https://doi.org/10.4081/jlimnol.2019.1893
Spatio-temporal variation of cyanobacteria and cyanotoxins in public supply reservoirs of the semi-arid region of Brazil
Cyanobacteria and cyanotoxins in reservoirs of the semi-arid region
Submitted: 11 February 2019
Accepted: 16 September 2019
Published: 31 October 2019
Accepted: 16 September 2019
Abstract Views: 1639
PDF: 650
HTML: 151
HTML: 151
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Cyanobacteria harmful algal blooms (CyanoHABs) have become increasingly frequent and intense in public supply reservoirs as a result of eutrophication and global climate change. The semi-arid region of Brazil has a well documented history of CyanoHABs but the underlying factors that control the excessive proliferation of these organisms and the production of their bioactive secondary metabolites are not comprehensively understood. This study aimed to identify the environmental factors that explain the spatial and temporal variations in the abundance of cyanobacteria and the concentration of cyanotoxins (microcystins, saxitoxins, and cylindrospermopsin) in semi-arid reservoirs. The following hypotheses were tested: (a) the largest biovolumes of potential toxin producing cyanobacteria occur when cyanotoxin concentrations are highest; and (b) the environmental factors that explain variations in biovolume of cyanobacteria also explain changes in cyanotoxins concentrations. Samples were taken from four reservoirs located in the Northeast region of Brazil, over a three-month period (October 2016 and February and June 2017). Of the 24 species of cyanobacteria identified, 13 were potentially toxin-producing. Physicochemical variables such as water volume of the reservoir, water transparency, soluble reactive phosphorus, and total phosphorus explained the abundance of cyanobacteria and the levels of cyanotoxins. These results corroborate the hypothesis that similar physicochemical conditions influence the abundance and diversity of cyanobacteria and cyanotoxins. Cyanobacterial blooms composed of more than one potential toxin producing species were observed in the studied reservoirs, where potential microcystin-producing species were the most common. Microcystins and saxitoxins were detected in all the reservoirs studied, while cylindrospermopsin and the cyanobacterium Cylindrospermopsis raciborskii were simultaneously recorded in only one reservoir (Camalaú Reservoir). Cylindrospermopsin was only detected in a reservoir for the first time in the State of Paraíba. Canonical redundancy analysis showed that the cyanotoxins were related to potential toxin producing species. These results corroborate the proposed hypothesis that there is a correlation between cyanotoxins and the biomass of potential producers. Also, there were situations where cyanotoxins were detected without the presence of potential producers. These results demonstrate the need for reassessment of potential toxin producing species of cyanobacteria in semi-arid reservoirs. This may lead to the identification and characterization of novel producers of these bioactive secondary metabolites.
Alvares CA, Stape JL, Sentelhas PC, de Moraes G, Leonardo J, Sparovek G, 2013. Köppen's climate classification map for Brazil. Meteorol. Z. 22:711-728.
DOI: https://doi.org/10.1127/0941-2948/2013/0507
Antunes JT, Leão PN, Vasconcelos VM, 2015. Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Front. Microbiol. 6: 473.
DOI: https://doi.org/10.3389/fmicb.2015.00473
Aragão-Tavares NKC, Moura AN, Bittencourt-Oliveira MC, 2013. Planktonic Cyanobacteria forming blooms in reservoirs of northeastern Brazil. Rev. Bras. Cienc. Agrar. 8:662-668.
DOI: https://doi.org/10.5039/agraria.v8i4a2985
Aragão-Tavares NKC, Moura AN, Dantas ÊW, 2017. Persistence and stability of phytoplankton communities in eutrophic reservoirs of northeastern Brazil. Braz J Bot. 40:749-759.
DOI: https://doi.org/10.1007/s40415-017-0387-y
Araújo LE, Neto JMM, Sousa FAS, 2009. Classification of annual rainfall and the rainy quarter of the year in the Paraíba river basin using Rain Anomaly Index (RAI). Rev. Ambient. Água. 4: 93-110.
DOI: https://doi.org/10.4136/ambi-agua.105
Armah A, Hiskia A, Kaloudis T, Chernoff N, Hill D, Antoniou MG, He X, Loftin K, O'Shea K, Zhao C, Pelaez M, Han C, Lynch TJ, 2013. A review on cylindrospermopsin: the global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environ. Sci. Process Impacts 15:1979-2003.
DOI: https://doi.org/10.1039/c3em00353a
APHA, 2012. Standard methods for the examination of water and wastewater. APHA, Wahsington DC.
Barbosa JEL, Medeiros ESFM, Brasil J, Cordeiro RS, Crispim MCB, Silva GHG, 2012. Aquatic systems in semi-arid Brazil: limnology and management. Acta Limnol Bras. 24:103-118.
DOI: https://doi.org/10.1590/S2179-975X2012005000030
Bernard C, Ballot A, Thomazeau S, Maloufi S, Furey A, Mankiewicz-Boczek J, Pawlik-Skowrońska B, Capelli C, Salmaso N, 2016. Appendix 2: Cyanobacteria associated with the production of cyanotoxins. In: J. Meriluoto, L. Spoof and G.A. Codd (eds.), Handbook of cyanobacterial monitoring and cyanotoxin analysis. J. Wiley & Sons, Ltd, Chichester.
DOI: https://doi.org/10.1002/9781119068761.app2
Bittencourt-Oliveira MC, Piccin-Santos V, Kujbida P, Moura AN, 2011. Cylindrospermopsin in water supply reservoirs in Brazil determined by immunochemical and molecular methods. J. WaterResour. 3:349-355.
DOI: https://doi.org/10.4236/jwarp.2011.36044
Bittencourt-Oliveira MC, Santos DMS, Moura NA, 2010. Toxic cyanobacteria in reservoirs in northeastern Brazil: detection using a molecular method. Braz. J. Biol. 70:1005-1010.
DOI: https://doi.org/10.1590/S1519-69842010000500012
Bittencourt-Oliveira MCD, Piccin-Santos V, Moura AN, Aragão-Tavares NK, Cordeiro-Araújo MK, 2014. Cyanobacteria, microcystins and cylindrospermopsin in public drinking supply reservoirs of Brazil. Na. Acad. Bras. Cienc. 86:297-310.
DOI: https://doi.org/10.1590/0001-3765201302512
Boopathi T, Ki JS, 2014. Impact of environmental factors on the regulation of cyanotoxin production. Toxins 6:1951-1978.
DOI: https://doi.org/10.3390/toxins6071951
Bouvy M, Molica M, Oliveira S, Marinho M, Beker B, 1999. Dynamics of a toxic cyanobacterial bloom (Cylindrospermopsis raciborskii) in a shallow reservoir in the semi-arid region of northeast Brazil. Aquat. Microb. Ecol. 20:285-297.
DOI: https://doi.org/10.3354/ame020285
Brasil J, Attayde JL, Vasconcelos FR, Dantas DD, Huszar VL, 2016. Drought-induced water-level reduction favors cyanobacteria blooms in tropical shallow lakes. Hydrobiologia 770:145-164.
DOI: https://doi.org/10.1007/s10750-015-2578-5
Buratti FM, Manganelli M, Vichi S, Stefanelli M, Scardala S, Testai E, Funari E, 2017. Cyanotoxins: Producing organisms, occurrence, toxicity, mechanism of action and evaluation toxicological risk to human health. Arch. Toxicol. 91:1049-1130.
DOI: https://doi.org/10.1007/s00204-016-1913-6
Cao X, Wang J, Liao J, Sun J, Huamg Y, 2016. The threshold response of phytoplankton community to nutriente gardient in a shallow eutrophic Chinese lake. Ecol. Indic. 61:258-267.
DOI: https://doi.org/10.1016/j.ecolind.2015.09.025
Carlson RE, 1977. Atrophic state index for lakes. Limnol. Oceanogr. 22:361-369.
DOI: https://doi.org/10.4319/lo.1977.22.2.0361
Carmichael WW, 1992. Cyanobacteria secondary metabolites - the cyanotoxins. J. Appl. Bacteriol. 72:445-459.
DOI: https://doi.org/10.1111/j.1365-2672.1992.tb01858.x
Chia MA, Cordeiro-Araújo MK, Lorenzi AS, Bittencourt-Oliveira MCD, 2017. Cylindrospermopsin induced changes in growth, toxin production and antioxidant response of Acutodesmus acuminatus and Microcystis aeruginosa under differing light and nitrogen conditions. Ecotox. Environ. Safe. 142:189-199.
DOI: https://doi.org/10.1016/j.ecoenv.2017.04.015
Chia MA, Jankowiak JG, Kramer BJ, Goleski JA, Huang IS, Zimba PV, Bittencourt-Oliveira MC, Gobler CJ, 2018. Succession and toxicity of Microcystis and Anabaena (Dolichospermum) blooms are controlled by nutrient-dependent allelopathic interactions. Harmful Algae 74:67-77.
DOI: https://doi.org/10.1016/j.hal.2018.03.002
Chorus I, Bartram J, 1999. Toxic cyanobacteria in water: a guide to the public health consequences, monitoring and management. Spon Press, London: 440 pp.
DOI: https://doi.org/10.1201/9781482295061
Costa IAS, Azevedo SMF, Senna PAC, Bernardo RR, Costa SM, Chellappa NT, 2006. Occurrence of toxin-producing cyanobacteria blooms in a Brazilian semiarid reservoir. Braz. J. Biol. 66:211-219.
DOI: https://doi.org/10.1590/S1519-69842006000200005
Cunha DGF, Dodds WK, Loiselle SA, 2018. Factors related to water quality and thresholds for microcystin concentrations in subtropical Brazilian reservoirs. Inland Waters 8:368-380.
DOI: https://doi.org/10.1080/20442041.2018.1492526
Dalu T, Wasserman RJ, 2018. Cyanobacteria dynamics in a small tropical reservoir: Understanding spatio-temporal variability and influence of environmental variables. Sci. Total Environ. 643:835-841.
DOI: https://doi.org/10.1016/j.scitotenv.2018.06.256
Dantas EW, Moura AN, Bittencourt-Oliveira MDC, 2011. Cyanobacterial blooms in stratified and destratified eutrophic reservoirs in semi-arid region of Brazil. An. Acad. Bras. Cienc. 83:1327-1338.
DOI: https://doi.org/10.1590/S0001-37652011000400019
Descy JP, Leprieur F, Pirlot S, Leporcq B, Van Wichelen J, Peretyatkp A, Teissier S, Codd GA, Triest L, Vyverman W, Wilmotte A, 2016. Identifying the factors diterming blooms of cyanobacteria in a set of shallow lakes. Ecol .Inform. 34:129-138.
DOI: https://doi.org/10.1016/j.ecoinf.2016.05.003
Dolman AM, Rücker J, Pick FR, Fastner J, Rohrlack T, Mishke U, Wiedner C, 2012. Cyanobacteria and Cyanotoxins: The influence of nitrogen versus phosphorus. PloS One 7:e38757.
DOI: https://doi.org/10.1371/journal.pone.0038757
Downing TG, Phelan RR, Downing S, 2015. A potential physiological role for cyanotoxins in cyanobacteria of arid environments. J. Arid. Environ. 112:147-151.
DOI: https://doi.org/10.1016/j.jaridenv.2014.02.005
Figueredo C, Pinto-Coelho RM, Lopes AMMB, Lima PHO, Gücker B, Giani A, 2016. From intermittent flowering to persistent cyanobacteria: identifying the main vectors in an urban tropical reservoir. J. Limnol. 75:445-454. doi: 10.4081/jlimnol.2016.1330.
DOI: https://doi.org/10.4081/jlimnol.2016.1330
Fortin N, Aranda-Rodriguez R, Jing H, Pick F, Bird D, Greer CW, 2010. Detection of microcystin – producing cyanobacteria in Missiquoi Bay, Quebec, Canada, using quantitative PCR. Appl. Environ. Microb. 76:5105-5112.
DOI: https://doi.org/10.1128/AEM.00183-10
Freitas EC, Pinheiro C, Rocha C, 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.
DOI: https://doi.org/10.1016/j.hal.2013.11.004
Fonseca JR, Vieira PCS, Kujbida P, Costa IAS, 2015. Cyanobacterial occurrence and detection of microcystins and saxitoxins in reservoirs of the Brazilian semi-arid. Acta Limnol. Bras. 27: 8-92.
DOI: https://doi.org/10.1590/S2179-975X2814
Funari E, Testai E, 2008. Human health risk assessment related to cyanotoxins exposure. Crit. Rev. Toxicol. 38:97-125.
DOI: https://doi.org/10.1080/10408440701749454
Gao Y, Cornwell JC, Stoecker DKE, Owens MS, 2012. Effects of pH increase by cyanobacteria on sediment nutrient fluxes and nitrification-denitrification coupled in a shallow freshwater estuary. Biogeosciences 9:2697-2710.
DOI: https://doi.org/10.5194/bg-9-2697-2012
Ger KA, Hansson LA, Lürling M, 2014. Understanding cyanobacteria‐zooplankton interactions in a more eutrophic world. Freshwater Biol. 59:1783-1798.
DOI: https://doi.org/10.1111/fwb.12393
Gkelis S, Zaoutsos N, 2014. Cyanotoxin occurrence and potentially toxin producing cyanobacteria in freshwaters of Greece: A multi-disciplinary approach. Toxicon 78:1-9.
DOI: https://doi.org/10.1016/j.toxicon.2013.11.010
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. 38:4395-4404.
DOI: https://doi.org/10.1016/j.watres.2004.08.004
Hackett JD, Wisecaver JH, Brosnahan ML, Kulis DM, Anderson DM, Bhattacharya D, Erdner DL, 2012. Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Mol Biol Evol. 30:70-78.
DOI: https://doi.org/10.1093/molbev/mss142
Hayes NM, Vanni MJ, 2018. Microcystin concentrations can be predicted with phytoplankton biomass and watershed morphology. Inland Waters 8:273-283.
DOI: https://doi.org/10.1080/20442041.2018.1446408
Hillebrand H, Dŭrselen C, Kírsctel D, Polligher U, Zohary T, 1999. Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 35:403-424.
DOI: https://doi.org/10.1046/j.1529-8817.1999.3520403.x
Huang J, Ji M, Xie Y, Wang S, He Y, Ran J, 2016. Global semi-arid climate change over last 60 years. Clim. Dynam. 46:1131-1150.
DOI: https://doi.org/10.1007/s00382-015-2636-8
Jespersen AM, Christoffersen K, 1987. Measurements of chlorophyll-a from phytoplankton usig etanol as extraction solvente. Arch. Hydrobiol. 109 445-454.
Jones GJ, Orr PT, 1994. Release and degradation of microcystin following algicide treatment of a Microeystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Water Res. 28: 871-876.
DOI: https://doi.org/10.1016/0043-1354(94)90093-0
Jovem-Azevêdo D, Bezerra-Neto JF, Azevêdo EL, Gomes WIA, Molozzi J, Feio MJ, 2019. Dipteran assemblages as functional indicators of extreme droughts. J. Arid Environ. 164:12-22.
DOI: https://doi.org/10.1016/j.jaridenv.2019.01.014
Kaebernick M, Neilan BA, 2001. Ecological and molecular investigations of cyanotoxin production. Microb. Ecol. 35:1-9.
DOI: https://doi.org/10.1111/j.1574-6941.2001.tb00782.x
Komárek J, 2013. Süßwasserflora von Mitteleuropa, Bd. 19/3: Cyanoprokaryota. rd part: Heterocytous Genera. Springer Spektrum: 1130 pp.
DOI: https://doi.org/10.1007/978-3-8274-2737-3
Komárek J, Anagostidis K, 1989. Modern approach to the classification system of cyanophytes 4- Nostocales. Arch. Hydrobiol. 56:247-345.
Komárek J, Anagnostidis K, 1999. Cyanoprokaryota. 1. Teil: Chroococcales. In: H. Ettl, G. Gärtner, H. Heynig, D. Mollenhauer (eds). Süsswasserflora von Mitteleuropa. 19/1. Springer Spektrum: 548 pp.
Komárek J, Anagostidis K, 2005. Cyanoprokaryota. 2. Teil: Oscillatoriales. In: B. Bündel, L. Krienitz, G. Gӓtner and M. Schagerl (eds.), Süsswasserflora von Mitteleuropa. Springer Spektrum: 759 pp.
Komárek J, Komárková-Lec-Nerová J, Sant’anna CL, Azevedo MTP, Senna PAC, 2002. Two common Mycrocystis species (Chroococcaales, Cyanobacteria) from tropical America, including M. panniformis sp. Algologie 23:159-177.
Kotak BG, Lam AK, Prepas EE, Hrudey SE, 2000. Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Can. J. Fish. Aquat. Sci. 57:1584-1593.
DOI: https://doi.org/10.1139/f00-091
Krol MS, Bronstert A, 2007. Regional integrated modelling of climate change impacts on natural resources and resource usage in semi-arid Northeast Brazil. Environ. Modell. Softw. 22:259-268.
DOI: https://doi.org/10.1016/j.envsoft.2005.07.022
Lahti K, 1997. Persistence of cyanobacterial hepatotoxin, microcystin-LR in particulate material and dissolved in lake water. Water Res. 31:1005-1012.
DOI: https://doi.org/10.1016/S0043-1354(96)00353-3
Lorenzen CJ, 1967. Determination of chlorophyll and pheo-pigments: Spectrofotometric equations. Limnol. Oceanogr.12: 343.
DOI: https://doi.org/10.4319/lo.1967.12.2.0343
Lorenzi AS, Cordeiro-Araújo MK, Chia MA, Bittencourt-Oliveira MC, 2018. Cyanotoxin contamination of semiarid drinking water supply reservoirs. Environ. Earth Sci. 77:595.
DOI: https://doi.org/10.1007/s12665-018-7774-y
Lorenzi AS, Chia MA, Piccin-Santos V, Bittencourt-Oliveira MDC, 2015. Microcystins and cylindrospermopsins molecular markers for the detection of toxic cyanobacteria: a case study of northeastern Brazilian reservoirs. Limnetica. 34:269-282.
Mantzouki E, Lürling M, Fastner J, De Senerpont Domis L, Wilk-Woźniak E, Koreivienė J, Seelen L, Teurlincx S, Verstijnen Y, Krztoń W, Walusiak E, Karosienė J, Kasperovičienė J, Savadova K, Vitonytė I, Cillero-Castro C, Budzyńska A, Goldyn R, Kozak A, Rosińska J, Szeląg-Wasielewska E, Domek P, Jakubowska-Krepska N, Kwasizur K, Messyasz B, Pełechata A, Pełechaty M, Kokocinski M, García-Murcia A, Real M, Romans E, Noguero-Ribes J, Duque DP, Fernández-Morán E, Karakaya N, Häggqvist K, Demir N, Beklioğlu M, Filiz N, Levi EE, Iskin U, Bezirci G, Tavşanoğlu ÜN, Özhan K, Gkelis S, Panou M, Fakioglu Ö, Avagianos C, Kaloudis T, Çelik K, Yilmaz M, Marcé R, Catalán N, Bravo AG, Buck M, Colom-Montero W, Mustonen K, Pierson D, Yang Y, Raposeiro PM, Gonçalves V, Antoniou MG, Tsiarta N, McCarthy V, Perello VC, Feldmann T, Laas A, Panksep K, Tuvikene L, Gagala I, Mankiewicz-Boczek J, Yağcı MA, Çınar Ş, Çapkın K, Yağcı A, Cesur M, Bilgin F, Bulut C, Uysal R, Obertegger U, Boscaini A, Flaim G, Salmaso N, Cerasino L, Richardson J, Visser PM, Verspagen JMH, Karan T, Soylu EN, Maraşlıoğlu F, Napiórkowska-Krzebietke A, Ochocka A, Pasztaleniec A, Antão-Geraldes AM, Vasconcelos V, Morais J, Vale M, Köker L, Akçaalan R, Albay M, Špoljarić Maronić D, Stević F, Žuna Pfeiffer T, Fonvielle J, Straile D, Rothhaupt K-O, Hansson L-A, Urrutia-Cordero P, Bláha L, Geriš R, Fránková M, Koçer MAT, Alp MT, Remec-Rekar S, Elersek T, Triantis T, Zervou S-K, Hiskia A, Haande S, Skjelbred B, Madrecka B, Nemova H, Drastichova I, Chomova L, Edwards C, Sevindik TO, Tunca H, Önem B, Aleksovski B, Krstić S, Vucelić IB, Nawrocka L, Salmi P, Machado-Vieira D, De Oliveira AG, Delgado-Martín J, García D, Cereijo JL, Gomà J, Trapote MC, Vegas-Vilarrúbia T, Obrador B, Grabowska M, Karpowicz M, Chmura D, Úbeda B, Gálvez JÁ, Özen A, Christoffersen KS, Warming TP, Kobos J, Mazur-Marzec H, Pérez-Martínez C, Ramos-Rodríguez E, Arvola L, Alcaraz-Párraga P, Toporowska M, Pawlik-Skowronska B, Niedźwiecki M, Pęczuła W, Leira M, Hernández A, Moreno-Ostos E, Blanco JM, Rodríguez V, Montes-Pérez JJ, Palomino RL, Rodríguez-Pérez E, Carballeira R, Camacho A, Picazo A, Rochera C, Santamans AC, Ferriol C, Romo S, Soria JM, Dunalska J, Sieńska J, Szymański D, Kruk M, Kostrzewska-Szlakowska I, Jasser I, Žutinić P, Gligora Udovič M, Plenković-Moraj A, Frąk M, Bańkowska-Sobczak A, Wasilewicz M, Özkan K, Maliaka V, Kangro K, Grossart H-P, Paerl HW, Carey CC, Ibelings BW, 2018. Temperature effects explain continental scale distribution of cyanobacterial toxins. Toxins 10: pii: E156. doi: 10.3390/toxins10040156.
DOI: https://doi.org/10.3390/toxins10040156
Martins ESPR, De Nys E, Molejón C, Biazeto B, Silva RFV, Engle N, 2015. [Monitor de secas do nordeste, em busca de um novo paradigma para a gestão de secas].[Report in Portuguese]. Água Brasil Séries, no. 10. World Bank Group, Washington, D.C.
Merel S, Villarín MC, Chung K, Snyder S, 2013. Spatial and thematic distribution of research on cyanotoxins. Toxicon 76:118-131.
DOI: https://doi.org/10.1016/j.toxicon.2013.09.008
Mohamed ZA, 2017. Macrophytes – cyanobacteria allelopathic interactions and their implications for water resources management - A review. Limnologica 63:122-132.
DOI: https://doi.org/10.1016/j.limno.2017.02.006
Monchamp ME, Pick FR, Beisner BE, Maranger R, 2014. Nitrogen forms influence microcystin concentration and composition via changes in cyanobacterial community structure. PloS One 9:e85573.
DOI: https://doi.org/10.1371/journal.pone.0085573
Moura AN, Aragão-Tavares NKC, Amorim CA, 2018. Cyanobacterial blooms in freshwaters bodies in a semiarid region, northeastern Brazil. J. Limnol. 77:179-188. doi: 10.4081/jlimnol.2017.1646.
DOI: https://doi.org/10.4081/jlimnol.2017.1646
Moura AN, Dantas EW, Oliveira HSB, Bittencourt-Oliveira, MC, 2011. Vertical and temporal dynamics of cyanobacteria in the Carpina potable water reservoir in northeastern Brazil. Braz J Biol. 71: 451-459.
DOI: https://doi.org/10.1590/S1519-69842011000300015
Mowe MA, Mitrovic SM, Lim RP, Furey A, Yeo DC, 2015. Tropical cyanobacterial blooms: a review of prevalence, problem taxa, toxins and influencing environmental factors. J Limnol. 74:205-224. doi: 10.4081/jlimnol.2014.1005.
DOI: https://doi.org/10.4081/jlimnol.2014.1005
Naselli‐Flores L, Barone R, Chorus I, Kurmayer R, 2007. Toxic cyanobacterial blooms in reservoirs under a semiarid Mediterranean climate: the magnification of a problem. Environ. Toxicol. 22: 399-404.
DOI: https://doi.org/10.1002/tox.20268
O’neil JM, Davis TW, Burford MA, Glober CJ, 2012. The rise of harmul cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 14:313-334.
DOI: https://doi.org/10.1016/j.hal.2011.10.027
Ohtani I, Moore RE, Runnegar MT, 1992. Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. J. Am. Chem. Soc. 114:7941-7942.
DOI: https://doi.org/10.1021/ja00046a067
Omidi A, Esterhuizen-Londt M, Pflugmacher S, 2018. Still challenging: the ecological function of the cyanobacterial toxin microcystin–What we know so far. Toxin Rev. 37:87-105.
DOI: https://doi.org/10.1080/15569543.2017.1326059
Paerl H, Otten TG, 2013. Flora of harmful cyanobacteria: causes, consequences and controls. Microb Ecol. 65:995-1010.
DOI: https://doi.org/10.1007/s00248-012-0159-y
Paerl HW, Hall NS, Calandrino ES, 2011. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic- induced change. Sci. Total Environ. 409:1739-1745.
DOI: https://doi.org/10.1016/j.scitotenv.2011.02.001
Paerl HW, Huisman J, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep. 1:27-37.
DOI: https://doi.org/10.1111/j.1758-2229.2008.00004.x
Paerl HW, Otten TG, Joyner AR, 2016. Moving towards adaptive management of cyanotoxin-impaired water bodies. Microbio.. Biotechnol. 9:641-651.
DOI: https://doi.org/10.1111/1751-7915.12383
Paerl HW, Paul VJ, 2012. Climate change: Links to global expansion of harmful cyanobacteria. Water Res. 46:1349-1363.
DOI: https://doi.org/10.1016/j.watres.2011.08.002
Panou M, Zervou SK, Kaloudis T, Hiskia A, Gkelis S, 2018. A Greek Cylindrospermopsis raciborskii strain: Missing link in tropic invader’s phylogeography tale. Harmful Algae 80:96-106.
DOI: https://doi.org/10.1016/j.hal.2018.10.002
Pawlik-Skowronska B, Toporowska M, 2016. How to mitigate cyanobacterial blooms and cyanotoxin production in eutrophic water reservoirs? Hydrobiologia 778:45-59.
DOI: https://doi.org/10.1007/s10750-016-2842-3
Piccin-Santos V, Bittencourt-Oliveira MC, 2012. toxic cyanobacteria in four brazilian water supply reservoirs. J. Environ. Prot. 3:68-73.
DOI: https://doi.org/10.4236/jep.2012.31009
Portella FHCO, Moura AN, Dantas EW, 2018. Variation in climate determines differences in the effects of abiotic variables on the phytoplankton community in tropical ecosystems. Mar. Freshwater Res. 69: 357.
DOI: https://doi.org/10.1071/MF17079
Ragab R, Prudhomme C, 2002. SW-Soil and Water: Climate change and water resources management in arid and semi-arid regions: prospective and challenges for the 21st Century. Biosyst. Eng. 81: 3-34.
DOI: https://doi.org/10.1006/bioe.2001.0013
Reynolds CS, Oliver R L, Walsby AE, 1987. Cyanobacterial dominance: The role of buoyancy regulation in dynamic lake environments. N. Zeal. J. Mar. Fresh. 21:379-390.
DOI: https://doi.org/10.1080/00288330.1987.9516234
Rigosi A, Hanson P, Hamilton DP, Hipsey M, Rusak JA, Bois J, Kim B, 2015. Determining the probability of cyanobacterial blooms: the application of Bayesian networks in multiple lake systems. Ecol. Appl. 25:186-199.
DOI: https://doi.org/10.1890/13-1677.1
Rocha Junior CAN, Costa MRA, Menezes RF, Attayde JL, Becker V, 2018. Water volume reduction increases eutrophication risk in tropical semi-arid reservoirs. Acta Limnol. Bras. 30:e106.
DOI: https://doi.org/10.1590/s2179-975x2117
Rojo C, Segura M, Cortés F, Rodrigo MA, 2013. Alelopathic effects of microcystin-LR on the germination, growth and metabolismo of five charophyte species and a submerged angiosperm. Aquat. Toxicol. 144-145:1-10.
DOI: https://doi.org/10.1016/j.aquatox.2013.09.013
Ross J, 1979. [Práticas de ecologia].[Book in Spanish]. Omega, Barcelona: 181 pp.
Rzymski P, Poniedziałek B, 2014. In search of environmental role of cylindrospermopsin: a review on global distribution and ecology of its producers. Water Res. 66:320-337.
DOI: https://doi.org/10.1016/j.watres.2014.08.029
Sierosławska A, Rymuszka A, Kalinowska R, Skowroński T, Bownik A, Pawlik‐Skowrońska B, 2010. Toxicity of cyanobacterial bloom in the eutrophic dam reservoir (Southeast Poland). Environ. Toxicol. Chem. 29:556-560.
DOI: https://doi.org/10.1002/etc.86
Sinang SC, Poh KB, Shamsudin S, Sinden A, 2015. Preliminary assessment of cyanobacteria diversity and toxic potential in ten freshwater lakes in Selangor, Malaysia. Bull. Environ. Contam. Toxicol. 95:542-547.
DOI: https://doi.org/10.1007/s00128-015-1620-7
Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Midgley PM, 2013. Climate change 2013: The physical science basis. Intergovernmental Panel on Climate Change, Working Group I Contribution to the IPCC Fifth Assessment Report (AR5) (Cambridge Univ Press, New York). 25:1535.
Te SH, Gin KYH, 2011. The dynamics of cyanobacteria and microcystin production in a tropical reservoir by inferetial modelling. Harmful Algae. 10:319-329.
DOI: https://doi.org/10.1016/j.hal.2010.11.006
Ter Braak CJF, Prentice IC, 1988. The theory of gradient analysis. Adv. Ecol.Res. 18:271-317.
DOI: https://doi.org/10.1016/S0065-2504(08)60183-X
Toledo Jr AP, Talarico M, Chinez SJ, Agudo EG, 1983. [A aplicação de modelos simplificados para a avaliação de processo da eutrofização em lagos e reservatórios Tropicais], p. 1-34.[Article in Prtuguese]. Proceedings of the 12th Congresso Brasileiro de Engenharia Sanitária, Rio de Janeiro, ABES.
Utermöhl H, 1958. Zur Vervollkom munng der quantitative phytoplankton methodik. Mitt. Internat. Verein Limnol. 9:1-38.
DOI: https://doi.org/10.1080/05384680.1958.11904091
Walls JT, Wyatt KH, Doll JC, Rubenstein EM, Rober AR, 2018. Hot and toxic: Temperature regulates microcystin release from cyanobacteria. Sci. Total Environ. 610-611:786-795.
DOI: https://doi.org/10.1016/j.scitotenv.2017.08.149
Walter JM, Lopes FAC, Lopes-Ferreira M, Vidal LM, Leomil FM, Azevedo GS, Oliveira RMS, Medeiros AJ, Melo ASO, Rezende CED, Tanuri A, Thompson FL, 2018. Occurrence of harmful cyanobacteria in drinking water from a severely drought-impacted semi-arid region. Front. Microbiol. 9:176.
DOI: https://doi.org/10.3389/fmicb.2018.00176
Wang X, Qin B, Gao G, Paerl HW, 2010a. Nutrient enrichment and selective predation by zooplankton promote Microcystis (Cyanobacteria) bloom formation. J. Plankton Res. 32:457-470.
DOI: https://doi.org/10.1093/plankt/fbp143
Wang Q, Niu Y, Xie P, Chen J, Ma Z, Tao, M, Guo L, 2010b. Factors affecting temporal and spatial variations of microcystins in Gonghu Bay of Lake Taihu, with potential risk of microcystin contamination to human health. Sci. World J. 10:1795-1809.
DOI: https://doi.org/10.1100/tsw.2010.172
Wiese M, D’agostino PM, Mihali TK, Moffitt MC, Neilan BA, 2010. Neurotoxic alkaloids: saxitoxin and its analogs. Mar. Drugs 8:2185-2211.
DOI: https://doi.org/10.3390/md8072185
Yang H, Xie P, Xu J, Zheng L, Deng D, Zhou Q, Wu S, 2006. Seasonal variation of microcystin concentration in Lake Chaohu, a shallow subtropical lake in the People's Republic of China. Bull. Environ. Contam. Toxicol. 77:367-374.
DOI: https://doi.org/10.1007/s00128-006-1075-y
Edited by
Andrea Lami, CNR-IRSA Verbania, ItalyHow to Cite
Silva, Ranielle Daiana dos Santos, Juliana Santos Severiano, Dayany Aguiar de Oliveira, Camila Ferreira Mendes, Vanessa Virgínia Barbosa, Mathias Ahii Chia, and José Etham de Lucena Barbosa. 2019. “Spatio-Temporal Variation of Cyanobacteria and Cyanotoxins in Public Supply Reservoirs of the Semi-Arid Region of Brazil: Cyanobacteria and Cyanotoxins in Reservoirs of the Semi-Arid Region”. Journal of Limnology 79 (1). https://doi.org/10.4081/jlimnol.2019.1893.
Similar Articles
- Dolores Planas, Serge Paquet, Importance of climate change-physical forcing on the increase of cyanobacterial blooms in a small, stratified lake , Journal of Limnology: Vol. 75 No. s1 (2016): Proceedings of the 6th National Congress of Limnology
- Stefan Sommer, Sarma Nandini, S.S.S. Sarma, Arpat Ozgul, Diego Fontaneto, Rotifers in Lake Orta: a potential ecological and evolutionary model system , Journal of Limnology: Vol. 75 No. s2 (2016): Lake Orta: a new lease on life
- Xiangyu Mu, James Brower, Donald I. Siegel, Anthony J. Fiorentino II, Shuqing An, Ying Cai, Delin Xu, Hao Jiang, Using integrated multivariate statistics to assess the hydrochemistry of surface water quality, Lake Taihu basin, China , Journal of Limnology: Vol. 74 No. 2 (2015)
- Diana Vaičiūtė, Mariano Bresciani, Marco Bartoli, Claudia Giardino, Martynas Bučas, Spatial and temporal distribution of coloured dissolved organic matter in a hypertrophic freshwater lagoon , Journal of Limnology: Vol. 74 No. 3 (2015)
- David Avalos-Cueva, Anatoliy Filonov, Iryna Tereshchenko, César O. Monzón, Federico Á. Velázquez-Muñoz, Thermal structure and circulation in Lake Chapala, Mexico , Journal of Limnology: Vol. 75 No. s1 (2016): Proceedings of the 6th National Congress of Limnology
- Najat Elkhiati, Mohamed Ramdani, José L. Espinar, Khalid Fahd, Laura Serrano, Ecological similarities between two Mediterranean wetlands: Sidi Boughaba (North-West Morocco) and the Doñana National Park (South-West Spain) , Journal of Limnology: Vol. 72 No. 2 (2013)
- Karolina Grabowska, Aleksandra Bukowska, Tomasz Kaliński, Bartosz Kiersztyn, Waldemar Siuda, Ryszard J. Chróst, Presence and identification of Legionella and Aeromonas spp. in the Great Masurian Lakes system in the context of eutrophication , Journal of Limnology: Vol. 79 No. 1 (2020)
- Luigi Hinegk, Luca Adami, Sebastiano Piccolroaz, Marina Amadori, Marcello Moretti, Marco Tubino, Marco Toffolon, Multidecadal analysis of Lake Garda water balance , Journal of Limnology: Vol. 82 (2023)
- Anna VISCONTI, Marina MANCA, Riccardo DE BERNARDI, Eutrophication-like response to climate warming: an analysis of Lago Maggiore (N. Italy) zooplankton in contrasting years , Journal of Limnology: Vol. 67 No. 2 (2008)
- Fred. Idiem' OPUTE, Contribution to the knowledge of algae of Nigeria. I. Desmids from the Warri/Forcados Estuaries. Part II. The elongate baculiform desmids , Journal of Limnology: Vol. 59 No. 2 (2000)
<< < 15 16 17 18 19 20 21 22 23 24 > >>
You may also start an advanced similarity search for this article.
List of Cited By :
