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Phytoplankton functional response to spatial and temporal differences in a cold and oligotrophic lake


We explored phytoplankton communities from a functional perspective in two connected but hydro-morphologically distinct basins during the ice-free period in the cold and oligotrophic Lake Tovel, Italy. Despite the absence of dispersal barriers, we expected a clear separation of the phytoplankton communities between basins based on their physical distinctions: a shallow and a deep basin with low and high water residence time, respectively. To investigate seasonal succession and spatiality, taxa were classified according to their functional groups (FGs) and traits (FTs). Relationships between functional classifications and environmental parameters were assessed by non-metric multidimensional scaling integrated with cluster analysis. Clustering of FGs and FTs was complementary and reflected different hydrological conditions of each basin: (i) more stable conditions and higher functional variation across seasons in the deep basin and (ii) less stable conditions and lower functional variation across seasons in the shallow basin. Phytoplankton functional composition evidenced how local conditions selected for corresponding functional attributes adapted to each basin’s environment. These results, together with the presence of rare, cold-tolerant taxa such as Pseudotetraëdriella kamillae and Stephanocostis chantaicus, highlighted the need for long-term phytoplankton studies, and the creation of a FG that includes cold-adapted, oligotrophic taxa.

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  1. AFNOR, 2003. Qualité de l’Eau : Guide pour l’échantillonnage en routine et le pré-traitement des diatomées benthiques de rivières – Norme NF EN 13946, Association Française de Normalisation (AFNOR).

  2. Avigliano, L., A. Vinocur, G. Chaparro, G. Tell & L. Allende, 2014. Influence of re-flooding on phytoplankton assemblages in a temperate wetland following prolonged drought. Journal of Limnology 73: 247–262.

  3. Bellinger, E. G. & D. C. Sigee, 2010. Freshwater algae: identification and use as bioindicators. Wiley-Blackwell, Chichester.

  4. Bessudova, A. Y., L. M. Sorokovikova, A. D. Firsova, A. Y. Kuz’mina, Tomberg IV & Y. V. Likhoshway, 2014. Changes in phytoplankton community composition along a salinity gradient from the lower Yenisei River to the Kara Sea, Russia. Botanica Marina 57: 225–239.

  5. Borsato, A. & P. Ferretti, 2006. Monitoraggio idrometrico del Lago di Tovel e del suo bacino. Studi Trentini di Scienze Naturali, Acta Biologica 81: 205–223.

  6. Cellamare, M., S. Morin, M. Coste & J. Haury, 2012. Ecological assessment of French Atlantic lakes based on phytoplankton, phytobenthos and macrophytes. Environmental Monitoring and Assessment 184: 4685–4708.

  7. Cellamare, M., P. de Tezanos Pinto, M. Leitão, M. Coste, S. Boutry & J. Haury, 2013. Using functional approaches to study phytoplankton communities in a temperate region exposed to tropical species dispersal. Hydrobiologia 702: 267–282.

  8. Corradini, F. & A. Boscaini, 2006. Fisica e chimica delle acque del Lago di Tovel (Trentino, Alpi centrali). Studi Trentini di Scienze Naturali, Acta Biologica 81: 307–326.

  9. Dickman, M., 1969. Some effects of lake renewal on phytoplankton productivity and species composition. Limnology and Oceanography 14: 660–666.

  10. Dillon, P. J., 1975. The phosphorus budget of Cameron Lake, Ontario: the importance of flushing rate to the degree of eutrophy of lakes. Limnology and Oceanography 20: 28–39.

  11. Dokulil, M. T., 1991. Contribution of green-algae to the phytoplankton assemblage in a mesotrophic lake, Mondsee, Austria. Archiv für Protistenkunde 139: 213–223.

  12. Dokulil, M. T., 2003. Algae as ecological bio-indicators. In Markert, B. A., A. M. Breure & H. G. Zeichmeister (eds.), Bioindicators and Biomonitors – Principles, Concepts and Applications. Elsevier, Amsterdam: 285–327.

  13. Eccel, E. & G. Toller, 2006. Inquadramento climatico del Lago di Tovel e del suo bacino. Studi Trentini di Scienze Naturali, Acta Biologica 81: 247–258.

  14. Flaim, G., F. Corradini, A. Borsato, P. Ferretti, E. Eccel, U. Obertegger & B. Borghi, 2006. The importance of hydraulic conditions in determining ecological equilibrium in Lake Tovel, Italy. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 29: 1327–1330.

  15. Flaim, G., U. Obertegger, A. Anesi & G. Guella, 2014. Temperature-induced changes in lipid biomarkers and mycosporine-like amino acids in the psychrophilic dinoflagellate Peridinium aciculiferum. Freshwater Biology 59: 985–997.

  16. Guiry, M. D. & G. M. Guiry, 2014. AlgaeBase. World-wide electronic publication. National University of Ireland. Searched on 12 Nov 2014.

  17. Hegewald, E., J. Padisák & T. Friedl, 2007. Pseudotetraëdriella kamillae: taxonomy and ecology of a new member of the algal class Eustigmatophyceae (Stramenopiles). Hydrobiologia 586: 107–116.

  18. Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.

  19. Izaguirre, I., A. Vinocur, G. Mataloni & M. Pose, 1998. Phytoplankton communities in relation to trophic status in lakes from Hope Bay (Antarctic Peninsula). Hydrobiologia 369–370: 73–87.

  20. Jones, H. L. J., 1997. A classification of mixotrophic protists based on their behaviour. Freshwater Biology 37: 35–43.

  21. 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.

  22. Kulbe, T., F. Anselmetti, M. Cantonati & M. Sturm, 2005. Environmental history of Lago di Tovel, Trento, Italy, revealed by sediment cores and 3.5 kHz seismic mapping. Journal of Paleolimnology 34: 325–337.

  23. Legendre, P. & E. D. Gallagher, 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271–280.

  24. Litchman, E. & C. A. Klausmeier, 2008. Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution, and Systematics 39: 615–639.

  25. 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.

  26. Lund, J. W. G., C. Kipling & E. D. Le Cren, 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11: 143–170.

  27. Lv, H., J. Yang, L. Liu, X. Yu, Z. Yu & P. Chiang, 2014. Temperature and nutrients are significant drivers of seasonal shift in phytoplankton community from a drinking water reservoir, subtropical China. Environmental Science and Pollution Research 21: 5917–5928.

  28. Madigan, M. T., J. M. Martinko, D. Stahl & D. P. Clark, 2010. Brock Biology of Microorganisms. Benjamin Cummings, San Francisco.

  29. McGill, B. J., B. J. Enquist, E. Weiher & M. Westoby, 2006. Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21: 178–185.

  30. Morgan-Kiss, R. M., J. C. Priscu, T. Pocock, L. Gudynaite-Savitch & N. P. A. Huner, 2006. Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiology and Molecular Biology Reviews 70: 222–252.

  31. Mouillot, D., N. A. J. Graham, S. Villéger, N. W. H. Mason & D. R. Bellwood, 2013. A functional approach reveals community responses to disturbances. Trends in Ecology & Evolution 28: 167–177.

  32. Naselli-Flores, L., 2013. Morphological analysis of phytoplankton as a tool to assess ecological state of aquatic ecosystems: the case of Lake Arancio, Sicily, Italy. Inland Waters 4: 15–26.

  33. 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.

  34. Nygaard, K. & A. Tobiesen, 1993. Bacterivory in algae: a survival strategy during nutrient limitation. Limnology and Oceanography 38: 273–279.

  35. Obertegger, U., M. G. Braioni & G. Flaim, 2006. The zooplankton of Lake Tovel. Studi Trentini di Scienze Naturali, Acta Biologica 81: 369–378.

  36. Obertegger, U., G. Flaim, M. G. Braioni, R. Sommaruga, F. Corradini & A. Borsato, 2007. Water residence time as a driving force of zooplankton structure and succession. Aquatic Sciences 69: 575–583.

  37. Obertegger, U., G. Flaim & R. Sommaruga, 2008. Multifactorial nature of rotifer water layer preferences in an oligotrophic lake. Journal of Plankton Research 30: 633–643.

  38. Obertegger, U., A. Borsato & G. Flaim, 2010. Rotifer-crustacean interactions in a pseudokarstic lake: influence of hydrology. Aquatic Ecology 44: 121–130.

  39. OECD, 1982. Eutrophication of Waters, Monitoring, Assessment and Control. Organisation for Economic Cooperation and Development, Paris.

  40. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. Henry, H. Stevens & H. Wagner, 2013. Vegan: Community Ecology Package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan.

  41. Olenina, I., S. Hajdu, I. Edler, A. Andersson, N. Wasmund, S. Busch, J. Göbel, S. Gromisz, S. Huseby, M. Huttunen, A. Jaanus, P. Kokkonen, I. Ledaine & E. Niemkiewicz, 2006. Biovolumes and size-classes of phytoplankton in the Baltic Sea. Baltic Sea Environment Proceedings 106: 1–144.

  42. Padisák, J., 2005. Phytoplankton. In Sullivan, P. E. & C. S. Reynolds (eds.), The Lakes Handbook 1: Limnology and Limnetic Ecology. Blackwell Publishing, Oxford: 251–308.

  43. 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.

  44. Paganelli, A., 1992. Lake Tovel (Trentino): limnological and hydrobiological aspects. Memorie dell’Istituto italiano di idrobiologia 50: 225–257.

  45. Pålsson, C. & W. Granéli, 2004. Nutrient limitation of autotrophic and mixotrophic phytoplankton in a temperate and tropical humic lake gradient. Journal of Plankton Research 26: 1005–1014.

  46. Quinn, G. P. & M. J. Keough, 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.

  47. R Development Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing. URL http://www.R-project.org.

  48. Reynolds, C. S., 1980. Phytoplankton assemblages and their periodicity in stratifying lake systems. Holarctic Ecology 3: 141–159.

  49. Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge.

  50. Reynolds, C. S., 1988. Functional morphology and the adaptive strategies of freshwater phytoplankton. In Sandgren, C. D. (ed.), Growth and Reproductive Strategies of Freshwater Phytoplankton. Cambridge University Press, Cambridge: 388–433.

  51. Reynolds, C. S., 1994. The long, the short and the stalled: on the attributes of phytoplankton selected by physical mixing in lakes and rivers. Hydrobiologia 289: 9–21.

  52. Reynolds, C. S., 1997. Vegetation Processes in the Pelagic: A Model for Ecosystem Theory. Ecology Institute, Oldendorf.

  53. 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.

  54. Reynolds, C. S., J. Padisák & U. Sommer, 1993. Intermediate disturbance in the ecology of phytoplankton and the maintenance of species diversity: a synthesis. Hydrobiologia 249: 183–188.

  55. Rigosi, A., C. C. Carey, B. W. Ibelings & J. D. Brookes, 2014. The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnology and Oceanography 59: 99–114.

  56. Rodrigues, D. F. & J. M. Tiedje, 2008. Coping with our cold planet. Applied and Environmental Microbiology 74: 1677–1686.

  57. Sandgren, C. D., 1988. The ecology of chrysophyte flagellates: their growth and perennation strategies as freshwater phytoplankton. In Sandgren, C. D. (ed.), Growth and reproductive strategies of freshwater phytoplankton. Cambridge University Press, Cambridge: 9–104.

  58. Scheffler, W. & J. Padisák, 2000. Stephanocostis chantaicus (Bacillariophyceae): morphology and population dynamics of a rare centric diatom growing in winter under ice in the oligotrophic Lake Stechlin, Germany. Algological Studies 133: 49–69.

  59. Scheffler, W. & G. Morabito, 2003. Topical observations on centric diatoms (Bacillariophyceae, Centrales) of Lake Como (N. Italy). Journal of Limnology 62: 47–60.

  60. Shatwell, T., J. Köhler & A. Nicklisch, 2013. Temperature and photoperiod interactions with silicon-limited growth and competition of two diatoms. Journal of Plankton Research 35: 957–971.

  61. Sommaruga, R., 2001. The role of solar UV radiation in the ecology of alpine lakes. Journal of Photochemistry and Photobiology B: Biology 62: 35–42.

  62. Sommer, U., 1986. The periodicity of phytoplankton in Lake Constance (Bodensee) in comparison to other deep lakes of central Europe. Hydrobiologia 138: 1–7.

  63. 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.

  64. Straubinger-Gansberger, N., M. N. Kaggwa & M. Schagerl, 2014. Phytoplankton patterns along a series of small man-made reservoirs in Kenya. Environmental Monitoring and Assessment 186: 5153–5166.

  65. Sun, J. & D. Liu, 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. Journal of Plankton Research 25: 1331–1346.

  66. Tilman, D., R. Kiesling, R. Sterner, S. S. Kilham & F. A. Johnson, 1986. Green, bluegreen and diatom algae: taxonomic differences in competitive ability for phosphorus, silicon and nitrogen. Archiv für Hydrobiologie 106: 473–485.

  67. Tittel, J., V. Bissinger, B. Zippel, U. Gaedke, E. Bell, A. Lorke, N. Kamjunke, 2003. Mixotrophs combine resource use to outcompete specialists: implications for aquatic food webs. Proceedings of the National Academy of Sciences of the United States of America 100: 12776–12781.

  68. Tolotti, M., F. Corradini, A. Boscaini & D. Calliari, 2007. Weather-driven ecology of planktonic diatoms in Lake Tovel (Trentino, Italy). Hydrobiologia 578: 147–156.

  69. van Donk, E. & S. S. Kilham, 1990. Temperature effects on silicon- and phosphorus-limited growth and competitive interactions among three diatoms. Journal of Phycology 26: 40–50.

  70. Violle, C., M.-L. Navas, D. Vile, E. Kazakou, C. Fortunel, I. Hummel & E. Garnier, 2007. Let the concept of trait be functional! Oikos 116: 882–892.

  71. Vogt, R. J., B. E. Beisner & Y. T. Prairie, 2010. Functional diversity is positively associated with biomass for lake diatoms. Freshwater Biology 55: 1636–1646.

  72. Weiher, E., D. Freund, T. Bunton, A. Stefanski, T. Lee & S. Bentivenga, 2011. Advances, challenges and a developing synthesis of ecological community assembly theory. Philosophical Transactions of the Royal Society B 366: 2403–2413.

  73. 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.

  74. Žutinić, P., M. Gligora Udovič, K. Kralj Borojević, A. Plenković-Moraj & J. Padisák, 2014. Morpho-functional classifications of phytoplankton assemblages of two deep karstic lakes. Hydrobiologia 740: 147–166.

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The first author was supported by a Short-Term Scientific Mission (STSM) and travel grant funded through the EU Cost Action ES1201 NETLAKE (Eleanor Jennings, Chair); this study was also supported by research activity funded by FEM–CRI (LTER Tovel). We are also grateful to Judit Padisák for taxonomic confirmation of the eustigmatophyte Pseudotetraëdriella kamillae. The authors thank the GIS Agrometeorology group (FEM) and especially Stefano Corradini for weather data. The authors also thank two reviewers for useful comments.

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Correspondence to Maria Cellamare.

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Guest editors: Luigi Naselli-Flores & Judit Padisák / Biogeography and Spatial Patterns of Biodiversity of Freshwater Phytoplankton

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Cellamare, M., Lançon, A.M., Leitão, M. et al. Phytoplankton functional response to spatial and temporal differences in a cold and oligotrophic lake. Hydrobiologia 764, 199–209 (2016). https://doi.org/10.1007/s10750-015-2313-2

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  • Functional approaches
  • Seasonal succession
  • Spatial distribution
  • Environmental filtering
  • Cold-tolerant taxa