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Production of microcystins in calcareous Mediterranean streams: The Alharabe River, Segura River basin in south-east Spain

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Abstract

The development of epilithic cyanobacteria communities in a Mediterranean calcareous stream in the province of Murcia (SE Spain) was studied during the course of one year in an attempt to clarify the environmental variables that influence the production of microcystins. The predominant cyanobacteria were species of Rivularia, which formed conspicuous colonies throughout the year. Seasonally, other species were abundant: Schizothrix fasciculata, Tolypothrix distorta and Phormidium splendidum. All the species collected produced microcystins to a varying degree (up to five varieties), while the benthic community as a whole produced concentrations as high as 20.45 mg m−2. At the same time, the presence of microcystins dissolved in water was confirmed. Among environmental variables, air temperature and silicate content were positively and strongly correlated with total microcystins, while nitrite, nitrate, orthophosphate, calcium and flow were negatively correlated with them. Dissolved microcystins were negatively correlated with microcystin LR, P.A.R. and total phosphorus and positively with rainfall. The production of microcystin YR seems to be regulated by different factors from those regulating the other main varieties (microcystin LR and microcystin RR). The data obtained indicate that all the tested benthic cyanobacteria produced microcystins in this shallow calcareous stream, which may contribute to their predominance in the prevailing conditions. The accumulation of microcystins in mucilaginous colonies of other groups of algae poses new questions concerning the possible ecological function of these compounds and needs further study.

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References

  • Aboal M (1989) Flora algal del río Benamor (Cuenca del Segura, SE de España). Limnetica 5: 1–11.

    Google Scholar 

  • Aboal M, Alcaraz FJ, Barreña J, Egidos AI (2003) El componente vegetal en los humedales de la Región de Murcia. Catalogación, evaluación de la rareza y propuesta de medidas para su conservación. Comunidad Autónoma de Murcia. Novograf, SA, Murcia, pp. 115.

    Google Scholar 

  • Aboal M, Puig MA (2005) Intracellular and dissolved microcystins in reservoirs of the river Segura basin, Murcia, SE Spain. Toxicon 45 (4): 509–518.

    Article  PubMed  Google Scholar 

  • Aboal M, Puig MA, Mateo P, Perona E (2002) Implications of cyanophyte toxicity on biological monitoring of calcareous streams in north–east Spain. J. appl. Phycol. 14: 49–56.

    Article  Google Scholar 

  • Aboal M, Puig MA, Ríos H, López-Jiménez E (2000) Relationship between macroinvertebrate diversity and cyanobacteria toxicity in streams. Verh. int. Verein. Limnol. 27: 555–559.

    Google Scholar 

  • APHA (1998) Standard Methods for the Examination of Water and Wastewater. 19th Edition. American Public Health Association, American Water Works Association, Water Pollution Control Federation, Washington, DC, p. 769.

  • Baker PD, Steffensen DA, Humpage AR, Nicholson BC, Falconer IR, Lanthois B, Fergusson KM, Saint CP (2001) Preliminary evidence of toxicity associated with the benthic cyanobacterium Phormidium in south Australia. Environ. Toxicol. 16(6): 506–511.

    Article  PubMed  Google Scholar 

  • Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J. Cell Biol. 58: 419–435.

    Article  PubMed  Google Scholar 

  • Bolch CJ, Orr PT, Jones GJ, Blackburn SI (1999) Genetic, morphological and toxicological variations among globally distributed strains of Nodularia (Cyanobacteria). J. Phycol. 35: 339–355.

    Article  Google Scholar 

  • Chapman PJ, Edwards AC, Cresser MS (2001) The nitrogen composition of streams in upland Scotland: Some regional and seasonal differences. Sci. Total Environ. 265: 65–83.

    Article  PubMed  Google Scholar 

  • Chen J, Xie P, Guo L, Zheng K, Ni L (2005) Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in a freshwater snail (Ballamya aeruginosa) from a large shallow, eutrophic lake of the subtropical China. Environ. Pollution 134: 423–430.

    Article  Google Scholar 

  • Chorus J, Bartram J (eds) (1999) Toxic Cyanobacteria in Water. A Guide to their Public Health Consequences, Monitoring and Management. World Health Organization, E & F N Spon,p. 416.

  • Codd GA, Ward CJ, Beattie KA, Bell SG (1999) Widening perceptions of the occurrence and significance of cyanobacterial toxins. In Peschek GA, Löffelhardt W, Schmetterer G (eds). The Phototrophic Prokaryotes. Kluwer Academic/Plenum Publishers, Dordrecht, The Netherlands, p. 836.

    Google Scholar 

  • Dow CS, Swoboda UK (2000) Cyanotoxins. In Whitton BA, Potts M (eds). The Ecology of Cyanobacteria. Their Diversity in Time and Space. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 613–632.

    Google Scholar 

  • Dyble J, Paerl HW, Neilan BA (2002) Genetic characterization of Cylindrospermopsis raciborskii (Cyanobacteria) isolates from diverse geographic origins based on nifH and cpcBA-IGS nucleotide sequence analysis. Appl. Environ. Microbiol. 68(5): 2567–2571.

    Article  PubMed  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.

    Article  PubMed  Google Scholar 

  • Falconer IR (1999) An overview of problems caused by toxic blue-green algae (Cyanobacteria) in drinking and recreational water. Environ. Toxicol. 14: 5–12.

    Article  Google Scholar 

  • Figueiredo DR, Azeitiero M, Esteves SM, Gonçalves FJM, Pereira, MJ (2004) Microcystin-producing blooms – a serious global public health issue. Ecotoxicol. Environ. Safety 59: 151–163.

    Article  PubMed  Google Scholar 

  • Gjolme N, Utkilen H (1996) The extraction and the stability of microcystin-RR in different solvents. Phycologia 35(6): 80–82.

    Google Scholar 

  • Gordon ND, McMahon TA, Finlayson BL (2004) Stream Hydrology: An introduction for ecologists. Wiley, NY, Ed. p. 444.

    Google Scholar 

  • Gromov BV, Vepritskiy AA, Titova NN, Mamkayeva KA, Alexandrova OV (1991) Production of the antibiotic cyanobacteria Lu-1 by Nostoc linckia CALU-892 (Cyanobacteria). J. Appl. Phycol. 3(1): 55–59.

    Google Scholar 

  • Henning M, Rohrlack T, Kohl, JG (2001) Responses of Daphnia galeata fed with Microcystis strains with rat hepatocyte and cell-line assays. In Chorus I (ed.), Cyanotoxins – Occurrence, Causes, Consequences. Springer, Berlin, pp. 317–324.

    Google Scholar 

  • Holloway JM, Dahlgren RA, Hansen B, Casey WH (1998) Contribution of bedrock nitrogen to high nitrate concentrations in stream water. Nature 395: 785–788.

    Article  Google Scholar 

  • Jang MH, Ha K, Lucas MC, Joo GJ, Takamuira N (2004) Changes in microcystins production by Microcystis aeruginosa exposed to phytoplanktivorous and omnivorous fish. Aquatic Toxicology 68: 51–55.

    Article  PubMed  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975). New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanzen 167: 191–194.

    Google Scholar 

  • Kearns KD, Hunter MD (2000) Green algal extracellular products regulate antialgal toxin production in a cyanobacterium. Environ. Microbiol. 2: 291–297.

    Article  PubMed  Google Scholar 

  • Kurmayer R, Jüttner F (1999) Strategies for the co-existence of zooplankton with the toxic cyanobacterium Planktothrix rubescens in Lake Zürich. J. Plankton Res. 21: 659–683.

    Article  Google Scholar 

  • Leandro SM, Gil MC, Delgadillo I (2003) Partial characterisation of exopolysaccharides exudated by planktonic diatoms maintained in batch cultures. Acta Oecologica 24: 49–55.

    Article  Google Scholar 

  • Livingstone D, Whitton BA (1984) Water chemistry and phosphatase activity of the blue-green alga Rivularia in Upper Teesdale streams. J. Ecol. 72: 405–421.

    Google Scholar 

  • Margalef R (1983) Limnología. Omega, Barcelona, p. 1010.

  • Margaletti E, Urbani R, Sist P, Ferrari CR, Cicero AM (2004) Abundance and chemical characterization of extracellular carbohydrates released by the marine Cylindrotheca fusiformis under N- and P- limitation. Eur. J. Phycol. 39: 133–142.

    Article  Google Scholar 

  • Marsálek B, Dolejs P, Sládecková A (1997) Algal toxins in Czech drinking water resources and treatment plants. Water Supply 18 (Special Subject): 6–9.

  • Meriluoto JAO, Ermsson JE, Harada KI, Dahlem AM, Sivonen K, Carmichael WW (1990). Internal surface reverse phase high-performance liquid chromatographic separation of the cyanobacterial peptide toxins microcystin-LR, -YR, -RR and nodularin. J. Chromatography 509: 390–395.

    Article  Google Scholar 

  • Malbrouck C, Trausch G, Deros P, Kestemont P (2004) Effect of microcystin-LR on protein phosphatase activity in fed and fasted juvenile goldfish Carassius auratus L. Toxicon 43: 295–301.

    Article  PubMed  Google Scholar 

  • Mez K, Hanselmann K, Preisig HR (1998) Environmental conditions in high mountain lakes containing toxic benthic cyanobacteria. Hydrobiologia 368: 1–15.

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for determination of phosphate in natural waters. Anal. Chim. Acta 27: 31–36.

    Article  Google Scholar 

  • Owen RP (1994) Biological and economic significance of benthic cyanobacteria in two Scottish Highland Lochs. In Codd GA, Jefferizs TM, Keevil CW, Potter E (eds). Detection Methods for Cyanobacterial Toxins. The Royal Society of Chemistry, Cambridge, pp.145–148.

    Google Scholar 

  • Pentecost A (1991) Calcification processes in algae and cyanobacterium. In Riding R (ed.). Calcareous Algae and Stromatolites. Springer-Verlag, Berlin-Heidelberg, pp. 3–20.

    Google Scholar 

  • Pinho GLL, Mourada da Rosa C, Yunes JS, Luquet CM, Blanchini A, Monserrat JM (2003) Toxic effects of microcystin in the hepatopancreas of the estuarine crab Chasmagnathus granulatus (Decapoda, Grapsidae). Comp. Biochem. Physiol. 135: 459–468.

    Google Scholar 

  • Prat N (2000) La qualitat ecològica del Llobregat, el Besòs, el Foix i la Tordera. Estudis de la qualitat ecològica dels rius. Vol 10. Ed. Diputació de Barcelona, p. 163.

  • Prat N (2002) La qualitat ecològica del Llobregat, el Besòs, el Foix i la Tordera. Estudis de la qualitat ecològica dels rius. Vol 12. Ed. Diputació de Barcelona. Electronic version.

  • Puig MA, Aboal M, Mateo P, Perona E (2000) Interactions between cyanobacteria and herbivore caddisflies in Spanish Mediterranean streams. Abstracts 10th International Symposium on Trichoptera, Postdam, Germany, 45.

  • Repka S, Meyerhöfer M, von Bröckel K, Sivonen K (2004) Association of cyanobacterial toxin nodularin with environmental factors and zooplancton in the Baltic Sea. Microbial Ecology 47: 350–358.

    Article  PubMed  Google Scholar 

  • Riding R (1991) Calcified cyanobacteria. In Riding R (ed.). Calcareous Algae and Stromatolites. Springer-Verlag, Berlin, Heidelberg, pp. 55–87.

    Google Scholar 

  • Ríos H (2000) Interacciones entre comunidades de cianobacterias epilíticas fluviales y poblaciones de efemerópteros herbívoros y plecópteros: Efectos de la toxicidad de las cianobacterias. Tesina de Licenciatura, Universidad de Girona,p. 78.

  • Sawyer R, Grisley LM (1967) The determination of ammonia in the ppb level solution. In Technicon Symposia. Vol 1, Automation in analytical chemical.

  • Schagerl M, Unterrrieder I, Angeler, DG (2002) Allelopathy among cyanoprokaryotes and other algae originating from lake Neusiedlersee (Austria) Int. Rev. Hydrol. 87(4): 365–374.

    Article  Google Scholar 

  • Sivonen K (1990) Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of an hepatotoxin production by Oscillatoria agardhii strains. Appl. environ. Microbiol. 56 (9): 2658–2666.

    PubMed  Google Scholar 

  • Staats N, Winder B, de Stal LJ, Mur LR (1999) Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum. Eur. J. Phycol. 34: 161–169.

    Article  Google Scholar 

  • Turner BL, Baxter R, Whitton BA (2003a). Nitrogen and phosphorus in soil solutions and drainage streams in Upper Teesdale, northern England: Implications of organic compounds for biological nutrient limitation. Sci. Total Environ. 314–316: 153–170.

    Google Scholar 

  • Turner BL, Chudek JA, Whitton BA, Baxter R (2003b) Phosphorus composition of upland soils polluted by long-term atmospheric nitrogen deposition. Biogeochemistry 65: 259–274.

    Article  Google Scholar 

  • Valdor R (2003) Toxicidad de extractos de cianofíceas sobre algas y bacterias en condiciones de laboratorio. Tesina de Licenciatura. Facultad de Biología. Universidad de Murcia, p. 70.

  • Whitton BA, Al-Shehri AM, Ellwood NTW, Turner BL (2005) Ecological aspects of phosphatase activity in cyanobacteria, eukaryotic algae and bryophytes. In Turner BL, Frossard E, Balwin DS (eds). Organic Phosphorus in the Environment. Commonwealth Agricultural Bureau International, Wallingford, UK, pp. 205–241.

    Google Scholar 

  • Xie L, Xie P, Li S, Tang H, Liu H (2003) The low TN/TP ratio, a cause or a result of Microcystis blooms?. Water Res. 37: 2073–2080.

    Article  PubMed  Google Scholar 

  • Yin Q, Carmichael WW, Evans WR (1997) Factors influencing growth and toxin production by cultures of the freshwater cyanobacterium Lyngbya wollei Farlow ex Gomont. J. Appl. Phycol. 9: 55–63.

    Article  Google Scholar 

  • Zehnder A (1985) Isolation and cultivation of large cyanophytes for taxonomic purposes. Arch. Hydrobiol. Suppl. 71 (Algological Studies 38/39): 281–289.

    Google Scholar 

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Aboal, M., Puig, M.Á. & Asencio, A.D. Production of microcystins in calcareous Mediterranean streams: The Alharabe River, Segura River basin in south-east Spain. J Appl Phycol 17, 231–243 (2005). https://doi.org/10.1007/s10811-005-2999-z

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