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Backer LC, Landsberg JH, Miller M, Keel K, Taylor TK (2013) Canine cyanotoxin poisonings in the United States (1920s–2012): review of suspected and confirmed cases from three data sources. Toxins 5:1597–1628. https://doi.org/10.3390/toxins5091597

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballot A (2004) Cyanobacteria and cyanobacterial toxins in three alkaline Rift Valley lakes of Kenya-Lakes Bogoria, Nakuru and Elmenteita. J Plankton Res 26:925–935. https://doi.org/10.1093/plankt/fbh084

    Article  CAS  Google Scholar 

  • Ballot A, Krienitz L, Kotut K, Wiegand C, Pflugmacher S (2005) Cyanobacteria and cyanobacterial toxins in the alkaline crater lakes Sonachi and Simbi, Kenya. Harmful Algae 4:139–150. https://doi.org/10.1016/j.hal.2004.01.001

    Article  CAS  Google Scholar 

  • Behm D (2003) Coroner cites algae in teen’s death. Milwaukee, WI, Milwaukee Journal Sentinel. In: Falconer IR (ed 2004) Cyanobacterial toxins of drinking water supplies, cylindrospermopsins and microcystins. CRC Press, New York

  • Bellem F (2014) As cianobactérias na água e a morbilidade e mortalidade na região do Alentejo. Dissertation, Universidade de Évora

  • Bellem F, Nunes S, Morais M (2013) Cyanobacteria toxicity: potential public health impact in south Portugal populations. J Toxicol Environ Health Part A 76(4–5):263–271

    CAS  PubMed  Google Scholar 

  • Beltran EC, Neilan BA (2000) Geographical segregation of the neurotoxin-producing cyanobacterium Anabaena circinalis. Appl Environ Microbiol 66:4468–4474

    CAS  PubMed  PubMed Central  Google Scholar 

  • Belykh O, Sorokovikova E, Galina AF, Oksana VK, Evgeniya SK, Maria VS, Sherbakova TA (2011) Presence and genetic diversity of microcystin-producing cyanobacteria (Anabaena and Microcystis) in Lake Kotokel (Russia, Lake Baikal Region). Hydrobiologia 671(1):241–252

    CAS  Google Scholar 

  • Beversdorf LJ, Rude K, Weirich CA, Bartlett SL, Seaman M, Kozik C, Biese P, Gosz T, Suha M, Stempa C, Shaw C, Hedman C, Piatt JJ, Miller TR (2018) Analysis of cyanobacterial metabolites in surface and raw drinking waters reveals more than microcystin. Water Res 140:280–290. https://doi.org/10.1016/j.watres.2018.04.032

    Article  CAS  PubMed  Google Scholar 

  • Billings WH (1981) Water-associated human illness in northeast Pennsylvania and its suspected association with blue-green algae blooms. In: Carmichael WW (ed) The water environment—algal toxins and health. Environmental Science Research. Springer, Boston, MA, pp 243–255. https://doi.org/10.1007/978-1-4613-3267-1_18

    Google Scholar 

  • Bláha L, Maršálek B (2003) Contamination of drinking water in the Czech Republic by microcystins. Archiv für Hydrobiologie 158(3):421–429

    Google Scholar 

  • Bláha L, Babica P, Maršálek B (2009) Toxins produced in cyanobacterial water bloom–toxicity and risks. Interdiscip Toxicol 2(2):36–41. https://doi.org/10.2478/v10102-009-0006-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Bláhová L, Babica P, Marsalkova E, Maršálek B, Blaha L (2007) Concentrations and seasonal trends of extracellular microcystins in freshwaters of the Czech Republic—results of the National Monitoring Program. Clean 35(4):348–354

    Google Scholar 

  • Bláhová L, Babica P, Adamovský O, Kohoutek J, Maršálek B, Bláha L (2008) Analyses of cyanobacterial toxins (microcystins, cylindrospermopsin) in the reservoirs of the Czech Republic and evaluation of health risks. Environ Chem Lett 6:223–227

    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. Archiv fuer Hydrobiologie 167(1–2):547–559

    CAS  Google Scholar 

  • Bonilla S, Haakonsson S, Somma A, Gravier A, Britos A, Vidal L, De León L, Brena BM, Pírez M, Piccini C, Martínez de la Escalera G, Chalar G, González-Piana M, Martigani F, Aubriot L (2015) Cianobacterias y cianotoxinas en ecosistemas límnicos de Uruguay. INNOTEC 10 (9–22). ISSN 1688-3691-9

  • Borges H, Branco L, Martins M, Lima C, Barbosa P, Lira G, Bittencourt-Oliveira MC, Molica RJR (2015) Cyanotoxin production and phylogeny of benthic cyanobacterial strains isolated from the northeast of Brazil. Harmful Algae 43:46–57

    CAS  Google Scholar 

  • Botes DP, Wessels PL, Kruger H, Runnegar MTC, Santikarn S, Smith RJ, Barna JCJ, Williams DH (1985) Structural studies on cyanoginosins-LR, YR, YA, and YM, peptide toxins from Microcystis aeruginosa. J Chem Soc Perkin 1:2747–2748

    Google Scholar 

  • Botha N, Gehringer MM, Downing TG, van de Venter M, Shephard EG (2004) The role of microcystin-LR in the induction of apoptosis and oxidative stress in CaCO2 cells. Toxicon 43:85–92

    CAS  PubMed  Google Scholar 

  • Bourke ATC, Hawes RB, Neilson A, Stallman ND (1983) An outbreak of hepatoenteritis (the Palm Island Mystery Disease) possibly caused by algal intoxication. Toxicon 3:45–48

    Google Scholar 

  • Boyer GL (2008) Cyanobacterial toxins in New York and the lower great lakes ecosystems. Adv Exp Med Biol 619:153–165. https://doi.org/10.1007/978-0-387-75865-7-7

    Article  CAS  PubMed  Google Scholar 

  • Boyer GL, Watzin CM, Shambaugh DA, Satchwell FM, Rosen HB, Mihuc T (2004) The occurrence of cyanobacterial toxins in lake champlain. In: Manley TO, Manley PL, Mihuc TB (eds) Lake champlain: partnerships and research in the new millennium. Kluwer Academic/Plenum Publishers, New York, pp 241–257

    Google Scholar 

  • Brown L (1973) Report nearly completed on Dying Lake. The Lakeland Ledger

  • Bruno M, Gallo P, Messineo V, Melchiorre S (2012) Health risk associated with microcystin presence in the environment: the Case of an Italian Lake (Lake Vico, Central Italy). IJEP 2:34–41

    Google Scholar 

  • Buratti FM, Manganelli M, Vichi S, Stefanelli M, Scardala S, Testai E, Funari E (2017) Cyanotoxins: producing organisms, occurrence, toxicity, mechanism of action and human health toxicological risk evaluation. Arch Toxicol 91(3):1049–1130. https://doi.org/10.1007/s00204-016-1913-6

    Article  CAS  PubMed  Google Scholar 

  • Byth S (1980) Palm Island mystery disease. Med J Aust 2:40–42

    CAS  PubMed  Google Scholar 

  • Cadel-Six S, Peyraud-Thomas C, Brient L, de Marsac NT, Rippka R, Méjean A (2007) Different genotypes of anatoxin-producing cyanobacteria coexist in the Tarn River, France. Appl Environ Microbiol 73:7605–7614. https://doi.org/10.1128/AEM.01225-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calvan BC (1997) Is dog toxic lake’s first victim?—officials concerned over spreading microbes. The Seattle Times. Friday final edition. Seattle B1

  • Carbis C, Rawlin G (1997) A study of feral carp, Cyprinus carpio L., exposed to Microcystis aeruginosa at Lake Mokoan, Australia, and possible implications for fish health. J Fish Dis 20:81–91. https://doi.org/10.1046/j.1365-2761.1997.d01-111.x

    Article  Google Scholar 

  • Cardona T, Sanchez-Baracaldo P, Rutherford AW, Larkum AW (2018) Early Archaean origin of photosystem II. Geobiology 17:127–150

    PubMed  PubMed Central  Google Scholar 

  • Carey CC, Haney JF, Cottingham KL (2007) First report of microcystin-LR in the cyanobacterium Gloeotrichia echinulata. Environ Toxicol 22:337–339. https://doi.org/10.1002/tox.20245

    Article  CAS  PubMed  Google Scholar 

  • Carmichael WW (1992) Cyanobacteria secondary metabolites—the cyanotoxins. J Appl Bacteriol 72:445–459

    CAS  PubMed  Google Scholar 

  • Carmichael WW (1994) An overview of toxic cyanobacterial research in the United States. In: Proc. of toxic cyanobacteria–a global perspective. Adelaide, South Australia: Australian Centre for Water Quality Research

  • Carmichael WW (2001) Assessment of blue-green algal toxins in raw and finished drinking water. AWWA Research Foundation, Denver, p 179

    Google Scholar 

  • Carmichael WW (2008) A world overview—one-hundred- twenty-seven years of research on toxic cyanobacteria—where do we go from here? Adv Exp Med Biol 619:105–125. https://doi.org/10.1007/978-0-387-75865-7_4

    Article  PubMed  Google Scholar 

  • Carmichael WW, Boyer GL (2016) Health impacts from cyanobacteria harmful algae blooms: implications for the North American Great Lakes. Harmful Algae 54:194–212

    PubMed  Google Scholar 

  • Carmichael WW, Gorham P (1978) Anatoxins from clones of Anabaena flos-aquae isolated from lakes of Western Canada. Mitteilung Internationale Vereinigung fuer Limnologie 21:285–295

    CAS  Google Scholar 

  • Carmichael WW, Li R (2006) Cyanobacteria toxins in the Salton Sea. Saline Syst 2:5. https://doi.org/10.1186/1746-1448-2-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carmichael WW, Jones CLA, Mahmood NA, Theiss WC, Krogh P (1985) Algal toxins and water-based disease. CRC Crit Rev Env Control 15(3):275–313

    CAS  Google Scholar 

  • Carmichael WW, Mahmood NA, Hyde EG (1990) Nat Toxins from cyanobacteria (blue-green algae). In: Hall S, Strichartz G (eds) Marine toxins: origin, structure, and molecular pharmacology. American Chemical Society, pp 87–106

  • Carmichael WW, Azevedo SM, An JS, Molica RJ, Jochimsen EM, Lau S, Rinehart KL, Shaw GR, Eaglesham GK (2001) Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ Health Perspect 109(7):663–668

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carmichael WW, Yuan M, Friday CF (2004) Human mortality from accidental ingestion of toxic cyanobacteria—a case reexamined [abstract]. In: Sixth International Conference on Toxic Cyanobacteria. Bergen, pp 61–62

  • Cazenave J, Wunderlin DA, Bistoni M de los A, Ame MV, Krause E, Pflugmacher S, Wiegand C (2005) Uptake, tissue distribution and accumulation of microcystin-RR in Corydoraspaleatus, Jenynsiamultidentata and Odontesthesbonariensis. A field and laboratory study. Aquat Toxicol 75(2):178–190

  • Ceglowska M, Torunska-Sifarz A, Kowalewska G, Mazur-Marzec H (2018) Specific chemical and genetic markers revealed a thousands-year presence of toxic Nodularia spumigena in the Baltic Sea. Mar Drugs 16:116. https://doi.org/10.3390/md16040116

    Article  CAS  PubMed Central  Google Scholar 

  • Chatziefthimiou AD, Richer R, Rowles H, Powell JT, Metcalf JS (2014) Cyanotoxins as a potential cause of dog poisonings in desert environments. Vet Rec 174(19):484–485. https://doi.org/10.1136/vr.g3176

    Article  PubMed  Google Scholar 

  • Chellappa NT, Chellappa SL, Chellappa S (2008) Harmful phytoplankton blooms and fish mortality in a eutrophicated reservoir of northeast Brazil Brazilian. Arch Biol Technol 51(4):831–844

    Google Scholar 

  • Chen L, Chen J, Zhang X, **e P (2015) A review of reproductive toxicity of microcystins. J Hazard Mater 301:381–399

    PubMed  Google Scholar 

  • Chorus I (2001) Introduction: cyanotoxins—research for environmental safety and human health. In: Chorus I (ed) Cyanotoxins. Springer, Berlin, pp 1–4

    Google Scholar 

  • Chorus I (2012) Current approaches to cyanotoxin risk assessment, risk management and regulations in different countries. Umweltbundesamt, Berlin

  • Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide for their public health consequences, monitoring and management. Published on behalf of WHO by E&FN Spon, London

    Google Scholar 

  • Chorus I, Falconer IR, Salas HJ, Bartram J (2000) Health risks caused by freshwater cyanobacteria in recreational waters. J Toxicol Environ Health B Crit Rev 3(4):323–347

    CAS  PubMed  Google Scholar 

  • Christopher P, Davis P, Falconer I, Bowling L, Dyson J (1991) Blue-green algae hit Lake Cargelligo. NSW Public Health Bull 2:110–113

    Google Scholar 

  • Cirés S, Ballot A (2016) A review of the phylogeny, ecology and toxin production of bloom-forming Aphanizomenon spp. and related species within the Nostocales (cyanobacteria). Harmful Algae 54:21–43

    PubMed  Google Scholar 

  • Claro R, Noste J, D’Espósito R (2010) Poisoning blue-green algae (Microcystis spp.) In cattle Department Gral (Intoxicación por algas verde azuladas (Microcystis spp.) en bovinos del Departamento Gral). Ortiz de Ocampo, de la zona de los llanos riojanos, pp 4–7

  • Codd GA (1995) The toxicity of benthic blue-green algae in Scottish freshwaters. Foundation for Water Res, Marlow, p 1995

    Google Scholar 

  • Codd GA (1996) Harmful algae news. IOC of UNESCO 15(4), United Nations Educational, Scientific and Cultural Organization, Paris

  • Codd GA, Beattie KA (1991) Cyanobacteria (blue-green algae) and their toxins: awareness and action in the United Kingdom. PHLS Microbiol Dig 8:82–86

    Google Scholar 

  • Codd GA, Metcalf JS (2014) Toxic and non-toxic cyanobacteria: evolving concepts. Perspect Phycol 1(1):3–5

    Google Scholar 

  • Codd GA, Edwards C, Beattie KA, Barr WM, Gunn GJ (1992) Fatal attraction to cyanobacteria? Nature 359:110–111

    CAS  PubMed  Google Scholar 

  • Codd GA, Edwards C, Beattie KA, Lawton LA, Campbell DL, Bell SG (1995) Toxins from cyanobacteria (blue-green algae)—the Pringsheim lecture. In: Schnepf E, Starr RC (eds) Algae, environment and human affairs (wiessner W. Biopress, Bristol, pp 1–17

    Google Scholar 

  • Codd GA, Ward CJ, Bell SG (1997) Cyanobacterial toxins: occurrence, modes of action, health effects and exposure routes. Arch Toxicol Suppl 19:399–410

    CAS  PubMed  Google Scholar 

  • Codd GA, Bell S, Kaya K, Ward C, Beattie K, Metcalf J (1999) Cyanobacterial toxins, exposure routes and human health. Eur J Phycol 34(4):405–415

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Codd GA, Lindsay J, Young FM, Morrison LF, Metcalf JS (2005b) Harmful cyanobacteria. In: Huisman J, Matthijs HCP, Visser PM (eds) Harmful cyanobacteria, vol 3. Aquatic Ecology Series, pp 1–23. https://doi.org/10.1007/1-4020-3022-3_1

  • Codd GA, Plinski A, Surosz W, Huson J, Fallowfield HJ (2015a) Publication in 1672 of animal deaths at the Tuchomskie Lake, northern Poland and a likely role of cyanobacterial blooms. Toxicon 108:285–286

    CAS  PubMed  Google Scholar 

  • Codd GA, Morton H, Baker PD (2015b) George Francis: a pioneer in the investigation of the quality of South Australia’s drinking water sources (1878–1883). Trans R Soc S Aust 139:164–170

    Google Scholar 

  • Cohen SG, Reif CB (1953) Cutaneous sensitization to blue-green algae. J Allergy 24:452–457

    CAS  PubMed  Google Scholar 

  • Connor HE (1977) Algae freshwater blooms. In: Conner HE (ed) The poisonous plants in New Zealand. 2nd ed. DSIR Bulletin 99. Government Printer, Wellington, pp 209–212

  • 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 

  • Cox PA, Banack SA, Murch SJ (2003) Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci USA 100:13380–13383

    CAS  PubMed  Google Scholar 

  • Cox PA, Banack SA, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa of cyanobacteria produce beta-N-methylamino-l-alanine, a neurotoxic amino acid. PNAS 102(14):5074–5078

    CAS  PubMed  Google Scholar 

  • Cronberg G (1999) Qualitative and quantitative investigations of phytoplankton in Lake Ringsjon, Scania, Sweden. Hydrobiologia 404:27–40

    Google Scholar 

  • Dadisman Q (1987) Toxic algae linked to death of cows, dogs. The Milwaukee Sentinel, 7 March 1987

  • Dantas EW, Moura AN, Bittencourt-Oliveira MC (2011) Cyanobacterial blooms in stratified and destratified eutrophic reservoirs in semi-arid region of Brazil. Ann Acad Bras Cienc 83:1327–1338

    CAS  Google Scholar 

  • Delcourt N, Claudepierre T, Maignien T, Arnich N, Mattei C (2018) Cellular and molecular aspects of the β-N-methylamino-l-alanine (BMAA) mode of action within the neurodegenerative pathway: facts and controversy. Toxins 10(6):1–15. https://doi.org/10.3390/toxins10010006

    Article  CAS  Google Scholar 

  • Devlin JP, Edwards OE, Gorham PR, Hunter MR, Pike RK, Stavric B (1977) Anatoxin-a, a toxic alkaloid from Anabaena flos-aquae NCR-44h. Can J Chem 55:1367–1371

    CAS  Google Scholar 

  • Dillenberg HO, Dehnel MK (1960) Toxic waterbloom in Saskatchewan, 1959. Can Med Assoc J 83(22):1151–1154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Đorđević NB, Simić SB, Ćirić AR (2015) First identification of the cylindrospermopsin (cyn)-producing cyanobacterium Cylindrospermopsis raciborskii (Woloszyńska) Seenayya & Subba Raju in Serbia. Fresenius Environ Bull 24:3736–3742

    Google Scholar 

  • dos Vieira JMS, de P Azevedo MT, de Oliveira Azevedo SMF, Honda RY, Corrêa B (2003) Microcystin production by Radiocystis fernandoi (Chroococcales, Cyanobacteria) isolated from a drinking water reservoir in the city of Belém, PA, Brazilian Amazonia region. Toxicon 42:709–713

    CAS  Google Scholar 

  • Drobac D, Svirčev Z, Tokodi N, Vidović M, Baltić V, Božić-Krstić V, Lazić D, Pavlica T (2011) Microcystins—potential risk factors in carcinogenesis of primary liver cancer in Serbia. Geogr Pannon 15(3):70–80

    Google Scholar 

  • Drobac D, Tokodi N, Kiprovski B, Malenčić D, Važić T, Nybom S, Meriluoto J, Svirčev Z (2017) Microcystin accumulation and potential effects on antioxidant capacity of leaves and fruits of Capsicum annuum. J Toxicol Environ Heal A 80:145–154

    CAS  Google Scholar 

  • Edmondson WT (1991) The uses of ecology: Lake Washington and Beyond. The University of Washington Press, Seattle

    Google Scholar 

  • Edwards C, Beattie KA, Scrimgeour CM, Codd GA (1992) Identification of anatoxin-a in benthic cyanobacteria (blue-green-algae) and in associated dog poisonings at Loch Insh, Scotland. Toxicon 30:1165–1175

    CAS  PubMed  Google Scholar 

  • Ehrenhaus C, Vigna MS (2006) Changes in the phytoplankton of Lake Planetario after a restoration process. Darwiniana 44(2):319–328

    Google Scholar 

  • El Saadi O, Cameron AS (1993) Illness associated with blue-green algae. Med J Aust 158:792–793

    PubMed  Google Scholar 

  • Elder GH, Hunter PR, Codd GA (1993) Hazardous freshwater cyanobacteria (blue-green algae). Lancet 341(8859):1519–1520

    CAS  PubMed  Google Scholar 

  • Eriksson JE, Meriluoto J, Lindholm T (1986) Can cyanobacterial toxins accumulate in aquatic food chains? In: Proceedings of the 4th international symposium of microbiol ecology, Ljubljana (Yugoslavia). Ljubljana, Yugoslavia, pp 658–658

  • Eriksson JE, Meriluoto J, Lindholm T (1989) Accumulation of a peptide toxin from the cyanobacterium Oscillatoria agardhii in the freshwater mussel Anodonta cygnea. Hydrobiology 183:211–216

    CAS  Google Scholar 

  • Faassen EJ, Harkema L, Begeman L, Lurling M (2012) First report of (homo)anatoxin-a and dog neurotoxicosis after ingestion of benthic cyanobacteria in The Netherlands. Toxicon 60:378–384. https://doi.org/10.1016/j.toxicon.2012.04.335

    Article  CAS  PubMed  Google Scholar 

  • Falconer IR (1996) Potential impact on human health of toxic cyanobacteria. Phycologia 35:6–11

    Google Scholar 

  • Falconer IR (1998) Algal toxins and human health. In: Hrubec J (ed) Handbook of environmental hemistry. Springer, Berlin, 5 part C, pp 53–88

    Google Scholar 

  • Falconer IR, Beresford AM, Runnegar MTC (1983) Evidence of liver damage by toxin from a bloom of the blue-green alga, Microcystis aeruginosa. Med J Aust 1:511–514

    CAS  PubMed  Google Scholar 

  • Fastner J, Erhard M, Carmichael WW, Sun F, Rinehart KL, Rönicke H, Chorus I (1999) Characterization and diversity of microcystins in natural blooms and strains of the genera Microcystis and Planktothrix from German freshwaters. Arch Hydrobiol 145(2):147–163

    CAS  Google Scholar 

  • Fastner J, Beulker C, Geiser B, Hoffmann A, Kröger R, Teske K, Hoppe J, Mundhenk L, Neurath H, Sagebiel D, Chorus I (2018) Fatal neurotoxicosis in dogs associated with tychoplanktic, anatoxin-a producing Tychonema sp. in mesotrophic Lake Tegel, Berlin. Toxins 10:60. https://doi.org/10.3390/toxins10020060

    PubMed Central  Google Scholar 

  • Fawell JK, James HA (1994) Toxins from blue-green algae: Toxicological assessment of anatoxin-a and a method for its determination in reservoir water. FWR Report No. FR0434/DoE 3728, Foundation of Water Res, Marlow, UK

  • Fawell JK, James CP, James HA (1994) Toxins from blue-green algae: Toxicological assessment of microcystin-LR and a method for its determination in water. Water Res Centre, Medmenham, pp 1–46

    Google Scholar 

  • Ferrão-Filho AS (2009) Bioaccumulation of cyanotoxins and its effects on aquatic organisms (Bioacumulação de cianotoxinas e seus efeitos em organismos aquáticos). Oecol Aust 13:272–312

    Google Scholar 

  • Fiore MF, Genuário DB, da Silva CSP, Shishido TK, Moraes LAB, Cantúsio Neto R, Silva-Stenico ME (2009) Microcystin production by a freshwater spring cyanobacterium of the genus Fischerella. Toxicon 53(7–8):754–761. https://doi.org/10.1016/j.toxicon.2009.02.010

    Article  CAS  PubMed  Google Scholar 

  • Firkins GS (1953) Toxic algae poisoning. Iowa State Coll Vet 15:151–153

    CAS  Google Scholar 

  • Fitzgeorge RB, Clark SA, Keevil CW (1994) Routes of intoxication. In: Codd GA, Jefferies TM, Keevil CW, Potter E (eds) Detection methods for cyanobacterial toxins. RSC, Cambridge, pp 69–74

    Google Scholar 

  • Fitzgerald SD, Poppenga RH (1993) Toxicosis due to microcystin hepatotoxins in three Holstein heifers. J Vet Diagn Investig 5:651–653

    CAS  Google Scholar 

  • Fleming LE, Rivero C, Burns J, Williams C, Bean JA, Shea KA, Stinn J (2002) Blue-green algal (cyanobacterial) toxins, surface drinking water, and liver cancer in Florida. Harmful Algae 1(2):157–168

    CAS  Google Scholar 

  • Flores E, Wolk CP (1986) Production, by filamentous, nitrogen- fixing cyanobacteria, of a bacteriocin and of other antibiotics that kill related strains. Arch Microbiol 145:215–219

    CAS  PubMed  Google Scholar 

  • Fogg GE, Stewart WDP, Fay P, Walsby AE (1973) The blue-green algae. Academic Press, London

    Google Scholar 

  • Francis G (1878) Poisonous Australian Lake. Nature 18:11–12

    Google Scholar 

  • Frank CA (2002) Microcystin-producing cyanobacteria in recreational waters in southwestern Germany. Environ Toxicol 17(4):361–366

    CAS  PubMed  Google Scholar 

  • Frazier K, Colvin B, Styer E, Hullinger G, Garcia R (1998) Microcystin toxicosis in cattle due to overgrowth of blue-green algae. Vet Hum Toxicol 40(1):23–24

    CAS  PubMed  Google Scholar 

  • Fujiki H, Sugimura T, Moore RE (1983) New classes of environmental tumor promoters: indole alkaloids and polyacetates. Environ Health Perspect 50:85–90

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiki H, Suganuma M, Suguri H, Yoshizawa S, Takagi K, Nakayasu M, Ojika M, Yamada K, Yasumoto T, Moore RE, Sugimura T (1990) New tumor promoters from marine natural products. In: Hall S, Strichartz G (eds) Marine toxins, origin, structure and molecular pharmacology, , vol 418, no 18. American Chemical Society, Washington D.C., pp 232–240

    Google Scholar 

  • Funari E, Testai E (2008) Human health risk assessment related to cyanotoxins exposure. Crit Rev Toxicol 38(2):97–125. https://doi.org/10.1080/10408440701749454

    Article  CAS  PubMed  Google Scholar 

  • Furey A, Crowley J, Hamilton B, Lehane M, James KJ (2005) Strategies to avoid the misidentification of anatoxin-a using mass spectrometry in the forensic investigation of acute neurotoxic poisoning. J Chromatogr A 1082:91–97

    CAS  PubMed  Google Scholar 

  • Galat DL, Verdin JP, Sims LL (1990) Large-scale patterns of Nodularia spumigena blooms in Pyramid Lake, Nevada, determined from Landsat imagery: 19721986. Hydrobiologia 197:147–164. https://doi.org/10.1007/BF00026947

    Article  Google Scholar 

  • Gerrath JF (2003) 9 Chapter-Conjugating green algae and desmids. In: Wehr JD, Sheath RG, Kociolek JP (eds) Freshwater Algae of North America: ecology and classification, pp 353–381. https://doi.org/10.1016/B978-012741550-5/50010-6

    Google Scholar 

  • Giannuzzi L, Sedan D, Echenique R, Andrinolo D (2011) An acute case of intoxication with cyanobacteria and cyanotoxins in recreational water in Salto Grande Dam, Argentina. Mar Drugs 9:2164–2175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gilroy DJ, Kauffman KW, Hall RA, Huang X, Chu FS (2000) Assessing potential health risks from microcystin toxins in blue-green algae dietary supplements. Environ Health Perspect 108:435–439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg D (2004) Advisories posted at lake; Toxic algae prompts officials to close Lake Neatahwanta. Syracuse Post Standard, 5 June 2004

  • Graham JL, Jones JR, Jones SB, Downing JA, Clevenger TE (2004) Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. Water Res 38(20):4395–4404

    CAS  PubMed  Google Scholar 

  • Griffiths BM (1938) Early references to waterbloom in British lakes. Proc Linn Soc Lond Bot 151:12–19

    Google Scholar 

  • Griffiths DJ, Saker ML (2003) The Palm Island mystery disease 20 years on: a review of research on the cyanotoxin cylindrospermopsin. Environ Toxicol 18(2):78–93

    CAS  PubMed  Google Scholar 

  • Gross EM, Wolk CP, Jutter F (1991) Fischerellin, a new allelochemical from the freshwater cyanobacterium Fischerella muscicola. J Phycol 27:686–692

    CAS  Google Scholar 

  • Gugger M, Lenoir S, Berger C, Ledreux A, Druart J-C, Humbert J-F, Guettea C, Bernarda C (2005) First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis. Toxicon 45:919–928. https://doi.org/10.1016/j.toxicon.2005.02.031

    Article  CAS  PubMed  Google Scholar 

  • Gunn G, Rafferty A, Rafferty G, Cockburn N, Edwards C, Beatty K, Codd GA (1992) Fatal canine neurotoxicosis attributed to blue green algae (cyanobacteria). Vet Rec 130(14):301–302. https://doi.org/10.1136/vr.130.14.301

    Article  CAS  PubMed  Google Scholar 

  • Haddix PL, Hughley CJ, Lechevallier MW (2007) Occurrence of microcystins in 33 US water supplies. J (Am Water Works Assoc) 99(9):118–125

    CAS  Google Scholar 

  • Hamill KD (2001) Toxicity in benthic freshwater cyanobacteria (blue-green algae): first observations in New Zealand. New Zeal J Mar Freshw Res 35:1057–1059. https://doi.org/10.1080/00288330.2001.9517062

    Article  Google Scholar 

  • Handeland K, Østensvik Ø (2010) Microcystin poisoning in roe deer (Capreolus capreolus). Toxicon 56:1076–1078. https://doi.org/10.1016/j.toxicon.2010.06.023

    Article  CAS  PubMed  Google Scholar 

  • Harding WR (1997) New regional emergence of cyanobacterial toxicosis. Harmful Algae News 16:12–13

    Google Scholar 

  • Harding WR, Paxton BR (2001) Cyanobacteria in South Africa: A review. WRC Report No, TT 153/O1

  • Harding WR, Rowe N, Wessels JC, Beattie KA, Codd GA (1995) Death of a dog attributed to the cyanobacterial (blue–green algal) hepatotoxin nodularin in South Africa. J S Afr Vet Med Assoc 66:256–259

    CAS  Google Scholar 

  • Hawkins PR (1986) Some aspects of the limnology of a small tropical impoundment and an assessment of two techniques for managing water quality, with special reference to the growth of cyanobacteria. Dissertation, James Cook University

  • Hawkins PR, Griffiths DJ (1993) Artificial destratification of a small tropical reservoir: effects upon the phytoplankton. Hydrobiologia 254:169–181

    Google Scholar 

  • Hawkins PR, Runnegar MT, Jackson AR, Falconer IR (1985) Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir. Appl Environ Microbiol 50:1292–1295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heise HA (1949) Symptoms of hay fever caused by algae. J Allergy 20:383–385

    Google Scholar 

  • Henriksen P, Carmichael WW, An J, Moestrup O (1997) Detection of an anatoxin-a(s)-like anticholin-esterase in natural blooms and cultures of cyanobacteria/blue–green algae from Danish lakes and in the stomach contents of poisoned birds. Toxicon 35:901–913

    CAS  PubMed  Google Scholar 

  • Hoeger SJ, Dietrich DR (2004) Possible health risks arising from consumption of blue-green algae food supplements. Sixth International Conference on Toxic Cyanobacteria; 21–27 Jun. Bergen, Norway. Abstract book, pp 30

  • Holland A, Kinner S (2013) Interpreting the possible ecological role(s) of cyanotoxins: compounds for competitive advantage and/or physiological aide? Mar Drugs 11(7):2239–2258

    PubMed  PubMed Central  Google Scholar 

  • Holtcamp W (2012) The emerging science of BMAA: do cyanobacteria contribute to neurodegenerative disease? Environ Health Perspect 120(3):a110–a116. https://doi.org/10.1289/ehp.120-a110

    Article  PubMed  PubMed Central  Google Scholar 

  • Howard NJ, Berry AE (1933) Algal nuisances in surface waters. Can J Public Health 24:377–384

    CAS  Google Scholar 

  • Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JMH, Visser PM (2018) Cyanobacterial blooms. Nat Rev Microbiol 16:471–483

    CAS  PubMed  Google Scholar 

  • Humpage AR, Rositano J, Baker PD, Nicholson BC, Steffensen DA, Bretag AH, Brown RK (1993) Paralytic shellfish poisons from freshwater blue-green algae. Med J Aust (Lett) 159(6):423

    CAS  Google Scholar 

  • Humpage AR, Rositano J, Breitag AH, Brown R, Baker PD, Nicholson WC, Steffensen DA (1994) Paralytic shellfish poisons from Australian cyanobacterial blooms. Aust J Mar Freshw Res 45(5):761–777

    CAS  Google Scholar 

  • Ito E, Satake M, Yasumoto T (2002) Pathological effects of lyngbyatoxin A upon mice. Toxicon 40:551–556

    CAS  PubMed  Google Scholar 

  • Jackson ARB, Runnegar MTC, Cumming RB, Brunner JF (1986) Experimental acute intoxication of young layer and broiler-chickens with the cyanobacterium (blue-green-alga) Microcystis aeruginosa. Avian Pathol 15:741–748

    CAS  PubMed  Google Scholar 

  • Jacoby JM, Kann J (2007) The occurrence and response to toxic cyanobacteria in the Pacific Northwest, North America. Lake Reserv Manag 23:123–143. https://doi.org/10.1080/07438140709353916

    Article  Google Scholar 

  • Janssen EML (2019) Cyanobacterial peptides beyond microcystins—a review on co-occurrence, toxicity, and challenges for risk assessment. Water Res 151:488–499

    CAS  PubMed  Google Scholar 

  • Jewel MAS, Affan MA, Khan S (2003) Fish mortality due to cyanobacterial bloom in an aquaculture pond in Bangladesh. Pak J Biol Sci 6:1046–1050

    Google Scholar 

  • Jiang W, Tan S, Hanaki Y, Irie K, Uchida H, Watanabe R, Suzuki T, Sakamoto B, Kamio M, Nagai H (2014) Two new lyngbyatoxin derivatives from the cyanobacterium, Moorea producens. Mar Drugs 12(12):5788–5800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jochimsen EM, Carmichael WW, An J, Cardo DM, Cookson ST, Holmes CEM, Antunes MB, de Melo Filho DA, Lyra TM, Barreto VS, Azevedo SM, Jarvis WR (1998) Liver failure and death after exposure to microcystins at a haemodialysis center in Brazil. N Engl J Med 338(13):873–878

    CAS  PubMed  Google Scholar 

  • Johnston BR, Jacoby JM (2003) Cyanobacterial toxicity and migration in a mesotrophic lake in western Washington, USA. Hydrobiologia 495:79–91

    CAS  Google Scholar 

  • Juday RE, Keller EJ, Horpestad A, Bahls LL, Glasser S (1977) A toxic bloom of Anabaena flos-aquae in Hebgen Reservoir Montana in 1977. The Water Environment Part of the series, pp 103–112

  • Kann J, Falter CM (1985) Blue-green algae toxicity in black lake, Kootenai County, Idaho. Idaho Water Resources Research Institute, Moscow, p 55

    Google Scholar 

  • Kann J, Falter CM (1987) Development of toxic blue-green algal blooms in Black lake, Kootenai County, Idaho. Lake Reserv Manag 3(1):99–108. https://doi.org/10.1080/07438148709354765

    Article  Google Scholar 

  • Kim B, Kim H-S, Park H-D, Choi K, Park J-G (1999) Microcystin content of cyanobacterial cells in Korean reservoirs and their toxicity. Korean J Limnol 32(4):288–294

    Google Scholar 

  • Kirkby C (1672) A relation of an inland sea, near Zanzick yielding at a certain season a green substance which causeth certain death, together with an observation about white amber: communicated by Mr. Kirkby in a letter written to the publisher from Danzick Decemb. 19, 1671. Philos Trans R Soc 7:4069–4070

  • Koker L, Akcaalan R, Oguz A, Gaygusuz O, Gurevin C, Akat Kose C, Gucver S, Karaaslan Y, Erturk A, Albay M, Kinaci C (2017) Distribution of toxic cyanobacteria and cyanotoxins in Turkish waterbodies. J Environ Prot Ecol 18(2):425–432

    CAS  Google Scholar 

  • Kós P, Gorzó G, Surányi G, Borbély G (1995) Simple and efficient method for isolation and measurement of cyanobacterial hepatotoxins by plant tests (Sinapis alba L.). Anal Biochem 225:49–53

    PubMed  Google Scholar 

  • Habermehl GG, Krebs, HC, Nemes P, Nagy G, Scheiber P (1997) Occurrence of toxic producing cyanobacteria in Hungary Isolation, separation and identification of microcystins. Z Naturforsch 52b:107–109

    CAS  Google Scholar 

  • Krienitz L, Ballot A, Kotut K, Wiegand C, Pütz S, Metcalf JS, Codd GA, Pflugmacher S (2003) Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya. FEMS Microbiol Ecol 43(2):141–148. https://doi.org/10.1111/j.1574-6941.2003.tb01053.x

    Article  CAS  PubMed  Google Scholar 

  • Kurki-Helasmo K, Meriluoto J (1998) Microcystin uptake inhibits growth and protein phosphatase activity in mustard (Sinapis alba L.) seedlings. Toxicon 36:1921–1926

    CAS  PubMed  Google Scholar 

  • Lawrence JF, Niedzwiadek B, Menard C, Lau BP, Lewis D, Kuiper-Goodman T, Carbone S, Holmes C (2001) Comparison of liquid chromatography/mass spectrometry, ELISA, and phosphatase assay for the determination of microcystins in blue-green algae products. J AOAC Int 84(4):1035–1044

    CAS  PubMed  Google Scholar 

  • Lawton LA, Edwards C, Beattie KA, Pleasance S, Dear GJ, Codd GA (1995) Isolation and characterization of microcystins from laboratory cultures and environmental samples of Microcystis aeruginosa and from an associated animal toxicosis. Nat Toxins 3:50–57

    CAS  PubMed  Google Scholar 

  • Lei L, Peng L, Huang X, Han BP (2014) Occurrence and dominance of Cylindrospermopsis raciborskii and dissolved cylindrospermopsin in urban reservoirs used for drinking water supply, South China. Environ Monit Assess 186(5):3079–3090. https://doi.org/10.1007/s10661-013-3602-8

    Article  CAS  PubMed  Google Scholar 

  • Lévesque B, Gervais MC, Chevalier P, Gauvin D, Anassour-Laouan-Sidi E, Gingras S, Fortin N, Brisson G, Greer C, Bird D (2014) Prospective study of acute health effects in relation to exposure to cyanobacteria. Sci Total Environ 466–467:397–403

    PubMed  Google Scholar 

  • Li R, Carmichael WW, Brittain S, Eaglesham GK, Shaw GR, Watanabe MM (2001) First report of the cyanotoxins cylindrospermopsin and deoxycylindrospermopsin from Raphidiopsis curvata (cyanobacteria). J Phycol 37:1121–1126

    CAS  Google Scholar 

  • Li H, **e P, Li GY, Hao L, **ong Q (2009) In vivo study on the effects of microcystin extracts on the expression profiles of proto-oncogenes (c-fos, c-jun and c-myc) in liver, kidney and testis of male Wistar rats injected i.v. with toxins. Toxicon 53:169–175

    CAS  PubMed  Google Scholar 

  • Li Y, Chen JA, Zhao Q, Pu C, Qiu Z, Zhang R, Shu W (2011) A cross-sectional investigation of chronic exposure to microcystin in relationship to childhood liver damage in the Three Gorges Reservoir Region, China. Environ Health Perspect 119(10):1483–1488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lindholm T, Eriksson JE, Meriluoto JAO (1989) Toxic cyanobacteria and water quality problems-Examples from a eutrophic lake on South west Finland. Water Res 23:481–486. https://doi.org/10.1016/0043-1354(89)90139-5

    Article  CAS  Google Scholar 

  • Lobner D, Piana PMT, Salous AK, Peoples RW (2007) β-N-Methylamino-l-alanine enhances neurotoxicity through multiple mechanisms. Neurobiol Dis 25:360–366

    CAS  PubMed  Google Scholar 

  • Loftin KA, Clark JM, Journey CA, Kolpin DW, Van Metre PC, Carlisle D, Bradley PM (2016a) Spatial and temporal variation in microcystin occurrence in wadeable streams in the southeastern United States. Environ Toxicol Chem 35(9):2281–2287. https://doi.org/10.1002/etc.3391

    Article  CAS  PubMed  Google Scholar 

  • Loftin KA, Graham JL, Hilborn ED, Lehmann SC, Meyer MT, Dietze JE, Griffith CB (2016b) Cyanotoxins in inland lakes of the United States: occurrence and potential recreational health risks in the EPA National Lakes Assessment 2007. Harmful Algae 56:77–90

    CAS  PubMed  Google Scholar 

  • Lopez-Rodas V, Costas E (1999) Preference of mice to consume Microcystis aeruginosa (toxin-producing cyanobacteria): a possible explanation for numerous fatalities of livestock and wildlife. Res Vet Sci 67:107–110

    CAS  PubMed  Google Scholar 

  • Lopez-Rodas V, Maneiro E, Lanzarot MP, Perdigones N, Costas E (2008) Mass wildlife mortality due to cyanobacteria in the Doñana National Park, Spain. Vet Rec 162:317–318. https://doi.org/10.1136/vr.162.10.317

    Article  CAS  PubMed  Google Scholar 

  • Lorenzi AS, Cordeiro-Araújo MK, Chia MA, Bittencourt-Oliveira MC (2018) Cyanotoxin contamination of semiarid drinking water supply reservoirs. Environ Earth Sci 77:595. https://doi.org/10.1007/s12665-018-7774-y

    Article  CAS  Google Scholar 

  • Lugomela C, Pratap HB, Mgaya YD (2006) Cyanobacteria blooms—a possible cause of mass mortality of Lesser Flamingos in Lake Manyara and Lake Big Momela, Tanzania. Harmful Algae 5:534–541. https://doi.org/10.1016/j.hal.2005.10.001

    Article  Google Scholar 

  • Lürling M, Faassen EJ (2013) Dog poisonings associated with a Microcystis aeruginosa bloom in the Netherlands. Toxins (Basel) 5(3):556–567

    Google Scholar 

  • Mackenthun KM, Herman EF, Bartsch AF (1948) A heavy mortality of fishes resulting from the decomposition of algae in the Yahara River, Wisconsin. Trans Am Fish Soc 75:175–180

    Google Scholar 

  • Mackintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA (1990) Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases1 and 2Afrom both mammals and higher plants. FEBS Lett 264:187–192

    CAS  PubMed  Google Scholar 

  • Mahakhant A, Sano T, Ratanachot P, Tong-a-ram T, Srivastava VC, Watanabe MM, Kaya K (1998) Detection of microcystins from cyanobacterial water blooms in Thailand fresh water. Psychol Res 42(s2):25–29. https://doi.org/10.1046/j.1440-1835.1998.00119.x

    Article  Google Scholar 

  • Mahmood WA, Carmichael WW (1987) Anatoxin-a(s), an anticholinesterase from the cyanobacterium Anabaena flos-aquae NRC- 525-17. Toxicon 25:1211–1227

    Google Scholar 

  • Mahmood NA, Carmichael WW, Pfahler D (1988) Anticholinesterase poisonings in dogs from a cyanobacterial (blue-green algae) bloom dominated by Anabaena flos-aquae. Am J Vet Res 49:500–503

    CAS  PubMed  Google Scholar 

  • Main DC, Berry PH, Peet RL, Robertson JP (1977) Sheep mortalities associated with the blue green alga Nodularia spumigena. Aust Vet J 53:578–581

    CAS  PubMed  Google Scholar 

  • Major Y, Kifle D, Spoof L, Meriluoto J (2018) Cyanobacteria and microcystins in Koka reservoir (Ethiopia). Environ Sci Pollut Res Int 25(27):26861–26873. https://doi.org/10.1007/s11356-018-2727-2

    Article  CAS  PubMed  Google Scholar 

  • Makower AK, Schuurmans JM, Groth D, Zilliges Y, Matthijs HCP, Dittmann E (2015) Transcriptomics-aided dissection of the intracellular and extracellular roles of microcystin in Microcystis aeruginosa PCC 7801. Appl Env Microbiol 81:544–554

    Google Scholar 

  • Mancera JEP, Vidal LAV (1994) Florecimiento de microalgas relacionado con mortandad de peces en el complejo lagunar cienega grande de Santa Marta, Caribe Colombiano. Anales del Instituto de Investigaciones Marinas de Punta de Betín 23(1):103–117

    Google Scholar 

  • Mancini M, Rodriguez C, Bagnis G, Liendo A, Prosperi C, Bonansea M, Tundisi JG (2010) Cyanobacterial bloom and animal mass mortality in a reservoir from Central Argentina. Braz J Biol 70(3):841–845

    CAS  PubMed  Google Scholar 

  • Marks J (1997) Water in California’s Carmel River is deemed unsafe to drink. Monterey County Herald

  • M-Hamvas M, Máthé C, Molnár E, Vasas G, Grigorszky I, Borbely G (2003) Microcystin-LR alters the growth, anthocyanin content and single-stranded DNase enzyme activities in Sinapis alba L. seedlings. Aquat Toxicol 62:1–9

    CAS  PubMed  Google Scholar 

  • Masango MG, Myburgh JG, Labuschagne L, Govender D, Bengis RG, Naicker D (2010) Assessment of Microcystis bloom toxicity associated with wildlife mortality in the Kruger National Park, South Africa. J Wildl Dis 46(1):95–102

    PubMed  Google Scholar 

  • Matsunaga S, Moore RE, Niemczura WP, Carmichael WW (1989) Anatoxin-a(s), a potent anticholinesterase from Anabaena flos-aquae. J Am Chem Soc 111:8021–8023

    CAS  Google Scholar 

  • Matsunaga H, Harada KI, Senma M, Ito Y, Yasuda N, Ushida S, Kimura Y (1999) Possible cause of unnatural mass death of wild birds in a pond in Nishinomiya, Japan: sudden appearance of toxic cyanobacteria. Nat Toxins 7(2):81–84

    CAS  PubMed  Google Scholar 

  • May V, McBarron EJ (1973) Occurrence of the blue-green alga, Anabaena circinalis Rabenh., in New South Wales and toxicity to mice and honey bees. Aust J Agric Res 39:264–266

    Google Scholar 

  • McAllister T (1991) Hunters share sad story of dogs poisoned by algae to alert others to danger. The Oregonian, 23 October 1991

  • McElhiney J, Lawton LA, Leifert C (2001) Investigations into the inhibitory effects of microcystins on plant growth, and the toxicity of plant tissues following exposure. Toxicon 39:1411–1420

    CAS  PubMed  Google Scholar 

  • McGregor GB, Fabbro LD (2000) Dominance of Cylindrospermopsis raciborskii (Nostocales, Cyanoprokaryota) in Queensland tropical and subtropical reservoirs: implications for monitoring and management. Lakes Reserv Res Manag 5:195–205

    Google Scholar 

  • McLeod JA, Bondar GF (1952) A case of suspected algal poisoning in Manitoba. Can J Public Health 43:347–350

    CAS  PubMed  Google Scholar 

  • Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013a) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327. https://doi.org/10.1016/j.envint.2013.06.013

    Article  CAS  PubMed  Google Scholar 

  • Merel S, Villarín MC, Chung K, Snyder S (2013b) Spatial and thematic distribution of research on cyanotoxins. Toxicon 76:118–131. https://doi.org/10.1016/j.toxicon.2013.09.008

    Article  CAS  PubMed  Google Scholar 

  • Meriluoto J, Codd GA (2005) TOXIC: cyanobacterial monitoring and cyanotoxin analysis. Åbo Akademi University Press, Åbo, p 149

    Google Scholar 

  • Meriluoto J, Spoof L, Codd GA (2017) Handbook of cyanobacterial monitoring and cyanotoxin analysis. Wiley, Chichester, p 548

    Google Scholar 

  • Metcalf JS, Codd GA (2004) Cyanobacterial toxins (cyanotoxins) in water. Foundation for Water Res Allen House, The Listons, Liston Road, Marlow, Bucks SL 7 1FD, UK

  • 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 

  • Metcalf JS, Richer R, Cox PA, Codd GA (2012) Cyanotoxins in desert environments may present a risk to human health. Sci Total Environ 421–422:118–123

    PubMed  Google Scholar 

  • Metcalf JS, Banack SA, Richer R, Cox PA (2015) Neurotoxic amino-acids and their isomers in desert environments. J Arid Environ 112:140–144

    Google Scholar 

  • Mez K, Hanselmann K, Naegeli H, Preisig HR (1996) Protein phosphatase-inhibiting activity in cyanobacteria from alpine lakes in Switzerland. Phycologia 35:133–139

    Google Scholar 

  • Mez K, Beattie K, Codd G, Hanselmann K, Hauser B, Naegeli H, Preisig H (1997) Identification of a microcystin in benthic cyanobacteria linked to cattle deaths on alpine pastures in Switzerland. Eur J Phycol 32:111–117

    Google Scholar 

  • Miller AP, Tisdale ES (1931) Epidemic of intestinal disorders in Charleston, West Virginia occurring simultaneously with unprecedented water supply conditions. Am J Public Health Res 21:198–200

    CAS  Google Scholar 

  • Milutinović A, Zorc-Pleskovič R, Petrovič D, Zorc M, Šuput D (2006) Microcystin-LR induces alterations in heart muscle. Folia Biol (Praha) 52:116–118

    Google Scholar 

  • Minasyan A, Christophoridis C, Wilson AE, Zervou S-K, Kaloudis T, Hiskia A (2018) Diversity of cyanobacteria and the presence of cyanotoxins in the epilimnion of Lake Yerevan (Armenia). Toxicon 150:28–38. https://doi.org/10.1016/j.toxicon.2018.04.021

    Article  CAS  PubMed  Google Scholar 

  • Mons MN, Van Egmond HP, Speijers GJA (1998) Paralytic shellfish poisoning: A review. RIVM Report 388802 005

  • Monteiro S, Santos R, Blaha L, Codd GA (2017) Lipopolysaccharide endotoxins. In: Meriluoto J, Spoof L, Codd GA (eds) Handbook of cyanobacterioal monitoring and cyanotoxin analysis. Wiley, Chichester UK, pp 164–172

    Google Scholar 

  • Moore RE (1984) Public health and toxins from marine blue-green algae. In: Ragelis EP (ed) Seafood toxins. ACS Symposium Series No. 262, American Chemical Society: Washington. pp 369–376

    Google Scholar 

  • Moore RE (1996) Cyclic peptides and depsipeptides from cyanobacteria: a review. J Ind Microbiol 16:134–143

    CAS  PubMed  Google Scholar 

  • Moore RE, Blackman AJ, Cheuk CE, Mynderse JS, Matsumoto GK, Clardy J, Woodard RW, Craig JC (1984) Absolute stereochemistries of the aplysiatoxins and oscillatoxin A. J Org Chem 49(13):2484–2489

    CAS  Google Scholar 

  • Moustaka-Gouni M, Hiskia A, Genitsaris S, Katsiapi M, Manolidi K, Zervou S-K, Christophoridis C, Triantis TM, Kaloudis T, Orfanidis S (2017) First report of Aphanizomenon favaloroi occurrence in Europe associated with saxitoxins and a massive fish kill in Lake Vistonis, Greece. Mar Freshwater Res 68(4):793–800

    CAS  Google Scholar 

  • Namikoshi M, Murakami T, Watanabe MF, Oda T, Yamada J, Tsujimura S, Nagai H, Oishi S (2003) Simultaneous production of homoanatoxin-a, anatoxin-a, and a new non-toxic 4-hydroxyhomoanatoxin-a by the cyanobacterium Raphidiopsis mediterranea Skuja. Toxicon 42(5):533–538

    CAS  PubMed  Google Scholar 

  • Nasri H, El Herry S, Bouaïcha N (2008) First reported case of turtle deaths during a toxic Microcystis spp. bloom in Lake Oubeira, Algeria. Ecotoxicol Environ Saf 71(2):535–544. https://doi.org/10.1016/j.ecoenv.2007.12.009

    Article  CAS  PubMed  Google Scholar 

  • National Rivers Authority (1990) Toxic blue-green algae. Water Quality Series No 2. National River Authority, London

  • Negri AP, Jones GJ, Hindmarsh M (1995) Sheep mortality associated with paralytic shellfish poisons from the cyanobacterium Anabaena circinalis. Toxicon 33(10):1321–1329

    CAS  PubMed  Google Scholar 

  • Novak B, Sensenbrenner L (2004) Toxin scare hits area lakes; Kegonsa Lake closed after dog suffers convulsions. The Capital Times, 9 June 2004

  • NSW Blue-Green Algae Task Force (1992) Final report of the NSW Blue-Green Algae Task Force. NSW Department of Water Resources, Parramatta

  • Oberholster PJ, Myburgh JG, Govender D, Bengis R, Botha A-M (2009) Identification of toxigenic Microcystis strains after incidents of wild animal mortalities in the Kruger National Park, South Africa. Ecotoxicol Environ Saf 72:1177–1182

    CAS  PubMed  Google Scholar 

  • Ohtani I, Moore RE, Runnegar MTC (1992) Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. J Am Chem Soc 114:7941–7942

    CAS  Google Scholar 

  • Oliva MG, Lugo A, Alcocer-Durand J, Peralata L, Oseguera LA (2009) Planktonic bloom-forming Nodularia in the saline Lake Alchichica, Mexico. Nat Res Environ Issues 15(1):22

    Google Scholar 

  • Onodera H, Oshima Y, Henriksen P, Yasumoto T (1997) Confirmation of anatoxin–a(s), in the cyanobacterium Anabaena lemmermannii, as the cause of bird kills in Danish lakes. Toxicon 35:1645–1648

    CAS  PubMed  Google Scholar 

  • Papadimitriou T, Katsiapi M, Vlachopoulos K, Christopoulos A, Laspidou C, Moustaka-Gouni M, Kormas K (2018) Cyanotoxins as the “common suspects” for the Dalmatian pelican (Pelecanus crispus) deaths in a Mediterranean reconstructed reservoir. Environ Pollut 234:779–787. https://doi.org/10.1016/j.envpol.2017.12.022

    Article  CAS  PubMed  Google Scholar 

  • Park H, Namikoshi M, Brittain SM, Carmichael WW, Murphy T (2001) [d-Leu1] microcystin-LR, a new microcystin isolated from waterbloom in a Canadian prairie lake. Toxicon 39:855–862. https://doi.org/10.1016/S0041-0101(00)00224-5

    Article  CAS  PubMed  Google Scholar 

  • Patterson GML, Bolis CM (1997) Fungal cell-wall polysaccharides elicit an antifungal secondary metabolite (Phytoalexin) in the cyanobacterium Syntonema acellatum. J Phycol 33:54–60

    CAS  Google Scholar 

  • Pearson L, Mihali T, Moffitt M, Kellmann R, Neilan B (2010) On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Mar Drugs 8:1650–1680

    CAS  PubMed  PubMed Central  Google Scholar 

  • Persson P, Sivonen K, Keto K, Kononen K, Niemi M, Viljamaa H (1984) Potentially toxic blue-green algae (cyanobacteria) in Finnish natural waters. Aqua Fenn 14:147–154

    Google Scholar 

  • Pilotto LS, Douglas RM, Burch MD, Cameron S, Beers M, Rouch GR, Robinson P, Kirk M, Cowie CT, Hardiman S, Moore C, Attewell RG (1997) Health effects of recreational exposure to cyanobacteria (blue-green algae) during recreational water-related activities. Aust N Z J Public Health 21(6):562–566

    CAS  PubMed  Google Scholar 

  • Pizzolon L, Tracanna B, Prósperi C, Guerrero JM (1999) Cyanobacterial blooms in Argentinean inland waters. Lakes Reserve Res Manag 4:101–105

    Google Scholar 

  • Pouria S, Andrade A, Barbosa J, Cavalcanti RL, Barreto VT, Ward CJ, Preiser W, Poon GK, Neild GH, Codd GA (1998) Fatal microcystin intoxication in hemodialysis unit in Caruaru, Brazil. Lancet 352(9121):21–26

    CAS  PubMed  Google Scholar 

  • Preece EP, Moore BC, Hardy FJ (2015) Transfer of microcystin from freshwater lakes to Puget Sound, WA and toxin accumulation in marine mussels (Mytilus trossulus). Ecotoxicol Environ Saf 122:98–105. https://doi.org/10.1016/j.ecoenv.2015.07.013

    Article  CAS  PubMed  Google Scholar 

  • Probert CS, Robinson RJ, Jayanthi V, Mayberry JF (1995) Microcystin hepatitis. Arq Gastroenterol 32:199

    CAS  PubMed  Google Scholar 

  • Puschner B, Hoff B, Tor E (2008) Diagnosis of anatoxin-a poisoning in dogs from North America. J Vet Diagn Investig 20:89–92

    Google Scholar 

  • Pybus MJ, Hobson DP, Onderka DK (1986) Mass mortality of bats due to probable blue–green algal toxicity. J Wildl Dis 22:449–450

    CAS  PubMed  Google Scholar 

  • Rankin KA, Alroy KA, Kudela RM, Oates SC, Murray MJ, Miller MA (2013) Treatment of cyanobacterial (microcystin) toxicosis using oral cholestyramine: case report of a dog from Montana. Toxins (Basel) 5(6):1051–1063

    Google Scholar 

  • Rantala A, Fewer DP, Hisbergues M, Rouhiainen L, Vaitomaa J, Borner T, Sivonen K (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc Natl Acad Sci 101:568–573

    CAS  PubMed  Google Scholar 

  • Rapala J, Robertson A, Negri AP, Berg KA, Tuomi P, Lyra C, Erkomaa K, Lahti K, Hoppu K, Lepistö L (2005) First report of saxitoxin in Finnish Lakes and possible associated effects on human health. Environ Tox 20(3):331–340

    CAS  Google Scholar 

  • Rastogi RP, Madamwar D, Incharoensakdi A (2015) Bloom dynamics of cyanobacteria and their toxins: environmental health impacts and mitigation strategies. Front Microbiol 6:1254. https://doi.org/10.3389/fmicb.2015.01254

    Article  PubMed  PubMed Central  Google Scholar 

  • Ressom R, Soong FS, Fitzgerald J, Turczynowicz L, El Saadi O, Roder D, Maynard T, Falconer I (1994) Health effects of toxic cyanobacteria (blue-green algae). Australian National Health and Medical Research Council, Looking Glass Press, Canberra, pp 1–108

    Google Scholar 

  • Reuter JE, Rhodes CL, Lebo ME, Kotzman M, Goldman CR (1993) The importance of nitrogen in Pyramid Lake (Nevada, USA), a saline, desert lake. Hydrobiologia 267:179–189. https://doi.org/10.1007/BF00018800

    Article  CAS  Google Scholar 

  • Rinehart KL, Harada K-I, Namikoshi M, Chen C, Harvis CA, Munro MHG, Blunt JW, Mulligan PE, Beasley VR, Dahlem AM, Carmichael WW (1988) Nodularin, microcystin, and the configuration of Adda. J Am Chem Soc 110(25):8557–8558

    CAS  Google Scholar 

  • Ringuelet RA, Olivier SR, Guarrera SA, Aramburu RH (1955) Comments on plankton and fish kills in Laguna del Monte [Buenos Aires, Argentina Republic] (Observaciones sobre an to plancton y mortandad de peces en Laguna del Monte [Buenos Aires, República Argentina]). Notas del Mus. La Plata, Sección Zool

    Google Scholar 

  • Rodger HD, Turnbull T, Edwards C, Codd GA (1994) Cyanobacterial (blue-green algal) bloom associated pathology in brown trout Salmo trutta L. in Loch Leven, Scotland. J Fish Dis 17:177–181

    Google Scholar 

  • Rose ET (1953) Toxic algae in Iowa lakes. Proc Iowa Acad Sci 60:738–745

    Google Scholar 

  • Rose J (2003) Environmental toxicology. CRC Press, pp 414. ISBN 9789056991401

  • Rücker J, Stüken A, Nixdorf B, Fastner J, Chorus I, Wiedner C (2007) Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. Toxicon 50(6):800–809

    PubMed  Google Scholar 

  • Saker ML, Thomas AD, Norton JH (1999) Cattle mortality attributed to the toxic cyanobacterium Cylindrospermopsis raciborskii in an outback region of North Queensland. Environ Tox 14:179–182

    CAS  Google Scholar 

  • Sanchez JA, Otero P, Alfonso A, Ramos V, Vasconcelos V, Aráoz R, Molgó J, Vieytes MR, Botana LM (2014) Detection of anatoxin-a and three analogs in Anabaena spp. cultures: new fluorescence polarization assay and toxin profile by LC-MS/MS. Toxins 6(2):402–415

    PubMed  PubMed Central  Google Scholar 

  • Schembri MA, Neilan BA, Saint CP (2001) Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ Tox 16:413–421

    CAS  Google Scholar 

  • Schwimmer D, Schwimmer M (1968) Medical aspects of phycology. In: Jackson D (ed) Algae, man, and the environment. In: Proceedings of an international symposium. [held At] Syracuse University June 18–30, 1968, Syracuse University Press, Syracuse, pp 279–358

  • Scott WE (1989) Occurrence and significance of toxic cyanobacteria in South Africa. Water Sci Technol 23:175–180

    Google Scholar 

  • Scott WE, Barlow DJ, Hauman JH (1981) Studies on the ecology, growth and physiology of toxic Microcystis aeruginosa in South Africa. Algal toxins and health. In: Carmichael WW (ed) The water environment. Plenum Press, New York, pp 49–69

    Google Scholar 

  • Sebbag L, Smee N, Van der Merwe D, Schmid D (2013) Liver failure in a dog following suspected ingestion of blue-green algae (Microcystis spp.): a case report and review of the toxin. J Am Anim Hosp Assoc 49:1–5

    Google Scholar 

  • Seifert M, McGregor G, Eaglesham G, Wickramasinghe W, Shaw G (2007) First evidence for the production of cylindrospermopsin and deoxy-cylindrospermopsin by the freshwater benthic cyanobacterium, Lyngbya wollei (Farlow ex Gomont) Speziale and Dyck. Harmful Algae 6:73–80. https://doi.org/10.1016/j.hal.2006.07.001

    Article  CAS  Google Scholar 

  • Shams S, Capelli C, Cerasino L, Ballot A (2015) Anatoxin-a producing Tychonema (cyanobacteria) in European waterbodies. Water Res 69:68–79. https://doi.org/10.1016/j.watres.2014.11.006

    Article  CAS  PubMed  Google Scholar 

  • Shaw GR, McKenzie RA, Wickramasinghe WA, Seawright AA, Eaglesham G, Moore MR (2002) Comparative toxicity of the cyanobacterial toxin cylindrospermopsin between mice and cattle: human implications. Xth Intern. Conf. on Harmful Algae. St. Pete Beach, Florida, USA

  • Shaw GR, McKenzie RA, Wickramasinghe WA, Seawright AA, Eaglesham GK, Moore MR (2004) Comparative toxicity of the cyanobacterial toxin cylindrospermopsin between mice and cattle: human implications. Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, pp 465–467

  • Sivonen K, Jones G (1999) Cyanobacterial toxins. In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: a guide to public health significance, monitoring and management. E&FN Spon, London, pp 41–111

    Google Scholar 

  • Sivonen K, Kononen K, Carmichael WW, Dahlem AM, Rinehart KL, Kiviranta J, Niemela SI (1989) Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and structure of the toxin. Appl Environ Microbiol 55(8):1990–1995

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sivonen K, Namikoshi M, Evans WR, Carmichael WW, Sun F, Rouhiainen L, Luukkainen R, Rinehart KL (1992) Isolation and characterization of a variety of microcystins from seven strains of the cyanobacterial genus Anabaena. Appl Environ Microbiol 58(8):2495–2500

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skulberg OM (1979) Toxic effects of blue green algae-first case of Microcystis poisoning reported from Norway (Giftvirkninger av blågrønnalger-første tilfelle av Microcystis forgiftning registrert i Norge). Tema-rapport 4, Norsk Institutt for Vannforskning, Oslo, 42

  • Skulberg OM, Skulberg R, Carmichael WW, Andersen RA, Matsunuga S, Moore RE (1992) Investigations of a neurotoxic oscillatorian strain (Cyanophyceae) and its toxin. Investigations of a neurotoxic oscillatorian strain (Cyanophyceae) and its toxin. Environ Tox Chem 11(3):321–329

    CAS  Google Scholar 

  • Smayda TJ (1974) Some experiments on the sinking characteristics of two freshwater diatoms. Limnol Oceanogr 19:628–635

    Google Scholar 

  • Soll MD, Williams MC (1985) Mortality of a white rhinoceros (Ceratotherium simum) suspected to be associated with the blue-green alga Microcystis aeruginosa. J S Afr Vet Assoc 56:49–51

    CAS  PubMed  Google Scholar 

  • Soltero RA, Nichols DG (1981) The recent blue-green algal blooms of Long Lake, Washington. In: Carmichael WW (ed) The water environment: algal toxins and health. Plenum Press, New York, pp 143–159

    Google Scholar 

  • Sonzogni WC, Repavich WM, Standridge JH, Wedepohl RE, Vennie JG (1988) A note on algal toxins in Wisconsin waters experiencing blue-green algal blooms. Lake Reserv Manag 4(2):281–285

    Google Scholar 

  • Spoof L, Catherine A (2017) Appendices 3. Tables of microcystins and nodularins. In: Meriluoto J, Spoof L, Codd GA (eds) Handbook of cyanobacterial monitoring and cyanotoxin analysis. section VIII, Wiley publisher. ISBN: 978-1-119-06868-6

  • Spoof L, Berg KA, Rapala J, Lahti K, Lepisto L, Metcalf JS, Codd GA, Meriluoto J (2006) First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environ Toxicol 21(6):552–560

    CAS  PubMed  Google Scholar 

  • Stewart I (2004) Recreational exposure to freshwater cyanobacteria: epidemiology, dermal toxicity and biological activity of cyanobacterial lipopolysaccharides. Ph.D. Thesis submitted for the degree of Doctor of Philosophy at the University of Queensland, pp 1–418

  • Stewart I, Schluter PJ, Shaw GR (2006a) Cyanobacterial lipopolysaccharides and human health–a review. Environ Health A Glob Access Sci Source 5:7

    Google Scholar 

  • Stewart I, Webb PM, Schluter PJ, Fleming LE, Burns JW Jr, Gantar M, Backer LC, Shaw GR (2006b) Epidemiology of recreational exposure to freshwater cyanobacteria-an international prospective cohort study. BMC Public Health 6:93

    PubMed  PubMed Central  Google Scholar 

  • Stewart I, Seawright AA, Shaw GR (2008) Cyanobacterial poisoning in livestock, wild mammals and birds—an overview. In: Hudnell HK (ed) Cyanobacterial harmful algal blooms state of the science and research needs. Springer, Berlin

    Google Scholar 

  • Steyn DG (1943) Poisoning of animals by algae on dams and pans. Farming S Afr 18:489–492

    CAS  Google Scholar 

  • Stoyneva-Gärtner MP, Descy J-P, Latli A, Uzunov BA, Pavlova VT, Bratanova Z, Babica P, Maršálek B, Meriluoto J, Spoof L (2017) Assessment of cyanoprokaryote blooms and of cyanotoxins in Bulgaria in a 15-years period (2000–2015). AIOL 8(1):131–152

    Google Scholar 

  • Svirčev Z, Krstić S, Miladinov-Mikov M, Baltić V, Vidović M (2009) Freshwater cyanobacterial blooms and primary liver cancer epidemiological studies in Serbia. J Environ Sci Health Part C 27(1):36–55

    Google Scholar 

  • Svirčev Z, Marković SB, Stevens T, Codd GA, Smalley I, Simeunović J, Obreht I, Dulić T, Pantelić D, Hambach U (2013a) Importance of biological loess crusts for loess formation in semi-arid environments. Q Int 296:206–215. https://doi.org/10.1016/j.quaint.2012.10.048

    Article  Google Scholar 

  • Svirčev Z, Drobac D, Tokodi N, Vidović M, Simeunović J, Miladinov-Mikov M, Baltić V (2013b) Epidemiology of primary liver cancer in Serbia and possible connection with cyanobacterial blooms. J Environ Sci Health Part C 31(3):181–200

    Google Scholar 

  • Svirčev Z, Drobac D, Tokodi N, Lužanin Z, Munjas AM, Nikolin B, Vuleta D, Meriluoto J (2014a) Epidemiology of cancers in Serbia and possible connection with cyanobacterial blooms. J Environ Sci Health Part C 32(4):319–337

    Google Scholar 

  • Svirčev Z, Tokodi N, Drobac D, Codd GA (2014b) Cyanobacteria in aquatic ecosystems in Serbia: effects on water quality, human health and biodiversity. Syst Biodivers 12(3):261–270

    Google Scholar 

  • Svirčev Z, Tokodi N, Drobac D (2017a) Review of 130 years of research on cyanobacteria in aquatic ecosystems in Serbia presented in a Serbian Cyanobacterial Database. AIOL 8(1):153–160. https://doi.org/10.4081/aiol.2017.6360

    Article  Google Scholar 

  • Svirčev Z, Drobac D, Tokodi N, Đenić D, Simeunović J, Hiskia A, Kaloudis T, Mijović B, Šušak S, Protić M, Vidović M, Onjia A, Nybom S, Važić T, Palanački Malešević T, Dulić T, Pantelić D, Vukašinović M, Meriluoto J (2017b) Lessons from the Užice case: how to complement analytical data. In: Meriluoto J, Spoof L, Codd GA (eds) Handbook of cyanobacterial monitoring and cyanotoxin analysis. Wiley Publisher, Amsterdam. https://doi.org/10.1002/9781119068761.ch31

    Google Scholar 

  • Svirčev Z, Drobac D, Tokodi N, Mijović B, Codd GA, Meriluoto J (2017c) Toxicology of microcystins with reference to cases of human intoxications and epidemiological investigations of exposures to cyanobacteria and cyanotoxins. Arch Toxicol 91(2):621–650

    PubMed  Google Scholar 

  • Svrcek C, Smith DW (2004) Cyanobacteria toxins and the current state of knowledge on water treatment options: a review. J Environ Eng Sci 3:155–185

    CAS  Google Scholar 

  • Tango PJ, Butler W (2008) Cyanotoxins in tidal waters of Chesapeake Bay. Northeast Nat 15:403–416. https://doi.org/10.1656/1092-6194-15.3.403

    Article  Google Scholar 

  • Teixeira M, Costa M, Carvalho V, Pereira M, Hage E (1993) Gastroenteritis epidemic in the area of the Itaparica Dam, Bahia, Brazil. Bull Pan Am Health Organ 27:244–253

    Google Scholar 

  • Theron CP (1990a) Kameelperdvrektes en die teenwoordigheid van Microcystis in Bloemhof Dam. DWAF-HRI Report N4/84/1

  • Theron CP (1990b) ‘n Ondersoek na die voorkoms van Microcystis in Klipdrif Dam. Institute for Water Quality Studies Report N4/84/1. Department of Water

  • Thomas AD, Saker ML, Norton JH, Olsen RD (1998) Cyanobacterium Cylindrospermopsis raciborskii as a probable cause of death in cattle in northern Queensland. Aust Vet J 76:592–594

    CAS  PubMed  Google Scholar 

  • Tisdale E (1931) Epidemic of intestinal disorders in Charleston, WVa, occurring simultaneously with unprecented water supply conditions. Am J Public Health 21:198–200

    CAS  Google Scholar 

  • Toerien DF, Scott WE, Pitout MJ (1976) Microcystis toxins, isolation, identification, implications. Water S Afr 2:160–162

    CAS  Google Scholar 

  • Trainer VL, Hardy FJ (2015) Integrative monitoring of marine and freshwater harmful algae in Washington State for public health protection. Toxins 7:1206–1234. https://doi.org/10.3390/toxins7041206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trevino-Garrison I, DeMent J, Ahmed FS, Haines-Lieber P, Langer T, Ménager H, Neff J, van der Merwe D, Carney E (2015) Human illnesses and animal deaths associated with freshwater harmful algal blooms-Kansas. Toxins (Basel) 7(2):353–366. https://doi.org/10.3390/toxins7020353

    Article  CAS  Google Scholar 

  • Turner P, Gammie A, Hollinrake K, Codd GA (1990) Pneumonia associated with contact with cyanobacteria. BMJ 300:1440–1441

    CAS  PubMed  PubMed Central  Google Scholar 

  • Turner AD, Dhanji-Rapkova M, O’Neill A, Coates L, Lewis A, Lewis K (2018) Analysis of microcystins in cyanobacterial blooms from freshwater bodies in England. Toxins 10(1):39. https://doi.org/10.3390/toxins10010039

    Article  CAS  PubMed Central  Google Scholar 

  • Ueno Y, Nagata S, Tsutsumi T, Hasegawa A, Watanabe M, Park HD, Chen GC, Chen G, Yu SZ (1996) Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 17(6):1317–1321

    CAS  PubMed  Google Scholar 

  • Van Apeldoorn ME, van Egmond HP, Speijers GJA, Bakker GJI (2007) Toxins of cyanobacteria. Mol Nutr Food Res 51:7–60

    PubMed  Google Scholar 

  • Van der Merwe D, Sebbag L, Nietfeld JC, Aubel MT, Foss A, Carney E (2012) Investigation of a Microcystis aeruginosa cyanobacterial freshwater harmful algal bloom associated with acute microcystin toxicosis in a dog. J Vet Diagn Investig 24:679–687

    Google Scholar 

  • Van Ginkel CE, Hohls BC (1999) Toxic Algae in Erfenis and Allemanskraal Dams. Occasional report by the Institute for Water Quality Studies, Department of Water Affairs and Forestry. N/C400/03/DEQ/1999

  • Van Halderen A, Harding WR, Wessels JC, Schneider DJ, Heine EWP, Van der Merwe J, Fourie JM (1995) Cyanobacterial (blue-green algae) poisoning of livestock in the Western Cape Province of South Africa. J S Afr Vet Assoc Tydskrif Van Die Suid-Afrikaanse Veterinere Vereniging 66:260–264

    PubMed  Google Scholar 

  • Van Hoof F (1994) The occurrence of toxic cyanobacteria in Europe (excluding the UK and Scandinavia). In: Steffensen DA, Nicholson BC (eds) Toxic cyanobacteria: current status of research and management. Australian Centre for Water Quality Research, Salisbury, pp 29–33

    Google Scholar 

  • Vasconcelos VM, Sivonen K, Evans WR, Carmichael WW, Namikoshi M (1996) Hepatotoxic microcystin diversity in cyanobacterial blooms collected in portuguese freshwaters. Water Res 30(10):2377–2384

    CAS  Google Scholar 

  • Veldee MV (1931) Epidemiological study of suspected waterborne gastroenteritis. Am J Public Health 21:1227–1235

    CAS  Google Scholar 

  • Vidal F, Sedan D, D’Agostino D, Cavalieri ML, Mullen E, Varela MMP, Flores C, Caixach J, Andrinolo D (2017) Recreational exposure during algal bloom in Carrasco beach, Uruguay: a liver failure case report. Toxins 9(9):267. https://doi.org/10.3390/toxins9090267

    Article  CAS  PubMed Central  Google Scholar 

  • Walker SR, Lund JC, Schumacher DG, Brakhage PA, McManus BC, Miller JD, Augustine MM, Carney JJ, Holland RS, Hoagland KD, Holz JC, Barrow TM, Rundquist DC, Gitelson AA (2008) Nebraska experience. In: Hudnell HK (ed) Cyanobacterial harmful algal blooms: state of the science and research needs, vol 619, Chapter 6. Springer Press, New York. Adv. Exp. Med. Biol., pp 139–152

  • Walter JM, Lopes FAC, Lopes-Ferreira M, Vidal LM, Leomil L, Melo F, de Azevedo GS, Oliveira RMS, Medeiros AJ, Melo ASO, De Rezende CE, Tanuri A, Thompson FL (2018) Occurrence of harmful cyanobacteria in drinking water from a severely drought-impacted semi-arid region. Front Microbiol 9:176. https://doi.org/10.3389/fmicb.2018.00176

    Article  PubMed  PubMed Central  Google Scholar 

  • Weise G, Drews G, Jann B, Jann K (1970) Identification and analysis of a lipopolysaccharide in cell walls of the blue-green algae Anacystis nidulans. Arch Microbiol 71:89–98

    CAS  Google Scholar 

  • Welker M, Chorus I, Fastner J (2004) Occurrence of cyanobacterial toxins (microcystins) in surface waters of rural Bangladesh—pilot study. Report. Water, Sanitation and Health Protection of the Human Environment WHO, Geneva

    Google Scholar 

  • Whitton BA (2012) Ecology of Cyanobacteria II: their diversity in space and time. Springer, London

    Google Scholar 

  • Wiese M, D’Agostino PM, Mihali TK, Moffitt MC, Neilan BA (2010) Neurotoxic alkaloids: saxitoxin and its analogs. Mar Drugs 8:2185–2211

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilding TK (2000) Rotorua lakes algae report. Environment Bay of Plenty, Whakatane

    Google Scholar 

  • Willén E, Ahlgren G, Tilahun G, Spoof L, Neffling M-R, Meriluoto J (2011) Cyanotoxin production in seven Ethiopian rift valley lakes. Inland Waters 1:81–91

    Google Scholar 

  • Williams B (2004) Dog dies after swim in kegonsa. Algae toxin in water may be to blame; officials will still test. Wis State Journal, 11 June 2004

  • Williamson M, Corbett S (1993) Investigating health risks from riverine blooms of blue green algae. NSW Public Health Bull 4:27–29

    Google Scholar 

  • Winterton D (2011) Report: toxic algae in east canyon reservoir. Standard Examiner, 6 March 2011

  • Wirsing B, Hoffmann L, Heinze R, Klein D, Daloze D, Braekman JC, Weckesser J (1998) First report on the identification of microcystin in a water bloom collected in Belgium. Syst Appl Microbiol 21(1):23–27. https://doi.org/10.1016/S0723-2020(98)80004-0

    Article  CAS  PubMed  Google Scholar 

  • Wood SA, Dietrich DR (2011) Quantitative assessment of aerosolized cyanobacterial toxins at two New Zealand lakes. J Environ Monit 13:1617–1624

    CAS  PubMed  Google Scholar 

  • Wood SA, Briggs LR, Sprosen J, Ruck JG, Wear RG, Holland PT, Bloxham M (2006) Changes in concentrations of microcystins in rainbow trout, freshwater mussels, and cyanobacteria in Lakes Rotoiti and Rotoehu. Environ Toxicol 21(3):205–222

    CAS  PubMed  Google Scholar 

  • Wood SA, Selwood AI, Rueckert A, Holland PT, Milne JR, Smith KF, Smits B, Watts LF, Cary CS (2007) First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand. Toxicon 50(2):292–301

    CAS  PubMed  Google Scholar 

  • Wood SA, Heath MW, Holland PT, Munday R, McGregor GB, Ryan KG (2010) Identification of a benthic microcystin-producing filamentous cyanobacterium (Oscillatoriales) associated with a dog poisoning in New Zealand. Toxicon 55(4):897–903. https://doi.org/10.1016/j.toxicon.2009.12.019

    Article  CAS  PubMed  Google Scholar 

  • World Health Organization (2003) Guidelines for safe recreational water environments. Vol 1, coastal and fresh waters. ISBN 92 4 154580 1, 33

  • https://books.google.rs/books/about/Current_Approaches_to_Cyanotoxin_Risk_As.html?id=jk9TlwEACAAJ&redir_esc=y

  • Yadav S, Sinha RP, Tyagi MB, Kumar A (2011) Cyanobacterial secondary metabolites. Int J Pharma Bio Sci 2:144–167

    CAS  Google Scholar 

  • Yoo RS (1995) Cyanobacterial (blue-green algal) toxins: a resource guide. American Water Works Association, Illinois

    Google Scholar 

  • Yoshida T, Makita Y, Nagata S, Tsutsumi T, Yoshida F, Sekijima M, Tamura S, Ueno Y (1997) Acute oral toxicity of microcystin-LR, a cyanobacterial hepatotoxin, in mice. Nat Toxins 5(3):91–95

    CAS  PubMed  Google Scholar 

  • Yoshizawa S, Matushi R, Watanabe MF, Harada KI, Ichhara A, Carmichael WW, Fujiki H (1990) Inhibition of protein phosphatases by microcystins and nodularin associated with hepatotoxicity. J Cancer Res Clin Oncol 116:609–614

    CAS  PubMed  Google Scholar 

  • Yu S-Z (1989) Drinking water and primary liver cancer. In: Tang ZY, Wu MC, **a SS (eds) primary liver cancer. China Academic Publishers, New York, pp 30–37

    Google Scholar 

  • Yu S-Z (1995) Primary prevention of hepatocellular carcinoma. J Gastroenterol Hepatol 10:674–682

    CAS  PubMed  Google Scholar 

  • Yu SZ, Chen Z-Q, Liu Y-K, Huang Z-Y, Zhao Y-F (1989) The aflatoxins and contaminated water in the etiological study of primary liver cancer. In: Natori S, Hashimoto K, Ueno Y (eds) Mycotoxins & phycotoxins. Elsevier, Amsterdam, pp 37–44

    Google Scholar 

  • Žegura B, Zajc I, Lah TT, Filipič M (2008) Patterns of microcystin-LR induced alteration of the expression of genes involved in response to DNA damage and apoptosis. Toxicon 51:615–623

    PubMed  Google Scholar 

  • Zhou L, Yu H, Chen K (2002) Relationship between microcystin in drinking water and colorectal cancer. Biomed Environ Sci 15:166–171

    PubMed  Google Scholar 

  • Zilberg B (1966) Gastroenteritis in Salisbury European children-a five-year study. Cent Afr J Med 12:164–168

    CAS  PubMed  Google Scholar 

  • Zimba P, Camus A, Allen E, Burkholder J (2006) Co-occurrence of white shrimp, Litopenaeus vannamei, mortalities and microcystin toxin in a southeastern USA shrimp facility. Aquaculture 261:1048–1055

    CAS  Google Scholar 

  • Znachor P, Jurczak T, Komárková J, Jezberová J, Mankiewicz J, Kastovská K, Zapomelová E (2006) Summer changes in cyanobacterial bloom composition and microcystin concentration in eutrophic Czech reservoirs. Environ Toxicol 21(3):236–243

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the funding of the Ministry of Education, Science and Technological Development of the Serbian Government (project number: 176020).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dijana Lalić.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Svirčev, Z., Lalić, D., Bojadžija Savić, G. et al. Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings. Arch Toxicol 93, 2429–2481 (2019). https://doi.org/10.1007/s00204-019-02524-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00204-019-02524-4

Keywords

Navigation