, Volume 830, Issue 1, pp 115–134 | Cite as

Predicting the dynamics of taxonomic and functional phytoplankton compositions in different global warming scenarios

  • Karine Borges MachadoEmail author
  • Ludgero Cardoso Galli Vieira
  • João Carlos Nabout
Primary Research Paper


It is important to predict how phytoplankton will respond to global warming, as changes in their composition can affect ecosystem functions. We evaluated the effect of water warming on the taxonomic and functional composition of phytoplankton and on chemical characteristics that affect their occurrence, such as dissolved oxygen, pH and conductivity. Microcosms were constructed outdoors and monitored over time. The temperature was manipulated to simulate different scenarios predicted for the future. Warming caused a reduction in dissolved oxygen, while the pH and conductivity remained unchanged. We found a joint effect of temperature and time on chlorophyll-a as well as on the species and functional groups. The substitution of species and groups occurred in a similar way between treatments. However, a greater number of Cyanophyceae individuals were found at higher temperatures, while Bacillariophyceae and Euglenophyceae species were found more commonly in the lower warming treatments. These results indicate that warming altered the taxonomic and functional composition of phytoplankton, causing species substitution as well as a change in their functional characteristics, which led to the predominance of small organisms. Thus, contribute to predicting how an increase in temperature might alter the patterns of dominance, homogenization and community dynamics in future warming scenarios.


Climate change Microcosm Microorganisms Temperature 



This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil (CAPES)–Finance Code 001. JCN thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) by research productivity grant. This paper is developed in the context of National Institutes for Science and Technology (INCT) in Ecology, Evolution and Biodiversity Conservation, supported by MCTIC/CNpq (proc. 465610/2014-5) and Fundação de Amparo a Pesquisa do Estado de Goiás (FAPEG). We thank the colleagues at the Laboratory of Biogeography and Aquatic Ecology of the Goiás State University for help in construction and filling microcosms.

Supplementary material

10750_2018_3858_MOESM1_ESM.pdf (797 kb)
Supplementary File 1 (PDF 797 kb)
10750_2018_3858_MOESM2_ESM.xlsx (183 kb)
Supplementary File 2 (XLSX 184 kb)


  1. Adams, G. L., D. E. Pichler, E. J. Cox, E. O’Gorman, A. Seeney, G. Woodward & D. C. Reuman, 2013. Diatoms can be important exception to temperature-size rules at species and community levels of organization. Global Change Biology 19: 3540–3552.PubMedPubMedCentralGoogle Scholar
  2. Anderson, N. J., 2000. Miniview: diatoms, temperature and climatic change. European Journal of Phycology 35: 307–314.Google Scholar
  3. Becker, V., L. Caputo, J. Ordóñes, R. Marcé, L. O. Crossetti & V. L. M. Huszar, 2010. Driving factors of the phytoplankton functional groups in a deep mediterranean reservoir. Water Research 44: 3345–3354.PubMedPubMedCentralGoogle Scholar
  4. Bellinger, E. G. & D. C. Sigee, 2010. Freshwater algae: Identification and use as bioindicators. Wiley Blackwell, United Kingdom.Google Scholar
  5. Berger, W. H. & F. L. Parker, 1971. Diversity of planktonic foraminifera in deep-sea sediments. Science 168: 1345–1347.Google Scholar
  6. Bertani, I., R. Primicerio & G. Rossetti, 2016. Extreme climatic event triggers a lake regime shift that propagates across multiple trophic levels. Ecosystems 19: 16–31.Google Scholar
  7. Brasil, J. & V. L. M. Huszar, 2011. O papel dos traços funcionais na ecologia do fitoplâncton continental. Oecologia Australis 15: 799–834.Google Scholar
  8. Broady, P. A. & F. Merican, 2012. Phylum Cyanobacteria, blue-green bacteria, blue-green algae. In Gordon, D. P. (ed.), New Zealand Inventory of Biodiversity: Kingdoms Bacteria, Protozoa, Chromista, Plantae, Fungi. Canterbury University Press, New Zealand: 50–69.Google Scholar
  9. Burgmer, T. & H. Hillebrand, 2011. Temperature mean and variance alter phytoplankton biomass and biodiversity in a long-term microcosm experiment. Oikos 120: 922–933.Google Scholar
  10. Callieri, C., 2017. Synechococcus plasticity under environmental changes. Microbiology Letters 364: 229.Google Scholar
  11. Carneiro, F. M., J. C. Nabout, L. C. G. Vieira, F. Roland & L. M. Bini, 2014. Determinants of chlorophyll-a concentration in tropical reservoirs. Hydrobiologia 740: 89–99.Google Scholar
  12. Carter, C. M., A. H. Ross, D. R. Schiel, C. Howard-Williams & B. Hayden, 2005. In situ microcosm experiments on the influence of nitrate and light on phytoplankton community composition. Journal of Experimental Marine Biology and Ecology 326: 1–13.Google Scholar
  13. Chen, B., 2015. Patterns of thermal limits of phytoplankton. Journal of Plankton Research 37: 285–292.Google Scholar
  14. Core Team R, 2016. R: a language and environmental for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 15 September 2017.
  15. Daufresne, M., K. Lengfellner & U. Sommer, 2009. Global warming benefits the small in aquatic ecosystems. PNAS 106: 12788–12793.PubMedGoogle Scholar
  16. Diaz, R. J. & D. L. Breitburg, 2009. The hypoxic environment. In Richards, J., A. Farrell & C. Brauner (eds), Fish Physiology: Hypoxia. Academic Press, Cambridge: 1–23.Google Scholar
  17. Dong, J., W. Zhou, L. Song & G. Li, 2015. Responses of phytoplankton functional groups to simulated winter warming. International Journal of Limnology Annales de Limnologie 51: 199–210.Google Scholar
  18. Dudgeon, D., A. H. Arthington, M. O. Gessner, Z. I. Kawabata, D. J. Knowler, C. Lévêque, R. J. Naiman, A. H. Prieur-Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81: 163–182.PubMedGoogle Scholar
  19. Ekvall, M. K. & L. A. Hanson, 2012. Differences in recruitment and life-history strategy alter zooplankton spring dynamics under climate-change conditions. PLoS ONE 7: e44614.PubMedPubMedCentralGoogle Scholar
  20. Esteves, F. A., 2011. Princípios de Limnologia, 3rd ed. Interciência, Rio de Janeiro.Google Scholar
  21. Feuchtmayr, H., D. McKee, I. F. Harvey, D. Atkinson & B. Moss, 2007. Response of macroinvertebrates to warming, nutrient addition and predation in large-scale mesocosm tanks. Hydrobiologia 584: 425–432.Google Scholar
  22. Feuchtmayr, H., R. Moran, K. Hatton, L. Connor, T. Heyes, B. Moss, I. Harvey & D. Atkinson, 2009. Global warming and eutrophication: effects on water chemistry and autotrophic communities in experimental hypertrophic shallow lake mesocosms. Journal Applied Ecology 46: 713–723.Google Scholar
  23. Field, C. B., M. J. Behrenfeld, J. T. Randerson & P. Falkowski, 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237–240.PubMedGoogle Scholar
  24. Finkel, Z. V., J. Beardall, K. J. Flynn, A. Quigg, T. A. V. Rees & J. A. Raven, 2010. Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research 32: 119–137.Google Scholar
  25. Flury, S., D. F. McGinnis & M. O. Gessner, 2010. Methane emissions from a freshwater marsh in response to experimentally simulated global warming and nitrogen enrichment. Journal of Geophysical Research 115: G01007.Google Scholar
  26. Fogg, G. E., 2001. Algal adaptation to stress – some general remarks. In Rai, L. C. & J. P. Gaur (eds), Algal Adaptation to Environmental Stress. Springer, Berlin: 1–19.Google Scholar
  27. Fu, F. X., M. E. Waner, Y. Zhang, Y. Feng & D. A. Hutchins, 2007. Effects of increase temperature and CO2 on photosynthesis, growth, and eçemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). Journal of Phycology 43: 485–496.Google Scholar
  28. Geraldes, P., C. Pascoal & F. Cássio, 2012. Effects of increased temperature and aquatic fungal diversity on litter decomposition. Fungal Ecology 5: 734–740.Google Scholar
  29. Golterman, H. L., R. S. Clymo & A. M. Ohnstad, 1978. Methods for physical and chemical analysis of freshwaters. Blackwell Scientific Publication, Oxford.Google Scholar
  30. González, J., E. Fernández, F. G. Figueiras & M. Varela, 2013. Subtle effects of the water soluble fraction of oil spills on natural phytoplankton assemblages enclosed in mesocosms. Estuarine, Coastal and Shelf Science 124: 13–23.Google Scholar
  31. Granéli, E., N. K. Vidyrathna, E. Furani, P. R. T. Cumaranatunga & R. Scenati, 2011. Can increases in temperature stimulate blooms of the toxic benthic dinoflagellate Ostreopsis ovata? Harmful Algae 10: 165–172.Google Scholar
  32. Heino, J., R. Virkkala & H. Toivonen, 2009. Climate change and freshwater biodiversity: detected patters, future trends and adaptations in northern regions. Biological Reviews 84: 39–54.Google Scholar
  33. Hennemann, M. C. & M. M. Petrucio, 2010. Seasonal phytoplankton response to increase temperature and phosphorus inputs in freshwater coastal lagoon, Southern Brazil: a microcosm bioassay. Acta Limnologica Brasiliensia 22: 295–305.Google Scholar
  34. Hoang, H. T. T., T. T. Duong, K. T. Nguyen, Q. T. P. Le, M. T. N. Luu, D. A. Trinh, A. H. Le, C. T. Ho, K. D. Dang, J. Némery, D. Orange & J. Klein, 2018. Impact of anthropogenic activities on water quality and plankton communities in the Day River (Red River Delta, Vietnam). Environmental Monitoring and Assessment 190: 67.Google Scholar
  35. Hofmann, G. E. & A. E. Todgham, 2010. Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annual Review of Physiology 72: 127–145.Google Scholar
  36. Huertas, E., M. Rouco, V. López-Rodas & E. Costas, 2011. Warming will affect phytoplankton differently: evidence through a mechanistic approach. Proceedings of the Royal Society B 278: 3534–3543.Google Scholar
  37. IPCC. 2014. Climate change 2014: Synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of IPCC. Switzerland, Geneva.Google Scholar
  38. Javaheri, N., R. Dries, A. Burson, L. J. Stal, P. M. A. Sloot & J. A. Kaandorp, 2015. Temperature affects the silicate morphology in a diatom. Nature Scientific Reports 5: 116–152.Google Scholar
  39. Jeppesen, E., B. Kronvang, M. Meerho, M. Søndergaard, K. M. Hansen, H. E. Andersen, T. L. Lauridisen, L. Liboriussen, M. Beklioglu, A. Özen & J. E. Olesen, 2009. Climate change effects on runoff, catchment phosphorus loading and lake ecological sate, and potential adaptations. Journal of Environmental Quality 38: 1930–1941.PubMedGoogle Scholar
  40. Jeppesen, E., B. Moss, H. Bennion, L. Carvalho, L. DeMeester, H. Feuchtmayr, N. Friberg, M. O. Gessner, M. Hefting, T. L. Lauridsen, L. Liboriussen, H. J. Malmquist, L. May, M. Meerhoff, J. S. Olafsson, M. B. Soons & J. T. A. Verhoeven, 2010. Interaction of climate change and eutrophication. In Kernan, M., R. W. Battarbee & B. Moss (eds), Climate Change Impacts on Freshwater Ecosystems. Blackwell, Hoboken: 120–151.Google Scholar
  41. Jeppesen, E., M. Meerhoff, T. A. Davidson, D. Trolle, M. Søndergaard, T. L. Lauridsen, M. Beklioglu, S. Brucet, P. Volta, I. González-Bergonzoni & A. Nielsen, 2014. Climate change impacts on lakes: an integrate ecological perspective based on a multi-faceted approach, with special focus on shallow lakes. Journal of Limnology 73: 84–107.Google Scholar
  42. Kosten, S., V. L. M. Huszar, E. Bécares, L. S. Costa, E. Donk, L. A. Hansson, E. Jeppesen, K. Kruk, G. Lacerot, N. Mazzeo, L. Meester, B. Moss, M. Lürling, T. Nõges, S. Romo & M. Scheffer, 2012. Warming climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118–126.Google Scholar
  43. Kratina, P., H. S. Greig, P. L. Thompson, T. S. A. Carvalho-Pereira & J. B. Shurin, 2012. Warming modifies trophic cascades and eutrophication in experimental freshwater communities. Ecology 93: 1421–1430.PubMedGoogle Scholar
  44. Kremer, C. T., M. K. Thomas & E. Litchman, 2017. Temperature and size scaling of phytoplankton population growth rates: reconciling the Eppley curve and the metabolic theory of ecology. Limnology and Oceanography 62: 1658–1670.Google Scholar
  45. Kruk, C., V. L. M. Huszar, E. T. H. M. Peeters, S. Bonilla, L. Costa, M. Lu, C. S. Reynolds & M. Scheffer, 2010. A morphological classification capturing functional variation in phytoplankton. Freshwater Biology 55: 614–627.Google Scholar
  46. Kruk, C., E. T. H. M. Peeters, E. H. Van Ness, V. L. M. Huszar, L. S. Costa & M. Scheffer, 2011. Phytoplankton community composition can be predicted best in terms of morphological groups. Limnology and Oceanography 56: 110–118.Google Scholar
  47. Kruk, C., A. M. Segura, E. T. H. M. Peeters, V. L. M. Huszar, L. S. Costa, S. Kosten, G. Lacerot & M. Scheffer, 2012. Phytoplankton species predictability increases towards warmer regions. Limnology and Oceanography 57: 1126–1135.Google Scholar
  48. Larson, C. A. & G. E. Belovsky, 2013. Salinity and nutrients influence species richness and evenness of phytoplankton communities in microcosm experiments from Great Salt lake, Utah, USA. Journal of Plankton Research 35: 1154–1166.Google Scholar
  49. Legendre, P. & L. Legendre, 1998. Numerical Ecology. Elsevier Science, Amsterdam.Google Scholar
  50. Lewandowska, A. & U. Sommer, 2010. Climate change and the spring bloom: a mesocosm study on the influence of light and temperature on phytoplankton and mesozooplankton. Marine Ecology Progress Series 405: 101–111.Google Scholar
  51. Lima-Ribeiro, M. S., S. Varela, J. González-Hernández, G. Oliveira, J. A. F. Diniz-Filho & L. C. Terribile, 2015. EcoClimate: a database of climate data from multiple models for past, present, and future for Macro ecologists and Biogeographers. Biodiversity Informatics 10: 1–21.Google Scholar
  52. Litchman, E. & C. A. Klausmeier, 2008. Trait-based community ecology of phytoplankton. Annual Review of Ecology, Evolution, and Systematics 39: 615–639.Google Scholar
  53. 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.Google Scholar
  54. Liu, X., X. Lu & Y. Chen, 2011. The effects of temperature and nutrient ratios on Microcystis blooms in lake Taihu, China: an 11-year investigation. Harmful Algae 10: 337–343.Google Scholar
  55. Lurgi, M., B. C. López & J. M. Montoya, 2012. Novel communities from climate change. Philosophical Transactions of the Royal Society B 367: 2913–2922.Google Scholar
  56. Lurling, M., F. Eshetu, E. J. Faassen, S. Kosten & V. L. M. Huszar, 2013. Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshwater Biology 58: 552–559.Google Scholar
  57. McKee, D., D. Atkinson, S. Collings, J. Eaton, L. Wolstenholme & B. Moos, 2000. Heated aquatic microcosms for climate change experiments. Freshwater Forum 14: 51–58.Google Scholar
  58. McKee, D., D. Atkinson, S. E. Collings, J. W. Eaton, A. B. Gill, I. Harvey, K. Hatton, T. Heyes, D. Wilson & B. Moss, 2003. Response of freshwater microcosm communities to nutrients, fish and elevated temperature during winter and summer. Limnology and Oceanography 48: 707–722.Google Scholar
  59. Montagnes, D. J. S. & D. J. Franklin, 2001. Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: reconsidering some paradigms. Limnology and Oceanography 46: 2008–2018.Google Scholar
  60. Moss, B., D. Mckee, D. Atkinson, S. E. Collings, J. W. Eaton, A. B. Gill, I. Harvey, K. Hatton, T. Heys & D. Wilson, 2003. How important is climate? Effects of warming, nutrient addition and fish on phytoplankton in shallow lake microcosms. Journal of Applied Ecology 40: 782–792.Google Scholar
  61. Moss, R., M. Babiker, S. Brinkman, E. Calvo, T. Cater, J. Edmonds, I. Elgizouli, S. Emori, L. Erda, K. Hibbard, R. Jones, M. Kainuma, J. Kelleher, J. F. Lamarque, M. Manning, N. Nakicenovic, B. O’Neill, R. Pichs, K. Riahi, S. Rose, R. Stouffer, D. V. Vuuren, J. Weyant, T. Wilbanks, J. P. V. Ypersele & M. Zurek, 2008. Towards new scenarios for analysis of emissions, climate change, impacts and response strategies. Technical Summary. Intergovernmental Panel on Climate Change, Geneva.Google Scholar
  62. Moss, R. H., J. A. Edmonds, K. A. Hibbard, M. R. Manning, S. K. Rose, D. P. V. Vuuren, T. R. Carter, S. Emori, M. Kainuma, G. A. Meehl, J. F. B. Mitchell, N. Nakicenovic, K. Riahi, S. J. Smith, R. J. Stouffer, A. M. Thomson, J. P. Weyant & T. J. Wilbanks, 2010. The next generation of scenarios for climate change research and assessment. Nature 463: 747–756.PubMedGoogle Scholar
  63. Moura, M. E. P., L. S. Rocha & J. C. Nabout, 2017. Effects of global climate change on chlorophyll-a concnetrations in a tropical aquatic system during a cyanobacterial blomm: a microcosm study. Ambiente & Água 12: 390–404.Google Scholar
  64. Nabout, J. C. & I. S. Nogueira, 2007. Spatial and temporal dynamics of phytoplankton functional group in a blocked valley (Brazil). Acta Limnologica Brasiliensia 19: 305–314.Google Scholar
  65. Nicolle, A., P. Hallgren, J. V. Einem, E. S. Kritzberg, W. Granéli, A. Persson & L. A. Hansson, 2012. Predict warming and browning affect timing and magnitude of plankton phonological events in lakes: a mesocosm study. Freshwater Biology 57: 684–695.Google Scholar
  66. Nogueira, P., R. B. Domingues & A. B. Barbosa, 2014. Are microcosm volume and sample pre-filtration relevant to evaluate phytoplankton growth? Journal of Experimental Marine Biology and Ecology 461: 323–330.Google Scholar
  67. O’Conner, M. I., M. F. Piehler, D. M. Leech, A. Anton & J. F. Bruno, 2009. Warming and resource availability shift food web structure and metabolism. PLoS Biology 7: e1000178.Google Scholar
  68. Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs & H. Wagner, 2017. Vegan: Community Ecology Package. R Package Version 2.4-4. Accessed 15 September 2017.
  69. Padisák, J., L. O. Crossetti & L. Naselli-Flores, 2009. Use and minuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621: 1–19.Google Scholar
  70. Paerl, H. W. & J. Huisman, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.PubMedPubMedCentralGoogle Scholar
  71. Paerl, H. W. & T. G. Otten, 2013. Harmful cyanobacterial blooms: causes, consequences and controls. Microbial Ecology 65: 995–1010.PubMedPubMedCentralGoogle Scholar
  72. Pulina, S., A. Brutemark, B. M. Padedda, L. M. Grubisic, C. T. Satta, T. Caddeo, P. Farina, N. Sechi & A. Lugliè, 2016. Effects of warming on a Mediterranean phytoplankton community. Web Ecology 16: 89–92.Google Scholar
  73. Rasconi, S., K. Winter & M. J. Kainz, 2017. Temperature increase anf fluctuation induce phytoplankton biodiversity loss – Evidence from a multi-seasonal mesocosm experiment. Ecology and Evolution. Scholar
  74. Reynolds, C. S., 2006. Ecology of Phytoplankton. Cambridge University Press, Cambridge.Google Scholar
  75. Reynolds, C. S., 2007. Variability in the provision and function of mucilage in phytoplankton: facultative responses to the environment. Hydrobiologia 578: 37–45.Google Scholar
  76. Reynolds, C. S., V. L. M. Huszar, C. Kruk, L. Naselli-Flores & S. Melo, 2002. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24: 417–428.Google Scholar
  77. Reznick, D., M. J. Bryant & F. Bashey, 2002. R- and K- selection revisited: the role of population regulation in the life-history evolution. Ecology 83: 1509–1520.Google Scholar
  78. Roland, F., V. L. M. Huszar, V. F. Farjalla, A. Enrich-Prast, A. M. Amado & J. P. H. B. Ometto, 2012. Climate change in Brazil: perspective on the biogeochemistry of inland waters. Brazilian Journal of Biology 72: 709–722.Google Scholar
  79. Santos, A. M. C., F. M. Carneiro & M. V. Cianciaruso, 2014. Predicting productivity in tropical reservoirs: the roles of phytoplankton taxonomic and functional diversity. Ecological Indicators 48: 428–435.Google Scholar
  80. Segura, A. M., F. Sarthou & C. Kruk, 2018. Morphology-based differences in the thermal response of freshwater phytoplankton. Biology Letters 14: 20170790.PubMedGoogle Scholar
  81. Senerpont Domis, L., W. M. Mooij & J. Huisman, 2007. Climate-induced shifts in an experimental phytoplankton community: a mechanistic approach. Hydrobiologia 584: 403–413.Google Scholar
  82. Senerpont Domis, L. N., A. S. G. Elser, V. L. M. Huszar, B. W. Ibelings, E. Jeppesen, S. Kosten, W. M. Mooij, F. Roland, U. Sommer, E. V. Donk, M. Winder & M. Lurling, 2013. Plankton dynamics under different climatic conditions in space and time. Freshwater Biology 58: 463–482.Google Scholar
  83. Simehgo. 2017. Sistema de Metereologia e Hidrologia do Estado de Goiás. Available in Accessed 20 August 2017.
  84. Sommer, U. & A. Lewandowska, 2011. Climate change and the phytoplankton spring bloom: warming and overwintering zooplankton have similar effects on phytoplankton. Global Change Biology 17: 154–162.Google Scholar
  85. Sommer, U., C. Paul & M. Moustaka-Gouni, 2015. Warming and ocean acidification effects on phytoplankton – From species shifts to size shifts within species in a mesocosm experiment. PLoS ONE 10: e0125239.PubMedPubMedCentralGoogle Scholar
  86. Staehr, P. A. & M. J. Birkeland, 2006. Temperature acclimation of growth, photosynthesis and respiration in two mesophilic phytoplankton species. Phycologya 45: 648–656.Google Scholar
  87. Stamenkovic’, M. & D. Hanelt, 2016. Geographic distribution and ecophysiology adaptations of desmids (Zygnematophyceae, Streptophyta) in relation to PAR, UV radiation and temperature: a review. Hydrobiologia 787: 1–26.Google Scholar
  88. Thomas, K. M., C. T. Kremer & E. Litchman, 2016. Environment and evolutionary history determine the global biogeography of phytoplankton temperature traits. Global Ecology and Biogeography 25: 75–86.Google Scholar
  89. Utermöhl, H., 1958. Zurvervoll kommung der continuousn phytoplankton-methodik. Mitteilungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 9: 1–38.Google Scholar
  90. Vollenweider, R. A., 1974. A Manual on Methods for Measuring Primary Production in Aquatic Environments. Blackwell Scientific Publications, London.Google Scholar
  91. Woodward, G., D. M. Perkins & L. E. Brown, 2010. Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philosophycal Transactions of the Royal Society B 365: 2093–2106.Google Scholar
  92. Yodzis, P., 1988. The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology 69: 508–515.Google Scholar
  93. Yvon-Durocher, G., J. M. Montoya, M. Trimmer & G. Woodward, 2011. Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems. Global Change Biology 17: 1681–1694.Google Scholar
  94. Yvon-Durocher, G., A. P. Allen, M. Cellamare, M. Dossena, K. J. Gaston, M. Leitão, J. M. Montoya, D. C. Reuman, G. Woodward & M. Trimmer, 2015. Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biology 13: e1002324.PubMedPubMedCentralGoogle Scholar
  95. Yvon-Durocher, G., C. E. Schaum & M. Trimmer, 2017. The temperature dependence of phytoplankton stoichiometry: investigating the roles of species sorting and local adaptation. Frontiers in Microbiology. Scholar
  96. Zar, J. H., 2010. Biostatistical Analysis. Pearson Print Hall, New Jersey.Google Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Karine Borges Machado
    • 1
    Email author
  • Ludgero Cardoso Galli Vieira
    • 2
  • João Carlos Nabout
    • 3
  1. 1.Instituto de Ciências BiológicasUniversidade Federal de GoiásGoiâniaBrazil
  2. 2.Universidade de Brasília (UnB)PlanaltinaBrazil
  3. 3.Universidade Estadual de GoiásAnápolisBrazil

Personalised recommendations