Estimating future cyanobacterial occurrence and importance in lakes: a case study with Planktothrix rubescens in Lake Geneva

Abstract

Among the multiple forms of freshwater pelagic cyanobacteria, the phycoerythrin-rich species Planktothrix rubescens is well adapted to temperate, deep and large lakes. In Lake Geneva, this filamentous and microcystin-producing species has been the dominant cyanobacterial species observed since the early years of this century. In addition to the trophic state (e.g., the phosphorus level), the influences of air and water temperature on the occurrence and development of cyanobacteria are particularly relevant in the context of global climate change. The latter may indeed be particularly marked for lakes in the Alpine region, with a rate of warming that may be twice as large as the global average. The impact of climate change on P. rubescens is thus an important challenge and it has been analysed in this study through two different approaches: (1) the extreme air temperature events as a proxy for future climate and (2) the multi adaptive regression splines (MARS) model to predict future P. rubescens biomass. These methods allowed us to determine whether Lake Geneva will still sustain an important biomass of P. rubescens in forthcoming years, provided there is no severe over-enrichment with nutrients in the future. The outcomes strongly suggest that the fraction of cyanobacterium could increase with respect to the total phytoplankton community by as much as 34 % by the end of this century and induce a significant change in the microalgal composition. Additionally, the results point to the fact that spring is a key period during which air temperature and nutrients become the determinant factors for outbreaks of this species in the subsequent seasons.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Anagnostidis K, Komarek J (1988) Modern approach to the classification system of cyanophytes. 3. Oscillatoriales. Archiv fur Hydrobiol 80:327–472

    Google Scholar 

  2. Anneville O, Leboulanger C (2001) Long-term changes in the vertical distribution of phytoplankton biomass and primary production in Lake Geneva: a response to the oligotrophication. Alti Associazione Italiano Oceanol Limnol 14:25–35

    Google Scholar 

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

    CAS  Article  Google Scholar 

  4. Anneville O, Mollinero JC, Souissi S, Balvay G, Gerdeaux D (2007) Long-term changes in the copepod community of Lake Geneva. J Plankton Res 29:49–59

    Article  Google Scholar 

  5. Anneville O, Domaizon I, Kerimoglu O, Rimet F, Jacquet S (2015) Blue-greens in a “greenhouse century”? New insights from field data of climate change impacts on cyanobacterial abundance. Ecosystems 18:441–458

    CAS  Article  Google Scholar 

  6. Beniston M (2007) Entering into the “greenhouse century”: recent record temperatures in Switzerland are comparable to the upper temperature quantiles in a greenhouse climate. Geophys Res Lett 34:L16710

    Article  Google Scholar 

  7. Berthon V, Marchetto A, Rimet F, Dormia E, Jenny JP, Pignol C, Perga ME (2013) Trophic history of French sub-alpine lakes over the last ~150 years: phosphorus reconstruction and assessment of taphonomic biases. J Limnol 72:417–429

    Article  Google Scholar 

  8. Blenckner T (2005). A conceptual model of climate-related effects on lake ecosystems. Hydrologia 533:1–14

  9. Briand JF, Jacquet S, Bernard C, Humbert JF (2003) Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. Vet Res 34:361–378

    CAS  Article  PubMed  Google Scholar 

  10. Briand JF, Jacquet S, Flinois C, Avois-Jacquet C, Maisonnette C, Leberre B, Humbert JF (2005) Variations in the microcystins production of Planktothrix rubescens (cyanobacteria) assessed by a four years in situ survey of Lac du Bourget (France) and by laboratory experiments. Microb Ecol 50:418–428

    Article  PubMed  Google Scholar 

  11. Bright DI, Walsby AE (2000) The daily integral of growth by Planktothrix rubescens calculated from growth rate in culture and irradiance in Lake Zurich. N Phytol 146:301–316

    Article  Google Scholar 

  12. Chorus I, Bartram J (1999) Toxic Cyanobacteria in water: a guide to public health consequences, monitoring and management. E & FN Spon, London

    Google Scholar 

  13. Davis PA, Dent M, Parker J, Reynolds CS, Walsby AE (2003) The annual cycle of growth rate and biomass change in Planktothrix spp. In Bleham Tarn, English Lake District

    Google Scholar 

  14. De Stasio BT, Golemgeski T, Livingston DM (2009) Temperature as a driving factor in aquatic ecosystems. In: Likens GE (ed) Encyclopedia of Inland Waters, Elsevier, Amsterdam, pp 690–698

  15. Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12

    CAS  Article  Google Scholar 

  16. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20

    Article  Google Scholar 

  17. Druart JC, Rimet F (2009) Dynamique du peuplement de diatomées pélagiques du Léman de 1974 à 2007. Arch des Sci 61:17–32

    Article  Google Scholar 

  18. Dupuis F, Hahn BJ (2009) Warm spring and summer water temperatures in small eutrophic lakes of the Canadian prairies: potential implications for phytoplankton and zooplankton. J Plankton Res 31(5):489–502

    CAS  Article  Google Scholar 

  19. Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz G, Nakamura M, Nakazawa Y, McC Overton J, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberon J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151

    Article  Google Scholar 

  20. Elliott JA (2010) The seasonal sensitivity of cyanobacteria and other phytoplankton to changes in flushing rate and water temperature. Glob Change Biol 16:864–876

    Article  Google Scholar 

  21. Feuillade J (1994) The cyanobacterium (blue-green alga) Oscillatoria rubescens DC. Arch Hydrobiol 41:77–93

    Google Scholar 

  22. Friedman JH (1991) Multivariate adaptive regression splines. Ann Stat 19:1–67

    Article  Google Scholar 

  23. Gallina N, Anneville O, Beniston M (2011) Impacts of extreme air temperatures on cyanobacteria in five deep peri-Alpine lakes. J Limnol 70(2):186–196

    Article  Google Scholar 

  24. Gallina N, Salmaso N, Morabito G, Beniston M (2013) Phytoplankton configuration in six deep lakes in the peri-Alpine region: are the key drivers related to eutrophication and climate? Aquat Ecol 47(2):177–193

    Article  Google Scholar 

  25. George G, Jennings E, Allot N (2010) The impact of climate change on lakes in Britain and Ireland. In: George DG (ed) The impact of climate change on european lakes, Aquatic Ecology Series 4. Springer, Netherlands, pp 359–386. doi:10.1007/978-90-481-2945-4_19

  26. Gomont M (1892) Monographie des Oscillariées (Nostocacées Homocystées). Deuxième partie. - Lyngbyées. Annales des Sciences Naturelles, Botanique, Série 716:91–264

  27. Graham MD, Vinebrooke R (2009) Extreme weather events alter planktonic communities in boreal lakes. Limnol Oceanogr 54:2481–2492

    Article  Google Scholar 

  28. Hastie T, Tibshirani R (S Language) (2011) Original R port by Friedrich Leisch, Kurt Hornik and Brian D. Ripley. Mda: Mixture and flexible discriminant analysis. R package version 0.4-2. http://CRAN.R-project.org/package=mda

  29. Hastie TJ, Tibshirani RJ (1990) Generalized additive models, vol 43 of monographs on statistics and applied probability. Chapman and Hall, London

  30. Hastie T, Tibshirani R, Friedmann J (2001) The Elements of statistical learing. Springer, New York

  31. Havens KE (2008) Cyanobacteria blooms: effect on aquatic ecosystems. Adv Exp Med Biol 619:733–747. doi:10.1007/978-0-387-75865-7_33

  32. Huber V, Wagner C, Gerten D, Adrian R (2012) To bloom or not to bloom: contrasting responses of cyanobacteria to recent heat waves explained by critical thresholds of abiotic drivers. Oecologia 169:245–256

    Article  PubMed  Google Scholar 

  33. Huisman J, Matthijs HCP, Visser PM, Ibelings BW, Mur LR, Walsby AE (2005) The ecophysiology of the harmful cyanobacterium Microcystis. Harmful Cyanobacteria. Vol3. Aquatic Ecology Series pp 109–142 Springer

  34. IPCC (2007) Climate change: synthesis report. Contribution of Working Groups I, II and III to the Fourth Assessment. In: Core Writing Team, Pachauri RK, Reisinger A (eds) Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland, p 104

  35. Jacquet S, Briand JF, Leboulanger C, Avois-Jacquet C, Paolini G, Oberhaus L, Tassin B, Vinçon-Leite B, Druart JC, Anneville O, Humbert JF (2005) The proliferation of the toxic cyanobacterium Planktothrix rubescens following restoration of the largest natural French lake (Lac du Bourget). Harmful Algae 4:651–672

    Article  Google Scholar 

  36. Jacquet S, Domaizon I, Anneville O (2012) Evolution de paramètres clés indicateurs de la qualité des eaux et du fonctionnement écologique des grands lacs péri-alpins (Léman, Annecy, Bourget): Etude comparative de trajectoires de restauration post-eutrophisation. Arch des Sci 65:225–242

    Google Scholar 

  37. Jacquet S, Domaizon I, Anneville O (2014a) The need for ecological monitoring of freshwaters in a changing world: A case study of Lakes Annecy, Bourget and Geneva. Environ Monit Assess 186:3455–3476

    Article  PubMed  Google Scholar 

  38. Jacquet S, Rimet F, Druart JC (2014b) Composition and dynamics of the phytoplanktonic communities in 3 large and deep Western European Lakes: an outline of the evolution from 2004 to 2012. In: Sebastia MT (ed) Phytoplankton: biology, classification and environmental impacts, chap 5. Nova Science Publishers, New York, pp 131–150

  39. Jacquet S, Kerimoglu O, Rimet F, Paolini G, Anneville O (2014c) Cyanobacterial bloom termination: the disappearance of Planktothrix rubescens from a large restored lake. Freshw Biol 59:2472–2487

    Article  Google Scholar 

  40. Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM (2008) Summer heatwave promote bloom of harmful Cyanobacteria. Glob Change Biol 14:495–512

    Article  Google Scholar 

  41. Leathwick JR, Rowe D, Richardson J, Elith J, Hastie T (2005) Using multivariate adaptive regression splines to predict the distributions of New Zealand’s freshwater diadromous fish. Freshw Biol 50:2034–2052

    Article  Google Scholar 

  42. Leathwick JR, Elith J, Hastie T (2006) Comparative performance of generalized additive models and multivariate adaptive regression splines for statistical modelling of species distributions. Ecol Model 199:188–196

    Article  Google Scholar 

  43. Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Ann Rev Ecol Evolut Syst 39:615–639

    Article  Google Scholar 

  44. Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10:1170–1181

    Article  PubMed  Google Scholar 

  45. Litchman E, De Tezanos Pinto P, Klausmeier CA, Thomas MK, Yoshiyama K (2010) Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653:15–38

    Article  Google Scholar 

  46. Livingstone DM (1993) Temporal Structure in the Deep–Water Temperature of Four Swiss Lakes: A Short–Term Climatic Change Indicator?  Verh. Internat. Verein. Limnol.25:75–81

  47. Livingstone DM (1997) Break–Up Dates of Alpine Lakes as Proxy Data for Local and Regional Mean Surface Air Temperatures.  Clim. Change 376:407–439

  48. Malchow H (1993) Spatio-temporal pattern formation in nonlinear non-equilibrium plankton dynamics. Proc R Soc B 251:103–109

    Article  Google Scholar 

  49. Micheletti S, Schanz F, Walsby AE (1998) The daily integral of photosynthesis by Planktothrix rubescens during summer stratification and autumnal mixing in Lake Zürich. New Phycol. 139:233–246

  50. Oberhaus L, Briand JF, Humbert JF (2008) Allelopathic growth inhibition by the toxic, bloom-forming cyanobacterium Planktothrix rubescens. FEMS Microbiol Ecol 66:243–249

    CAS  Article  PubMed  Google Scholar 

  51. Paerl HW, Millie DF (1996) Physiological ecology of toxic aquatic cyanobacteria. Phycologia 35:160–167

  52. Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58

    CAS  Article  PubMed  Google Scholar 

  53. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1:27–37

    CAS  Article  PubMed  Google Scholar 

  54. Pearl HW, Fulton RS, Moisander PH, Dyble J (2001) Harmful freshwater algal bloom, with an emphasis on cyanobacteria. Sci World J 1:76–113

    Article  Google Scholar 

  55. Pelletier J, Orand A (1978) Appareil de prélèvement d’un échantillon dans un fluide. INRA patent

  56. Perroud M, Goyette S (2010) Impact of warmer climate on Lake Geneva water-temperature profiles. Borel Env Res. 15:225–278

    Google Scholar 

  57. Reynolds CS (1984) The ecology of freshwater phytoplankton. Cambridge university Press, Cambridge, New York, pp 384

  58. Reynolds CS (2006) Ecology of phytoplankton. Ecology, Biodiversity and Conservation. Cambridge. University Press, Cambridge

    Google Scholar 

  59. Reynolds CS (1997) Vegetation processes in the pelagic: a model for ecosystem theory. Ecology Institute, Oldendorf Luhe

  60. Rimet F, Druart JC, Anneville O (2009) Exploring the dynamics of plankton diatom communities in Lake Geneva using emergent self-organizing maps (1974–2007). Ecol Inform 4:99–101

    Article  Google Scholar 

  61. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/

  62. Robarts RD, Zohary T (1987) Temperature effect on Photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zealand Journal of Marine and Freshwater Research 21:391–339

  63. Salmaso N, Buzzi F, Garibaldi L, Morabito G, Simona M (2012) Effects of nutrient availability and temperature on phytoplankton development: a case study from large lakes south of the Alps. Aquat Sci 74:555–570. doi:10.1007/s00027-012-0248-5

  64. Savichtcheva O, Debroas D, Perga ME, Arnaud F, Villar C, Lyautey E, Kirkham A, Chardon C, Alric B, Domaizon I (2014) Effects of nutrients and warming on Planktothrix dynamics and diversity: a palaeolimnological view based on sedimentary DNA and RNA. Freshw Biol 60:31–49

    Article  Google Scholar 

  65. Schatz D, Keren Y, Vardi A, Sukenik Carmeli S, Börner T, Dittman E, Kaplan A (2007) Towards a clarification of the biological role of microcystins, a family of cyanobacterial toxins. Environ Microbiol 9(4):965–970

    CAS  Article  PubMed  Google Scholar 

  66. Scheffer M, Rinaldi S, Gragnani A, Mur RL, van Nes EH (1997) On the dominance of filamentus cyanobacteria in shallow, turbid lakes. Ecology 78:272–282

    Article  Google Scholar 

  67. Shatwell T, Köhler J, Nicklish A (2008) Warming promotes cold-adapted phytoplankton in temperate lakes and opens a loophole for Ocillatoriales in spring. Glob Change Biol 14:1–7

    Article  Google Scholar 

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

  69. Stollenwerk N, Drepper FR, Siegel H (2001) Testing nonlinear stochastic model on phytoplankton biomass time series. Ecol Model 144:261–277

    Article  Google Scholar 

  70. Tadonléké RT (2010) Evidence of warming effects on phytoplancton productivity rates and their dependence on eutrophication status. Limnol Oceanogr 55:973–982

    Article  Google Scholar 

  71. Talling JF (1957) The phytoplankton population as a compound photosynthetic system. N Phytol 56:133–149

    Article  Google Scholar 

  72. Tapolczai K, Anneville O, Padisak J, Salmoso N, Morabito G, Zohary T, Tadonléké RT, Rimet F (2015) Occurrence and mass development of Mougeotia spp. (Zygnemataceae) in large, deep lakes. Hydrobiologia 745:17–29

    CAS  Article  Google Scholar 

  73. Tillmans AR, Wilson AE, Pick FR, Sarnelle O (2008) Meta-analysis of cyanobacterial effects on zooplankton population growth rate: species-specific responses. Fundam Appl Limnol 171(4):285–295

    Article  Google Scholar 

  74. Tonaru Z et al (2015) Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecol Lett 18:375–384

    Article  Google Scholar 

  75. Uthermöhl H (1958) Zur Vervollkommnung der quantative Phytoplankton-Methodik. Mitt Inst Verh Limn 9:1–38

    Google Scholar 

  76. Vanni MJ, Layne CD, Arnott SE (1997) “Top-down” trophic interactions in lakes: effects of fish on nutrient dynamics. Ecology 78:1–20

    Google Scholar 

  77. Visser PM, Ibelings BW, Mur LR, Walsby AE (2005) The ecophysiology of the harmful cyanobacterium Microcystis. In: Huisman J, Matthijs HCP, Visser PM (eds) Harmful Cyanobacteria. Aquatic Ecology Series, Vol 3. Springer, Netherlands, pp 109–142

  78. Vollenweider RA, Kerekes J (1982) Eutrophication of waters. Monitoring, assessment and control. OECD Cooperative programme on monitoring of inland waters (Eutrophication control), Environment Directorate, OECD, Paris, p 154

  79. Wetzel RG (2001) Limnology: lake and river ecosystems, 3rd edn. Academic Press, San Diego

  80. Whipple GC, Jackson DD (1899). Asterionella—its biology, its chemistry and its effect on water supplies. New English water work association, pp 1–25

  81. Wiegand C, Pflugmacher S (2005) Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicology and Applied Pharmaclogy. 203:201–218

Download references

Acknowledgments

This project was supported through a fellowship of the University of Geneva granted to N. Gallina. We are grateful to J.-C. Druart and F. Rimet who carried out the phytoplankton determination and counts. We would also like to acknowledge a number of other persons who were involved in sampling and data processing: J. C. Hustache, P. Chifflet, J. Lazzarotto, P. Perney, D. Barbet and G. Monet. Data are issued from © SOERE OLA-IS, INRA Thonon-les-Bains, CIPEL, developed by Eco-Informatics ORE INRA Team. This study is a contribution to the Observatory on alpine LAkes (OLA): http://www6.inra.fr/soere-ola.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nicole Gallina.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gallina, N., Beniston, M. & Jacquet, S. Estimating future cyanobacterial occurrence and importance in lakes: a case study with Planktothrix rubescens in Lake Geneva. Aquat Sci 79, 249–263 (2017). https://doi.org/10.1007/s00027-016-0494-z

Download citation

Keywords

  • Lake Geneva
  • Global warming
  • Statistical model
  • Cyanobacteria
  • Planktothrix rubescens
  • Lake ecology