Climate change has been causing the increase in frequency, severity, and duration of harmful algal blooms, which makes the establishment of water management strategies indispensable. For cyanobacteria, several methods are currently used in monitoring programs. However, these methods are time-consuming and require specialists, and results are usually not provided within an adequate timeframe for taking timely mitigation actions. This work proposes a strategy for a faster, easier, and more cost-effective monitoring of cyanobacterial blooms, using a stepwise approach based on fluorometric determination of phycocyanin at an early stage. Complementary parameters (chlorophyll a, enumeration of dominant cyanobacterial species and cyanotoxin potential and quantification) are determined when necessary, thus progressively allocating human and financial resources within the monitoring program. This strategy was applied and validated using nine lentic eutrophic freshwater bodies prone to the occurrence of cyanobacterial blooms. Samples were sequentially evaluated, and the study ended up with two samples that showed high health risks. However, according to WHO guidelines, eight of the nine samples would be classified as having “moderate risk of adverse health effects” and could lead to preventive measures that would have an important regional economic impact. Therefore, the present approach proved to be a promising alternative to increase the effectiveness and accuracy of the risk assessment process in water bodies where cyanobacterial blooms occur.
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2006/7/CE (2006) Directive 2006/7/CE of the European Parliament and of the Council of 15 February (2006) concerning the management of bathing water quality and repealing Directive 76/160/CEE. Official Journal of the European Union. 4.3.2006, L64/37.
Ahn, C. Y., Chung, A. S., & Oh, H. M. (2002). Rainfall, phycocyanin and N:P ratios related to cyanobacterial blooms in a Korean large reservoir. Hydrobiologia, 474, 117–124.
Ahn, C. Y., Joung, S. H., Yoon, S. K., & Oh, H. M. (2007). Alternative alert system for cyanobacterial bloom, using phycocyanin as a level determinant. The Journal of Microbiology, 45(2), 98–104.
Al-Tebrineh, J., Kaan Mihali, T., Pomati, F., & Neilan, B. (2010). Detection of saxitoxin-producing cyanobacteria and Anabaena circinalis in environmental water blooms by quantitative PCR. Applied and Environmental Microbiology, 76(23), 7836–7842.
Anderson, D. M., Cembella, A. D., & Hallegraeff, G. M. (2012). Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annual Review of Marine Science, 4, 143–176.
Antunes, J. T., Leão, P. N., & Vasconcelos, V. M. (2015). Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Frontiers in Microbiology, 6, 1–13.
APHA. (1999). In L. S. Clesceri, A. E. Greenberg, & A. D. Eaton (Eds.), Standard methods for the examination of water and wastewater (20th ed.). Washington, DC: American Public Health Association.
Baron-Sola, A., Ouahid, Y., & del Campo, F. F. (2012). Detection of potentially producing cylindrospermopsin and microcystin strains in mixed populations of cyanobacteria by simultaneous amplification of cylindrospermopsin and microcystin gene regions. Ecotoxicology and Environmental Safety, 75(1), 102–108.
Bastien, C., Cardin, R., Veilleux, E., Deblois, C., Warren, A., & Laurion, L. (2011). Performance evaluation of phycocyanin probes for the monitoring of cyanobacteria. Journal of Environmental Monitoring, 13, 110–118.
Bellinger, G. E., & Sigee, D. C. (2010). Freshwater algae: identification and use as bioindicators (2nd ed.). Spain: Wiley-Blackwell.
Bond, N. R., Lake, P. S., & Arthington, A. H. (2008). The impacts of drought on freshwater ecosystems: an Australian perspective. Hydrobiologia, 600, 3–16.
Bowling, L., Ryan, D., Holliday, J., & Honeyman, G. (2012). Evaluation of in situ fluorometry to determine cyanobacterial abundance in the Murray and Lower Darling rivers, Australia. River Research and Applications, 29, 1059–1071.
Brient, L., Lengronne, M., Bertrand, E., Rolland, D., Sipel, A., Steinmann, D., Baudin, I., et al. (2008). A phycocyanin probe as a tool for monitoring cyanobacteria in freshwater bodies. RSC, 10, 248–255.
Bukowska, A., Bielczyńska, A., Karnkowska, A., Chróst, R. J., & Jasser, I. (2014). Molecular (PCR-DGGE) versus morphological approach: analysis of taxonomic composition of potentially toxic cyanobacteria in freshwater lakes. Aquatic Biosystems, 10, 2–10.
Carmichael, W. W. (1995). Toxic Microcystis and the environment. In: WHO (2003). Guidelines for safe recreational water environments. Coastal and fresh waters, vol 1. Geneva: World Health Organization.
Chang, D. W., Hobson, P., Burch, M., & Lin, T. F. (2012). Measurement of cyanobacteria using in-vivo fluoroscopy—effect of cyanobacterial species, pigments, and colonies. Water Research, 46, 5037–5048.
Chorus, I., & Bartram, J. (1999). Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. London: E & FN Spon.
Chorus, I., Falconer, I. R., Salas, H. J., & Bartram, J. (2000). Health risks caused by freshwater cyanobacteria in recreational waters. Journal of Toxicology and Environmental Health. Part B, Critical Reviews, 3(4), 323–347.
Codd, G. A., Azevedo, S. M. F. O., Bagchi, S. N., Burch, M. D., Carmichael, W. W., Harding, W. R., Kaya, K., et al. (2005). CYANONET a global network for cyanobacterial bloom and toxin risk management. Paris: International Hydrological Programme (IHP) of the United Nations Educational, Scientific and Cultural Organization (UNESCO).
Cronberg, G., & Annadotter, H. (2006). Manual on aquatic cyanobacteria. A photo guide and a synopsis of their toxicology. Denmark: International Society for the Study of Harmful AlgaeUnited Nations Educational, Scientific and Cultural Organisation.
de Figueiredo, D., Azeiteiro, U. M., Esteves, S., Gonçalves, F., & Pereira, M. (2004a). Microcystin-producing blooms—a serious global public health issue. Ecotoxicology and Environmental Safety, 59, 151–163.
de Figueiredo, D. R., Azeiteiro, U. M., Gonçalves, F., & Pereira, M. J. (2004b). Aphanizomenon flos-aquae grown under different nutrient concentrations and the effects of its exudates on growth of two green algae. Fresenius Environmental Bulletin, 13(7), 657–664.
de Figueiredo, D., Alves, A., Pereira, M. J., & Correia, A. (2009). Molecular characterization of bloom-forming Aphanizomenon strains isolated from Vela Lake (western central Portugal). Journal of Plankton Research, 32(2), 239–252.
de Figueiredo, D., Gonçalves, A., Castro, B., Gonçalves, F., Pereira, M. J., & Correia, A. (2011). Differential inter- and intra-specific responses of Aphanizomenon strains to nutrient limitation and algal growth inhibition. Journal of Plankton Research, 33(10), 1606–1616.
de Figueiredo, D. R., Castro, B. B., Pereira, M. J., & Correia, A. (2012). Bacterioplankton community composition in Portuguese water bodies under a severe summer drought. Community Ecology, 13(2), 185–193.
Granéli, E., Weberg, M., & Salomon, P. S. (2008). Harmful algal blooms of allelopathic microalgal species: the role of eutrophication. Harmful Algae, 8(1), 94–102.
Gregor, J., & Maršálek, B. (2005). A simple in vivo fluorescence method for the selective detection and quantification of freshwater cyanobacteria and eukaryotic algae. Acta Hydrochimica et Hydrobiologica, 33(2), 142–148.
Hallegraeff, G. M. (2010). Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. Journal of Phycology, 46(2), 220–235.
Hudnell, H. K. (2010). The state of U.S. freshwater harmful algal blooms assessments, policy and legislation. Toxicon, 55(5), 1024–1034.
Izydorczyk, K., Carpentier, C., Mrówczynski, J., Wagenvoort, A., Jurczak, T., & Tarczynska, M. (2009). Establishment of an Alert Level Framework for cyanobacteria in drinking water resources by using the Algae Online Analyser for monitoring cyanobacterial chlorophyll a. Water Research, 43(4), 989–996.
Jähnichen, S., Long, B. M., & Petzoldt, T. (2011). Microcystin production by Microcystis aeruginosa: direct regulation by multiple environmental factors. Harmful Algae, 12, 95–104.
Janse, I., Kardinaal, W. E. A., Meima, M., Visser, P. M., Zwart, G., & Fastner, J. (2004). Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Applied and Environmental Microbiology, 70(7), 3979–3987.
Joung, S., Kim, C., Ahn, C., & Jang, K. (2006). Simple method for a cell count of the colonial cyanobacterium, Microcystis sp. The Journal of Microbiology, 44(5), 562–565.
Kellmann, R., Mills, T., & Neilan, B. A. (2006). Functional modeling and phylogenetic distribution of putative cylindrospermopsin biosynthesis enzymes. Journal of Molecular Evolution, 62(3), 267–280.
Koskenniemi, K., Lyra, C., Rajaniemi-Wacklin, P., Jokela, J., & Sivonen, K. (2007). Quantitative real-time PCR detection of toxic Nodularia cyanobacteria in the Baltic Sea. Applied and Environmental Microbiology, 73(7), 2173–2179.
Kosol, S., Schmidt, J., & Kurmayer, R. (2009). Variation in peptide net production and growth among strains of the toxic cyanobacterium Planktothrix spp. European Journal of Phycology, 44(1), 49–62.
Lewitus, A. J., Horner, R. A., Caron, D. A., Garcia-Mendoza, E., Hickey, B. M., Hunter, M., Huppert, D. D., et al. (2012). Harmful algal blooms along the North American west coast region: history, trends, causes, and impacts. Harmful Algae, 19, 133–159.
Macário, I. E., Castro, B., Nunes, M. S., Antunes, S., Pizarro, C., Coelho, C., Gonçalves, F., et al. (2015). New insights towards the establishment of phycocyanin concentration thresholds considering species-specific variability of bloom-forming cyanobacteria. Hydrobiologia, 757, 155–165.
Mansilha, C. R., Coelho, C. A., Heitor, A. M., Amado, J., Martins, J. P., & Gameiro, P. (2009). Bathing waters: new directive, new standards, new quality approach. Marine Pollution Bulletin, 58(10), 1562–1565.
Marion, J. W., Lee, J., Wilkins, J. R., Lemeshow, S., Lee, C., Waletzko, E. J., & Buckley, T. J. (2012). In vivo phycocyanin flourometry as a potential rapid screening tool for predicting elevated microcystin concentrations at eutrophic lakes. Environmental Science & Technology, 46(8), 4523–4531.
Merel, S., Walker, D., Chicana, R., Snyder, S., Baurès, E., & Thomas, O. (2013). State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environment International, 59, 303–327.
Metcalf, J. S. and Codd, G. A. (2012). Cyanotoxins. In: B. A. Whitton (Ed.), The ecology of cyanobacteria II—their diversity in space and time (pp. 651–675).
Moreira, C., Martins, A., Azevedo, J., Freitas, M., Regueiras, A., Vale, M., Antunes, A., et al. (2011). Application of real-time PCR in the assessment of the toxic cyanobacterium Cylindrospermopsis raciborskii abundance and toxicological potential. Applied Microbiology and Biotechnology, 92(1), 189–197.
Moreira, C., Azevedo, J., Antunes, A., & Vasconcelos, V. (2013). Cylindrospermopsin: occurrence, methods of detection and toxicology. Journal of Applied Microbiology, 114(3), 605–620.
Padisák, J. (1997). Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archive für Hydrobiologie, Suplement, 107, 563–593.
Park, B. S., Li, Z., Kang, Y.-H., Shin, H. H., Joo, J.-H. and Han, M.-S. (2017). Distinct bloom dynamics of toxic and non-toxic Microcystis (Cyanobacteria) subpopulations in Hoedong reservoir (Korea). Microbial Ecology.
Pearson, L. A., & Neilan, B. A. (2008). The molecular genetics of cyanobacterial toxicity as a basis for monitoring water quality and public health risk. Current Opinion in Biotechnology, 19(3), 281–288.
Rasmussen, J. P., Giglio, S., Monis, P. T., Campbell, R. J., & Saint, C. P. (2008). Development and field testing of a real-time PCR assay for cylindrospermopsin-producing cyanobacteria. Journal of Applied Microbiology, 104, 1503–1515.
Saker, M. L., Nogueira, I. C. G., & Vasconcelos, V. M. (2003). Distribution and toxicity of Cylindrospermopsis raciborskii (Cyanobacteria) in Portuguese freshwaters. Limnetica, 22, 129–136.
Saker, M. L., Fastner, J., Dittmann, E., Christiansen, G., & Vasconcelos, V. M. (2005). Variation between strains of the cyanobacterium Microcystis aeruginosa isolated from a Portuguese river. Journal of Applied Microbiology, 99(4), 749–757.
Schembri, M. A., Neilan, B. A., & Saint, C. P. (2001). Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environmental Toxicology, 16, 413–421.
Sevilla, E., Martin-Luna, B., Vela, L., Bes, M. T., Fillat, M. F., & Peleato, M. L. (2008). Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environmental Microbiology, 10, 2476–2483.
Srivastava, A., Singh, S., Ahn, C. Y., Oh, H. M., & Asthana, R. K. (2013). Monitoring approaches for a toxic cyanobacterial bloom. Environmental Scientific & Technology, 47, 8999–9013.
Tillett, D., Parker, D. L., & Neilan, B. A. (2001). Detection of toxigenicity by a probe for the microcystin synthetase A gene (mcyA) of the cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies. Applied and Environmental Microbiology, 67(6), 2810–2818.
Utermöhl, H. (1958). Zur Vervollkommnung der quantitative Phytoplankton-Methodik. Mitteilungen Internationale Vereiningung fuer Theorestiche und Angewandte Limnologie, 9, 1–38.
Valério, E., Pereira, P., Saker, M. L., Franca, S., & Tenreiro, R. (2005). Molecular characterization of Cylindrospermopsis raciborskii strains isolated from Portuguese freshwaters. Harmful Algae, 4(6), 1044–1052.
Vardi, A., Schatz, D., Beeri, K., Motro, U., Sukenik, A., Levine, A., & Kaplan, A. (2002). Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Current Biology, 12(20), 1767–1772.
Vasconcelos, V. (2006). Eutrophication, toxic cyanobacteria and cyanotoxins: when ecosystems cry for help. Limnetica, 25, 425–432.
WHO (2003). Algae and cyanobacteria in fresh water—guidelines for safe recreational water environments, vol 1 (pp. 136–158). Geneva: World Health Organization.
Wood, S. A., Heath, M. W., Kuhajek, J., & Ryan, K. G. (2010). Fine-scale spatial variability in anatoxin-a and homoanatoxin-a concentrations in benthicCoastal and fresh waters cyanobacterial mats: implication for monitoring and management. Journal of Applied Microbiology, 109, 2011–2018.
This work was supported by European Funds through COMPETE and by National Funds through the Portuguese Science Foundation (FCT) within project PEst-C/MAR/LA0017/2013 and UID/AMB/50017/2013. Daniela de Figueiredo was supported by FCT, by means of a post-doctoral grant (SFRH/BPD/74184/2010).
A correction to this article is available online at https://doi.org/10.1007/s10661-017-6361-0.
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Macário, I.P.E., Castro, B.B., Nunes, I.M.S. et al. Stepwise strategy for monitoring toxic cyanobacterial blooms in lentic water bodies. Environ Monit Assess 189, 620 (2017). https://doi.org/10.1007/s10661-017-6292-9
- Cyanobacterial blooms
- Health risk assessment