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Strict coupling between the development of Planktothrix rubescens and microcystin content in two nearby lakes south of the Alps (lakes Garda and Ledro)

Published online by Cambridge University Press:  18 November 2013

Nico Salmaso ,
Adriano Boscaini ,
Shiva Shams  and
Leonardo Cerasino
Nico Salmaso*
Affiliation:
IASMA Research and Innovation Centre, Istituto Agrario di S. Michele all'Adige – Fondazione E. Mach, Via E. Mach 1, 38010 S. Michele all'Adige, Trento, Italy
Adriano Boscaini
Affiliation:
IASMA Research and Innovation Centre, Istituto Agrario di S. Michele all'Adige – Fondazione E. Mach, Via E. Mach 1, 38010 S. Michele all'Adige, Trento, Italy
Shiva Shams
Affiliation:
IASMA Research and Innovation Centre, Istituto Agrario di S. Michele all'Adige – Fondazione E. Mach, Via E. Mach 1, 38010 S. Michele all'Adige, Trento, Italy Human and Environmental Toxicology Group, Department of Biology, University of Konstanz, P.O. Box X-918, D-78457, Konstanz, Germany
Leonardo Cerasino
Affiliation:
IASMA Research and Innovation Centre, Istituto Agrario di S. Michele all'Adige – Fondazione E. Mach, Via E. Mach 1, 38010 S. Michele all'Adige, Trento, Italy
*
*Corresponding author: nico.salmaso@fmach.it
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Abstract

Cyanobacteria and their principal cyanotoxins were studied in the largest Italian lake (Lake Garda, 65 m a.s.l.) and in a near smaller reservoir (Lake Ledro, 652 m a.s.l.). The two lakes share a fraction of water due to a pipe pumping water from and into the lakes and the same dominant cyanobacterial species (Planktothrix rubescens). Despite the differences in the concentrations of cyanotoxins (mostly microcystins, MCs) and biovolumes of P. rubescens (BVPr) (over one order of magnitude), the Bayesian analyses linking these two variables showed striking similarities, suggesting the existence of similar toxic genotypes colonizing the two water bodies and a constitutive MC production. It was stressed that a greater sensitivity and reliability in the management strategies aimed at minimizing the risks due to cyanobacteria should also contemplate the use of specific lake-tailored models linking MCs and BVPr.

Keywords

CyanobacteriaPlanktothrix rubescensmicrocystinsrisk assessmentBayesian analysis
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 49 , Issue 4 , 2013 , pp. 309 - 318
Copyright
© EDP Sciences, 2013

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References

Akcaalan, R., Young, F.M., Metcalf, J.S., Morrison, L.F., Albay, M. and Codd, G.A., 2006. Microcystin analysis in single filaments of Planktothrix spp. in laboratory cultures and environmental blooms. Water Res., 40, 1583–1590.CrossRefGoogle ScholarPubMed
Almodóvar, A., Nicola, G.G. and Nuevo, M., 2004. Effects of a bloom of Planktothrix rubescens on the fish community of a Spanish reservoir. Limnetica, 23, 167–178.Google Scholar
Anneville, O., Gammeter, S. and Straile, D., 2005. Phosphorus decrease and climate variability: mediators of synchrony in phytoplankton changes among European peri-alpine lakes. Freshw. Biol., 50, 1731–1746.CrossRefGoogle Scholar
APHA, AWWA and WEF, 2000. Standard Methods for the Examination of Water and Wastewater (19th edn), American Public Health Association, Washington.
Azevedo, S.M.F., Carmichael, W.W., Jochimsen, E.M., Rinehart, K.L., Lau, S., Shaw, G.R. and Eaglesham, G.K., 2002. Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology, 182, 441–446.CrossRefGoogle Scholar
Bogialli, S., Nigro Di Gregorio, F., Lucentini, L., Ferretti, E., Ottaviani, M., Ungaro, N., Abis, P.P. and Cannarozzi De Grazia, M., 2013. Management of a toxic cyanobacterium bloom (Planktothrix rubescens) affecting an Italian drinking water basin: a case study. Environ. Sci. Technol., 47, 574–583.CrossRefGoogle ScholarPubMed
Buzzi, F., 2002. Phytoplankton assemblages in two sub-basins of Lake Como. J. Limnol., 61, 117–128.CrossRefGoogle Scholar
Carraro, E., Guyennon, N., Hamilton, D., Valsecchi, L., Manfredi, E.C., Viviano, G., Salerno, F., Tartari, G. and Copetti, D., 2012. Coupling high-resolution measurements to a three-dimensional lake model to assess the spatial and temporal dynamics of the cyanobacterium Planktothrix rubescens in a medium-sized lake. Hydrobiologia, 698, 77–95.CrossRefGoogle Scholar
Cerasino, L. and Salmaso, N., 2012. Diversity and distribution of cyanobacterial toxins in the Italian subalpine lacustrine district. Oceanol. Hydrobiol. St., 41, 54–63.CrossRefGoogle Scholar
Chorus, I., 2012. Current Approaches to Cyanotoxin Risk Assessment, Risk Management and Regulations in Different Countries, Federal Environment Agency (Umweltbundesamt), Dessau-Roßlau, Germany, 147, Available online at: http://www.uba.de/uba-info-medien-e/4390.html.Google Scholar
D'alelio, D., Gandolfi, A., Boscaini, A., Flaim, G., Tolotti, M. and Salmaso, N., 2011. Planktothrix populations in subalpine lakes: selection for strains with strong gas vesicles as a function of lake depth, morphometry and circulation. Freshwat. Biol., 56, 1481–1493.CrossRefGoogle Scholar
de los Ríos, A., Ascaso, C., Wierzchos, J., Fernández-Valiente, E. and Quesada, A., 2004. Microstructural characterization of cyanobacterial mats from the McMurdo Ice Shelf, Antarctica. Appl. Environ. Microbiol., 70, 569–580.CrossRefGoogle ScholarPubMed
Dietrich, D. and Hoeger, S., 2005. Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach? Toxicol. Appl. Pharm., 203, 273–289.CrossRefGoogle ScholarPubMed
Dokulil, M.T. and Teubner, K., 2012. Deep living Planktothrix rubescens modulated by environmental constraints and climate forcing. Hydrobiologia, 698, 29–46.CrossRefGoogle Scholar
Ellison, A.M., 2004. Bayesian inference in ecology. Ecol. Lett., 7, 509–520.CrossRefGoogle Scholar
Fleming, L.E., Rivero, C., Burns, J., William, C., Bean, J.A., Shea, K.A. and Stinn, J., 2002. Blue green algae (cyanobacterial) toxins, surface drinking water, and liver cancer in Florida. Harmful Algae, 1, 57–168.CrossRefGoogle Scholar
Gallina, N., Anneville, O. and Beniston, M., 2011. Impacts of extreme air temperatures on cyanobacteria in five deep peri-Alpine lakes. J. Limnol., 70, 186–196.CrossRefGoogle Scholar
Gallina, N., Salmaso, N., Morabito, G. and Beniston, M., 2013. Phytoplankton configuration in six deep lakes in the peri-Alpine region: are the key drivers related to eutrophication and climate? Aquat. Ecol., 47, 177–193.CrossRefGoogle Scholar
Guzzella, L., Ghislanzoni, L., Pozzoni, F., Cerasino, L. and Salmaso, N., 2010. Determinazione di tossine algali (microcistine e nodularina) nelle acque superficiali. Notiziario dei metodi analitici, IRS-CNR, 1, 17–31.Google Scholar
Hobbs, N.T. and Hilborn, R., 2006. Alternatives to statistical hypothesis testing in ecology: a guide to self teaching. Ecol. Appl., 16, 5–19.CrossRefGoogle ScholarPubMed
Hudnell, H.K. (ed.), 2008. Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs, Springer, NY, USA, 949.CrossRefGoogle ScholarPubMed
Humbert, J.F., Quiblier, C. and Gugger, M., 2010. Molecular approaches for monitoring potentially toxic marine and freshwater phytoplankton species. Anal. Bioanal. Chem., 397, 1723–1732.CrossRefGoogle ScholarPubMed
Humpage, A.R., 2008. Toxin types, toxicokinetics and toxicodynamics. Adv. Exp. Med. Biol., 619, 383–415.CrossRefGoogle ScholarPubMed
Jacquet, S., Briand, J.-F., Leboulanger, C., Avois-Jacquet, C., Oberhaus, L., Tassin, B., Vinçon-Leite, B., Paolini, G., Druart, J.-C., Anneville, O. and Humbert, J.-F., 2005. The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural French lake (Lac du Bourget). Harmful Algae, 4, 651–672.CrossRefGoogle Scholar
Kardinaal, W.E.A. and Visser, P.M., 2005. Dynamics of cyanobacterial toxins. Sources of variability in microcystin concentrations. In: Huisman, J., Matthijs, H.C.P. and Visser, P.M. (eds.), Harmful Cyanobacteria, Springer, Dordrecht, 41–63.Google Scholar
Kass, R.E. and Raftery, A.E., 1995. Bayes Factors. J. Am. Stat. Assoc., 90, 773–795.CrossRefGoogle Scholar
Kéry, M., 2010. Introduction to WinBUGS for Ecologists. A Bayesian Approach to Regression, ANOVA, Mixed Models and Related Analyses, Academic Press – Elsevier, Burlington, MA, USA, 302.Google Scholar
Kristiansen, J., 1996. Dispersal of freshwater algae – a review. Hydrobiologia, 336, 151–157.CrossRefGoogle Scholar
Kurmayer, R. and Gumperberger, M., 2006. Diversity of microcystin genotypes among populations of the filamentous cyanobacteria Planktothrix rubescens and Planktothrix agardhii. Mol. Ecol., 15, 3849–3861.CrossRefGoogle ScholarPubMed
Kurmayer, R., Schober, E., Tonk, L., Visser, P.M. and Christiansen, G., 2011. Spatial divergence in the proportions of genes encoding toxic peptide synthesis among populations of the cyanobacterium Planktothrix in European lakes. FEMS Microbiol. Lett., 317, 127–37.CrossRefGoogle ScholarPubMed
Lunn, D.J., Thomas, A., Best, N. and Spiegelhalter, D., 2000. WinBUGS – a Bayesian modelling framework: concepts, structure, and extensibility. Stat. Comput., 10, 325–337.CrossRefGoogle Scholar
Lyck, S., 2004. Simultaneous changes in cell quotas of microcystin, chlorophyll a, protein and carbohydrate during different growth phases of a batch culture experiment with Microcystis aeruginosa. J. Plankton. Res., 26, 727–736.CrossRefGoogle Scholar
Martin, A.D., Quinn, K.M. and Park, J.H., 2011. MCMCpack: Markov Chain Monte Carlo in R. J. Stat. Soft., 42, 1–21.CrossRefGoogle Scholar
McCarthy, M.A., 2007. Bayesian Methods for Ecology, Cambridge University Press, Cambridge, 296.CrossRefGoogle Scholar
McCarthy, M.A. and Masters, P., 2005. Profiting from prior information in Bayesian analyses of ecological data. J. Appl. Ecol., 42, 1012–1019.CrossRefGoogle Scholar
Meriluoto, J. and Codd, G.A. (eds.), 2005. TOXIC Cyanobacterial monitoring and cyanotoxin analysis. Acta Acad. Aboensis B, 65, 149.Google Scholar
Messineo, V., Mattei, D., Melchiorre, S., Salvatorea, G., Bogialli, S., Salzano, R., Mazza, R., Capelli, G. and Bruno, M., 2006. Microcystin diversity in a Planktothrix rubescens population from Lake Albano (Central Italy). Toxicon, 48, 160–174.CrossRefGoogle Scholar
Metcalf, J.S. and Codd, G.A., 2012. Cyanotoxins. In: Whitton, B.A. (ed.), Ecology of Cyanobacteria II, Springer, Dordrecht, 651–675.CrossRefGoogle Scholar
Metcalf, J.S., Richer, R., Cox, P.A. and Codd, G.A., 2012. Cyanotoxins in desert environments may present a risk to human health. Sci. Total Environ., 421–422, 118–123.CrossRefGoogle Scholar
Morabito, G., Ruggiu, D. and Panzani, P., 2002. Recent dynamics (1995–1999) of the phytoplankton assemblages in Lago Maggiore as a basic tool for defining association patterns in the Italian deep lakes. J. Limnol., 61, 129–145.CrossRefGoogle Scholar
Naselli-Flores, L. and Barone, R., 2000. Phytoplankton dynamics and structure: a comparative analysis in natural and man-made water bodies of different trophic state. Hydrobiologia, 438, 65–74.CrossRefGoogle Scholar
Naselli-Flores, L., Barone, R., Chorus, I. and Kurmayer, R., 2007. Toxic cyanobacterial blooms in reservoirs under a semiarid mediterranean climate: the magnification of a problem. Environ. Toxicol., 22, 399–404.CrossRefGoogle Scholar
Nehring, S., 1998. Non-indigenous phytoplankton species in the North-Sea: supposed region of origin and possible transport vector. Arch. Fish. Mar. Res., 46, 181–194.Google Scholar
Neilan, B.A., Pearson, L.A., Muenchhoff, J., Moffitt, M.C. and Dittmann, E., 2012. Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ. Microbiol., 15, 1239–1253.CrossRefGoogle ScholarPubMed
Nürnberg, G.K., LaZerte, B.D. and Olding, D.D., 2003. An artificially induced Planktothrix rubescens surface bloom in a small kettle lake in Southern Ontario compared to blooms world-wide. Lake Reserv. Manag., 19, 307–322.CrossRefGoogle Scholar
Okello, W., Ostermaier, V., Portmann, C., Gademann, K. and Kurmayer, R., 2010. Spatial isolation favours the divergence in microcystin net production by Microcystis in Ugandan freshwater lakes. Water Res., 44, 2803–2814.CrossRefGoogle ScholarPubMed
Paerl, H., 2008. Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. In: Hudnell, H.K. (ed.), Cyanobacterial Harmful Algal Blooms: State of the Science and Research Needs, Springer, New York, 217–237.CrossRefGoogle Scholar
Paulino, S., Valério, E., Faria, N., Fastner, J., Welker, M., Tenreiro, R. and Pereira, P., 2009. Detection of Planktothrix rubescens (Cyanobacteria) associated with microcystin production in a freshwater reservoir. Hydrobiologia, 621, 207–211.CrossRefGoogle Scholar
Peretyatko, A., Teissier, S., De Backer, S. and Triest, L., 2010. Assessment of the risk of cyanobacterial bloom occurrence in urban ponds: probabilistic approach. Ann. Limnol. - Int. J. Lim., 46, 121–133.CrossRefGoogle Scholar
R Core Team, 2013. R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. Available online at: http://www.R-project.org/.
Reynolds, C.S., 2006. The Ecology of Phytoplankton, Cambridge University Press, Cambridge, 535.CrossRefGoogle Scholar
Rott, E., Salmaso, N. and Hoehn, E., 2007. Quality control of Utermöhl based phytoplankton biovolume estimates – an easy task or a Gordian knot? Hydrobiologia, 578, 141–146.CrossRefGoogle Scholar
Salmaso, N., 2002. Ecological patterns of phytoplankton assemblages in Lake Garda: seasonal, spatial and historical features. J. Limnol., 61, 95–115.CrossRefGoogle Scholar
Salmaso, N., 2011. Interactions between nutrient availability and climatic fluctuations as determinants of the long term phytoplankton community changes in Lake Garda, Northern Italy. Hydrobiologia, 660, 59–68.CrossRefGoogle Scholar
Salmaso, N., Buzzi, F., Garibaldi, L., Morabito, G. and Simona, M., 2012a. Effects of nutrient availability and temperature on phytoplankton development: a case study from large lakes south of the Alps. Aquat. Sci., 74, 555–570.CrossRefGoogle Scholar
Salmaso, N., Naselli-Flores, L. and Padisák, J., 2012b. Impairing the largest and most productive forest on our planet: how do human activities impact phytoplankton? Hydrobiologia, 698, 375–384.CrossRefGoogle Scholar
Sedmak, B., Eleršek, T., Grach-Pogrebinsky, O., Carmeli, S., Sever, N. and Lah, T.T., 2008. Ecotoxicologically relevant cyclic peptides from cyanobacterial bloom (Planktothrix rubescens) – a threat to human and environmental health. Radiol. Oncol., 42, 102–113.CrossRefGoogle Scholar
Sivonen, K. and Börner, T., 2008. Bioactive compounds produced by cyanobacteria. In: Herrero, A. and Flores E. (eds.), The Cyanobacteria. Molecular Biology, Genomics and Evolution, Caister Academic Press, Norfolk, UK, 159–197.Google Scholar
Sivonen, K. and Jones, G.J., 1999. Cyanobacterial toxins. In: Chorus, I. and Bartram, J. (eds.), Toxic Cyanobacteria in Water: A Guide to their Public Health Consequences, Monitoring and Management, Spon, London, UK, 41–111.Google Scholar
Sturtz, S., Ligges, U. and Gelman, A., 2005. R2WinBUGS: a package for running WinBUGS from R. J. Stat. Softw., 12, 1–16.CrossRefGoogle Scholar
Svircev, Z., Krstic, S., Miladinov-Milkov, M., Baltic, V. and Vldovic, M., 2009. Freshwater cyanobacterial blooms and primary liver cancer epidemiological studies in Serbia. J. Environ. Sci. Heal. C, 27, 36–55.CrossRefGoogle ScholarPubMed
Ueno, Y., Nagata, S., Tsutsumi, T., Hasegawa, A., Watanabe, M.F., Park, H.D., Chen, G.C., Chen, G. and Yu, S.Z., 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, 1317–1321.CrossRefGoogle ScholarPubMed
Valério, E., Faria, N., Paulino, S. and Pereira, P., 2008. Seasonal variation of phytoplankton and cyanobacteria composition and associated microcystins in six Portuguese freshwater reservoirs. Ann. Limnol. - Int. J. Lim., 44, 189–196.CrossRefGoogle Scholar
Walsby, A.E. and Schanz, F., 2002. Light-dependent growth rate determines changes in the population of Planktothrix rubescens over the annual cycle in Lake Zürich, Switzerland. New Phytol., 154, 671–687.CrossRefGoogle Scholar
WHO, World Health Organization, 2008. Guidelines for Drinking-water Quality (3rd edn,), incorporating the first and second addenda. Volume 1 Recommendations. WHO, Geneva, 515.
Yéprémian, C., Gugger, M.F., Briand, E., Catherine, A., Berger, C., Quiblier, C. and Bernard, C., 2007. Microcystin ecotypes in a perennial Planktothrix agardhii bloom. Water Res., 41, 4446–4456.CrossRefGoogle Scholar
Yu, S.Z., 1989. Drinking water and primary liver cancer. In: Tang, Z.Y., Wu, M.C. and Xia, S.S. (eds.), Primary Liver Cancer, Springer, Berlin, 30–37.Google Scholar
Zhou, L., Yu, H. and Chen, K., 2002. Relationship between microcystin in drinking water and colorectal cancer. Biomed. Env. Sci., 15, 166–171.Google ScholarPubMed