, Volume 698, Issue 1, pp 47–60 | Cite as

Resource ratio and human impact: how diatom assemblages in Lake Maggiore responded to oligotrophication and climatic variability

  • Giuseppe MorabitoEmail author
  • Alessandro Oggioni
  • Martina Austoni


Diatoms have been often used to track trophic changes from sedimentary records: recent studies demonstrated that these organisms can even be valuable indicators of climatic variability, although it is often difficult to discriminate the role of trophic and climatic drivers. Moving from the hypothesis that oligotrophication and climate affected the composition of the diatom assemblages by changing the resource ratio, we analysed the vernal diatoms succession in Lake Maggiore, between 1984 and 2007, using multivariate techniques (cluster analysis, canonical correspondence analysis, multivariate regression trees), in order to single out the oligotrophication effects from those attributable to climatic variability. Our results point out that Si, TP, temperature and wind emerged as key explanatory variables in species selection, with a stronger link between trophic and climatic drivers after the lake reached a stable oligotrophic status. Peculiar climate-driven events (deep mixing and floods) affected the in-lake Si:P ratio, giving an advantage to diatoms that are excellent P, but poor Si competitors. The classical role of Fragilaria and Tabellaria as early-warning indicators of eutrophication should be reconsidered, taking into account that both can be useful indicators of climate change, when links between their physiological resource needs and environmental data coming from robust limnological investigations can be established.


Diatoms Seasonal succession Oligotrophication Meteorological variability Nutrient ratio Climate change 

Supplementary material

10750_2012_1094_MOESM1_ESM.pdf (356 kb)
Supplementary material 1 (PDF 356 kb)


  1. Ambrosetti, W., L. Barbanti & A. Rolla, 2006a. Annuario dell’Osservatorio Meteorologico di Pallanza. 1997–2003. CNR Istituto per lo Studio degli Ecosistemi, Verbania Pallanza: 38 pp.Google Scholar
  2. Ambrosetti, W., L. Barbanti & A. Rolla, 2006b. Annuario dell’Osservatorio Meteorologico di Pallanza. 2004–2005. CNR Istituto per lo Studio degli Ecosistemi, Verbania Pallanza: 70 pp.Google Scholar
  3. Ambrosetti, W., L. Barbanti & A. Rolla, 2007. Annuario dell’Osservatorio Meteorologico di Pallanza. 2006. CNR Istituto per lo Studio degli Ecosistemi, Verbania Pallanza: 51 pp.Google Scholar
  4. Ambrosetti, W., L. Barbanti & A. Rolla, 2008. Annuario dell’Osservatorio Meteorologico di Pallanza. 2007. CNR Istituto per lo Studio degli Ecosistemi, Verbania Pallanza: 56 pp.Google Scholar
  5. Anderson, N., 2000. Diatoms, temperature and climatic change. European Journal of Phycology 35: 307–314.Google Scholar
  6. Anneville, O., S. Souissi, S. Gammeter & D. Straile, 2004. Seasonal and inter-annual scales of variability in phytoplankton assemblages: comparison of phytoplankton dynamics in three peri-alpine lakes over a period of 28 years. Freshwater Biology 49: 98–115.CrossRefGoogle Scholar
  7. Arca, G. & L. Barbanti, 1986. Annuario 1984 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 10: 81 pp.Google Scholar
  8. Arca, G. & L. Barbanti, 1987. Annuario 1985 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 13: 81 pp.Google Scholar
  9. Arca, G. & L. Barbanti, 1989. Annuario 1986 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 20: 83 pp. Google Scholar
  10. Arca, G. & L. Barbanti, 1989. Annuario 1987 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 21: 83 pp.Google Scholar
  11. Arca, G. & L. Barbanti, 1990. Annuario 1988 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 25: 88 pp.Google Scholar
  12. Arca, G. & L. Barbanti, 1991. Annuario 1989 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 31: 79 pp.Google Scholar
  13. Baldi, E., 1949. La situation actuelle de la recherche limnologique après le Congrès de Zurich. Revue suisse Hydrologie 11: 637–649.Google Scholar
  14. Barbanti, L., 1992. Annuario 1990 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 34: 77 pp. Google Scholar
  15. Barbanti, L., 1993. Annuario 1991 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 41: 72 pp.Google Scholar
  16. Barbanti, L., 1994. Annuario 1992 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 48: 80 pp.Google Scholar
  17. Barbanti, L., 1995. Annuario 1993 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 52: 72 pp.Google Scholar
  18. Barbanti, L., 1995. Annuario 1994 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 53: 74 pp.Google Scholar
  19. Barbanti, L., 1996. Annuario 1995 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 58: 70 pp. Google Scholar
  20. Barbanti, L., 1997. Annuario 1996 dell’Osservatorio Meteorologico di Pallanza. Documenta, Istituto Italiano di Idrobiologia, 62: 68 pp.Google Scholar
  21. Bennion, H. & R. Battarbee, 2007. The European Union Water Framework Directive: opportunities for palaeolimnology. Journal of Paleolimnology 38: 285–295.CrossRefGoogle Scholar
  22. Bigler, C., L. von Gunten, A. F. Lotter, S. Hausmann, A. Blass, C. Ohlendorf & M. Sturm, 2007. Quantifying human-induced eutrophication in Swiss mountain lakes since AD 1800 using diatoms. Holocene 17: 1141–1154.CrossRefGoogle Scholar
  23. Birks, H., V. Jones & N. Rose, 2004. Recent environmental change and atmospheric contamination on Svalbard as recorded in lake sediments—an introduction. Journal of Paleolimnology 31: 403–410.CrossRefGoogle Scholar
  24. Bray, J. R. & J. T. Curtis, 1957. An ordination of the upland forest communities of Southern Wisconsin. Ecological Monographs 27: 325–349.CrossRefGoogle Scholar
  25. Breiman, L., J. H. Friedman, R. A. Olshen & C. J. Stone, 1984. Classification and Tree Regression. Wadsworth and Brooks/Cole, Monterey.Google Scholar
  26. de Bernardi, R., G. Giussani, M. Manca & D. Ruggiu, 1988. Long-term dynamics of plankton communities in Lago Maggiore (N. Italy). Verhandlungen Internationale Vereinigung Limnologie 23: 729–733.Google Scholar
  27. De’ath, G., 2002. Multivariate Regression Trees: a new technique for modelling species-environments relationships. Ecology 83: 1105–1117.Google Scholar
  28. Dokulil, M. T. & K. Teubner, 2005. Do phytoplankton communities correctly track trophic changes? An assessment using directly measured and palaeolimnological data. Freshwater Biology 50: 1594–1604.CrossRefGoogle Scholar
  29. Dokulil, M. T. & Teubner, 2011. Eutrophication and climate change: present situation and future scenarios. In Ansari, A. A., S. Singh Gill, G. R. Lanza & W. Rast (eds), Eutrophication: Causes, Consequences and Control, 1st ed. Springer, Berlin: 1–16.Google Scholar
  30. Dokulil, M. T., K. Teubner, A. Jagsch, U. Nickus, R. Adrian, D. Straile, T. Jankowski, A. Herzig & J. Padisák, 2009. The impact of climate change in Central Europe. In George, D. G. (ed.), The Impact of Climate Change on European lakes. Aquatic Ecology Series, Vol. 4. Springer, Dordrecht: 387–409.Google Scholar
  31. Gibson, C. E., 1981. Silica budgets and the ecology of planktonic diatoms in an unstratified Lake (Lough Neagh, N. Ireland). Internationale Revue der Gesamten Hydrobiologie 66: 641–664.CrossRefGoogle Scholar
  32. Guilizzoni, P., G. Bonomi, G. Galanti & D. Ruggiu, 1983. Relationship between sedimentary pigments and primary production: evidence from core analyses of twelve Italian lakes. Hydrobiologia 103: 103–106.CrossRefGoogle Scholar
  33. Kamenir, Y. & G. Morabito, 2009. Lago Maggiore oligotrophication as seen from the long-term evolution of its phytoplankton taxonomic size structure. Journal of Limnology 68: 146–161.CrossRefGoogle Scholar
  34. Kilham, S. E., S. S. Kilham & R. E. Hecky, 1986. Hypothesized resource relationships among African planktonic diatoms. Limnology Oceanography 31: 1169–1181.CrossRefGoogle Scholar
  35. Kilham, S. E., Theriot & S. Fritz, 1996. Linking planktonic diatoms and climate change in the large lakes of the Yellowstone ecosystem using resource theory. Limnology and Oceanography 41: 1052–1062.CrossRefGoogle Scholar
  36. Kirilova, E. P., P. Bluszcz, O. Heiri, H. Cremer, C. Ohlendorf, A. F. Lotter & B. Zolitschka, 2008. Seasonal and interannual dynamics of diatom assemblages in Sacrower See (NE Germany): a sediment trap study. Hydrobiologia 614: 159–170.CrossRefGoogle Scholar
  37. Kirilova, E. P., O. Heiri, P. Bluszcz, B. Zolitschka & A. F. Lotter, 2011. Climate-driven shifts in diatom assemblages recorded in annually laminated sediments of Sacrower See (NE Germany). Aquatic Sciences 73: 201–210.CrossRefGoogle Scholar
  38. Köster, D. & R. Pienitz, 2006. Seasonal diatom variability and paleolimnological inferences—a case study. Journal of Paleolimnology 35: 395–416.CrossRefGoogle Scholar
  39. Leitao, M., S. Morata, S. Rodriguez & J. Vergon, 2003. The effect of perturbations on phytoplankton assemblages in a deep reservoir (Vouglans, France). Hydrobiologia 502: 73–83.CrossRefGoogle Scholar
  40. Makulla, A. & U. Sommer, 1993. Relationships between resource ratios and phytoplankton species composition during spring in 5 North German lakes. Limnology and Oceanography 38: 846–856.CrossRefGoogle Scholar
  41. Manca, M. & D. Ruggiu, 1998. Consequences of pelagic food-web changes during a long-term lake oligotrophication process. Limnology and Oceanography 43: 1368–1373.CrossRefGoogle Scholar
  42. Manca, M., A. Calderoni & R. Mosello, 1992. Limnological research in Lago Maggiore: studies on hydrochemistry and plankton. Memorie Istituto Italiano Idrobiologia 50: 171–200.Google Scholar
  43. Manca, M., N. Cavicchioni & G. Morabito, 2000. First observations on the effect of complete overturn of Lake Maggiore on plankton and primary production. International Review of Hydrobiology 85: 209–222.CrossRefGoogle Scholar
  44. Manca, M., M. Portogallo & M. E. Brown, 2007. Shifts in phenology of Bythotrephes longimanus and its modern success in Lake Maggiore as a result of changes in climate and trophy. Journal of Plankton Research 29: 515–525.CrossRefGoogle Scholar
  45. Marchetto, A., A. Lami, S. Musazzi, J. Massaferro, L. Langone & P. Guilizzoni, 2004. Lake Maggiore (N. Italy) trophic history: fossil diatom, plant pigments, and chironomids, and comparison with long-term limnological data. Quaternary International 113: 97–110.CrossRefGoogle Scholar
  46. Morabito, G., 2001. Relationships between phytoplankton dynamics in Lake Maggiore and local climate in the period 1978–’98. Atti Associazione Italiana Oceanologia e Limnologia 14: 147–156.Google Scholar
  47. Morabito, G. & A. Pugnetti, 2000. Primary productivity and related variables in the course of the trophic evolution of Lake Maggiore. Verhandlungen Internationale Vereinigung der Limnologie 27: 2934–2937.Google Scholar
  48. Nõges, P., R. Adrian, O. Anneville, L. Arvola, T. Blenckner, G. George, T. Jankowski, M. Järvinen, S. Maberly, J. Padisák, D. Straile, K. Teubner & G. Weyhenmeyer, 2009. The impact of variations in the climate on seasonal dynamics of phytoplankton. In George, D. G. (ed.), The Impact of Climate Change on European Lakes. Aquatic Ecology Series, Vol. 4. Springer, Dordrecht: 253–274.Google Scholar
  49. Ravera, O. & R. A. Vollenweider, 1968. Oscillatoria rubescens D.C. as an indicator of Lago Maggiore eutrophication. Schweizerische Zeitschrift Hydrologie 30: 374–380.Google Scholar
  50. R Development Core Team, 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0,
  51. Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.Google Scholar
  52. Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cambridge University Press, New York.CrossRefGoogle Scholar
  53. Ruggiu, D., G. Morabito, P. Panzani & A. Pugnetti, 1998. Trends and relations among basic phytoplankton characteristics in the course of the long-term oligotrophication of Lake Maggiore (Italy). Hydrobiologia 370: 243–257.CrossRefGoogle Scholar
  54. Rühland, K., A. M. Paterson & J. P. Smol, 2008. Hemispheric-scale patterns of climate-related shifts in planktonic diatoms from North American and European lakes. Global Change Biology 14: 2740–2754.Google Scholar
  55. Salmaso, N., 1996. Seasonal variation in the composition and rate of change of the phytoplankton community in a deep subalpine lake (Lake Garda, Northern Italy). An application of nonmetric multidimensional scaling and cluster analysis. Hydrobiologia 337: 49–68.CrossRefGoogle Scholar
  56. Salmaso, N., 2005. Effects of climatic fluctuations and vertical mixing on the interannual trophic variability of Lake Garda, Italy. Limnology and Oceanography 50: 553–565.CrossRefGoogle Scholar
  57. Saros, J., S. Interlandi, A. Wolfe & D. Engstrom, 2003. Recent changes in the diatom community structure of lakes in the Beartooth Mountain Range, USA. Arctic Antarctic and Alpine Research 35: 18–23.CrossRefGoogle Scholar
  58. Schindler, D. W., 2001. The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Canadian Journal Fisheries and Aquatic Sciences 58: 18–29.CrossRefGoogle Scholar
  59. Smol, J., A. P. Wolfe, H. J. B. Birks, M. S. V. Douglas, V. J. Jones, A. Korhola, R. Pienitz, K. Rühland, S. Sorvari, D. Antoniades, S. J. Brooks, M. Fallu, M. Hughes, B. E. Keatley, T. E. Laing, N. Michelutti, L. Nazarova, M. Nyman, A. M. Paterson, B. Perren, R. Quinlan, M. Rautio, E. Saulnier-Talbot, S. Siitonen, N. Solovieva & J. Weckström, 2005. Climate-driven regime shifts in the biological communities of arctic lakes. Proceedings of the National Academy of Sciences of the United States of America 102: 4397–4402.PubMedCrossRefGoogle Scholar
  60. Sommer, U., 1988. Growth and survival strategies of planktonic diatoms. In Sandgren, C. D. (ed.), Growth and reproductive strategies of freshwater phytoplankton. Cambridge University Press, Cambridge: 227–260.Google Scholar
  61. Sommer, U., 1993. Phytoplankton competition in PluBsee: a field test of the resource-ratio hypothesis. Limnology & Oceanography 38: 838–845.CrossRefGoogle Scholar
  62. Tartari, G. A. & R. Mosello, 1997. Metodologie analitiche e controlli di qualità nel laboratorio chimico dell’Istituto Italiano di Idrobiologia. Documenta, Istituto Italiano di Idrobiologia 60: 160 pp.Google Scholar
  63. ter Braak, C. J. F. & P. Smilauer, 2002. CANOCO Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca.Google Scholar
  64. Tilman, D., S. S. Kilham & P. Kilham, 1982. Phytoplankton community ecology: the role of limiting nutrients. Annual Review of Ecology and Systematics 13: 349–372.CrossRefGoogle Scholar
  65. Wessels, M., K. Mohaupt, R. Kummerlin & A. Lenhard, 1999. Reconstructing past eutrophication trends from diatoms and biogenic silica in the sediment and the pelagic zone of Lake Constance, Germany. Journal of Paleolimnology 21: 171–192.CrossRefGoogle Scholar
  66. Winder, M. & D. A. Hunter, 2008. Temporal organization of phytoplankton communities linked to physical forcing. Oecologia 156: 179–192.PubMedCrossRefGoogle Scholar
  67. Znachor, P., E. Zapomelova, K. Rehakova, J. Nedoma & K. Simek, 2008. The effect of extreme rainfall on summer succession and vertical distribution of phytoplankton in a lacustrine part of a eutrophic reservoir. Aquatic Sciences 70: 77–86.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Giuseppe Morabito
    • 1
    Email author
  • Alessandro Oggioni
    • 1
    • 2
  • Martina Austoni
    • 1
  1. 1.CNR, Istituto per lo Studio degli EcosistemiVerbania-PallanzaItaly
  2. 2.Unità Organizzativa di SupportoCNR – Istituto per il Rilevamento Elettromagnetico dell’AmbienteMilanoItaly

Personalised recommendations