Skip to main content

Advertisement

SpringerLink
Log in

Cyanobacteria dominance drives zooplankton functional dispersion

  • PHYTOPLANKTON & BIOTIC INTERACTIONS
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahlgren, G., I. B. Gustafsson & M. Boberg, 1992. Fatty acid content and chemical composition of freshwater microalgae. Journal of Phycology 28: 37–50.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Arndt, H., 1993. Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates)—a review. Hydrobiologia 255: 231–246.

    Article  Google Scholar 

  • Barnett, A. & B. E. Beisner, 2007. Zooplankton biodiversity and lake trophic state: Explanations invoking resource abundance and distribution. Ecology 88: 1675–1686.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Carpenter, S. R. & J. F. Kitchell, 1996. The trophic cascade in lakes. Cambridge University Press, England.

    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 

  • 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.

    Article  CAS  Google Scholar 

  • Chase, J. M., 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328: 1388–1391.

    Article  CAS  Google Scholar 

  • Cotner, J. B. & B. A. Biddanda, 2002. Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5: 105–121.

    Article  CAS  Google Scholar 

  • DeMott, W. R., 1986. The role of taste in food selection by freshwater zooplankton. Oecologia 69: 334–340.

    Article  Google Scholar 

  • DeMott, W. R. & F. Moxter, 1991. Foraging cyanobacteria by copepods: Responses to chemical defense and resource abundance. Ecology 72: 1820–1834.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Díaz, S. & M. Cabido, 2001. Vive la différence: Plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 16: 646–655.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • Gasol, J. M. & C. M. Duarte, 2000. Comparative analyses in aquatic microbial ecology: How far do they go? FEMS Microbiology Ecology 31: 99–106.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ghadouani, A., B. Pinel-Alloul & E. E. Prepas, 2003. Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshwater Biology 48: 363–381.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hansson, L. A., S. Gustafsson, K. Rengefors & L. Bomark, 2007. Cyanobacterial chemical warfare affects zooplankton community composition. Freshwater Biology 52: 1290–1301.

    Article  CAS  Google Scholar 

  • Harrison, S., M. Vellend & E. I. Damschen, 2011. ‘Structured’beta diversity increases with climatic productivity in a classic dataset. Ecosphere 2: 1–13.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hébert, M. P., B. E. Beisner & R. Maranger, 2016. A meta-analysis of zooplankton functional traits influencing ecosystem function. Ecology 97: 1069–1080.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kassen, R., A. Buckling, G. Bell & P. B. Rainey, 2000. Diversity peaks at intermediate productivity in a laboratory microcosm. Nature 406: 508–512.

    Article  CAS  Google Scholar 

  • Kiørboe, T., 2011. How zooplankton feed: Mechanisms, traits, and trade-offs. Biological Reviews 86: 311–339.

    Article  Google Scholar 

  • 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 

  • 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.

  • 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.

    Article  CAS  Google Scholar 

  • Laliberté, E., P. Legendre & B. Shipley, 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12

  • Laliberté, E. & P. Legendre, 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91: 299–305.

    Article  Google Scholar 

  • Litchman, E., M. D. Ohman & T. Kiørboe, 2013. Trait-based approaches to zooplankton communities. Journal of Plankton Research 35: 473–484.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • MacArthur, R. H., 1970. Species packing and competitive equilibria for many species. Theoretical Population Biology 1: 1–11.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Obertegger, U., H. A. Smith, G. Flaim & R. L. Wallace. 2011. Using the guild ratio to characterize pelagicrotifer communities. Hydrobiologia 662: 157–162.

    Article  Google Scholar 

  • Paerl, H. W. & J. Huisman, 2009. Climate change: A catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.

    Article  CAS  Google Scholar 

  • Paerl, H. W. & V. J. Paul, 2012. Climate change: Links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Petchey, O. L. & K. J. Gaston, 2002. Functional diversity (FD), species richness and community composition. Ecology Letters 5: 402–411.

    Article  Google Scholar 

  • Pla, L., F. Casanoves & J. Di Rienzo, 2011. Quantifying Functional Biodiversity. Springer, Berlin.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • R Core Team, 2015. R: A language and environment for statistical computing

  • Ruttner-Kolisko, A., 1977. Suggestions for biomass calculation of plankton rotifers. Arch. Hydrobiologia 8: 71–76.

    Google Scholar 

  • Sarnelle, O. & A. E. Wilson, 2005. Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnology and Oceanography 50: 1565–1570.

    Article  Google Scholar 

  • Schreiber, U. 1998. Chlorophyll fluorescence: New instruments for special applications. In Photosynthesis: Mechanisms and Effects. Springer, Dordrecht: 4253–4258.

  • 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.

    Article  CAS  Google Scholar 

  • Steinberg, C. E. & H. M. Hartmann, 1988. Planktonic bloom-forming cyanobacteria and the eutrophication of lakes and rivers. Freshwater Biology 20: 279–287.

    Article  Google Scholar 

  • Sterner, R. W., 2009. Role of zooplankton in aquatic ecosystems. In Likens, G. E. (ed.), Encyclopedia of Inland Waters. Elsevier, Oxford: 678–688.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Van den Hoek, C., D. Mann & H. M. Jahns, 1995. Algae: An Introduction to Phycology. Cambridge University Press, New York.

    Google Scholar 

  • Vanni, M., 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology, Evolution, and Systematics 33: 341–370.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wetzel, R. G. & G. E. Likens, 1990. Limnological Analyses. 2nd ed. Springer, New York.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

  1. Laboratory of Limnology, Department of Ecology, Institute of Biology, Federal University of Rio de Janeiro, CCS, Cidade Universitária, Rio de Janeiro, Brazil

    Iollanda I. P. Josué

  2. Department of Biology, Institute of Biology, Federal University of Juiz de Fora, Juiz de Fora, Brazil

    Iollanda I. P. Josué, Simone J. Cardoso, Marcela Miranda & Fabio Roland

  3. Aquatic Ecology and Water Quality Management Group, Department of Environmental Sciences, Wageningen University, Wageningen, The Netherlands

    Maíra Mucci

  4. Center for Biosciences, Federal University of Rio Grande do Norte, Natal, Brazil

    Kemal Ali Ger

  5. Laboratory of Ecology and Physiology of Phytoplankton, Department of Plant Biology, University of Rio de Janeiro State, Rio de Janeiro, Brazil

    Marcelo Manzi Marinho

Authors
  1. Iollanda I. P. Josué
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simone J. Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marcela Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maíra Mucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kemal Ali Ger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabio Roland
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcelo Manzi Marinho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iollanda I. P. Josué.

Additional information

Guest editors: Hugo Sarmento, Irina Izaguirre, Vanessa Becker & Vera L. M. Huszar / Phytoplankton and its Biotic Interactions

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Josué, I.I.P., Cardoso, S.J., Miranda, M. et al. Cyanobacteria dominance drives zooplankton functional dispersion. Hydrobiologia 831, 149–161 (2019). https://doi.org/10.1007/s10750-018-3710-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3710-0

Keywords

Search

Navigation