Skip to main content
SpringerLink
Log in

Effects of bottom-up and top-down controls on the temporal distribution of planktonic heterotrophic nanoflagellates are dependent on water depth

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

We evaluated the relative importance of bottom-up and top-down mechanisms in controlling the density of a heterotrophic nanoflagellate (HNF) community in a shallow lake (Guaraná Lake) on the Paraná River floodplain (State of Mato Grosso do Sul, Brazil). Samples were taken monthly from March 2007 through February 2008, in three strata (surface, middle and bottom). Bacterial and cladoceran densities were the variables most associated with HNF density. However, there was a gradual decoupling between HNF and bacteria from the subsurface to the bottom of the lake. Most likely, this was caused by high predation by cladocerans on HNF in the deeper layer. Our results suggest that the overwhelming dominance of a single type of control on HNF dynamics may be more the exception than the rule.

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
Fig. 5

Similar content being viewed by others

References

  • Adrian, R. & B. Schneider-Olt, 1999. Top–down effects of crustacean zooplankton on pelagic microorganisms in a mesotrophic lake. Journal of Plankton Research 21: 2175–2190.

    Article  Google Scholar 

  • Adrian, R., S. A. Wickham & N. M. Butler, 2001. Trophic interactions between zooplankton and the microbial community in contrasting food webs: the epilimnion and deep chlorophyll maximum of a mesotrophic lake. Aquatic Microbial Ecology 24: 83–97.

    Article  Google Scholar 

  • Araújo, M. F. F. & M. J. L. Godinho, 2009. Short-term variations of virus-like particles in a tropical lake: relationship with microbial communities (bacteria, ciliates and flagellates). Microbiological Research 164: 411–419.

    Article  PubMed  Google Scholar 

  • Arndt, H., 1993. Rotifers as predators on components of the microbial web. Hydrobiologia 255(256): 231–246.

    Article  Google Scholar 

  • Arndt, H., D. Dietrich, B. Auer, E. J. Cleven, T. Gräfenhan, M. Weitere & A. P. Mylnikov, 2000. Functional diversity of heterotrophic flagellates in aquatic ecosystems. In Leadbeater, B. S. C. & J. C. Green (eds), The Flagellates: Unity, Diversity and Evolution. Taylor & Francis, London: 240–268.

    Google Scholar 

  • Auer, B. & H. Arndt, 2001. Taxonomic composition and biomass of heterotrophic flagellates in relation to lake trophy and season. Freshwater Biology 46: 959–972.

    Article  Google Scholar 

  • Auer, B. & H. Arndt, 2004. Comparison of pelagic food webs in lakes along a trophic gradient and with seasonal aspects: influence of resources and predation. Journal of Plankton Research 26: 697–709.

    Article  Google Scholar 

  • Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil & F. Thingstad, 1983. The ecological role of water column microbes in the sea. Marine Ecology Progress Series 10: 257–263.

    Article  Google Scholar 

  • Becker, C., H. Feuchtmayr, D. Brepohl, B. Santer & M. Boersma, 2004. Differential impacts of copepods and cladocerans on lake seston, and resulting effects on zooplankton growth. Hydrobiologia 526: 197–207.

    Article  CAS  Google Scholar 

  • Berdjeb, L., J. F. Ghiglione & S. Jacquet, 2011. Bottom–up versus top–down control of hypo- and epilimnion free-living bacterial community structures in two neighboring freshwater lakes. Applied and Environmental Microbiology 77: 3591–3599.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Berglund, J., K. Samuelsson, T. Kull, U. Muren & A. Andersson, 2005. Relative strength of resource and predation limitation of heterotrophic nanoflagellates in a low-productive sea area. Journal of Plankton Research 27: 923–935.

    Article  Google Scholar 

  • Berninger, U. G., B. J. Finlay & P. Kuuppo-Leinikki, 1991. Protozoan control of bacterial abundances in freshwaters. Limnology and Oceanography 36: 139–147.

    Article  Google Scholar 

  • Bettarel, Y., T. Sime-Ngando, M. Bouvy, R. Arfi & C. Amblard, 2005. Low consumption of virus-sized particles by heterotrophic nanoflagellates in two lakes of the French Massif Central. Aquatic Microbial Ecology 39: 205–209.

    Article  Google Scholar 

  • Bjørnsen, P. K., 1986. Automatic determination of bacterioplankton biomass by means of image analysis. Applied Environmental Microbiology 51: 1199–1204.

    PubMed Central  PubMed  Google Scholar 

  • Bottrell, H. H., A. Duncan, Z. M. Gliwicz, E. Grygierek, A. Herzig, A. Hillbricht-Ilkowska, H. Kurasawa, P. Larsson & T. Weglenska, 1976. A review of some problems in zooplankton production studies. Norwegian Journal of Zoology 24: 419–456.

    Google Scholar 

  • Brett, M. T. & C. R. Goldman, 1997. Consumer versus resource control in freshwater pelagic food webs. Science 275: 384–386.

    Article  CAS  PubMed  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretical Approach. Springer, New York.

    Google Scholar 

  • Burns, C. W. & M. Schallenberg, 1996. Relative impacts of copepods, cladocerans and nutrients on the microbial food web of a mesotrophic lake. Journal of Plankton Research 18: 683–714.

    Article  Google Scholar 

  • Burns, C. W. & M. Schallenberg, 2001. Calanoid copepods versus cladocerans: Consumer effects on protozoa in lakes of different trophic status. Limnology and Oceanography 46: 1558–1565.

    Article  CAS  Google Scholar 

  • Carrias, J. F., C. Amblard, C. Quiblier-Lloberas & G. Bourdier, 1998. Seasonal dynamics of free and attached heterotrophic nanoflagellates in an oligotrophic lake. Freshwater Biology 39: 91–101.

    Article  Google Scholar 

  • Fenchel, T., 1982. Ecology of heterotrophic flagellates IV. Quantitative occurrence and importance as bacterial consumers. Marine Ecology Progress Series 9: 35–42.

    Article  Google Scholar 

  • Fermani, P., N. Diovisalvi, A. Torremorell, L. Lagomarsino, H. E. Zagarese & F. Unrein, 2013. The microbial food web structure of a hypertrophic warm-temperate shallow lake, as affected by contrasting zooplankton assemblages. Hydrobiologia 714: 115–130.

    Article  CAS  Google Scholar 

  • Finlay, B. J., K. J. Clarke, A. J. Cowling, R. M. Hidle, A. Rogerson & U. G. Berninger, 1988. On the abundance and distribution of protozoa and their food in a productive freshwater pond. European Journal of Protistology 23: 205–217.

    Article  CAS  PubMed  Google Scholar 

  • Gasol, J. M., 1994. A framework for the assessment of top–down vs bottom–up control of heterotrophic nanoflagellate abundance. Marine Ecology Progress Series 113: 291–300.

    Article  Google Scholar 

  • Gasol, J. M. & D. Vaqué, 1993. Lack of coupling between heterotrophic nanoflagellates and bacteria: a general phenomenon across aquatic systems? Limnology and Oceanography 38: 665–670.

    Article  Google Scholar 

  • Gasol, J. M., A. M. Simons & J. Kalff, 1995. Patterns in the top–down vs bottom–up regulation of heterotrophic nanoflagellates. Journal of Plankton Research 17: 1879–1903.

    Article  Google Scholar 

  • Golterman, H. L., R. S. Clymo & M. A. M. Ohnstad, 1978. Methods for Physical and Chemical Analysis of Freshwater. Blackwell Scientific Publication, London.

    Google Scholar 

  • Hunter, M. & P. W. Price, 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom–up and top–down forces in natural communities. Ecology 73: 724–732.

    Google Scholar 

  • Jackson, D. A., 1993. Stopping rules in principal component analyses: a comparison of heuristical and statistical approaches. Ecology 74: 2204–2214.

    Article  Google Scholar 

  • Johnson, J. B. & K. S. Omland, 2004. Model selection in ecology and evolution. Trends in Ecology and Evolution 19: 101–108.

    Article  PubMed  Google Scholar 

  • Jones, R. I., 1992. The influence of humic substances on lacustrine planktonic food chains. Hydrobiologia 229: 73–91.

    Article  CAS  Google Scholar 

  • Jürgens, K. & G. Stolpe, 1995. Seasonal dynamics of crustacean zooplankton, heterotrophic nanoflagellates and bacteria in a shallow, eutrophic lake. Freshwater Biology 33: 27–38.

    Article  Google Scholar 

  • Jürgens, K., J. M. Gasol, R. Massana & C. Pedrós-Alió, 1994. Control of heterotrophic bacteria and protozoans by Daphnia pulex in the epilimnion of Lake Cisó. Archiv für Hydrobiologie 131: 55–78.

    Google Scholar 

  • Jürgens, K., S. A. Wickham, K. O. Rothhaupt & B. Santer, 1996. Feeding rates of macro- and microzooplankton on heterotrophic nanoflagellates. Limnology and Oceanography 41: 1833–1839.

    Article  Google Scholar 

  • Kalff, J., 2002. Limnology. Prentice Hall, New Jersey.

    Google Scholar 

  • Kent, A. D., S. E. Jones, A. C. Yannarell, J. M. Graham, G. H. Lauster, T. K. Kratz & E. W. Triplett, 2004. Annual patterns in bacterioplankton community variability in a humic lake. Microbial Ecology 48: 550–560.

    Article  CAS  PubMed  Google Scholar 

  • Kosolapova, N. G. & D. B. Kosolapov, 2009. The diversity and distribution of heterotrophic nanoflagellates in the eutrophic Lake Nero. Inland Water Biology 2: 42–49.

    Article  Google Scholar 

  • Laybourn-Parry, J. E. M. & J. D. Parry, 2000. Flagellates and the microbial loop. In Leadbeater, B. S. C. & J. Green (eds), The Flagellates: Unity, Diversity and Evolution. Taylor & Francis, London: 216–239.

    Google Scholar 

  • Laybourn-Parry, J. & A. Rogerson, 1993. Seasonal patterns of protozooplankton in Lake Windermere, England. Archiv für Hydrobiologie 129: 25–43.

    Google Scholar 

  • Mackereth, J. F. H., J. Heron & J. F. Talling, 1978. Water analysis: some revised methods for limnologists. Scientific Publications of the Freshwater Biological Association 36: 1–120.

    Google Scholar 

  • Madoni, P., 1984. Estimation of the size of freshwater ciliate populations by a sub-sampling technique. Hydrobiologia 111: 201–206.

    Article  Google Scholar 

  • Manly, B. F. J., 1994. Multivariate Statistical Methods: A Primer. Chapman & Hall, London.

    Google Scholar 

  • Mariottini, G. L. & L. Pane, 2003. Ecology of planktonic heterotrophic flagellates. A Review. Biology Forum 96: 55–72.

    Google Scholar 

  • Merrell, J. R. & D. K. Stoecker, 1998. Differential grazing on protozoan microplankton by developmental stages of the calanoid copepod Eurytemora affinis Poppe. Journal of Plankton Research 20: 289–304.

    Article  Google Scholar 

  • Nakano, S., P. M. Manage, Y. Nishibe & Z. Kawabata, 2001. Trophic linkage among heterotrophic nanoflagellates, ciliates and metazoan zooplankton in a hypereutrophic pond. Aquatic Microbial Ecology 25: 259–270.

    Article  Google Scholar 

  • Pace, M. L. & D. Vaqué, 1994. The importance of Daphnia in determining mortality rates of protozoans and rotifers in lakes. Limnology and Oceanography 39: 985–996.

    Article  Google Scholar 

  • Patterson, D. J. & J. Larsen, 1991. The Biology of Free-Living Heterotrophic Flagellates. Clarendon Press, Oxford.

    Google Scholar 

  • Pereira, D. G., L. F. M. Velho, T. A. Pagioro & F. A. Lansac-Tôha, 2005. Abundância de nanoflagelados heterotróficos no plâncton de reservatórios com distintos graus de trofia. Acta Scientiarum, Biological Sciences 27: 43–50.

    Article  Google Scholar 

  • Pereira, D. G., B. T. S. Silva, J. C. Camargo, L. F. M. Velho, G. M. Pauleto & F. A. Lansac-Tôha, 2010. Effects of eutrophication on flagellates associated with Eichhornia crassipes: an experimental approach. International Review of Hydrobiology 95: 72–85.

    Article  Google Scholar 

  • Rangel, T. F., J. A. F. Diniz-Filho & L. M. Bini, 2010. SAM: a comprehensive application for spatial analysis in macroecology. Ecography 33: 46–50.

    Article  Google Scholar 

  • Rejas, D., K. Muylaert & L. De Meester, 2005. Trophic interactions within the microbial food web in a tropical floodplain lake (Laguna Bufeos, Bolivia). Revista de Biología Tropical 53: 85–96.

    PubMed  Google Scholar 

  • Salonen, K. & T. Hammar, 1986. On the importance of dissolved organic matter in the nutrition of zooplankton in some lake waters. Oecologia 68: 246–253.

    Article  Google Scholar 

  • Salonen, K., P. Kankaala, T. Tulonen, T. Hammar, M. James, T. R. Metsälä & L. Arvola, 1992. Planktonic food chains of a highly humic lake. II. A mesocosm experiment in summer during dominance of heterotrophic processes. Hydrobiologia 229: 143–157.

    Article  CAS  Google Scholar 

  • Samuelsson, K., J. Berglund & A. Andersson, 2006. Factors structuring the heterotrophic flagellate and ciliate community along a brackish water primary production gradient. Journal of Plankton Research 28: 345–359.

    Article  Google Scholar 

  • Sanders, R. W. & K. G. Porter, 1990. Bacterivorous flagellates as food resources for the freshwater crustacean zooplankter Daphnia ambigua. Limnology and Oceanography 35: 188–191.

    Article  Google Scholar 

  • Sanders, R. W., K. G. Porter, S. J. Bennett & A. E. De Biase, 1989. Seasonal pattern of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnology and Oceanography 34: 673–687.

    Article  Google Scholar 

  • Sanders, R. W., D. A. Caron & U. G. Berninger, 1992. Relationship between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Marine Ecology Progress Series 86: 1–14.

    Article  Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 1993. Preservation and storage of samples for enumeration of heterotrophic protists. In Kemp, P., B. Sherr, E. Sherr & J. Cole (eds), Current Methods in Aquatic Microbial Ecology. Lewis Publishers, New York: 207–212.

    Google Scholar 

  • Sherr, E. B. & B. F. Sherr, 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81: 293–308.

    Article  CAS  PubMed  Google Scholar 

  • Sleigh, M. A., 2000. Trophic strategies. In Leadbeater, B. S. C. & J. Green (eds), The Flagellates: Unity, Diversity and Evolution. Taylor & Francis, London: 147–166.

    Google Scholar 

  • Stoecker, D. K. & J. M. Capuzzo, 1990. Predation on protozoa: its importance to zooplankton. Journal of Plankton Research 12: 891–908.

    Article  Google Scholar 

  • Tadonleké, R., B. Pinel-Alloul, N. Bourbonnais & F. R. Pick, 2004. Factors affecting the bacteria-heterotrophic nanoflagellate relationship in oligo–mesotrophic lakes. Journal of Plankton Research 26: 681–695.

    Article  Google Scholar 

  • Tarbe, A.-L., F. Unrein, S. Stenuite, S. Pirlot, H. Sarmento, D. Sinyinza & J.-P. Descy, 2011. Protist herbivory: a key pathway in the pelagic food web of Lake Tanganyika. Microbial Ecology 62: 314–323.

    Article  PubMed  Google Scholar 

  • Teixeira, C., J. G. Tundisi & M. B. Kutner, 1965. Plankton studies in a mangrove environment. II: the standing-stock and some ecological factors. Boletim do Instituto Oceanográfico 24: 23–41.

    Google Scholar 

  • Tzaras, A. & F. R. Pick, 1994. The relations between bacterial and heterotrophic flagellate abundance in oligotrophic to mesotrophic temperate lakes. Marine Microbial Food Webs 8: 347–355.

    Google Scholar 

  • Walz, N., 1995. Rotifer populations in plankton communities: energetics and life history strategies. Experientia 51: 437–453.

    Article  CAS  Google Scholar 

  • Weisse, T., 1990. Trophic interactions among heterotrophic microplankton, nanoplankton and bacteria in Lake Constance. Hydrobiologia 191: 111–122.

    Article  Google Scholar 

  • Weisse, T., 1991. The annual cycle of heterotrophic freshwater nanoflagellates: role of bottom–up versus top–down control. Journal of Plankton Research 13: 167–185.

    Article  Google Scholar 

  • Wieltschnig, C., A. K. T. Kirschner, A. Steitz & B. Velimirov, 2001. Weak coupling between heterotrophic nanoflagellates and bacteria in a eutrophic freshwater environment. Microbial Ecology 2: 159–167.

    Google Scholar 

  • Yang, E. J., H. Kang, S. Yoo & J. Hyun, 2009. Contribution of auto- and heterotrophic protozoa to the diet of copepods in the Ulleung Basin, East Sea/Japan Sea. Journal of Plankton Research 31: 647–659.

    Article  Google Scholar 

  • Zingel, P., H. Agasild, T. Noges & V. Kisand, 2007. Ciliates are the dominant grazers on pico- and nanoplankton in a shallow, naturally highly eutrophic lake. Microbial Ecology 53: 134–142.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank V. F. Farjalla, S. Jati, Janet W. Reid, and two anonymous reviewers for fruitful comments on an earlier version of the manuscript. The authors also thank the post-graduate course in Ecology of Continental Aquatic Habitats (PEA, Maringá State University) and NUPELIA for financial support, material, equipment and facilities during the sampling. This study was supported by the Brazilian Research Council (CNPq) and the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES).

Author information

Authors and Affiliations

  1. Universidade Estadual de Maringá, Nupelia 5790, Maringá, PR, 87020-900, Brazil

    Bianca Trevizan Segovia & Luiz Felipe Machado Velho

  2. Universidade Federal de Goiás, DE, Goiânia, GO, 74001-970, Brazil

    Danielle Goeldner Pereira & Luis Mauricio Bini

Authors
  1. Bianca Trevizan Segovia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danielle Goeldner Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis Mauricio Bini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luiz Felipe Machado Velho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luis Mauricio Bini.

Additional information

Handling editor: Mariana Meerhoff

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Segovia, B.T., Pereira, D.G., Bini, L.M. et al. Effects of bottom-up and top-down controls on the temporal distribution of planktonic heterotrophic nanoflagellates are dependent on water depth. Hydrobiologia 736, 155–164 (2014). https://doi.org/10.1007/s10750-014-1904-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-014-1904-7

Keywords

Search

Navigation