, Volume 644, Issue 1, pp 279–287 | Cite as

Long-term trends of epilimnetic and hypolimnetic bacteria and organic carbon in a deep holo-oligomictic lake

  • Roberto BertoniEmail author
  • Cristiana Callieri
  • Gianluca Corno
  • Serena Rasconi
  • Emanuele Caravati
  • Mario Contesini
Primary research paper


We analysed the long-term dynamics (1980–2007) of hypolimnetic and epilimnetic bacterial abundances and organic carbon concentrations, both dissolved (DOC) and particulate (POC), in the deep holo-oligomictic Lake Maggiore, included in the Southern Alpine Lakes Long-Term Ecological Research (LTER) site. During the 28 years of investigation, bacterial abundance and POC concentrations did not decrease with declining phosphorus concentrations, while DOC concentrations showed a pronounced decrease in the epi- and hypolimnion. We used the annual mean total lake heat content and total annual precipitation as climate-related variables, and in-lake total phosphorus as a proxy for trophic state. The model (forward stepwise regression, FSR) showed that reduced anthropogenic pressure was more significant than climate change in driving the trend in DOC concentrations. Bacterial dynamics in the hypolimnion mirrored the fluctuations observed in the epilimnion, but average cell abundance was three times lower. The FSR model indicates that bacterial number variability was dependent on POC in the epilimnion and DOC in the hypolimnion. In the hypolimnion, cell biovolumes for rod and coccal morphotypes were significantly larger than in the epilimnion.


Long-term dynamics DOC and POC Bacteria Cell biovolume Chlorophyll a Holo-oligomictic Lake Maggiore 



Some of the data presented came from research on Lake Maggiore supported by the International Commission for the Protection of Italian-Swiss Waters (CIPAIS). We are indebted to Michela Rogora for assistance during statistical analyses of long-term data and for providing data on phosphorus; and to Walter Ambrosetti, who provided data on the heat content of the lake and on annual precipitation.


  1. Albright, L. J. & S. K. McCrae, 1987. Annual cycle of bacterial specific biovolumes in Howe Sound, a Canadian West Coast fjord Sound. Applied Environmental Microbiology 53: 2739–2744.Google Scholar
  2. Ambrosetti, W. & L. Barbanti, 1999. Deep water warming in lakes: an indicator of climatic change. Journal of Limnology 58: 1–9.Google Scholar
  3. Ambrosetti, W., L. Barbanti & N. Sala, 2003. Residence time and physical processes in lake. Journal of Limnology 62: 1–15.Google Scholar
  4. Ambrosetti, W., L. Barbanti & A. Rolla, 2006. The climate of Lago Maggiore area during the last fifty years. Journal of Limnology 65: 1–62.Google Scholar
  5. Ambrosetti, W., L. Barbanti & E. A. Carrara, 2010. Mechanisms of hypolimnion erosion in a deep lake (Lago Maggiore, N. Italy). Journal of Limnology 69: 3–14.Google Scholar
  6. Bernard, L., C. Courties, P. Servais, M. Troussellier, M. Petit & P. Lebaron, 2000. Relationships among bacterial cell size, productivity, and genetic diversity in aquatic environments using cell sorting and flow cytometry. Microbial Ecology 40: 148–158.PubMedGoogle Scholar
  7. Bertoni, R., 1978. Automatic determination of carbon an nitrogen in suspended matter of natural water with Carlo Erba 1106 CHN elemental analyzer. Memorie dell’Istituto Italiano di Idrobiologia 36: 297–301.Google Scholar
  8. Bertoni, R., C. Callieri, G. Morabito, M. L. Pinolini & A. Pugnetti, 1998. Quali-quantitative changes in organic carbon production during the oligotrophication of Lake Maggiore, Italy. Verhandlungen International Vereinigung Limnologie 26: 300–304.Google Scholar
  9. Bertoni, R., R. Piscia & C. Callieri, 2004. Horizontal heterogeneity of seston, organic carbon and picoplankton in the photic zone of Lago Maggiore, Northern Italy. Journal of Limnology 63: 244–249.Google Scholar
  10. Bertoni, R., C. Callieri, E. Caravati, M. Contesini, G. Corno & D. Manca, 2008. Indagini sull’ambiente pelagico. Carbonio organico e popolamenti batterici eterotrofi. In C.N.R.-I.S.E. Ricerche sull’evoluzione del Lago Maggiore. Aspetti Limnologici. Programma quinquennale 2003–2007. Campagna 2007 e Rapporto quinquennale 2003–2007. Commissione Internazionale per la protezione delle acque italo-svizzere: 67–72.Google Scholar
  11. Bjørnsen, P. K., B. Riemann, J. Pock-Steen, T. G. Nielsen & S. J. Horsted, 1989. Regulation of bacterioplankton production and cell volume in a eutrophic estuary. Applied Environmental Microbiology 55: 1512–1518.Google Scholar
  12. Callieri, C. & R. Piscia, 2002. Photosynthetic efficiency and seasonality of autotrophic picoplankton in Lago Maggiore after its recovery. Freshwater Biology 47: 941–956.CrossRefGoogle Scholar
  13. Callieri, C., G. Corno, E. Caravati, S. Rasconi, M. Contesini & R. Bertoni, 2009. Bacteria, Archaea, and Crenarchaeota in the epilimnion and hypolimnion of a deep holo-oligomictic lake. Applied Environmental Microbiology 75: 7298–7300.CrossRefGoogle Scholar
  14. Chrzanowski, T. H., R. D. Crotty & G. J. Hubbard, 1988. Seasonal variation in cell volume of epilimnetic bacteria. Microbial Ecology 16: 155–163.CrossRefGoogle Scholar
  15. Cole, J. J., G. E. Likens & D. L. Strayer, 1982. Photosynthetically produced dissolved organic carbon: an important source for planktonic bacteria. Limnology and Oceanography 27: 1080–1090.CrossRefGoogle Scholar
  16. Cole, J. J., M. L. Pace, N. F. Caraco & G. S. Steinhart, 1993. Bacterial biomass and cell size distributions in lakes: more and larger cells in anoxic waters. Limnology and Oceanography 38: 1627–1632.CrossRefGoogle Scholar
  17. Crump, B. C., J. A. Baross & C. A. Simenstad, 1998. Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquatic Microbial Ecology 14: 7–18.CrossRefGoogle Scholar
  18. Dokulil, M. T., A. Jagsch, G. D. George, O. Anneville, T. Jankowski, B. Wahl, B. Lenhart, T. Bleckner & K. Teubner, 2006. Twenty years of spatially coherent deepwater warming in lakes across Europe related to North-Atlantic oscillation. Limnology and Oceanography 51: 2787–2793.Google Scholar
  19. Evans, C. D., D. T. Monteith & D. M. Cooper, 2005. Long-term increases in surface water dissolved organic carbon: observations, possible causes and environmental impacts. Environmental Pollution 137: 55–71.CrossRefPubMedGoogle Scholar
  20. Grossart, H. P. & H. Ploug, 2001. Microbial degradation of organic carbon and nitrogen on diatom aggregates. Limnology and Oceanography 46: 267–277.CrossRefGoogle Scholar
  21. Hansen, L., G. F. Krog & M. Søndergaard, 1986. Decomposition of lake phytoplankton. 1. Dynamics of short-term decomposition. Oikos 46: 37–44.CrossRefGoogle Scholar
  22. Helsel, D. R., D. K. Mueller & J. R. Slack, 2006. Computer program for the Kendall family of trend tests. U.S. Geological Survey Scientific Investigations Report 2005–5275, 4 p.Google Scholar
  23. Hipel, K. W. & A. I. McLeod, 2005. Time series modelling of water resources and environmental systems.
  24. Hirsh, R. M. & J. R. Slack, 1984. A nonparametric trend test for seasonal data with serial dependence. Water Resources Research 20: 727–732.Google Scholar
  25. Holm-Hansen, O. & B. Rieman, 1978. Chlorophyll a determination: improvements in methodology. Oikos 30: 438–447.CrossRefGoogle Scholar
  26. Horner-Devine, M. C., M. A. Leibold, V. H. Smith & B. J. M. Bohannan, 2003. Bacterial diversity patterns along a gradient of primary productivity. Ecology Letters 6: 613–622.Google Scholar
  27. Jeppesen, E., M. Søndergaard, J. P. Jensen, et al., 2005. Lake responses to reduced nutrient loading-an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.CrossRefGoogle Scholar
  28. Kamijunke, N., D. Straile & U. Gaedke, 2009. Response of heterotrophic bacteria, autotrophic picoplankton and heterotrophic nanoflagellates to re-oligotrophication. Journal of Plankton Research 31: 899–907.CrossRefGoogle Scholar
  29. Lindström, E. S., 2000. Bacterioplankton community composition in five lakes differing in trophic status and humic content. Microbial Ecology 40: 104–113.Google Scholar
  30. Lindström, E. S., M. P. Kamst-van Agterveld & G. Zwart, 2005. Distribution of typical freshwater bacterial groups is associated with pH, temperature and lake water retention time. Applied Environmental Microbiology 71: 8201–8206.Google Scholar
  31. Monika, W. & D. E. Schindler, 2004. Climatic effects on the phenology of lake processes. Global Change Biology 10: 1844–1856.CrossRefGoogle Scholar
  32. Monteith, D. T., J. L. Stoddard, C. D. H. Evans, A. de Wit, M. Forsius, T. Høgasen, A. Wilander, B. L. Skjelkvale, D. S. Jeffries, J. Vuorenmaa, B. Keller, J. Kopacek & J. Vesely, 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450: 537–541.CrossRefPubMedGoogle Scholar
  33. Morabito, G., D. Ruggiu & P. Panzani, 2002. Recent dynamics (1995–1999) of the phytoplankton assemblages in Lago Maggiore as a basic tool for defining association patterns in the Italian deep lakes. Journal of Limnology 61: 129–145.Google Scholar
  34. Morabito, G., A. Oggioni & P. Panzani, 2003. Phytoplankton assemblage at equilibrium in large and deep subalpine lakes: a case study from Lago Maggiore (N. Italy). Hydrobiologia 502: 37–48.Google Scholar
  35. Mosello, R. & D. Ruggiu, 1985. Nutrient load, trophic condition and restoration prospects of Lake Maggiore. Internationale Revue der Gesamten Hydrobiologie 70: 63–75.CrossRefGoogle Scholar
  36. Raven, J. A. & R. J. Geider, 1988. Temperature and algal growth. New Phytologist 110: 441–461.CrossRefGoogle Scholar
  37. Rogora, M., 2007. Considerazioni generali sull’evoluzione del chimismo delle acque lacustri e tributarie. In C.N.R.-I.S.E. Ricerche sull’evoluzione del Lago Maggiore. Aspetti limnologici. Programma quinquennale 2003–2007. Campagna 2007 e Rapporto quinquennale 2003–2007. Commissione Internazionale per la protezione delle acque italo svizzere: 89–97.Google Scholar
  38. Salmaso, N., G. Morabito, R. Mosello, L. Garibaldi, M. Simona, F. Buzzi & D. Ruggiu, 2003. A synoptic study of phytoplankton in the deep lakes south of the Alps (lakes Garda, Iseo, Como, Lugano and Maggiore). Journal of Limnology 62: 207–227.Google Scholar
  39. Salmaso, N., G. Morabito, F. Buzzi, L. Garibaldi, M. Simona & R. Mosello, 2006. Phytoplankton as an indicator of the water quality of the deep lakes south of the Alps. Hydrobiologia 563: 167–187.CrossRefGoogle Scholar
  40. Salmaso, N., G. Morabito, L. Garibaldi & R. Mosello, 2007. Trophic development of the deep lakes south of the Alps: a comparative analysis. Fundamental and Applied Limnology, Archives Fur Hydrobiologie 170: 177–196.CrossRefGoogle Scholar
  41. Straile, D., D. Livingstone, G. Weyhenmeyer & D. George, 2003. The response of freshwater ecosystems to climate variability associated with the North Atlantic Oscillation. In Hurrell, J., Y. Kushnir, G. Ottersen & M. Visbeck (eds), The North Atlantic Oscillation: Climatic Significance and Environmental Impact, Vol. 134. Geophysical Monograph Series. American Geophysical Union, Washington, DC: 263–279.Google Scholar
  42. Straza, T. R. A., M. T. Cottrell, H. W. Ducklow & D. L. Kirchman, 2009. Geographic and phylogenetic variation in bacterial biovolume as revealed by protein and nucleic acid staining. Applied Environmental Microbiology 75: 4028–4034.CrossRefGoogle Scholar
  43. Talling, J. F. & D. Driver, 1961. Some problems in the estimation of chlorophyll a in phytoplankton. Proceedings of the 10th Pacific Science Congress, Honolulu: 142–146.Google Scholar
  44. Wiebe, W. J., W. M. Sheldon Jr. & L. R. Pomeroy, 1992. Bacterial growth in the cold: evidence for an enhanced substrate requirement. Applied Environmental Microbiology 58: 359–364.Google Scholar
  45. Zhang, J., J. Hudson, R. Neal, J. Sereda, T. Clair, M. Turner, D. Jeffries, P. Dillon, L. Molot, K. Somers & R. Hesslein, 2010. Long-term patterns of dissolved organic carbon in lakes across eastern Canada: evidence of a pronounced climate effect. Limnology and Oceanography 55: 30–42.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Roberto Bertoni
    • 1
    Email author
  • Cristiana Callieri
    • 1
  • Gianluca Corno
    • 1
    • 2
  • Serena Rasconi
    • 3
  • Emanuele Caravati
    • 1
  • Mario Contesini
    • 1
  1. 1.CNR - Institute of Ecosystem StudyVerbania PallanzaItaly
  2. 2.Limnological Station, Institute of Plant BiologyUniversity of ZurichKilchbergSwitzerland
  3. 3.UMR CNRS 6023, Université B. PascalClermont FerrandFrance

Personalised recommendations