Brazilian Journal of Biological Sciences (ISSN 2358-2731)

Home Archive v. 3, no. 5 (2016) Cochero


Vol. 3, No. 5, p. 165-179 - Jun. 30, 2016


Fluvial biofilm responses to joint changes in nutrients, temperature, turbidity and water velocity: an ex situ experiment

Joaquín Cochero and Nora Gómez

The aim of this study was to explore the responses of the epipelic biofilm of a Pampean stream with little impact from human activity to two environmental conditions, with joint modifications in nutrients, temperature, water velocity and turbidity. The experiment was conducted using artificial channels and lasted five weeks. The biological variables measured included chlorophyll-a content, bacterial biomass, ash-free dry weight, total carbohydrate concentration, total respiratory activity, and biofilm composition. Results show that the species' composition of the biofilm was affected, although no other structural or metabolic variables measured were. These results highlight the importance of including structural parameters to measure rapid changes in water quality, even when analyzing the effects of co-occurring variables.

Epipelic biofilms; Water quality; Artificial channels; Temperature; Nutrients.


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APHA. Standard methods for examination of water and wastewater. 20 ed. Washington: American Public Health Association, American Water Works Association and Water Pollution Control Federation, 1998.

Artigas, J.; García-Berthou, E.; Bauer, D. E.; Castro, M. I.; Cochero, J.; Colautti, D. C.; Cortelezzi, A.; Donato, J. C.; Elosegi, A.; Feijoó, C. Global pressures, specific responses, effects of nutrient enrichment in streams from different biomes. Environmental Research Letters, v. 8, no. 1, 13 p, 2013.

Bakeman R. Recommended effect size statistics for repeated measures designs. Behaviour Research and Methods, v. 37, no. 3, p. 379-384, 2005.

Bartram, J.; Ballance, R. (Eds.). Water quality monitoring: A practical guide to the design and implementation of freshwater quality studies and monitoring programmes. London: UNESCO, WHO and UNEP, 1996. Available from: <>. Accessed in: Feb. 08, 2016.

Blenkinsopp, S. A.; Lock, M. A. The measurement of electron transport system activity in river biofilms. Water Research, v. 24, p. 441-445, 1990.

Bonnineau, C.; Guasch, H.; Proia, L.; Ricart, M.; Geiszinger, A.; Romaní, A. M.; Sabater, S. Fluvial biofilms: a pertinent tool to assess Β-blockers toxicity. Aquatic Toxicology, v. 96, no. 3, p. 225-233, 2010. .

Bourrelly, P. Les algues d'eau douce. Tome I: Algues vertes. Paris: éditions N. Boubée & Cie., 1966.

Bourrelly, P. Les algues d'eau douce. Tome II: Algues jaunes et brunes. Paris: éditions N. Boubée & Cie., 1968.

Bourrelly, P. Les algues d'eau douce. Tome III: Algues bleues et rouges. Paris: éditions N. Boubée & Cie., 1970.

Bratbak, G.; Dundas, I. Bacterial dry matter content and biomass estimations. Appl. Environmental Microbiology, v. 48, no. 4, p. 755-757, 1984.

Breitburg, D. L.; Baxter, J. W.; Hatfield, C.; Howarth, R. W.; Jones, C. G.; Lovett, G. M.; Wigand, C. Understanding effects of multiple stressors: ideas and challenges. In: Pace, M.; Groffman, P. (Eds.). Successes, limitations and frontiers in ecosystem science. New York: Springer, 1998. p. 416-431.

Clarke, K. R. Non parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, v. 18, p. 117-143, 1993.

Cochero, J.; Romaní, A. M.; Gómez, N. Delayed response of microbial epipelic biofilm to nutrient addition in a Pampean stream. Aquatic Microbial Ecology, v. 69, no. 2, p. 145-155, 2013.

Cohen, J. Statistical power analysis for the behavioral sciences. 2. ed. New York: Academic Press, 1988.

Crain, C. M. Interactions between marsh plant species vary in direction and strength depending on environmental and consumer context. Journal of Ecology, v. 96, no. 1, p. 166-173, 2008.

Davies-Colley, R. J.; Smith, D. G. Turbidity, suspended sediment, and water clarity, a review. Journal of American Water Resources, v. 37, no. 5, p. 1085-1101, 2001.

Davies-Colley, R. J.; Quinn, J. M.; Hickey, C. W.; Ryan, P. A. Effects of clay discharges on streams. 1. Optical properties and epilithon. Hydrobiologia, v. 248, no. p. 215-234, 1992.

Dodds, W. K.; Smith, V. H.; Lohman, K. Nitrogen and phosphorus relationships to benthic algal biomass in temperate streams. Canadian Journal of Fisheries and Aquatic Sciences, v. 59, no. 5, p. 865-874, 2002.

Dubois, M.; Gilles, K. A.; Hamilton, J. K.; Rebers, P. A.; Smith, F. Colorimetric method for determination of sugars and related substances. Analytical Chemistry, v. 28, no. 3, p. 350-356, 1956.

Feijoó, C. S.; Lombardo, R. J. Baseline water quality and macrophyte assemblages in Pampean streams: a regionnal approach. Water Research, v. 41, no. 7, p. 1399-1410, 2007.

Freeman, C.; Lock, M. A. The biofilm polysaccharide matrix: a buffer against changing organic substrate supply? Limnology and Oceanography, v. 40, no. 2, p. 273-278, 1995.

Giorgi, A.; Feijoó, C.; Tell, G. Primary producers in a Pampean stream: temporal variation and structuring role. Biodiversity & Conservation, v. 14, no. 7, p. 1699-1718, 2005.

Gómez, N.; Sierra, M. V.; Cortelezzi, A.; Rodrigues Capítulo, A. Effects of discharges from the textile industry on the biotic integrity of benthic assemblages. Ecotoxicology and Environmental Safety, v. 69, no. 3, p. 472-479, 2008. 10.1016/j.ecoenv.2007.03.007

Gómez, N.; Donato, J. C.; Giorgi, A.; Guasch, H.; Mateo, P.; Sabater, S. La biota de los ríos: los microorganismos autótrofos. In: Elosegui, A.; Sabater, S. Conceptos y técnicas en ecología fluvial. Bilbao: Fundación BBVA, 2009. p. 219-242. Available from: <>. Accessed in: Feb. 08, 2016.

Guasch, H.; Martí, E.; Sabater, S. Nutrient enrichment effects on biofilm Metabolism in a Mediterranean stream. Freshwater Biology, v. 33, p. 373-383, 1995.

Halpern, B. S.; Selkoe, K. A.; Micheli, F.; Kappel, C. V. Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conservation Biology, v. 21, no. 5, p. 1301-1315, 2007.

Halpern, B. S.; McLeod, K. L.; Rosenberg, A. A.; Crowder, L. B. Managing for cumulative impacts in ecosystem-based management through ocean zoning. Ocean & Coastal Management, v. 51, no. 3, p. 203-211, 2008.

Horner, R. R.; Welch, E. B. Stream periphyton development in relation to current velocity and nutrients. Canadian Journal of Fisheries and Aquatic Sciences, v. 38, p. 449-457, 1981.

Horner, R. R.; Welch, E. B.; Seeley, M. R.; Jacoby, J. M. Responses of periphyton to changes in current velocity, suspended sediment and phosphorus concentration. Freshwater Biology, v. 24, no. 2, p. 215-232, 1990.

Hulme, M.; Sheard, N. Climate change scenarios for Argentina. Norwich, UK: Climatic Research Unit, 1999.

INDEC - Instituto Nacional de Estadística y Censos. Censo Nacional de Población, Hogares y Viviendas 2010. Available from: <>. Accessed in: Feb. 08, 2016.

Komárek, J.; Anagnostidis, K. Cyanoprokaryota. 1. Teil: Chroococcales. Jena-Stuttgart-Lübeck-Ulm, Germany: Gustav Fischer, 1999.

Komárek, J.; Anagnostidis, K. Cyanoprokaryota. 2. Teil: Oscillatoriales. Jena-Stuttgart-Lübeck-Ulm, Germany: Gustav Fischer, 2005.

Krammer, K.; Lange-Bertalot, H. Süßwasswasserflora von Mitteleuropa, Bacillariophyceae. 1: Naviculaceae. Stuttgart: Gustav Fischer Verlag, 1986.

Krammer, K.; Lange-Bertalot, H. Süßwasswasserflora von Mitteleuropa, Bacillariophyceae. 2: Bacillariaceae, Epithemiaceae, Surirellaceae. Stuttgart: Gustav Fischer Verlag, 1988.

Krammer, K.; Lange-Bertalot, H. Süßwasswasserflora von Mitteleuropa, Bacillariophyceae. 3: Centrales, Fragilariaceae, Eunotiaceae. Stuttgart: Gustav Fischer Verlag, 1991a.

Krammer, K.; Lange-Bertalot, H. Süßwasswasserflora von Mitteleuropa, Bacillariophyceae. 4: Achnanthaceae, Literaturverzeichnis. Stuttgart: Gustav Fischer Verlag, 1991b.

Labat, D.; Goddéris, Y.; Probst, J. L.; Guyot, J. L. Evidence for global runoff increase related to climate warming. Advances in Water Resources, v. 27, no. 6, p. 631-642, 2004. Available from: <>. Accessed in: Feb. 08, 2016.

Lange, K.; Townsend, C. R.; Matthaei, C. D. Can biological traits of stream invertebrates help disentangle the effects of multiple stressors in an agricultural catchment? Freshwater Biology, v. 59, no. 12, p. 2431-2446, 2014.

Licursi, M.; Gómez, N. Benthic diatoms and some environmental conditions in three lowland streams. Annales de Limnologie - International Journal of Limnology, v. 38, no. 2, p. 109-118, 2002. Available from: <>. Accessed in: Feb. 08, 2016.

Licursi, M.; Gómez, N.; Sabater, S. Effects of nutrient enrichment on epipelic diatom assemblages in a nutrient-rich lowland stream, Pampa Region, Argentina. Hydrobiologia, v. 766, no. 1, p. 135-150, 2016.

Lock, M. A.; Wallace, R. R.; Costerton, J. W.; Ventullo, R. M.; Charlton, S. E. River epilithon, toward a structural-functional model. Oikos, v. 42, p. 10-22, 1984.

Malmqvist, B.; Rundle, S. Threats to the running water ecosystems of the world. Environmental Conservation, v. 29, no. 2, p. 134-153, 2002.

Marxsen, J.; Witzel, K. P. Significance of extracellular enzymes for organic matter degradation and nutrient regeneration in small streams. In: Chróst, R. J. (Ed.). Microbial enzymes in aquatic environments. New York: Springer-Verlag, 1991. p. 270-285.

Meybeck, M. Carbon, nitrogen and phosphorus transport by world rivers. American J. Science, v. 282, p. 401-450, 1982.

Meybeck, M. Global chemical weathering of surficial rocks estimated from river dissolved loads. American J. Science, v. 287, 401-428, 1987.

Olapade, O. A.; Leff, L. G. Seasonal response of stream biofilm communities to dissolved organic matter and nutrient enrichments. Applied Environmental Microbiology, v. 71, no. 5, p. 2278-2287, 2005.

Olejnik, S.; Algina, J. Generalized eta and omega squared statistics, measures of effect size for some common research designs. Psychological Methods, v. 8, no. 4, p. 434-447, 2003.

Ormerod, S. J.; Dobson, M.; Hildrew, A. G.; Townsend, C. R. Multiple stressors in freshwater ecosystems. Freshwater Biology, v. 55, no. s1, p. 1-4, 2010.

Palmer, C. M. A composite rating of algae tolerating organic pollution. Journal of Phycology, v. 5, no. 1, p. 78-82, 1968.

Piggott, J. J.; Lange, K.; Townsend, C. R.; Matthaei, C. D. Multiple stressors in agricultural streams: a mesocosm study of interactions among raised water temperature, sediment addition and nutrient enrichment. PloS One, v. 7, no. 11, e49873, 2012.

Piggott, J. J.; Salis, R. K.; Lear, G.; Townsend, C. R.; Matthaei, C. D. Climate warming and agricultural stressors interact to determine stream periphyton community composition. Global Change Biology, v. 21, no. 1, p. 206-222, 2015.

Porter, K. G.; Feig, Y. G. The use of DAPI for identifying and counting aquatic microflora. Limnology & Oceanography, v. 41, p. 595-604, 1980.

Proia, L. Biofilm responses to multiple stressors associated to global change in river ecosystems. Girona: Universitat de Girona, 2012. (Ph.D. Thesis). Available from: <>. Accessed in: Feb. 08, 2016.

Revenga, C.; Campbell, I.; Abell, R.; de Villiers, P.; Bryer, M. Prospects for monitoring freshwater ecosystems towards the 2010 targets. Philosophical Transactions of the Royal Society B Biological Sciences, v. 360, no. 1454, p. 397-413, 2005.

Rodrigues Capítulo, A.; Gómez, N.; Giorgi, A. D. N.; Feijoó, C. Global changes in Pampean lowland streams (Argentina), implications for biodiversity and functioning. Hydrobiologia, v. 657, no. 1, p. 53-70, 2010.

Romaní, A. M.; Sabater, S. Influence of algal biomass on extracellular enzyme activity in river biofilms. Microbial Ecology, v. 41, no. 16, p. 16-24, 2000.

Romaní, A. M.; Artigas, J.; Camacho, A.; Graça, M. A. S.; Pascoal, C. La biota de los ríos, los microorganismos heterotróficos. In: Elosegui, A.; Sabater, S. (Eds.). Conceptos y técnicas en ecología fluvial. Bilbao: Fundación BBVA, 2009. p. 219-242. Available from: <>. Accessed in: Feb. 08, 2016.

Romaní, A. M.; Guasch, H.; Balaguer, M. D. Aquatic biofilms: ecology, water quality and wastewater treatment. Girona: Caister Academic Press, 2016.

Sierra, M. V.; Gómez, N.; Marano, A. V.; Di Siervi, M. A. Caracterización funcional y estructural del biofilm epipélico en relación al aumento de la urbanización en un arroyo de la Llanura Pampeana (Argentina). Ecología Austral, v. 23, no. 2, p. 108-118, 2013. Available from: <>. Accessed in: Feb. 08, 2016.

Sierra, M. V.; Gómez, N. Structural characteristics and oxygen consumption of the epipelic biofilm in three lowland streams exposed to different land uses. Water, Air, and Soil Pollution, v. 186, no. 1/4, p. 115-127, 2007.

Stevenson, R. J. An introduction to algal ecology in freshwater benthic habitats. In: Stevenson, R. J.; Bothwell, M. L.; Lowe, R. L.; Thorp, J. H. (Eds.). Algal ecology: freshwater benthic ecosystems. San Diego: Academic Press, 1996. p. 3-30.

Streble, H.; Krauter, D. Atlas de los microorganismos de agua dulce: la vida en una gota de agua. Barcelona: Omega, 1987.

Strickland, J. D. H.; Parsons, T. R. A practical handbook of seawater analysis: pigment analysis. Ottawa: B. Journal of the Fisheries Research Board of Canada, 1968.

Sutherland, I. W. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology, v. 147, pt. 1, p. 3-9, 2001.

Tell, G.; Conforti, V. Euglenophyta pigmentadas de la Argentina. Stuttgart: Gebruder Borntraeger Verlagsbuchhandlung, 1986.

Van Dam, H.; Mertens, A.; Sinkeldam, J. A coded checklist and ecological indicator values of freshwater diatoms from The Netherlands. Netherlands of Journal of Aquatic Ecology, v. 28, no. 1, p. 117-133, 1994.

Venter, O.; Brodeur, N. N.; Nemiroff, L.; Belland, B.; Dolinsek, I. J.; Grant, J. W. Threats to endangered species in Canada. Bioscience, v. 56, no. 11, p. 903-910, 2006. 56[903:TT

Villanueva, V. D.; Font, J.; Schwartz, T.; Romaní, A. M. Biofilm formation at warming temperature: acceleration of microbial colonization and microbial interactive effects. Biofouling, v. 27, no. 1, p. 59-71, 2011.

von Schiller, D.; Martí, E.; Riera, J. L.; Sabater, F. Effects of nutrients and light on periphyton biomass and nitrogen uptake in Mediterranean streams with contrasting land uses. Freshwater Biology, 52, no. 5, p. 891-906, 2007.

Winer, B. J. Statistical principles in experimental design. New York: McGraw Hill, 1971.