, Volume 831, Issue 1, pp 149–161 | Cite as

Cyanobacteria dominance drives zooplankton functional dispersion

  • Iollanda I. P. JosuéEmail author
  • Simone J. Cardoso
  • Marcela Miranda
  • Maíra Mucci
  • Kemal Ali Ger
  • Fabio Roland
  • Marcelo Manzi Marinho


Accelerated eutrophication reduces water quality and shifts plankton communities. However, its effects on the aquatic food web and ecosystem functions remain poorly understood. Within this context, functional ecology can provide valuable links relating community traits to ecosystem functioning. In this study, we assessed the effects of eutrophication and cyanobacteria blooms on zooplankton functional diversity in a tropical hypereutrophic lake. Phytoplankton and zooplankton communities and limnological characteristics of a tropical Brazilian Lake (Southeast, Brazil) were monitored monthly from April 2013 to October 2014. Lake eutrophication indicators were total phosphorus, total chlorophyll-a, and chlorophyll-a per group (blue, green, and brown). The variation of major phytoplankton taxonomic group biomass was calculated and used as a proxy for changes in phytoplankton composition. Zooplankton functional diversity was assessed through functional dispersion and the community-weighted mean trait value. Regressions were performed between the lake eutrophication indicators, the phytoplankton biomass variation, and zooplankton functional dispersion. Our results suggest that eutrophication and cyanobacterial dominance change the composition of zooplankton traits and reduce functional dispersion, leading to zooplankton niche overlap. These findings are important because they provide a meaningful view of phytoplankton-zooplankton trophic interactions and contribute to an improved understanding their functional effects on aquatic ecosystems.


Plankton Freshwater Biodiversity Eutrophication Microbial food quality 



We thank the Museu Mariano Procópio staff and Felipe Siqueira Pacheco for fieldwork support. This work was supported by Coordination for the Improvement of Higher Education Personnel (CAPES) (fellowships to IIPJ and SJC) and the National Council for Scientific and Technological Development (CNPq) (473141/2013-2 to FR).

Supplementary material

10750_2018_3710_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 19 kb)


  1. Ahlgren, G., I. B. Gustafsson & M. Boberg, 1992. Fatty acid content and chemical composition of freshwater microalgae. Journal of Phycology 28: 37–50.CrossRefGoogle Scholar
  2. Alvares, C. A., J. L. Stape, P. C. Sentelhas, G. de Moraes, J. Leonardo & G. Sparovek, 2014. Köppen's climate classification map for Brazil. Meteorologische Zeitschrift 22: 711–728.CrossRefGoogle Scholar
  3. Arndt, H., 1993. Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates)—a review. Hydrobiologia 255: 231–246.CrossRefGoogle Scholar
  4. Barnett, A. & B. E. Beisner, 2007. Zooplankton biodiversity and lake trophic state: Explanations invoking resource abundance and distribution. Ecology 88: 1675–1686.CrossRefGoogle Scholar
  5. Bec, A., D. Martin-Creuzburg & E. von Elert, 2006. Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnology and Oceanography 51: 1699–1707.CrossRefGoogle Scholar
  6. Bini, L. M., V. L. Landeiro, A. A. Padial, T. Siqueira & J. Heino, 2014. Nutrient enrichment is related to two facets of beta diversity for stream invertebrates across the United States. Ecology 95: 1569–1578.CrossRefGoogle Scholar
  7. Bouvy, M., M. Pagano & M. Troussellier, 2001. Effects of a cyanobacterial bloom (Cylindrospermopsis raciborskii) on bacteria and zooplankton communities in Ingazeira reservoir (northeast Brazil). Aquatic Microbial Ecology 25: 215–227.CrossRefGoogle Scholar
  8. Boyero, L., M. A. G. Tonin, J. Pérez, A. Swafford, V. Ferreira, A. Landeira-Dabarca, M. Alexandrou, M. O. Gessner, B. G. McKie & R. J. Albariño, 2017. Riparian plant litter quality increases with latitude. Scientific Reports 7: 10562.CrossRefGoogle Scholar
  9. Brett, M. T. & D. C. Müller-Navarra, 1997. The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biology 38: 483–499.CrossRefGoogle Scholar
  10. Brett, M. T., M. J. Kainz, S. J. Taipale & H. Seshan, 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proceedings of the National Academy of Sciences 106: 21197–21201.CrossRefGoogle Scholar
  11. Carpenter, S. R. & J. F. Kitchell, 1996. The trophic cascade in lakes. Cambridge University Press, England.Google Scholar
  12. Carpenter, S. R., J. F. Kitchell & J. R. Hodgson, 1985. Cascading trophic interactions and lake productivity. BioScience 35: 634–639.CrossRefGoogle Scholar
  13. Chapin III, F. S., E. S. Zavaleta, V. T. Eviner, R. L. Naylor, P. M. Vitousek, H. L. Reynolds, D. U. Hooper, S. Lavorel, O. E. Sala, S. E. Hobbie & M. C. Mack, 2000. Consequences of changing biodiversity. Nature 405: 234–242.CrossRefGoogle Scholar
  14. Chase, J. M., 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328: 1388–1391.CrossRefGoogle Scholar
  15. Cotner, J. B. & B. A. Biddanda, 2002. Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5: 105–121.CrossRefGoogle Scholar
  16. DeMott, W. R., 1986. The role of taste in food selection by freshwater zooplankton. Oecologia 69: 334–340.CrossRefGoogle Scholar
  17. DeMott, W. R. & F. Moxter, 1991. Foraging cyanobacteria by copepods: Responses to chemical defense and resource abundance. Ecology 72: 1820–1834.CrossRefGoogle Scholar
  18. DeMott, W. R., Q. X. Zhang & W. W. Carmichael, 1991. Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnology and Oceanography 36: 1346–1357.CrossRefGoogle Scholar
  19. DeMott, W. R., R. D. Gulati & E. Van Donk, 2001. Daphnia food limitation in three hypereutrophic Dutch lakes: evidence for exclusion of large-bodied species by interfering filaments of cyanobacteria. Limnology and Oceanography 46: 2054–2060.CrossRefGoogle Scholar
  20. Díaz, S. & M. Cabido, 2001. Vive la différence: Plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16: 646–655.CrossRefGoogle Scholar
  21. Dumont, H. J., I. Van De Velde & S. Dumont, 1975. The dry weight estimate of biomass in a selection of Cladocera, Copepoda, and Rotifera from the plankton, periphyton, and benthos of continental waters. Oecologia 19: 75–97.CrossRefGoogle Scholar
  22. Engström-Öst, J., A. Brutemark, A. Vehmaa, N. H. Motwani & T. Katajisto, 2015. Consequences of a cyanobacteria bloom for copepod reproduction, mortality and sex ratio. Journal of Plankton Research 37: 388–398.CrossRefGoogle Scholar
  23. Ersoy, Z., E. Jeppesen, S. Sgarzi, I. Arranz, M. Cañedo-Argüelles, X. D. Quintana, F. Landkildehus, T. L. Lauridsen, M. Bartrons & S. Brucet, 2017. Size-based interactions and trophic transfer efficiency are modified by fish predation and cyanobacteria blooms in Lake Mývatn, Iceland. Freshwater Biology 62: 1942–1952.Google Scholar
  24. Figueredo, C. C., R. M. Pinto-Coelho, A. M. M. Lopes, P. H. Lima, B. Gücker & A. Giani, 2016. From intermittent to persistent cyanobacterial blooms: Identifying the main drivers in an urban tropical reservoir. Journal of Limnology 75: 445–454.Google Scholar
  25. Gasol, J. M. & C. M. Duarte, 2000. Comparative analyses in aquatic microbial ecology: How far do they go? FEMS Microbiology Ecology 31: 99–106.CrossRefGoogle Scholar
  26. Ger, K. A., R. Panosso & M. Lürling, 2011. Consequences of acclimation to Microcystis on the selective feeding behavior of the calanoid copepod Eudiaptomus gracilis. Limnology and Oceanography 56: 2103–2114.CrossRefGoogle Scholar
  27. Ger, K. A., P. Urrutia-Cordero, P. C. Frost, L. A. Hansson, O. Sarnelle, A. E. Wilson & M. Lürling, 2016. The interaction between cyanobacteria and zooplankton in a more eutrophic world. Harmful Algae 54: 128–144.CrossRefGoogle Scholar
  28. Ghadouani, A., B. Pinel-Alloul & E. E. Prepas, 2003. Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshwater Biology 48: 363–381.CrossRefGoogle Scholar
  29. Hairston Jr., N. G., C. L. Holtmeier, W. Lampert, L. J. Weider, D. M. Post, J. M. Fischer, C. E. Caceres, J. A. Fox & U. Gaedke, 2001. Natural selection for grazer resistance to toxic cyanobacteria: Evolution of phenotypic plasticity? Evolution 55: 2203–2214.CrossRefGoogle Scholar
  30. Hansson, L. A., S. Gustafsson, K. Rengefors & L. Bomark, 2007. Cyanobacterial chemical warfare affects zooplankton community composition. Freshwater Biology 52: 1290–1301.CrossRefGoogle Scholar
  31. Harrison, S., M. Vellend & E. I. Damschen, 2011. ‘Structured’beta diversity increases with climatic productivity in a classic dataset. Ecosphere 2: 1–13.CrossRefGoogle Scholar
  32. Heathcote, A. J., C. T. Filstrup, D. Kendall & J. A. Downing, 2016. Biomass pyramids in lake plankton: Influence of Cyanobacteria size and abundance. Inland Waters 6: 250–257.CrossRefGoogle Scholar
  33. Hébert, M. P., B. E. Beisner & R. Maranger, 2016. A meta-analysis of zooplankton functional traits influencing ecosystem function. Ecology 97: 1069–1080.CrossRefGoogle Scholar
  34. Hébert, M. P., B. E. Beisner & R. Maranger, 2017. Linking zooplankton communities to ecosystem functioning: Toward an effect-trait framework. Journal of Plankton Research 39: 3–12.CrossRefGoogle Scholar
  35. Hillebrand, H., C. D. Durselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.CrossRefGoogle Scholar
  36. Hooper, D. U., F. S. Chapin, J. J. Ewel, A. Hector, P. Inchausti, S. H. Lavorel, J. Lawton, D. M. Lodge, M. Loreau, S. Naeem, B. Schmid, H. Setälä, A. J. Symstad, J. Vandermeer & D. A. Wardle, 2005. Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecological Monographs 75: 3–35.CrossRefGoogle Scholar
  37. Kassen, R., A. Buckling, G. Bell & P. B. Rainey, 2000. Diversity peaks at intermediate productivity in a laboratory microcosm. Nature 406: 508–512.CrossRefGoogle Scholar
  38. Kiørboe, T., 2011. How zooplankton feed: Mechanisms, traits, and trade-offs. Biological Reviews 86: 311–339.CrossRefGoogle Scholar
  39. Komárek, J. & K. Anagnostidis, 1998. Cyanoprokaryota. 1. Teil Chroococcales. In Ettl, H., G. Gärtner, H. Heynig & D. Möllenhauer (eds), Sübwasserflora von Mitteleuropa. Gustav Fischer Verlag, Stuttgart: 1–548.Google Scholar
  40. Komárek, J. & K. Anagnostidis, 2005. Cyanoprokaryota. 2. Teil Oscillatoriales. In: B. Büdel, L. Krienitz, G. Gärtner & M. Schagerl (eds). Sübwasserflora von Mitteleuropa. Elsevier: Spektrum Akademischer Verlag, Munique.Google Scholar
  41. Kosiba, J., W. Krztoń & E. Wilk-Woźniak, 2018. Effect of microcystins on proto-and metazooplankton is more evident in artificial than in natural waterbodies. Microbial Ecology 75: 293–302.CrossRefGoogle Scholar
  42. Laliberté, E., P. Legendre & B. Shipley, 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12Google Scholar
  43. Laliberté, E. & P. Legendre, 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91: 299–305.CrossRefGoogle Scholar
  44. Litchman, E., M. D. Ohman & T. Kiørboe, 2013. Trait-based approaches to zooplankton communities. Journal of Plankton Research 35: 473–484.CrossRefGoogle Scholar
  45. Lund, J. W. H., C. Kipling & E. D. Cren, 1958. The inverted microscope method of estimating algal number and statistical basis of estimating by counting. Hydrobiologia 11: 143–170.CrossRefGoogle Scholar
  46. Lürling, M., 2003. Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus. Limnology and Oceanography 48: 2214–2220.CrossRefGoogle Scholar
  47. MacArthur, R. H., 1970. Species packing and competitive equilibria for many species. Theoretical Population Biology 1: 1–11.CrossRefGoogle Scholar
  48. Miranda, M., N. Noyma, F. S. Pacheco, L. de Magalhães, E. Pinto, S. Santos, M. F. A. Soares, V. L. Huszar, M. Lürling & M. M. Marinho, 2017. The efficiency of combined coagulant and ballast to remove harmful cyanobacterial blooms in a tropical shallow system. Harmful Algae 65: 27–39.CrossRefGoogle Scholar
  49. Moss, B., S. Kosten, M. Meerhoff, R. W. Battarbee, E. Jeppesen, N. Mazzeo, K. Havens, G. Lacerot, Z. Liu, L. De Meester & H. Paerl, 2011. Allied attack: Climate change and eutrophication. Inland Waters 1: 101–105.CrossRefGoogle Scholar
  50. Müller-Navarra, D. C., M. T. Brett, A. M. Liston & C. R. Goldman, 2000. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403: 74–77.CrossRefGoogle Scholar
  51. Obertegger, U., H. A. Smith, G. Flaim & R. L. Wallace. 2011. Using the guild ratio to characterize pelagicrotifer communities. Hydrobiologia 662: 157–162.CrossRefGoogle Scholar
  52. Paerl, H. W. & J. Huisman, 2009. Climate change: A catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.CrossRefGoogle Scholar
  53. Paerl, H. W. & V. J. Paul, 2012. Climate change: Links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.CrossRefGoogle Scholar
  54. Paerl, H. W., R. S. Fulton, P. H. Moisander & J. Dyble, 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. The Scientific World Journal 1: 76–113.CrossRefGoogle Scholar
  55. Panosso, R., P. E. R. Carlsson, B. Kozlowsky-Suzuki, S. M. Azevedo & E. Granéli, 2003. Effect of grazing by a neotropical copepod, Notodiaptomus, on a natural cyanobacterial assemblage and on toxic and non-toxic cyanobacterial strains. Journal of Plankton Research 25: 1169–1175.CrossRefGoogle Scholar
  56. Pavoine, S., J. Vallet, A. B. Dufour, S. Gachet & H. Daniel, 2009. On the challenge of treating various types of variables: Application for improving the measurement of functional diversity. Oikos 118: 391–402.CrossRefGoogle Scholar
  57. Petchey, O. L. & K. J. Gaston, 2002. Functional diversity (FD), species richness and community composition. Ecology Letters 5: 402–411.CrossRefGoogle Scholar
  58. Pla, L., F. Casanoves & J. Di Rienzo, 2011. Quantifying Functional Biodiversity. Springer, Berlin.Google Scholar
  59. Ptacnik, R., A. G. Solimini, T. Andersen, T. Tamminen, P. Brettum, L. Lepistö, E. Willén & S. Rekolainen, 2008. Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proceedings of the National Academy of Sciences of the United States of America 105: 5134–5138.CrossRefGoogle Scholar
  60. Rangel, L. M., M. C. S. Soares, R. Paiva & L. H. Silva, 2016. Morphology-based functional groups as effective indicators of phytoplankton dynamics in a tropical cyanobacteria-dominated transitional river–reservoir system. Ecological Indicators 64: 217–227.CrossRefGoogle Scholar
  61. R Core Team, 2015. R: A language and environment for statistical computingGoogle Scholar
  62. Ruttner-Kolisko, A., 1977. Suggestions for biomass calculation of plankton rotifers. Arch. Hydrobiologia 8: 71–76.Google Scholar
  63. Sarnelle, O. & A. E. Wilson, 2005. Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnology and Oceanography 50: 1565–1570.CrossRefGoogle Scholar
  64. Schreiber, U. 1998. Chlorophyll fluorescence: New instruments for special applications. In Photosynthesis: Mechanisms and Effects. Springer, Dordrecht: 4253–4258.Google Scholar
  65. Soares, M. C. S., M. Lürling, R. Panosso & V. Huszar, 2009. Effects of the cyanobacterium Cylindrospermopsis raciborskii on feeding and life-history characteristics of the grazer Daphnia magna. Ecotoxicology and Environmental Safety 72: 1183–1189.CrossRefGoogle Scholar
  66. Steinberg, C. E. & H. M. Hartmann, 1988. Planktonic bloom-forming cyanobacteria and the eutrophication of lakes and rivers. Freshwater Biology 20: 279–287.CrossRefGoogle Scholar
  67. Sterner, R. W., 2009. Role of zooplankton in aquatic ecosystems. In Likens, G. E. (ed.), Encyclopedia of Inland Waters. Elsevier, Oxford: 678–688.CrossRefGoogle Scholar
  68. Sterner, R. W. & D. O. Hessen, 1994. Algal nutrient limitation and the nutrition of aquatic herbivores. The Annual Review of Ecology, Evolution and Systematics 25: 1–29.CrossRefGoogle Scholar
  69. Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik: Mit 1 Tabelle und 15 abbildungen im Text und auf 1 Tafel. Internationale Vereinigung für theoretische und angewandte Limnologie: Mitteilungen 9: 1–38.Google Scholar
  70. Van den Hoek, C., D. Mann & H. M. Jahns, 1995. Algae: An Introduction to Phycology. Cambridge University Press, New York.Google Scholar
  71. Vanni, M., 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology, Evolution, and Systematics 33: 341–370.CrossRefGoogle Scholar
  72. 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.CrossRefGoogle Scholar
  73. Vogt, R. J., P. R. Peres-Neto & B. E. Beisner, 2013. Using functional traits to investigate the determinants of crustacean zooplankton community structure. Oikos 122: 1700–1709.CrossRefGoogle Scholar
  74. Wetzel, R. G. & G. E. Likens, 1990. Limnological Analyses. 2nd ed. Springer, New York.Google Scholar
  75. Wilson, A. E., O. Sarnelle & A. R. Tillmanns, 2006. Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: Meta-analyses of laboratory experiments. Limnology and Oceanography 51: 1915–1924.CrossRefGoogle Scholar
  76. Yang, Z., F. Kong, X. Shi & H. Cao, 2006. Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia 563: 225–230.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Iollanda I. P. Josué
    • 1
    • 2
    Email author
  • Simone J. Cardoso
    • 2
  • Marcela Miranda
    • 2
  • Maíra Mucci
    • 3
  • Kemal Ali Ger
    • 4
  • Fabio Roland
    • 2
  • Marcelo Manzi Marinho
    • 5
  1. 1.Laboratory of Limnology, Department of Ecology, Institute of BiologyFederal University of Rio de JaneiroRio de JaneiroBrazil
  2. 2.Department of Biology, Institute of BiologyFederal University of Juiz de ForaJuiz de ForaBrazil
  3. 3.Aquatic Ecology and Water Quality Management Group, Department of Environmental SciencesWageningen UniversityWageningenThe Netherlands
  4. 4.Center for BiosciencesFederal University of Rio Grande do NorteNatalBrazil
  5. 5.Laboratory of Ecology and Physiology of Phytoplankton, Department of Plant BiologyUniversity of Rio de Janeiro StateRio de JaneiroBrazil

Personalised recommendations