Abstract
We tested the hypotheses that the ciliate assemblages in moderately eutrophic lake are controlled by the effective crustacean predation, and the high abundances of planktonic ciliates in highly eutrophic and turbid lake are due to insufficient regulation by crustacean zooplankton. A food tracer method coupled with natural assemblage of microciliates labeled with fluorescent microparticles was used to measure the cladoceran and copepod predation rates on planktonic ciliates and to estimate the carbon flow between the ciliate–crustacean trophic links. The results revealed that the microciliates (15–40 μm) were consumed by all dominant cladoceran and copepod species in both the lakes studied, mainly by Chydorus sphaericus and cyclopoid copepods in Lake Võrtsjärv, and by Daphnia spp. and Bosmina spp. in Lake Peipsi. The grazing loss in moderately eutrophic Peipsi indicated strong top-down control of ciliates mainly by cladocerans. The extraordinary abundant population of planktonic ciliates having a predominant role in the food web in highly eutrophic and turbid Võrtsjärv is explained by the measured low crustacean predation rates on ciliates. The estimated carbon flow from the ciliates to crustaceans suggest that in eutrophic lakes majority of the organic matter channeled via metazooplankton to higher trophic levels may originate from the microbial loop.
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References
Adrian, R. & B. Schneider-Olt, 1999. Top-down effects of crustacean zooplankton in a mesotrophic lake. Journal of Plankton Research 21: 2175–2190.
Agasild, H., P. Zingel, I. Tõnno, J. Haberman & T. Nõges, 2007. Contribution of different zooplankton groups in grazing on phytoplankton in shallow eutrophic Lake Võrtsjärv (Estonia). Hydrobiologia 584: 167–177.
Carrick, H. J., G. L. Fahnenstiel, E. F. Stoermer & R. G. Wetzel, 1991. The importance of zooplankton–protozoan trophic couplings in Lake Michigan. Limnology and Oceanography 36: 1325–1335.
Chow-Fraser, P. & G. Sprules, 1986. Inhibitory effect of Anabaena sp. on in situ filtering rate of Daphnia. Canadian Journal of Fisheries and Aquatic Sciences 64: 1831–1834.
DeMott, W. R. & M. D. Watson, 1991. Remote detection of algae by copepods: responses to algal size, odors and motility. Journal of Plankton Research 13: 1203–1222.
Dolan, J. R. & D. W. Coats, 1991. A study of feeding in predacious ciliates using prey ciliates labelled with fluorescent microspheres. Journal of Plankton Research 13: 609–627.
Dumont, H. J., I. Van de Velde & S. Dumont, 1975. The dry weight estimate of biomass and a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19: 75–97.
Gilbert, J. J., 1994. Jumping behaviour in the oligotrich ciliates Strobilidium velox and Halteria grandinella, and its significance as a defence against rotifer predators. Microbial Ecology 27: 189–200.
Haberman, J., 1998. Zooplankton of Lake Võrtsjärv. Limnologica 28: 49–65.
Haberman, J., 2001. Zooplankton. In Pihu, E. & J. Haberman (eds), Lake Peipsi: Flora and Fauna. Sulemees, Tartu: 50–68.
Haberman, J., R. Laugaste & T. Nõges, 2007. The role of cladocerans reflecting the trophic status of two large and shallow Estonian lakes. Hydrobiologia 584: 157–166.
Hansen, A.-M., 2000. Response of ciliates and Cryptomonas to the spring cohort of a cyclopoid copepod in a hypertrophic lake. Journal of Plankton Research 22: 185–203.
Hwang, S.-J. & R. Heath, 1999. Zooplankton bacterivory at coastal and offshore sites of Lake Erie. Journal of Plankton Research 21: 699–719.
Jeppesen, E., J. P. Jensen, M. Sondergaard, T. Lauridsen & F. Landkildehus, 2000. Trophic structure, species richness and biodiversity in Danish lakes: changes along phosphorus gradient. Freshwater Biology 45: 201–218.
Joaquim-Justo, C., C. Detry, F. Caufman & J. P. Thomé, 2004. Feeding of planktonic rotifers on ciliates: a method using natural ciliate assemblages labelled with fluorescent microparticles. Journal of Plankton Research 26: 1289–1299.
Järvalt, A., A. Kangur, K. Kangur, P. Kangur & E. Pihu, 2004. Fishes and fisheries management. In Haberman, J., E. Pihu & A. Raukas (eds), Lake Võrtsjärv. Estonian Encyclopaedia Publishers Ltd, Tallinn: 335–345.
Jürgens, K. & K. Šimek, 2000. Growth and feeding characteristics of an oligotrichous ciliate. Aquatic Microbial Ecology 22: 57–68.
Kisand, V. & P. Zingel, 2000. Dominance of ciliate grazing on bacteria during spring in a shallow eutrophic lake. Aquatic Microbial Ecology 22: 135–142.
Laugaste, R. & J. Haberman, 2005. Seasonality of zoo- and phytoplankton in Lake Peipsi as a function of water temperature. Proceedings of the Estonian Academy of Sciences, Biology, Ecology 54: 18–39.
Levine, S. N., R. F. Zehrer & C. W. Burns, 2005. Impact of resuspended sediment on zooplankton feeding in Lake Waihola, New Zealand. Freshwater Biology 50: 1515–1536.
Lokk, S., V. Kisand & K. Piirimäe, 2001. Bacterplankton. In Pihu, E. & J. Haberman (eds), Lake Peipsi: Flora and Fauna. Sulemees, Tartu: 23–30.
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.
Mohr, S. & R. Adrian, 2000. Functional responses of the rotifers Brachionus calyciflorus and Brachionus rubens feeding on armoured and unarmoured ciliates. Limnology and Oceanography 45: 1175–1179.
Nixdorf, B. & H. Arndt, 1993. Seasonal changes in the plankton dynamics of a Eutrophic Lake including the microbial web. International Revue der gesamten Hydrobiologie 78: 403–410.
Nõges, T., R. Laugaste, P. Nõges & I. Tõnno, 2008. Critical N:P ratio for cyanobacteria and N2-fixing species in the large shallow temperate lakes Peipsi and Võrtsjärv, North-East Europe. Hydrobiologia 599: 77–86.
Nõges, T., V. Kisand, A. Põllumäe, L. Tuvikene & P. Zingel, 1998a. Plankton seasonal dynamics and its controlling factors in shallow polymictic eutrophic lake Võrtsjärv, Estonia. International Revue der gesamten Hydrobiologie 83: 279–296.
Nõges, T., P. Nõges, J. Haberman, V. Kisand, K. Kangur, A. Kangur & A. Järvalt, 1998b. Food web structure in shallow eutrophic Lake Võrtsjärv (Estonia). Limnologica 28: 115–128.
Oom-Wilms, A. L., 1997. Are bacteria an important food source for rotifers in eutrophic lakes? Journal of Plankton Research 19: 1125–1141.
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.
Pihu, E. & A. Kangur, 2001. Fishes and fisheries management. In Pihu, E. & J. Haberman (eds), Lake Peipsi. Flora and Fauna, Sulemees, Tartu: 100–111.
Putt, M. & D. K. Stoecker, 1989. An experimentally determinedcarbon: volume ratio for marine ‘oligotrichous’ ciliates from estuarine and coastal waters. Limnology and Oceanography 34: 1097–1103.
Sanders, R. W., K. G. Porter, S. J. Bennett & A. E. DeBiase, 1989. Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnology and Oceanography 34: 673–687.
Sherr, E. B. & B. F. Sherr, 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology 81: 293–308.
Smalley, G. W., D. W. Coats & E. J. Adam, 1999. A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquatic Microbial Ecology 17: 167–179.
Sommer, F., H. Stibor, U. Sommer & B. Velimirov, 2000. Grazing by mesozooplankton from Kiel Bight, Baltic Sea, on different sized algae and natural seston size fractions. Marine Ecology Progress Series 199: 43–532.
Starast, H., A. Milius, T. Möls & A. Lindpere, 2001. Hydrochemistry of Lake Peipsi. In Nõges, T. (ed.), Lake Peipsi: Meteorology, Hydrology. Hydrochemistry, Sulemees, Tartu: 97–131.
Šimek, K., J. Macek, J. Seda & V. Vyhnalek, 1990. Possible food chain relationships between bacterioplankton, protozoans, and cladocerans in a reservoir. International Revue der gesamten Hydrobiologie 75: 583–596.
Tammert, H. & V. Kisand, 2004. Bacterplankton. In Haberman, J., E. Pihu & A. Raukas (eds), Lake Võrtsjärv. Estonian Encyclopaedia Publishers Ltd, Tallinn: 207–215.
Ueyama, S., H. Katsumaru, T. Suzaki & Y. Nakaoka, 2005. Halteria grandinella: a rapid swimming ciliate with a high frequency of ciliary beating. Cell Motility and the Cytoskeleton 60: 4214–4222.
Utermöhl, H., 1958. Zur Vervollkommung der quantitativen Phytoplanktonmethodik. Mitteilungen Internationale Vereiningung fuer Theoretische und Angewandte Limnologie 9: 1–38.
Ventelä, A.-M., K. Wiackowski, M. Moilainen, V. Saarikari, K. Vuorio & J. Sarvala, 2002. The effect of small zooplankton on the microbial loop and edible algae during a cyanobacterial bloom. Freshwater Biology 47: 1807–1819.
Weisse, T. & A. Frahm, 2002. Direct and indirect impact of two common rotifer species (Keratella spp.) on two abundant ciliate species (Urotricha furcata, Balanion planctonicum). Freshwater Biology 47: 53–64.
Weisse, T., H. Müller, R. M. Pinto-Coelho, A. Schweizer, D. Springmann & G. Baldringer, 1990. Response of the microbial loop to the phytoplankton spring bloom in a large prealpine lake. Limnology and Oceanography 35: 781–794.
Wiackowski, K., M. T. Brett & C. R. Goldman, 1994. Differential effects of zooplankton species on ciliate community structure. Limnology and Oceanography 39: 486–492.
Wickham, S. A., 1995a. Trophic relations between cyclopoid copepods and ciliated protists: complex interactions link the microbial and classic food webs. Limnology and Oceanography 40: 1173–1181.
Wickham, S. A., 1995b. Cyclops predation on ciliates: species-specific differences and functional responses. Journal of Plankton Research 17: 1633–1646.
Wickham, S. A. & J. J. Gilbert, 1991. Relative vulnerabilities of natural rotifer and ciliate communities to cladocerans: laboratory and field experiments. Freshwater Biology 26: 77–86.
Zingel, P. & J. Haberman, 2008. A comparison of zooplankton densities and biomass in Lakes Peipsi and Võrtsjärv (Estonia): rotifers and crustaceans versus ciliates. Hydrobiologia 599: 153–159.
Zingel, P. & T. Nõges, 2008. Protozoan grazing in shallow macrophyte- and plankton lakes. Archiv für Hydrobiologie 171: 15–25.
Zingel, P., H. Agasild, T. Nõges & V. Kisand, 2007. Ciliates are the dominant grazers on pico- and nanoplankton in a shallow, naturally highly eutrophic lake. Microbial Ecology 53: 134–142.
Zöllner, E., B. Santer, M. Boersma, H.-G. Hoppe & K. Jürgens, 2003. Cascading predation effects of Daphnia and copepods on microbial food web components. Freshwater Biology 48: 2174–2193.
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Funding for this research was provided by the Estonian Ministry of Education (SF 0170011508), and the Estonian Science Foundation grants 8511 and 8969. The authors are grateful to anonymous referees for their valuable comments and suggestions that helped us improve the manuscript.
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Agasild, H., Zingel, P. & Nõges, T. Live labeling technique reveals contrasting role of crustacean predation on microbial loop in two large shallow lakes. Hydrobiologia 684, 177–187 (2012). https://doi.org/10.1007/s10750-011-0981-0
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DOI: https://doi.org/10.1007/s10750-011-0981-0