Comparison of morpho-functional phytoplankton classifications in human-impacted shallow lakes with different stable states

  • Irina Izaguirre
  • Luz Allende
  • Roberto Escaray
  • José Bustingorry
  • Gonzalo Pérez
  • Guillermo Tell
Part of the Developments in Hydrobiology book series (DIHY, volume 221)


The morpho-functional classifications of phytoplankton have been recently proposed as useful tools in the aquatic biomonitoring. In this study, we compared three different classifications in a range of different environmental conditions, a set of six shallow lakes with different stable states. The studied lakes are located in the Pampa Plain from Argentina, a region highly impacted as a consequence of the human activities. Among the selected lakes, three are in a turbid state, two of which have high phytoplankton abundances (phytoplankton-turbid), and one shows a high concentration of suspended inorganic matter (inorganic-turbid). Two lakes are clear and profusely colonized by submerged plants (clear-vegetated). Only one lake shows a typical alternative steady-state behavior, shifting turbid periods of high phytoplankton biomass with periods of more transparency and development of submerged macrophytes. We compared the three morpho-functional classifications applied by means of multivariate analyses in order to explore how much the variance of the biomass of the phytoplankton functional groups (for each functional classification) was explained by the environmental variables. The analyses performed showed a clear separation of the human-impacted turbid lakes from the clear-vegetated lakes. The advantages and disadvantages of the different morpho-functional classifications are discussed, concluding that the functional approach is adequate to analyze the phytoplankton communities in aquatic systems subjected to anthropogenic influence and for monitoring them.


Phytoplankton morpho-functional classifications Alternative steady states Shallow lakes Human impact Pampa Plain 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allende, L., G. Tell, H. Zagarese, A. Torremorell, G. Pérez, J. Bustingorry, R. Escaray & I. Izaguirre, 2009. Phytoplankton and primary production in clear-vegetated, inorganic-turbid and algal-turbid shallow lakes from the Pampa plain (Argentina). Hydrobiologia 624: 45–60.CrossRefGoogle Scholar
  2. APHA AWWA WEF, 2005. Standard Methods for the Examination of Water & Wastewater. American Public Health Association, American Water Works Association, Water Environment Federation, Washington.Google Scholar
  3. Cano, M. G., M. A. Casco, L. C. Solari, M. E. Mac Donagh, N. A. Gabellone & M. C. Claps, 2008. Implications of rapid changes in chlorophyll-a of plankton, epipelon and epiphyton in a Pampean shallow lake: an interpretation in terms of a conceptual model. Hydrobiologia 614: 33–45.CrossRefGoogle Scholar
  4. Devercelli, M., 2006. Phytoplankton of the middle Paraná River during an anomalous hydrological period: a morphological and functional approach. Hydrobiologia 563: 465–478.CrossRefGoogle Scholar
  5. Gleason, H. A., 1926. The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club 53: 7–26.CrossRefGoogle Scholar
  6. Hillebrand, H., C. D. D. Dürselen, U. Kirschtel, T. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.CrossRefGoogle Scholar
  7. Huisman, J., R. R. Jonker, C. Zonneveld & F. J. Weissing, 1999. Competition for light between phytoplankton species: experimental tests of mechanistic theory. Ecology 80: 211–222.CrossRefGoogle Scholar
  8. Hurley, J. P., 1988. Analysis of aquatic pigments by high performance liquid chromatography. Journal of Analytical Purification 3: 12–16.Google Scholar
  9. Izaguirre, I. & A. Vinocur, 1994. Typology of shallow lakes of the Salado River basin (Argentina), based on phytoplankton communities. Hydrobiologia 277: 49–62.CrossRefGoogle Scholar
  10. Jobbágy, E. G., M. D. Nosetto, C. S. Santoni & G. Baldi, 2008. El desafío ecohidrológico de las transiciones entre sistemas leñosos y herbáceos en la llanura Chaco-Pampeana. Ecología Austral 18: 305–322.Google Scholar
  11. Kruk, C., N. Mazzeo, G. Lacerot & C. S. Reylnolds, 2002. Classification schemes for phytoplankton: a local validation of a functional approach to the analysis of species temporal replacement. Journal of Plankton Research 24: 901–912.CrossRefGoogle Scholar
  12. Kruk, C., V. L. M. Huszar, E. T. H. M. Peeters, S. Bonilla, L. Costa, M. Lürling, C. S. Reynolds & M. Scheffer, 2010. A morphological classification capturing functional variation in phytoplankton. Freshwater Biology 55: 614–627.CrossRefGoogle Scholar
  13. Kruk, C., E. T. H. M. Peeters, E. H. Van Nes, V. L. M. Huszar, L. S. Costa & M. Scheffer, 2011. Phytoplankton community composition can be predicted best in terms of morphological groups. Limnology and Oceanography 56: 110–118.CrossRefGoogle Scholar
  14. Laurion, I., A. Lami & R. Sommaruga, 2002. Distribution of mycosporine-like aminoacids and photoprotective carotenoids among freshwater phytoplankton assemblages. Aquatic Microbial Ecology 26: 283–294.CrossRefGoogle Scholar
  15. Litchman, E., P. de Tezanos Pinto, C. A. Klausmeier, M. K. Thomas & K. Yoshiyama, 2010. Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653: 15–28.CrossRefGoogle Scholar
  16. Llames, M. E., L. Lagomarsino, N. Diovisalvi, P. Fermani, A. M. Torremorell, G. Pérez, F. Unrein, J. Bustingorry, R. Escaray, M. Ferraro & H. Zagarese, 2009. The effects of light availability in shallow, turbid waters: a mesocosm study. Journal of Plankton Research 31: 1517–1529.CrossRefGoogle Scholar
  17. Mantoura, R. F. C. & C. A. Llewellyn, 1983. The rapid determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase high-performance liquid chromatography. Analytica Chimica Acta 151: 297–314.CrossRefGoogle Scholar
  18. Margalef, R., 1978. Life forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1: 493–509.Google Scholar
  19. Naselli-Flores, L. & R. Barone, 2011. Fight on plankton! Or, phytoplankton shape and size as adaptive tools to get ahead in the struggle for life. Cryptogamie, Algologie 32: 157–204.Google Scholar
  20. Naselli-Flores, L., J. Padisák, M. T. Dokulil & I. Chorus, 2003. Equilibrium/steady-state concept in phytoplankton ecology. Hydrobiologia 502: 395–403.CrossRefGoogle Scholar
  21. Padisák, J., L. O. Crossetti & L. Naselli-Flores, 2009. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621: 1–19.CrossRefGoogle Scholar
  22. Pérez, G. L., A. Torremorell, J. Bustingorry, R. Escaray, P. Pérez, M. Diéguez & H. Zagarese, 2010. Optical characteristics of shallow lakes from the Pampa and Patagonia regions of Argentina. Limnologica 40: 30–39.CrossRefGoogle Scholar
  23. Quirós, R. & E. Drago, 1999. The environmental state of Argentinean lakes: an overview. Lakes and Reservoirs: Research and Management 4: 55–64.CrossRefGoogle Scholar
  24. Quirós, R., A. M. Renella, M. B. Boveri, J. J. Rosso & A. Sosnovsky, 2002. Factores que afectan la estructura y el funcionamiento de las lagunas pampeanas. Ecología Austral 12: 175–185.Google Scholar
  25. Quirós, R., M. B. Boveri, C. A. Petrachi, A. M. Renella, J. J. Rosso, A. Sosnovsky & H. T. von Bernard, 2006. Los efectos de la agriculturización del humedal pampeano sobre la pampeano sobre la eutrofización de sus lagunas. In Tundisi, J. G. T., Matsumura-Tundisi & C. Sidagis Galli (eds), Eutrofização na América do Sul: Causas, conseqüèncias e tecnologias de gerenciamento e controle: 1–16.Google Scholar
  26. Reynolds, C. S., 1980. Phytoplankton assemblages and their periodicity in stratifying lake systems. Holarctic Ecology 3: 141–159.Google Scholar
  27. Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.Google Scholar
  28. Reynolds, C. S., 1997. Vegetation Processes in the Pelagic: A Model for Ecosystem Theory. Excellence in Ecology. Ecology Institute, Oldendorf/Luhe.Google Scholar
  29. Reynolds, C. S., 1998. What factors influence the species composition of phytoplankton in lakes of different trophic status. Hydrobiologia 369(370): 11–26.CrossRefGoogle Scholar
  30. Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  31. Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Melo, 2002. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24: 417–428.CrossRefGoogle Scholar
  32. Salmaso, N. & J. Padisák, 2007. Morpho-functional groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578: 97–112.CrossRefGoogle Scholar
  33. Sarmento, H. & J.-P. Descy, 2008. Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes. Journal of Applied Phycology 20: 1001–1011.CrossRefGoogle Scholar
  34. Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology and Evolution 8: 275–279.PubMedCrossRefGoogle Scholar
  35. Sharp, J. H., E. T. Peltzer, M. J. Alperin, G. Cauwet, J. W. Farrington, B. Fry, D. M. Karl, J. H. Martin, A. Spitzy, S. Tugrul & C. A. Carlson, 1993. Procedures subgroup report. Marine Chemistry 41: 37–49.CrossRefGoogle Scholar
  36. Sierra, E. M., M. E. Fernández Long & C. Bustos, 1994. Cronología de inundaciones y sequías en el noreste de la provincia de Buenos Aires 1911–89. Revista de la Facultad de Agronomía 14: 241–249.Google Scholar
  37. Silvoso, J., I. Izaguirre & L. Allende, 2011. Picoplankton structure in clear and turbid eutrophic shallow lakes: a seasonal study. Limnologica 41: 181–190.CrossRefGoogle Scholar
  38. Søndergaard, M. & B. Moss, 1998. Impact of submerged macrophytes on phytoplankton in shallow freshwater lakes. Ecological Studies 131: 115–132.CrossRefGoogle Scholar
  39. Stomp, M., J. Huisman, F. de Jongh, A. J. Veraart, D. Gerla, M. Rijkeboer, B. W. Ibelings, U. I. A. Wollenzien & L. J. Stal, 2004. Adaptive divergence in pigment composition promotes phytoplankton biodiversity. Nature 432: 104–107.PubMedCrossRefGoogle Scholar
  40. Sun, J. & D. Liu, 2003. Geometric models for calculating cell biovolumen and surface area for phytoplankton. Journal of Plankton Research 25: 1331–1346.CrossRefGoogle Scholar
  41. ter Braak, C. J. F., 1988. CANOCO – a FORTRAN program for canonical community ordination by [partial] [detrended] [canonical] corresoondence analysis, principal components analysis and redundancy analysis. Report LWA-88-02, Agricultural Mathematics Group, Wageningen.Google Scholar
  42. Tolotti, M., E. Rott, H. Thies & R. Psenner, 2005. Functional species groups of phytoplankton in relation to lake restoration: a long term study of Piburger See, Austria. Verhandlungen der Vereingung fuer theorestische und angewandte Limnologie 29: 891–894.Google Scholar
  43. Torremorell, A., J. Bustingorry, R. Escaray & H. Zagarese, 2007. Seasonal dynamics of a large, shallow lake, laguna Chascomús: the role of light limitation and other physical variables. Limnologica 37: 100–108.CrossRefGoogle Scholar
  44. Torremorell, A., M. E. Llames, G. L. Pérez, R. Escaray, J. Bustingorry & H. Zagarese, 2009. Annual patterns of phytoplankton density and primary production in a large, shallow lake: the central role of light. Freshwater Biology 54: 437–449.CrossRefGoogle Scholar
  45. Utermöhl, H., 1958. Zur Vervollkommnung der quantitative Phytoplankton Methodik. Mitteilungen Internationale Vereinigung Limnologie 9: 1–38.Google Scholar
  46. Venrick, E. L., 1978. How many cells to count? In Sournia, A. (ed.), Phytoplankton Manual. UNESCO, Paris: 167–180.Google Scholar
  47. Weithoff, G., 2003. The concepts of ‘plant functional types’ and ‘functional diversity’ in lake phytoplankton – a new understanding of phytoplankton ecology? Freshwater Biology 48: 1669–1675.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Irina Izaguirre
    • 1
    • 2
  • Luz Allende
    • 1
    • 2
  • Roberto Escaray
    • 3
  • José Bustingorry
    • 3
  • Gonzalo Pérez
    • 2
    • 3
  • Guillermo Tell
    • 1
    • 2
  1. 1.Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina
  3. 3.Instituto de Investigaciones Biotecnológicas, Instituto Tecnológico de Chascomús (IIB-INTECH), CONICETChascomúsArgentina

Personalised recommendations