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Plasticity in phytoplankton annual periodicity: an adaptation to long-term environmental changes

  • LARGE AND DEEP PERIALPINE LAKES
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Abstract

Because phytoplankton communities exhibit seasonal patterns driven by changes in physical factors, grazing pressure, and nutrient limitations, climate change, in combination with local phosphorus management policies are expected to impact phytoplankton annual dynamic. We used long-term monitoring data from Lake Geneva (from 1974 to 2010) to test if changes in phytoplankton seasonal succession across years is related to re-oligotrophication, inter-annual variability in thermal conditions, and Daphnia sp. density. We used a Bayesian method to identify species assemblages and wavelet analysis to detect transient dynamics in seasonal periodicity. A decrease in phosphorus concentrations appeared to play a major role in the inter-annual replacement of species assemblages. Furthermore, some species assemblages exhibited a change in their seasonal periodicity that was most likely induced by changes in Daphnia sp. density. Finally, we demonstrated that flexibility in the pattern of phytoplankton seasonal successions played a stabilizing role at the community level. The results suggest that phenology and inter-annual changes in seasonal dynamics of phytoplankton assemblages are important components to consider for explaining long-term variability in phytoplankton community.

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References

  • Adrian, R., C. M. O’Reilly, H. Zagarese, et al., 2009. Lakes as sentinels of climate change. Limnology and Oceanography 54: 2283–2297.

    Article  Google Scholar 

  • Anderson, S. L. & L. McIntosh, 1991. Light-activated heterotrophic growth of the cyanobacterium Synechocystis sp. strain PCC 6803: a blue-light-requiring process. Journal of Bacteriology 173: 2761–2767.

    Article  CAS  Google Scholar 

  • Anneville, O. & C. Leboulanger, 2001. Long-term changes in the vertical distribution of phytoplankton in the deep Alpine Lake Geneva: a response to the reoligotrophication. AttiAssociazioneitaliana di oceanologia e limnologia 14: 25–35.

    Google Scholar 

  • Anneville, O., V. Ginot, J.-C. Druart & N. Angeli, 2002a. Long-term study (1974-1998) of seasonal changes in the phytoplankton in Lake Geneva: a multi-table approach. Journal of Plankton Research 24: 993–1007.

    Article  CAS  Google Scholar 

  • Anneville, O., S. Souissi, V. Ginot, F. Ibanez, J.-C. Druart & N. Angeli, 2002b. Temporal mapping of phytoplankton assemblages in Lake Geneva: annual and interannual changes in their patterns of succession. Limnology and Oceanography 47: 1355–1366.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Anneville, O., C. Kaiblinger, R. D. Tadonléké, J.-C. Druart & M. T. Dokulil, 2008. Contribution of Long-term monitoring to the European Water Framework Directive implementation. In: Sengupta M. & Dalwani R. (eds), Proceedings of Taal 2007: The 12th World Lake Conference, pp. 1122–1131.

  • Anneville, O., S. Souissi, J.-C. Molinero & D. Gerdeaux, 2009. Influences of human activity and climate on the stock-recruitment dynamics of whitefish, Coregonus lavaretus, in Lake Geneva. Fisheries Management and Ecology 16: 492–500.

    Article  Google Scholar 

  • Anneville, O., E. Lasne, J. Guillard, R. Eckmann, J. D. Stockwell, C. Gillet & D. L. Yule, 2015. Impact of fishing and stocking practices on Coregonid diversity. Food and Nutrition Sciences 6: 1045–1055.

    Article  Google Scholar 

  • Billis, K., M. Billini, H. J. Tripp, N. C. Kyrpides & K. Mavromatis, 2014. Comparative Transcriptomics between Synechococcus PCC 7942 and Synechocystis PCC 6803 Provide Insights into Mechanisms of Stress Acclimation. PLoS ONE. https://doi.org/10.1371/journal.pone.0109738.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blenckner, T., R. Adrian, D. Livingstone, et al., 2007. Large-scale climatic signatures in lakes across Europe: a meta-analysis. Global Change Biology 13: 1314–1326.

    Article  Google Scholar 

  • Bourrelly, P., 1972. Les algues d’eau douce, Tome I. Les algues vertes, Paris: 1–572.

    Google Scholar 

  • Bourrelly, P., 1981. Les algues d’eau douce, Tome II. Les algues jaunes et brunes, Paris: 1–517.

    Google Scholar 

  • Bourrelly, P., 1985. Les algues d’eau douce, Tome III. Les algues bleues et rouges, Paris: 1–606.

    Google Scholar 

  • Carey, C. C., P. Hanson, R. C. Lathrop & A. L. St Amand, 2016. Using wavelet analyses to examine variability in phytoplankton seasonal succession and annual periodicity. Journal of Plankton Research 38: 27–40.

    Article  CAS  Google Scholar 

  • Carpenter, S. R., J. F. Kitchell & J. R. Hodgson, 1985. Cascading trophic interactions and lake productivity. Bioscience 35: 634–639.

    Article  Google Scholar 

  • Cazelles, B. & L. Stone, 2003. Detection of imperfect population synchrony in an uncertain world. Journal of Animal Ecology 72: 953–968.

    Article  Google Scholar 

  • De Senerpont Domis, L., W. M. Mooij & J. Huisman, 2007. Climate-induced shifts in an experimental phytoplankton community: a mechanistic approach. Hydrobiologia 584: 403–413.

    Article  Google Scholar 

  • Directive, 2000. Directive 2000/60/EC of the European Parliament and of the council of 23 October 2000 establishing a framework for community action in the field of water policy. Official Journal of the European Communities L327: 1–72.

    Google Scholar 

  • Dokulil, M., A. Jagsch, G. D. George, et al., 2006. Twenty years of spatially coherent deep water warming in lakes across Europe related to the North Atlantic Oscillation. Limnology and Oceanography 51: 2787–2793.

    Article  Google Scholar 

  • Domaizon, I., O. Savichtcheva, D. Debroas, et al., 2013. DNA from lake sediments reveals the long-term dynamics and diversity of Synechococcus assemblages. Biogeosciences 10: 3817–3838.

    Article  Google Scholar 

  • Dröscher, I., K. Finlay, A. Patoine & P. R. Leavitt, 2008. Daphnia control of the spring clear-water phase in six polemic lakes of varying productivity and size. Verhandlungen des Internationalen Verein Limnologie 30: 186–190.

    Google Scholar 

  • Druart, J.-C. & F. Rimet, 2008. Protocole et analyse du phytoplancton de l’INRA: prélèvement, dénombrement, et biovolumes. INRA, p. 200.

  • Dufrêne, M. & P. Legendre, 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366.

    Google Scholar 

  • Durant, J. M., D. O. Hjermann, G. Ottersen & N. C. Stenseth, 2007. Climate and the match or mismatch between predator requirements and resource availability. Climate Research 33: 271–283.

    Article  Google Scholar 

  • Edwards, M. & A. J. Richardson, 2004. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430: 881–884.

    Article  CAS  Google Scholar 

  • Favre, S., 1998. Biomanipulations en milieu lacustres. le Léman. Université de Franche-comté, Recherche de contrôle descendant poisson-zooplancton dans un grand lac alpin: 52.

    Google Scholar 

  • Gonzalez, A. & M. Loreau, 2009. The causes and consequences of compensatory dynamics in ecological communities. Annual Review of Ecology, Evolution, and Systematics 40: 393–414.

    Article  Google Scholar 

  • Gowen, R. J., Y. Collos, P. Tett, et al., 2015. Response of diatom and dinoflagellate lifeforms to reduced phosphorus loadings: a case study in the Thau lagoon, France. Estuarine, Coastal and Shelf Science 162: 45–52.

    Article  CAS  Google Scholar 

  • Grinsted, A., J. C. Moore & S. Jevrejeva, 2004. Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Processes in Geophysics 11: 561–566.

    Article  Google Scholar 

  • Hansen, G. & W. Cramer, 2015. Global distribution of observed climate change impacts. Nature Climate Change 5: 182–185. https://doi.org/10.1038/nclimate2529.

    Article  Google Scholar 

  • Holling, C. S., 1973. Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 4: 1–23.

    Article  Google Scholar 

  • Hsieh, C.-H., C.-S. Chen, T.-S. Chiu, K.-T. Lee, F.-J. Shieh, J.-Y. Pan & M.-A. Lee, 2009. Time series analyses reveal transient relationships between abundance of larval anchovy and environmental variables in the coastal waters southwest of Taiwan. Fisheries Oceanography 18: 102–117.

    Article  Google Scholar 

  • Hutchinson, G. E., 1961. The paradox of the plankton. American Naturalist 95: 137–145.

    Article  Google Scholar 

  • Jacquet, S., I. Domaizon & O. Anneville, 2014a. The need for ecological monitoring of freshwaters in a changing world: a case study of Lakes Annecy, Bourget and Geneva. Environmental Monitoring and Assessment 186: 3455–3476.

    Article  Google Scholar 

  • Jacquet, S., O. Kerimoglu, F. Rimet, G. Paolini & O. Anneville, 2014b. Cyanobacterial bloom termination: the disappearance of Planktothrix rubescens from Lake Bourget (France) after restoration. Freshwater Biology 59: 2472–2487.

    Article  Google Scholar 

  • Jeppesen, E., M. Sondergaard, 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.

    Article  CAS  Google Scholar 

  • Jochimsen, M. C., R. Kümmerlin & D. Straile, 2013. Compensatory dynamics and the stability of phytoplankton biomass during four decades of eutrophication and oligotrophication. Ecology Letters 16: 81–89.

    Article  Google Scholar 

  • Kaiblinger, C., O. Anneville, R. Tadonleke, F. Rimet, J.-C. Druart, J. Guillard & M. T. Dokulil, 2009. Central European water quality indices applied to long-term data from peri-alpine lakes: test and possible improvements. Hydrobiologia 633: 67–74.

    Article  CAS  Google Scholar 

  • Kruk, C., N. Mazzeo, G. Lacerot & C. S. Reynolds, 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.

    Article  Google Scholar 

  • Laine, L. & M.-M. Perga, 2015. The zooplankton of Lake Geneva. Rapport pour la Commission Internationale pour la protection des Eaux du Léman contre la pollution, Campagne 2014, pp. 127–136.

  • Lampert, W., W. Fleckner, H. Rai & B. E. Taylor, 1986. Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnology and Oceanography 31: 478–490.

    Article  Google Scholar 

  • Lampert, W. & U. Sommer, 2007. Limnoecology. The Ecology of Lakes and Streams. Oxford University Press, Oxford: 324.

    Google Scholar 

  • Lazzarotto, J., P. Quetin & A. Klein, 2013. Evolution physic-chimique des eaux du Léman et données météorologiques. Rapport de la Commission Internationale pour la protection des Eaux Léman contre la pollution, Campagne 2012, pp. 16–46.

  • Legendre, P. & L. Legendre, 1998. Numerical Ecology. Developments in Environmental Modelling, 2nd ed. 20. © Elsevier Science B.V., Amsterdam: 853.

    Google Scholar 

  • Litchman, E., K. F. Edwards, C. A. Klausmeier & M. K. Thomas, 2012. Phytoplankton niches, traits and eco-evolutionary responses to global environmental change. Marine Ecology Progress Series 470: 235–248.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Manca, M., M. Rogora & N. Salmaso, 2015. Inter-annual climate variability and zooplankton: applying teleconnection indices to two deep subalpine lakes in Italy. Journal of Limnology 74: 123–132.

    Google Scholar 

  • Molinero, J. C., O. Anneville, S. Souissi, L. Lainé & D. Gerdeaux, 2007. Decadal changes in water temperature and ecological time-series in Lake Geneva, Europe: relationship to subtropical Atlantic climate variability. ClimateResearch 34: 15–23.

    Google Scholar 

  • Monod, R., P. Blanc & C.Corvi, 1984. Le régime thermique du Léman. CIPEL, (ed). Le Léman synthèse 1957–1982. Lausanne. pp. 75–88.

  • Moutin, T., T. F. Thinsgtad, F. Van Wambeke, D. Marie, G. Slawyk, P. Raimbault & H. Claustre, 2002. Does competition for nanomolar phosphate supply explain the predominance of the cyanobacterium Synechococcus? Limnology and Oceanography 47: 1562–1567.

    Article  CAS  Google Scholar 

  • O’Reilly, et al., 2015. Rapid and highly variable warming of lake surface waters around the globe. Geophysical Research Letters. https://doi.org/10.1002/2015GL066235.

    Article  Google Scholar 

  • Pace, M. L., J. J. Cole, S. R. Carpenter & J. F. Kitchell, 1999. Trophic cascade revealed in diverse ecosystems. Trends in Ecology and Evolution 14: 483–488.

    Article  CAS  Google Scholar 

  • Poloczanska, E. S., C. J. Brown, W. J. Sydeman, et al., 2013. Global imprint of climate change on marine life. Nature Climate Change 3: 919–925.

    Article  Google Scholar 

  • Pomati, F., B. Matthews, J. Jokela, A. Schildknecht & B. Ibelings, 2011. Effects of re-oligotrophication and climate warming on plankton richness and community stability in a deep mesotrophic lake. Oikos 121: 1317–1327.

    Article  Google Scholar 

  • Porter, K., 1976. Enhancement of algal growth and productivity by grazing zooplankton. Science 192: 1332–1334.

    Article  CAS  Google Scholar 

  • Repka, S., 1997. Effects of food type on the life history of Daphnia clones from lakes differing in trophic state. I. Daphnia galeata feeding on Scenedesmus and Oscillatoria. Freshwater Biology 38: 675–683.

    Article  Google Scholar 

  • Reynolds, C. S., 1984. The ecology of freshwater phytoplankton. Cambridge University Press, Cambridge p: 384.

    Google Scholar 

  • Reynolds, C. S., 1988. The concept of ecological succession applied to seasonal periodicity of freshwater phytoplankton. Verhandlungen des InternationalenVereinLimnologie 23: 683–691.

    Google Scholar 

  • Reynolds, C. S., 1992. Dynamics, selection and composition of phytoplankton in relation to vertical structure in lakes. ArchivfürHydrobiologie 35: 13–31.

    Google Scholar 

  • Reynolds, C. S., 1998. What factors influence the species composition of phytoplankton in lakes of different trophic status? Hydrobiologia 369(370): 11–26.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rosén, G., 1981. Phytoplankton indicators and their relations to certain chemical and physical factors. Limnologica 13: 263–290.

    Google Scholar 

  • Roy, S. & J. Chattopadhyay, 2007. Towards a resolution of “the paradox of the plankton”: a brief overview of the proposed mechanisms. Ecological complexity 4: 26–33.

    Article  Google Scholar 

  • Schindler, D. E., J. B. Armstrong & T. E. Reed, 2015. The portfolio concept in ecology and evolution. Frontiers in Ecology and the Environment 13: 257–263.

    Article  Google Scholar 

  • Sommer, U., R. Adrian, L. D. Domis, et al., 2012. Beyond the Plankton Ecology Group (PEG) Model: mechanisms driving plankton succession. Annual Review of Ecology, Evolution and Systematics 43: 429–448.

    Article  Google Scholar 

  • Sommer, U., Z. M. Gliwicz, W. Lampert & A. Ducan, 1986. The PEG model of a seasonal succession of planktonic events in fresh waters. Archiv für Hydrobiologie 106: 433–471.

    Google Scholar 

  • Sotton, B., J. Guillard, O. Anneville, M. Maréchal, O. Savichtcheva & I. Domaizon, 2014. Trophic transfer of microcystins through the lake pelagic food web: evidence for the role of zooplankton as a vector in fish contamination. Science of the Total Environment 466–467: 152–163.

    Article  Google Scholar 

  • Souissi, S., F. Ibanez, R. Ben Hamadou, J. Boucher, A. C. Cathelineau, F. Blanchard & J. C. Poulard, 2001. A new multivariate mapping method for studying species assemblages and their habitats: example using bottom trawl surveys in the Bay of Biscay (France). Sarsia 86: 527–542.

    Article  Google Scholar 

  • Straile, D., 2002. North Atlantic Oscillation synchronizes food-web interactions in central European lakes. Proceedings of the Royal Society of London, Series B: Biological Sciences 269: 391–395.

    Article  Google Scholar 

  • Straile, D., M. C. Jochimsen & R. Kümmerlin, 2015. Taxonomic aggregation does not alleviate the lack of consistency in analyzing diversity in long-term phytoplankton monitoring data: a rejoinder to Pomati et al. (2015). Freshwater Biology 60: 1060–1067.

    Article  Google Scholar 

  • Strong, D. R., 1992. Are trophic cascade all wet? Differentiation and donor-control in species ecosystems. Ecology 73: 747–754.

    Article  Google Scholar 

  • Tapolczai, K., O. Anneville, J. Padisak, et al., 2015. Occurrence and mass development of Mougeotia spp. (Zygnemataceae) in large, deep lakes. Hydrobiologia 745: 17–29.

    Article  CAS  Google Scholar 

  • Thackeray, S. J., I. D. Jones & S. C. Maberly, 2008. Long-term change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climatic change. Journal of Ecology 96: 523–535.

    Article  Google Scholar 

  • Tõnno, I., H. Künnap & T. Nõges, 2003. The role of zooplankton grazing in the formation of “clear water phase” in a shallow charophyte dominated lake. Hydrobiologia 506(509): 353–358.

    Article  Google Scholar 

  • Torrence, C. & G. P. Compo, 1998. A practical guide to wavelet analysis. Bulletin of the American Meteorological Society 79: 61–78.

    Article  Google Scholar 

  • Utermöhl, H., 1958. ZurVervollkommung der quantitativen Phytoplankton-methodik. Mitteilungen Internationale Vereinigung für theoretische und angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Vadadi-Fülöp, C. & L. Hufnagel, 2014. Climate change and phytoplankton phenology in freshwater: current trends and future commitments. Journal of Limnology 73: 1–16.

    Article  Google Scholar 

  • Verberk, W. C. E. P., C. G. E. Van Noordwijk & A. G. Hildrew, 2013. Delivering on a promise: integrating species traits to transform descriptive community ecology into a predictive science. Freshwater Science 32: 531–547.

    Article  Google Scholar 

  • Walters, A. W., M. D. A. G. Sagrario & D. E. Schindler, 2014. Species- and community-level responses combine to drive phenology of lake phytoplankton. Ecology 94: 2188–2194.

    Article  Google Scholar 

  • Weithoff, G., M. R. Rocha & U. Gaedke, 2015. Comparing seasonal dynamics of functional and taxonomic diversity reveals the driving forces underlying phytoplankton community structure. Freshwater Biology 60: 758–767.

    Article  Google Scholar 

  • Winder, M. & D. E. Schindler, 2004. Climatic effects on the phenology of lake processes. Global Change Biology 10: 1844–1856.

    Article  Google Scholar 

  • Winder, M. & J. E. Cloern, 2010. The annual cycles of phytoplankton biomass. Philosophical transactions of the royal society B 365: 3215–3226.

    Article  Google Scholar 

  • Wolfram, G. & M. Dokulil, 2007. Qualitätselement phytoplankton: felderhebung, probenahme, probenaufarbeitung und ergebnisermittlung. p. 50.

  • Yang, Y., K. Pettersson & J. Padisak, 2015. Repetitive baselines of phytoplankton succession in an unstably stratified temperate lake (Lake Erken, Sweden): a long-term analysis. Hydrobiologia 764: 211–227.

    Article  Google Scholar 

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Acknowledgements

We would like to thank Isabelle Domaizon for helpful comments and Jason Stockwell for English editing. This study is a contribution to the Bio-Asia FASCICLE project that was funded by the French Ministry of Foreign Affairs and the French Ministry of Education in collaboration with the CNRS and INRA for the French partners (see https://www.fascicle.cnrs.fr/). CIPEL (International Commission for the Protection of Lake Geneva) supported GD, and the data were from © SOERE OLA-IS, INRA Thonon-les-Bains, CIPEL.

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  1. INRA (Institut national de la recherche agronomique), Université Savoie Mont Blanc, CARRTEL, 74200, Thonon-les-Bains, France

    Orlane Anneville, Gaël Dur & Frédéric Rimet

  2. Creative Science Unit (Geosciences), Faculty of Science, Shizuoka University, 836 Ohya, Suruga-ku, Shizuoka, 422-8529, Japan

    Gaël Dur

  3. Université de Lille, CNRS, Université du Littoral Côte d’Opale, UMR 8187, LOG, Laboratoire d’Océanoie et de Géosciences, 62930, Wimereux, France

    Gaël Dur & Sami Souissi

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  1. Orlane Anneville
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Correspondence to Orlane Anneville.

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Guest editors: Nico Salmaso, Orlane Anneville, Dietmar Straile, & Pierluigi Viaroli / Large and deep perialpine lakes: ecological functions and resource management

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Anneville, O., Dur, G., Rimet, F. et al. Plasticity in phytoplankton annual periodicity: an adaptation to long-term environmental changes. Hydrobiologia 824, 121–141 (2018). https://doi.org/10.1007/s10750-017-3412-z

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