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Chl-a fluorescence parameters as biomarkers of metal toxicity in fluvial biofilms: an experimental study

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Abstract

A study was carried out to evaluate the sensitivity of different chlorophyll-a (chl-a) fluorescence parameters measured in freshwater biofilms as metal pollution biomarkers of short- and long-term metal exposures at environmentally realistic concentrations. A microcosm experiment was performed using indoor channels. Mature biofilms were exposed from hours to weeks to three different treatments: No-Metal, Zn (400 μg l−1); and Zn plus Cd (400 μg l−1 and 20 μg l−1, respectively). Metal concentration was based on a real case study: the Riou-Mort River (France). Biofilms exposed to Zn bioaccumulated similar Zn contents per dry weight to those exposed to the mixture (Zn plus Cd) causing a similar inhibition of the effective quantum yield \((\Upphi_{\text{M}}^{\prime})\) during the first hours of exposure. A reduction of the algal biomass, a shift in the community composition (a high reduction of diatoms), a reduction of the maximal quantum yield (ΦM) and a strong reduction of non-photochemical quenching (NPQ) were observed from day 14 until the end of the experiment (35 days). The results indicate that the effects of the metal mixture present in the Riou-Mort on biofilms could be attributed to Zn toxicity. The use of a set of chl-a fluorescence measurements, including photochemical and NPQ parameters, are recommended as a reliable biomarker tool box to evaluate both short- and long-term effects of metals on biofilms containing oxygenic photoautotrophs, suggesting its use in field applications.

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References

  • ACA-Catalan water ageny [available on internet at http://aca-web.gencat.cat].

  • Admiraal, W., H. Blanck, M. Buckert-de Jong, H. Guasch, N. Ivorra, V. Lehmann, B. A. H. Nystroe, M. Paulsoon & S. Sabater, 1999. Short-term toxicity of zinc to microbenthic algae and bacteria in a metal polluted stream. Water Research 33: 1989–1996.

    Article  CAS  Google Scholar 

  • American public health association (APHA), 1989. Standard methods for the examination of water and wastewater, 17 edition. -APHA, Washington, DC.

  • Barranguet, C., F. P. Van den Ende, M. Rugers, A. M. Breure, M. Greudanus, J. J. Sinke & W. Admiraal, 2003. Copper-induced modifications of the trophic relations in riverine algal-bacterial biofilms. Environmental Toxicology and Chemistry 22: 1340–1349.

    PubMed  CAS  Google Scholar 

  • Behra, R., R. Landwehrjohann, K. Vogel, B. Wagner & L. Sigg, 2002. Copper and zinc content of periphyton from two rivers as a function of dissolved metal concentration. Aquatic Science 64: 300–306.

    Article  CAS  Google Scholar 

  • Bilger, W. & O. Björkman, 1990. Role of xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research 25: 174–185.

    Google Scholar 

  • Blanck, H., W. Admiraal, R. F. M. J. Cleven, H. Guasch, M. A. G. T. van den Hoop, N. Ivorra, B. Nyström, M. Paulsson, R. P. Petterson, S. Sabater & G. M. J. Tubbing, 2003. Variability in zinc tolerance, measured as incorporation of radio-labeled carbon dioxide and thymidine, in periphyton communities sampled from 15 European river stretches. Archives of Environmental Contamination and Toxicology 44: 17–29.

    Article  PubMed  CAS  Google Scholar 

  • Bonnineau, C., B. Bonet, N. Corcoll & H. Guasch, 2011. Catalase in fluvial biofilms: a comparison between different extraction methods and example of application in a metal-polluted river. Ecotoxicology 20: 293–303.

    Google Scholar 

  • Chaloub, R. M., C. C. P. de Magalhaes & C. P. dos Santos, 2005. Early toxic effects of Zinc on PSII of Synechocystis aquatilis F. aquatilis (Cyanophyceae). Journal of Phycology 41: 1162–1168.

    Article  CAS  Google Scholar 

  • Clarke, K. R. & R. M. Warwick, 2001. Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd ed. PRIMER-E, Plymouth, UK.

    Google Scholar 

  • Clements, W. H. & M. C. Newman, 2002. Community Ecotoxicology. John Wiley & Sons, LTD, West Sussex, UK: 336.

    Book  Google Scholar 

  • Deckert, J., 2005. Cadmium toxicity in plants: Is there any analogy to its carcinogenic effect in mammalian cells? BioMetals 18: 475–481.

    Article  PubMed  CAS  Google Scholar 

  • Dodds, W. K., B. J. F. Biggs & R. L. Lowe, 1999. Photosynthesis irradiance patterns in benthic microalgae: variations as a function of assemblage thickness and community structure. Journal of Phycology 35: 42–53.

    Article  Google Scholar 

  • Duong, T. T., S. Morin, M. Coste, O. Herlory, A. Feurtet-Mazel & A. Boudou, 2010. Experimental toxicity and bio-accumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity. Science of the Total Environment 408: 552–562.

    Article  PubMed  CAS  Google Scholar 

  • Escher, B. I. & J. L. M. Hermens, 2002. Modes of action in ecotoxicology: their role in body burdens, species sensitivity, QSARs, and mixture effects. Environmental Science and Technology 20: 4201–4217.

    Article  Google Scholar 

  • Faller, P., K. Kienzler & A. Krieger-Liszkay, 2005. Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of Photosystem II by competitive binding to the essential Ca2+ site. Biochimica et Biophysica Acta 1706: 158–164.

    Article  PubMed  CAS  Google Scholar 

  • Farag, A. M., D. A. Nimick, B. A. Kimball, S. E. Church, D. D. Harper & W. G. Brumbaugh, 2007. Concentrations of metals in water, sediment, biofilm, benthic macroinvertebrates, and fish in the Boulder River watershed, Montana, and the role of colloids in metal uptake. Archives of Environmental Contamination and Toxicology 52: 397–409.

    Article  PubMed  CAS  Google Scholar 

  • Fishcer, H., A. Sachse, C. E. W. Steinberg & M. Pusch, 2002. Differential retention and utilization of dissolved organic carbon by bacteria in river sediments. Limnology and Oceanography 47: 1702–1711.

    Article  Google Scholar 

  • Genter, R. B., D. S. Cherry, E. P. Smith & J. J. Cairns, 1987. Algal-periphyton population and community changes from zinc stress in stream mesocosms. Hydrobiologia 153: 261–275.

    Article  CAS  Google Scholar 

  • Genty, B., J.-M. Briantais & N. R. Baker, 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990: 87–92.

    CAS  Google Scholar 

  • Gold, C., A. Feurtet-Mazel, M. Coste & A. Boudou, 2003a. Impacts of Cd and Zn on the development of periphytic diatom communities in artificial streams located along a river pollution gradient. Archives of Environmental Contamination and Toxicology 44: 189–197.

    Article  PubMed  CAS  Google Scholar 

  • Gold, C., A. Feurtet-Mazel, M. Coste & A. Boudou, 2003b. Effects of cadmium stress on periphytic diatom communities in indoor artificial streams. Freshwater Biology 48: 316–328.

    Article  CAS  Google Scholar 

  • Guasch, H. & S. Sabater, 1998. Estimation of the annual primary production of stream epilithic biofilms based on photosynthesis-irradiance relations. Archiv für Hydrobiologie 141: 469–481.

    Google Scholar 

  • Guasch, H., M. Paulsson & S. Sabater, 2002. Effect of copper on algal communities from oligotrophic calcareous streams. Journal of Phycology 38: 241–248.

    Article  CAS  Google Scholar 

  • Guasch, H., W. Admiraal & S. Sabater, 2003. Contrasting effects of organic and inorganic toxicants on freshwater periphyton. Aquatic Toxicology 64: 165–175.

    Article  PubMed  CAS  Google Scholar 

  • Guasch, H., A. Serra, N. Corcoll, B. Bonet & M. Leira, 2010a. Metal ecotoxicology in fluvial biofilms: potential influence of water scarcity. In Sabater, S. & D. Barceló (eds), Water Scarcity in the Mediterranean: Perspectives Under Global Change. Springer, Berlin, Germany: 41–54.

    Chapter  Google Scholar 

  • Guasch, H., G. Atli, B. Bonet, N. Corcoll, M. Leira & A. Serra, 2010b. Discharge and the response of biofilms to metal exposure in Mediterranean rivers. Hydrobiologia 657: 143–157.

    Article  CAS  Google Scholar 

  • Hall, R. O. J. & J. L. Meyer, 1998. The trophic significance of bacteria in a detritus-based stream food web. Ecology 79: 1995–2012.

    Article  Google Scholar 

  • Hassler, C. S. & K. J. Wilkinson, 2003. Failure of the biotic ligand and free-ion activity models to explain zinc bioaccumulation by Chlorella kesslerii. Environmental Toxicology and Chemistry 22: 620–626.

    PubMed  CAS  Google Scholar 

  • Hassler, C. S., R. Behra & K. J. Wilkinson, 2005. Impact of zinc acclimation on bioaccumulation and homeostasis in Chlorella kesslerii. Aquatic Toxicology 74: 139–149.

    Article  PubMed  CAS  Google Scholar 

  • Hawes, I., 1993. Photosynthesis in thick cyanobacterial films: a comparison of annual and perennial antarctic mat communities. Hydrobiologia 252: 203–209.

    Article  CAS  Google Scholar 

  • Hill, W. R. & H. L. Boston, 1991. Community development alters photosynthesis-irradiance relations in stream periphyton. Limnology and Oceanography 36: 1375–1389.

    Article  CAS  Google Scholar 

  • Hill, W. R., M. G. Ryon, J. G. Smith, S. M. Adams, H. L. Boston & A. J. Stewart, 2010. The role of periphyton in mediating the effects of pollution in a stream ecosystem. Environmental Management 45: 563–576.

    Article  PubMed  Google Scholar 

  • Ilangovan, K., R. O. Cañizares-Villanueva, S. González-Moreno & D. Voltolina, 1998. Effect of cadmium and zinc on respiration and photosynthesis in suspended and immobilized cultures of Chlorella vulgaris and Scenedesmus acutus. Bulletin of Environmental Contamination and Toxicology 60: 936–943.

    Article  PubMed  CAS  Google Scholar 

  • Ivorra, N., J. Hettelaar, G. M. J. Tubbing, M. H. S. Kraak & W. Admiraal, 1999. Translocation of microbenthic algal assemblages used for in situ analysis of metal pollution in rivers. Archives of Environmental Contamination and Toxicology 37: 19–28.

    Article  PubMed  CAS  Google Scholar 

  • Ivorra, N., S. Bremer, H. Guasch, M. H. S. Kraak & W. Admiraal, 2000. Differences in the sensitivity of benthic microalgae to Zn and Cd regarding biofilm development and exposure history. Environmental Toxicology and Chemistry 19: 1332–1339.

    Article  CAS  Google Scholar 

  • Jeffrey, S. W. & G. F. Humphrey, 1975. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemical Physiology Pflanz 167: 191–194.

    CAS  Google Scholar 

  • Juneau, P., D. Dewez, S. Matsui, S. G. Kim & R. Popovic, 2001. Evaluation of different algal species sensitivity to mercury and metolachlor by PAM-fluorometry. Chemosphere 45: 589–598.

    Article  PubMed  CAS  Google Scholar 

  • Juneau, P., B. Qiu & C. Deblois, 2007. Use of chlorophyll fluorescence as a tool for determination of herbicide toxic effect: review. Toxicological and Environmental Chemistry 89: 309–325.

    Article  Google Scholar 

  • Kautsky, H. & A. Hirsch, 1931. Neue Versuche zur Kohlensäureassimilation. Naturwissenschaften 19: 964.

    Article  CAS  Google Scholar 

  • Küpper, H., F. Küpper & M. Spiller, 1998. In situ detection of heavy metal substituted chlorophylls in water plants. Photosynthesis Research 58: 123–133.

    Article  Google Scholar 

  • Laviale, M., J. Prygiel & A. Créach, 2010. Light modulated toxicity of isoproturon toward natural stream periphyton photosynthesis: a comparison between constant and dynamic light conditions. Aquatic Toxicology 97: 334–342.

    Article  PubMed  CAS  Google Scholar 

  • Lazar, D., 1999. Chlorophyll a fluorescence induction. Biochimica et Biophysica Acta 1412: 1–28.

    Article  PubMed  CAS  Google Scholar 

  • Le Faucheur, S., R. Behra & L. Sigg, 2005. Thiol and metal contents in periphyton exposed to elevated copper and zinc concentrations: a field and microcosm study. Environmental Science and Technology 39: 8099–8107.

    Article  PubMed  CAS  Google Scholar 

  • Lock, M. A., R. R. Wallace, J. W. Costerton, R. M. Ventullo & S. E. Charlton, 1984. River epilithon: toward a structural-functional model. Oikos 42: 10–22.

    Article  Google Scholar 

  • Mallick, N. & F. H. Mohn, 2003. Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalgae Scenedesmus. Ecotoxicology and Environmental Safety 55: 64–69.

    Article  PubMed  CAS  Google Scholar 

  • Margalef, R., 1983. Limnología. Ediciones Omega, Barcelona: 1010 pp.

  • Martínez-Abaigar, J. & E. Núñez-Olivera, 1998. Ecophysiology of photosynthetic pigments in aquatic bryophytes. In Bates, J. W., N. W. Ashton & J. G. Duckett (eds), Bryology for the Twenty-First Century. Maney Publishing and the British Bryological Society, Leeds, UK: 277–292.

    Google Scholar 

  • Meylan, S., R. Behra & L. Sigg, 2003. Accumulation of copper and zinc in periphyton in response to dynamic variations of metal speciation in freshwater. Environmental Science and Technology 37: 5204–5212.

    Article  PubMed  CAS  Google Scholar 

  • Morin, S., M. Vivas-Nogues, T. T. Duong, A. Boudou, M. Coste & F. Delmas, 2007. Dynamics of benthic diatom colonization in a cadmium/zinc-polluted river (Riou-Mort, France). Fundamental and Applied Limnology 168: 179–187.

    Article  CAS  Google Scholar 

  • Morin, S., T. T. Duong, A. Dabrin, A. Coynel, O. Herlory, M. Baudrimont, F. Delmas, G. Durrieu, J. Schäfer, P. Winterton, G. Blanc & M. Coste, 2008. Long-term survey of heavy-metal pollution, biofilm contamination and diatom community structure in the Riou Mort watershed, South-West France. Environmental Pollution 151: 532–542.

    Article  PubMed  CAS  Google Scholar 

  • Moustakas, M., T. Lanaras, L. Symeonidis & S. Karataglis, 1994. Growth and some photosynthetic characteristics of field grown Avena sativa under copper and lead stress. Photosynthetica 30: 389–396.

    CAS  Google Scholar 

  • Murphy, J. & J. P. Riley, 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27: 31–36.

    Article  CAS  Google Scholar 

  • Niyogi, K. K., 2000. Safety valves for photosynthesis. Current Opinion in Plant Biology 3: 455–460.

    Article  PubMed  CAS  Google Scholar 

  • Paul, B. J. & H. C. Duthie, 1989. Nutrient cycling in the epilithon of running waters. Canadian Journal of Botany 67: 2302–2309.

    Article  CAS  Google Scholar 

  • Paulsson, M., B. Nyström & H. Blanck, 2000. Long-term toxicity of zinc to bacteria and algae in periphyton communities from the river Göta Älv, based on a microcosm study. Aquatic Toxicology 47: 243–257.

    Article  CAS  Google Scholar 

  • Paulsson, M., V. Mansson & H. Blanck, 2002. Effects of zinc on the phosphorus availability to periphyton communities from the river Göta Älv. Aquatic Toxicology 56: 103–113.

    Article  PubMed  CAS  Google Scholar 

  • Perales-Vega, H. V., S. González-Moreno, C. Montes-Horcasitas & R. O. Cañizares-Villanueva, 2007. Growth, photosynthetic and respiratory responses to sub-lethal copper concentrations in Scenedesmus incrassatulus (Chlorophyceae). Chemosphere 67: 2274–2281.

    Article  Google Scholar 

  • Posthuma, L., G. W. Suter & T. P. Traas, 2001. Species Sensitivity Distributions in Ecotoxicology. CRC Press, Boca Raton, FL.

    Book  Google Scholar 

  • Ralph, P. J. & M. D. Burchett, 1998. Photosynthetic response of Halophila ovalis to heavy metal stress. Environmental Pollution 103: 91–101.

    Article  CAS  Google Scholar 

  • Ralph, P. J., R. A. Smith, C. M. O. Macinnis-Ng & C. R. Seery, 2007. Use of fluorescence-based ecotoxicological bioassays in monitoring toxicants and pollution in aquatic systems: review. Toxicological and Environmental Chemistry 89: 589–607.

    Article  CAS  Google Scholar 

  • Rashid, A., E. L. Camm & A. K. M. Ekramoddoullah, 1994. Molecular mechanism of action of Pb2+ and Zn2+ on water oxidizing complex of photosystem II. FEBS Letters 350: 296–298.

    Article  PubMed  CAS  Google Scholar 

  • Rhea, D. T., D. D. Harper, A. M. Farag & W. G. Brumbaugh, 2006. Biomonitoring in the Boulder river watershed, Montana, USA: metal concentrations in biofilm and macroinvertebrates, and relations with macroinvertebrate assemblage. Environmental Monitoring and Assessment 115: 381–393.

    Article  PubMed  CAS  Google Scholar 

  • Ricart, M., H. Guasch, M. Alberch, D. Barceló, C. Bonnineau, A. Geiszinger, M. Farré, J. Ferrer, F. Ricciardi, A. M. Romaní, S. Morin, L. Proia, Ll. Sala, D. Sureda & S. Sabater, 2010a. Triclosan persistence through wastewater treatment plants and its potential toxic effects on river biofilms. Aquatic Toxicology 100: 346–353.

    Article  PubMed  CAS  Google Scholar 

  • Ricart, M., H. Guasch, D. Barceló, R. Brix, M. H. Conceição, A. Geiszinger, M. J. de López Alda, J. C. López-Doval, I. Muñoz, C. Postigo, A. M. Romaní, M. Villagrasa & S. Sabater, 2010b. Primary and complex stressors in polluted mediterranean rivers: pesticide effects on biological communities. Journal of Hydrology 383: 52–61.

    Article  CAS  Google Scholar 

  • Romaní, A. M., 2010. Freshwater Biofilms. In Dürr, S. & J. C. Thomason (eds), Biofouling. Wiley-Blackwell, Oxford, UK: 137–163.

    Google Scholar 

  • Romaní, A. M. & S. Sabater, 2001. Structure and activity of rock and sand biofilms in a Mediterranean stream. Ecology 82: 3232–3245.

    Google Scholar 

  • Romaní, A. M., A. Giorgi, V. Acuña & S. Sabater, 2004. The influence of substratum type and nutrient supply on biofilm organic matter utilization in streams. Limnology and Oceanography 49: 1713–1721.

    Article  Google Scholar 

  • Rosenqvist, E. & O. Van Kooten, 2003. Chlorophyll fluorescence: a general description and nomenclature. In DeEll, J. R. & P. M. A. Toivonen (eds), Practical Applications of Chlorophyll Fluorescence in Plant Biology. Kluwer Academic Publishers, Dordrecht, Netherlands.

    Google Scholar 

  • Rotter, S., F. Sans-Piché, G. Streck, R. Altenburger & M. Schmitt-Jansen, 2011. Active bio-monitoring of contamination in aquatic systems—an in situ translocation experiment applying the PICT concept. Aquatic Toxicology 101: 228–236.

    Article  PubMed  CAS  Google Scholar 

  • Rysgaard, S., M. Kühl, R. N. Glud & J. W. Hansen, 2001. Biomass, production and horizontal patchiness of sea ice algae in a high-Arctic fjord (Young Sound, NE Greenland). Marine Ecology Progress Series 223: 15–26.

    Article  Google Scholar 

  • Sabater, S., H. Guasch, M. Ricart, A. Romaní, G. Vidal, C. Klünder & M. Schmitt-Jansen, 2007. Monitoring the effect of chemicals on biological communities: the biofilm as an interface. Analytical and Bioanalytical Chemistry 387: 1425–1434.

    Article  PubMed  CAS  Google Scholar 

  • Samson, G., J. C. Morissette & R. Popovic, 1988. Copper quenching of the variable fluorescence in Dunaliella tertiolecta. New evidence for a copper inhibition effect on PSII photoinhibitory. Photochemistry and Photobiology 48: 329–332.

    Article  CAS  Google Scholar 

  • Santos, A., J. L. Santos, I. Aparicio & E. Alonso, 2010. Fractionation and distribution of metals in Guadiamar river sediments (SW Spain). Water, Air, and Soil Pollution 207: 103–113.

    Article  CAS  Google Scholar 

  • Schmitt, J., D. Nivens, D. C. White & H. C. Flemming, 1995. Changes of biofilm properties in response to sorbed substances—an FTIR-ATR study. Water Science and Technology 32: 149–155.

    Article  CAS  Google Scholar 

  • Schmitt-Jansen, M. & R. Altenburger, 2008. Community-level microalgal toxicity assessment by multiwavelength-excitation PAM fluorometry. Aquatic Toxicology 86: 49–58.

    Article  PubMed  CAS  Google Scholar 

  • Schreiber, U., 1998. Chlorophyll fluorescence: new instruments for special applications. In Garab, G. (ed.), Photosynthesis: Mechanisms and Effects, Vol. V. Kluwer Academic Publishers, Dordrecht: 4253–4258.

    Google Scholar 

  • Schreiber, U., U. Schliwa & W. Bilger, 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10: 51–62.

    Article  CAS  Google Scholar 

  • Serra, A., N. Corcoll & H. Guasch, 2009. Copper accumulation and toxicity in fluvial periphyton: the influence of exposure history. Chemosphere 74: 633–664.

    Article  PubMed  CAS  Google Scholar 

  • Sheldon, F. & K. F. Walker, 1997. Changes in biofilms induced by flow regulation could explain extinctions of aquatic snails in the lower River Murray, Australia. Hydrobiologia 347: 97–108.

    Article  CAS  Google Scholar 

  • Sheoran, I. S. & R. Sing, 1992. Effect of heavy metals on photosynthesis in higher plants. In Arbol, Y. P., P. Mohanty & Govindjee (eds), Photosynthesis: Photoreaction to Plant Productivity. Kluwer Academic Publishers, The Netherlands: 225–255.

  • Silver, S., 1998. Genes for all metals—a bacterial view of the periodic table. The 1996 Thom Award Lecture. Journal of Industrial Microbiology & Biotechnology 20: 1–12.

    Article  CAS  Google Scholar 

  • Takamura, N., F. Kasai & M. M. Watanabe, 1989. Effect of Cu, Cd and Zn on photosynthesis of freshwater benthic algae. Journal of Applied Phycology 1: 39–52.

    Article  CAS  Google Scholar 

  • Wang, J., M. Zhang, J. Xu & Y. Wang, 1995. Reciprocal effect of Cu, Cd, Zn on a kind of marine alga. Water Research 29: 209–214.

    Article  CAS  Google Scholar 

  • Zhou, W., P. Juneau & B. Qiu, 2006. Growth and photosynthetic responses of the bloom-forming cyanobacterium Microcystis aeruginosa to elevated levels of cadmium. Chemosphere 65: 1738–1746.

    Article  PubMed  CAS  Google Scholar 

  • Zvezdanovic, J. & D. Markovic, 2009. Copper, iron, and zinc interactions with chlorophyll in extracts of photosynthetic pigments studied by VIS spectroscopy. Russian Journal of Physical Chemistry A 83: 1542–1546.

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by the Spanish Ministry project FLUVIALFITOMARC (CGL2006-12785), FLUVIALMULTISTRESS (CTM2009-14111-C02-01), and the EC project KEYBIOEFFECTS (MRTN-CT-2006-035695). The authors express their thanks to the ‘Serveis Tècnics de Recerca’ of the University of Girona for offering their facilities and technical assistance during the metal analysis.

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Corcoll, N., Bonet, B., Leira, M. et al. Chl-a fluorescence parameters as biomarkers of metal toxicity in fluvial biofilms: an experimental study. Hydrobiologia 673, 119–136 (2011). https://doi.org/10.1007/s10750-011-0763-8

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