Skip to main content

Advertisement

SpringerLink
Log in

Drivers of highly diverse planktonic ciliate assemblages in peat bog pools from Tierra del Fuego (Argentina)

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

Abstract

Peatlands often encompass shallow pools, wherein dystrophic and colored acid waters host a remarkably diverse biota, with ciliates likely playing a key role in their short trophic webs. In the Sphagnum magellanicum-dominated Rancho Hambre peat bog, a 2-year study was conducted in five pools with different morphometric and trophic characteristics, in order to identify main environmental variables driving ciliate species richness, abundance, biomass, and diversity. Overall species richness (125 taxa) was much higher than in northern Hemisphere counterparts. Deep minerotrophic pools hosted the richest communities, showing similar seasonal abundance patterns and the highest species turnover. Although all pools shared the same dominant ciliates, similarity in taxonomic composition among them was generally low (J = 0.22–0.35). Moreover, IndVal analysis showed that rare and occasional species were highly indicative of different pools. Euryoecious, heterotrophic species, occurred in all sites, while mixotrophs were typical from shallow ombrotrophic pools. Rimostrombidium hyalinum was the most indicative species of a deep ombrotrophic pool. A CCA revealed that the abundances of potential ciliate preys, i.e., picophytoplankton, bacterioplankton, and heterotrophic flagellates, were the most significant regulators of abundances of this group. Therefore, ciliate structure and dynamics were influenced by pool morphometry and physical and chemical features, but foremost by interactions with other plankton communities.

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
Fig. 6

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 

  • Archbold, J. H. G. & J. Berger, 1985. A qualitative assessment of some metazoan predators of Halteria grandinella, a common freshwater ciliate. Hydrobiologia 126: 97–102.

    Article  Google Scholar 

  • APHA, 2005. Standard Methods for the Examination of Water and Wastewaters, 21st ed. American Public Health Association APHA, AWWA, WEF, Washington DC.

    Google Scholar 

  • Beaver, J. R. & T. L. Crisman, 1981. Acid precipitation and the response of ciliated protozoans in Florida lakes. Verhandlungen des Internationalen Verein Limnologie 21: 353–358.

    Google Scholar 

  • Beaver, J. R. & T. L. Crisman, 1982. The trophic response of ciliated protozoans in freshwater lakes. Limnology and Oceanography 27: 246–253.

    Article  Google Scholar 

  • Beaver, J. R. & T. L. Crisman, 1989. Analysis of the community structure of planktonic ciliated protozoa relative to trophic state in Florida lakes. Hydrobiologia 174: 177–184.

    Article  CAS  Google Scholar 

  • Berger, H., 1999. Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biologicae 78: 1–1080.

    Article  Google Scholar 

  • Bienert Jr, R. W., J. R. Beaver & T. L. Crisman, 1991. The contribution of ciliated protozoa to zooplankton biomass in an acidic, subtropical lake. Journal of Protozoology 38: 352–354.

    Article  Google Scholar 

  • Borcard, D., F. Gillet & P. Legendre, 2011. Numerical Ecology with R. Springer, New York.

    Book  Google Scholar 

  • De Cáceres, M. & P. Legendre, 2009. Associations between species and groups of sites: indices and statistical inference. Ecology 90: 3566–3574.

    Article  PubMed  Google Scholar 

  • Dufrêne, M. & P. Legendre, 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366.

    Google Scholar 

  • Foissner, W. & S. Wölfl, 1994. Revision of the genus Stentor Oken (Protozoa, Ciliophora) and description of S. araucanus nov. spec. from South American lakes. Journal of Plankton Research 16: 255–289.

    Article  Google Scholar 

  • Foissner, W. & H. Berger, 1996. A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshwater Biology 35: 375–482.

    Google Scholar 

  • Foissner, W., H. Blatterer, H. Berger & F. Kohmann, 1991. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems – Band I: Cyrtophorida, Oligotrichida, Hypotrichia, Colpodea. Informationsberichte des Bayer, Landesamtes für Wasserwirtschaft, München.

  • Foissner, W., H. Berger & F. Kohmann, 1992. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems – Band II: Peritrichia, Heterotrichida, Odontostomatida. Informationsberichte des Bayer, Landesamtes für Wasserwirtschaft, München.

  • Foissner, W., H. Berger & F. Kohmann, 1994. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems – Band III: Hymenostomata, Prostomatida, Nassulida. Informationsberichte des Bayer, Landesamtes für Wasserwirtschaft, München.

  • Foissner, W., H. Berger, H. Blatterer & F. Kohmann, 1995. Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems – Band IV: Gymnostomates, Loxodes, Suctoria. Informationsberichte des Bayer, Landesamtes für Wasserwirtschaft, München.

  • Foissner, W., H. Berger & J. Schaumburg, 1999. Identification and Ecology of Limnetic Plankton Ciliates. Informationsberichte des Bayer, Landesamtes für Wasserwirtschaft, München.

    Google Scholar 

  • Foissner, W., A. Chao & L. A. Katz, 2008. Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodiversity and Conservation 17: 345–363.

    Article  Google Scholar 

  • González Garraza, G., G. Mataloni, R. Iturraspe, R. Lombardo, S. Camargo & M. V. Quiroga, 2012. The limnological character of bog pools in relation to meteorological and hydrological features. Mires and Peat 10: 1–14.

    Google Scholar 

  • Hammer, Ø., D. A. T. Harper & P. D. Ryan, 2001. PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontologia Electronica 4: 1–9.

    Google Scholar 

  • Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403–424.

    Article  Google Scholar 

  • Iturraspe, R., 2010. Las Turberas de Tierra del Fuego y el Cambio Climático Global. Fundación Humedales/Wetlands International, Buenos Aires.

    Google Scholar 

  • Kahl, A., 1930–1935. Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) eine Bearbeitung der freilebenden und ectocommensalen Infusorien der Erde, unter Ausschluss der marinen Tintinnidae. In Dahl, F. (ed.), Die Tierwelt Deutschlands. G. Fischer, Jena: 1–866.

  • Kalinowska, K., 2000. Ciliates in small humic lakes (Masurian Lakeland, Poland): relationship to acidity and trophic parameters. Polish Journal of Ecology 48: 169–183.

    Google Scholar 

  • Kreutz, M. & W. Foissner, 2006. The Sphagnum Ponds of Simmelried in Germany: A Biodiversity Hot-spot for Microscopic Organisms. Protozoological Monographs, Vol. 3. Shaker Publishers, Aachen.

  • Küppers, G. C., T. da Silva Paiva, B. do Nascimento Borges, M. L. Harada, G. González Garraza & G. Mataloni, 2011. An Antarctic ciliate, Parasterkiella thompsoni (Foissner) nov. gen., nov. comb., recorded in Argentinean peat-bogs: morphology, morphogenesis, and molecular phylogeny. European Journal of Protistology 47: 103–123.

    Article  PubMed  Google Scholar 

  • Lara, E., C. V. W. Seppey, G. González Garraza, D. Singer, M. V. Quiroga & G. Mataloni, 2015. Planktonic eukaryote molecular diversity: discrimination of minerotrophic and ombrotrophic peatland pools in Tierra del Fuego (Argentina). Journal of Plankton Research 37: 645–655.

    Article  Google Scholar 

  • Lepš, J. & P. Šmilauer, 2003. Multivariate Analysis of Ecological Data Using CANOCO. Cambridge University Press, Cambridge.

    Google Scholar 

  • Lynn, D. H., 2008. The Ciliated Protozoa. Characterization, Classification, and Guide to the Literature, 3rd ed. Springer, Ontario.

    Google Scholar 

  • Macek, M., K. Šimek & T. Bittl, 2001. Conspicuous peak of oligotrichous ciliates following winter stratification in a bog lake. Journal of Plankton Research 23: 353–363.

    Article  CAS  Google Scholar 

  • Magurran, A. E., 2004. Measuring Biological Diversity. Blackwell Science Publishing, Oxford.

    Google Scholar 

  • Mataloni, G., 1997. Flora Algal de las Turberas de Tierra del Fuego. Contribución del Instituto Antártico Argentino No. 467. Instituto Antártico Argentino, Buenos Aires.

  • Mataloni, G. & G. Tell, 1996. Comparative analysis of the phytoplankton communities of a peat bog from Tierra del Fuego (Argentina). Hydrobiologia 325: 101–112.

    Article  CAS  Google Scholar 

  • Mataloni, G., G. González Garraza & A. Vinocur, 2015. Landscape-driven environmental variability largely determines abiotic characteristics and phytoplankton patterns in peat bog pools (Tierra del Fuego, Argentina). Hydrobiologia 751: 105–125.

    Article  CAS  Google Scholar 

  • Mieczan, T., 2007a. Planktonic ciliates in peat ponds of different acidity (E Poland). Electronic Journal of Polish Agricultural Universities, Biology 10: 1–10.

    Google Scholar 

  • Mieczan, T., 2007b. Relationship among ciliated protozoa and water chemistry in small peat-bog reservoirs (Łęczna-Włodawa Lakeland, Eastern Poland). Oceanological and Hydrobiological Studies 36: 77–86.

    Article  CAS  Google Scholar 

  • Mieczan, T., 2010a. Vertical microzonation of testate amoebae and ciliates in peatbog waters in relation to physical and chemical parameters. Polish Journal of Ecology 58: 729–740.

    Google Scholar 

  • Mieczan, T., 2010b. Vertical micro-zonation of testate amoebae and ciliates in peatland waters in relation to potential food resources and grazing pressure. International Review on Hydrobiology 95: 86–102.

    Article  Google Scholar 

  • Mieczan, T. & D. Siczek, 2010. Horizontal distribution of ciliated protozoa between the Sphagnum mat and open water zone in a shallow peat-bog pools. Teka Komisji Ochrony i Kształtowania Środowiska Przyrodniczego 7: 260–271.

    Google Scholar 

  • Mieczan, T. & M. Tarkowska-Kukuryk, 2013. Diurnal dynamics of the microbial loop in peatlands: structure, function and relationship to environmental parameters. Hydrobiologia 717: 189–201.

    Article  CAS  Google Scholar 

  • Müller, H. & W. Geller, 1993. Maximum growth rates of aquatic ciliated Protozoa – the dependence on body size and temperature reconsidered. Archiv für Hydrobiologie 126: 315–327.

    Google Scholar 

  • Packroff, G., 2000. Protozooplankton in acid mining lakes with special respect to ciliates. Hydrobiologia 433: 157–166.

    Article  Google Scholar 

  • Putt, M. & D. K. Stoecker, 1989. An experimentally determined carbon:volume ratio for marine ‘oligotrichous' ciliates from estuarine and coastal waters. Limnology and Oceanography 34: 1097–1103.

    Article  Google Scholar 

  • Quiroga, M. V., F. Unrein, G. González Garraza, G. Küppers, R. Lombardo, M. C. Marinone, S. Menú Marque, A. Vinocur & G. Mataloni, 2013. The plankton communities from peat bog pools: structure, temporal variation and environmental factors. Journal of Plankton Research 35: 1234–1253.

    Article  Google Scholar 

  • Quiroga, M. V., A. Valverde, G. Mataloni & D. Cowan, 2015. Understanding diversity patterns in bacterioplankton communities from a sub-Antarctic peatland. Environmental Microbiology Reports 7: 547–553.

    Article  PubMed  Google Scholar 

  • Roig, C. & F. A. Roig, 2004. Consideraciones generales. In Blanco, D. E. & V. M. de la Balze (eds), Los Turbales de la Patagonia, Bases para su Inventario y la Conservación de su Biodiversidad. Fundación Humedales, Wetlands International, Buenos Aires: 5–21.

    Google Scholar 

  • Rydin, H. & J. K. Jeglum, 2006. The Biology of Peatlands. Oxford University Press, Oxford.

    Book  Google Scholar 

  • Searles, P. S., B. R. Kropp, S. D. Flint & M. M. Caldwell, 2001. Influence of solar UV-B radiation on peatland microbial communities of southern Argentinia. New Phytologist 152: 213–221.

    Article  Google Scholar 

  • Sharp, J. H., E. T. Peltzer, M. J. Alperin, G. Gauwet, J. W. Farrington, B. Fry, D. M. Karl, J. H. Martin, A. Spitzy, S. Tugrul & C. A. Carlson, 1993. DOC procedures subgroup report. Marine Chemistry 41: 37–49.

    Article  CAS  Google Scholar 

  • Sime Ngando, T. & C. A. Grolière, 1991. Effets quantitatifs des fixateurs sur la conservation des ciliés planctoniques d’eau douce. Archiv für Protistenkunde 140: 109–120.

    Article  Google Scholar 

  • Šimek, K., J. Bobkovh, M. Macek & J. Nedoma, 1995. Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: a study at the species and community level. Limnology and Oceanography 40: 1077–1090.

    Article  Google Scholar 

  • Šimek, K., M. Macek, J. Pernthaler, V. Straskrabova & R. Psenner, 1996. Can freshwater planktonic ciliates survive on a diet of picoplankton? Journal of Plankton Research 18: 597–613.

    Article  Google Scholar 

  • Šimek, K., D. Babenzien, T. Bittl, R. Koschel, M. Macek, J. Nedoma & J. Vrba, 1998. Microbial food webs in an artificially divided acidic bog lake. International Review of Hydrobiol 83: 3–18.

    Article  Google Scholar 

  • Sonntag, B., M. Summerer & R. Sommaruga, 2007. Sources of mycosporine-like amino acids in planktonic Chlorella-bearing ciliates (Ciliophora). Freshwater Biology 52: 1476–1485.

    Article  CAS  PubMed Central  Google Scholar 

  • Sonntag, B., M. C. Strüder-Kypke & M. Summerer, 2008. Uroleptus willi nov. sp., a euplanktonic freshwater ciliate (Dorsomarginalia, Spirotrichea, Ciliophora) with algal symbionts: morphological description including phylogenetic data of the small subunit rRNA gene sequence and ecological notes. Densia 23: 279–288.

    Google Scholar 

  • Summerer, M., B. Sonntag, P. Hörtnagl & R. Sommaruga, 2009. Symbiotic ciliates receive protection against UV damage from their algae: a test with Paramecium bursaria and Chlorella. Protist 160: 233–243.

    Article  PubMed  Google Scholar 

  • Tadonléké, R. D., D. Planas & M. Lucotte, 2005. Microbial food webs in boreal humic lakes and reservoirs: ciliates as a major factor related to the dynamics of the most active bacteria. Microbial Ecology 49: 325–341.

    Article  PubMed  Google Scholar 

  • ter Braak C. J. F. & P. Šmilauer, 1998. CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination (vers. 4). Microcomputer Power, Ithaca, NY.

  • Utermöhl, H., 1958. Zur Vervollkommung der quatitativen Phytopankton-Methodik. Internationale Vereiningung für Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Weisse, T. & P. Stadler, 2006. Effect of pH on growth, cell volume, and production of freshwater ciliates, and implications for their distribution. Limnology and Oceanography 51: 1708–1715.

    Article  CAS  Google Scholar 

  • Wilbert, N., 1975. Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos 64: 171–179.

    Google Scholar 

  • Zar, J. H., 2010. Biostatistical Analysis. Pearson Prentice Hall, Upper Saddle River.

    Google Scholar 

Download references

Acknowledgments

The Agencia Nacional de Promoción Científica y Tecnológica (PICT 2006 1697) and Consejo Nacional de Investigaciones Científicas y Técnicas are greatly acknowledged for financial support. The authors thank the Dirección Provincial de Recursos Hídricos de la Provincia de Tierra del Fuego and the Centro Austral de Investigaciones Científicas y Tecnológicas (CADIC-CONICET) for most valuable logistic support. Ciliate countings were performed at the Instituto de Limnología Dr. R. A. Ringuelet. Copepod identifications were possible due to the valuable help of Silvina Menu Marque, who also commented the draft version of the manuscript. We are also grateful to Rodolfo Iturraspe and Sergio Camargo for helping during the field work and to everyone that participated in the surveys. Finally, we would like to thank the reviewers for comments and suggestions that improved this manuscript.

Author information

Authors and Affiliations

  1. División Invertebrados, Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Av. Ángel Gallardo 470, C1405DJR, Buenos Aires, Argentina

    G. C. Küppers

  2. Instituto de Investigación e Ingeniería Ambiental (3iA), Universidad Nacional de San Martín, Campus Miguelete, 25 de Mayo y Francia, 1650, San Martín, Provincia de Buenos Aires, Argentina

    G. C. González Garraza & G. Mataloni

  3. Laboratorio de Ecología y Fotobiología Acuática, Instituto de Investigaciones Biotecnológicas-Instituto Tecnológico de Chascomús (IIB-INTECH), UNSAM-CONICET, Intendente Marino Km 8.2, CP (B 7130 IWA), Chascomús, Buenos Aires, Argentina

    M. V. Quiroga

  4. Departamento de Ecología, Genética y Evolución (DEGE), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria, Ciudad Autónoma de Buenos Aires, C1428EHA, Buenos Aires, Argentina

    R. Lombardo & A. Vinocur

  5. Departamento de Biodiversidad y Biología Experimental (DBBE), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria, Ciudad Autónoma de Buenos Aires, C1428EHA, Buenos Aires, Argentina

    M. C. Marinone & A. Vinocur

Authors
  1. G. C. Küppers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. C. González Garraza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. V. Quiroga
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Lombardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. C. Marinone
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Vinocur
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Mataloni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. C. Küppers.

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

Küppers, G.C., González Garraza, G.C., Quiroga, M.V. et al. Drivers of highly diverse planktonic ciliate assemblages in peat bog pools from Tierra del Fuego (Argentina). Hydrobiologia 773, 117–134 (2016). https://doi.org/10.1007/s10750-016-2686-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2686-x

Keywords

Search

Navigation