Log in

Ciliates are the Dominant Grazers on Pico- and Nanoplankton in a Shallow, Naturally Highly Eutrophic Lake

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Abundance and biomass of the microbial loop members [bacteria, heterotrophic nanoflagellates (HNF), and ciliates] were seasonally measured in the naturally eutrophic and shallow (2.8 mean depth) Lake Võrtsjärv, which has a large open surface area (average 270 km2) and highly turbid water (Secchi depth <1 m). Grazing rates (filter feeding rates) on 0.5-, 3-, and 6-μm-diameter particles were measured to estimate pico- and nanoplankton grazing (filter feeding) by micro- and metazooplankton. Among grazers, HNF had a low abundance (<50 cells mL−1) and, due to their low specific filtering rates, they only grazed a minor fraction of the bacterioplankton (≤4.2% of total grazing). Ciliates were relatively abundant (≤158 cells mL−1) and, considering their high specific feeding rates, were able to graze more than 100% of the bacterial biomass production in the open part of the lake, whereas the average daily grazing accounted for 9.3% of the bacterial standing stock. Ciliates were potentially important grazers of nanoplanktonic organisms (on average, approximately 20% of the standing stock of 3-μm-size particles was grazed daily). Metazooplankton grazed a minor part of the bacterioplankton, accounting for only 0.1% of standing stock of bacteria. Grazing on nanoplankton (3–6 μm) by metazooplankton was higher (0.4% of standing stock). The hypothesis is proposed that ciliates dominate due to a lack of top–down regulation by predators, and HNF have a low abundance due to strong grazing pressure by ciliates.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Agasild, H, Nõges, T (2005) Cladoceran and rotifer grazing on bacteria and phytoplankton in two shallow eutrophic lakes: in situ measurement with fluorescent microspheres. J Plankton Res 27: 1155–1174

    Google Scholar 

  2. Beaver, JR, Crisman, TL (1989) The role of ciliated protozoa in pelagic freshwater ecosytems. Microbial Ecol 17: 111–136

    Article  Google Scholar 

  3. Biddanda, B, Opsahl, S, Benner, R (1994) Plankton respiration and carbon flux through bacterioplankton on the Louisiana Shelf. Limnol Oceanogr 39: 1259–1275

    CAS  Google Scholar 

  4. Bloem, J (1989) Bacterial production, protozoan grazing, and mineralization in stratified Lake Vechten. Dissertation

  5. Borsheim, KY, Bratbak, G (1987) Cell volume to cell carbon conversion factors for bacteriovorous Monas sp. enriched from sea water. Mar Ecol Prog Ser 36: 171–175

    Google Scholar 

  6. Bottrell, HH, Duncan, A, Gliwicz, ZM, Grygierek, E, Herzig, A, Hillbricht-Illkowska, A, Kurasawa, H, Larsson, P, Weglenska, T (1976) A review of some problems in zooplankton production studies. Norw J Zool 419–456

  7. Comerma, M, Garcia, JC, Armengol, J, Romero, M, Šimek, K (2001) Planktonic food web structure along the Sau Reservoir (Spain) in summer 1997. Int Rev Hydrobiol 86: 195–209

    Article  CAS  Google Scholar 

  8. del Giorgio, PA, Cole, JJ, Cimbleris, A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385: 148–151

    Article  Google Scholar 

  9. Diehl, S, Feissel, M (2001) Intraguild prey suffer from enrichment of their resources: a microcosm experiment with ciliates. Ecology 82: 2977–2983

    Article  Google Scholar 

  10. Dumont, HJ, Van de Velde, I, Dumont, S (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

    Article  Google Scholar 

  11. Foissner, W, Berger, H, Schaumburg, J (1999) Identification and ecology of limnetic plancton ciliates. Bayerisches Landesamt für Wasserwirtschaft, München

    Google Scholar 

  12. Gasol, JM (1995) Patterns in the top–down versus bottom–up regulation of heterotrophic nanoflagellates in temperate lakes. J Plankton Res 17: 1879–1903

    Article  Google Scholar 

  13. Hansen, AM (2000) Response of ciliates and Cryptomonas to the spring cohort of a cyclopoid copepod in a shallow hypereutrophic lake. J Plankton Res 22: 185–203

    Article  Google Scholar 

  14. Infante, A, Abella, SEB (1985) Inhibition of Daphnia by Oscillatoria in Lake Washington. Limnol Oceanogr 30: 1046–1052

    Google Scholar 

  15. Jürgens, K (1994) Impact of Daphnia on planktonic microbial food webs. A review. Mar Microb Food Webs 8: 295–324

    Google Scholar 

  16. Jürgens, K, Jeppesen, E (2000) The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. J Plankton Res 22: 1047–1070

    Article  Google Scholar 

  17. Jürgens, K, Skibbe, O, Jeppensen, E (1999) Impact of metazooplankton on the composition and population dynamics of planktonic ciliates in a shallow, hypertrophic lake. Aquat Microb Ecol 17: 61–75

    Google Scholar 

  18. Kim, HW, Hwang, SJ, Joo, GJ (2000) Zooplankton grazing on bacteria and phytoplankton in a regulated large river (Nakdong River, Korea). J Plankton Res 22: 1559–1577

    Article  CAS  Google Scholar 

  19. Kisand, V, Nõges, T (1998) Seasonal dynamics of bacterio- and phytoplankton in large and shallow eutropic Lake Võrtsjärv, Estonia. Int Rev Hydrobiol 83: 205–216

    Google Scholar 

  20. Kisand, V, Zingel, P (2000) Dominance of ciliate grazing on bacteria during spring in a shallow eutrophic lake. Aquat Microb Ecol 22: 135–142

    Google Scholar 

  21. Lampert, W, Fleckner, W, Rai, H, Taylor, BE (1986) Phytoplankton control by grazing zooplankton—a study on the spring clear-water phase. Limnol Oceanogr 31: 478–490

    Google Scholar 

  22. Lignell, R (1992) Problems in filtration fractionation of 14C primary productivity samples. Limnol Oceanogr 37: 172–178

    CAS  Google Scholar 

  23. Loferer-Krossbacher, M, Klima, J, Psenner, R (1998) Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Appl Environ Microbiol 64: 688–694

    PubMed  CAS  Google Scholar 

  24. Macek, M, Šimek, K, Bittl, T (2001) Conspicuous peak of oligotrichous ciliates following winter stratification in a bog lake. J Plankton Res 23: 353–363

    Article  CAS  Google Scholar 

  25. Nakano, S, Koitabashi, T, Ueda, T (1998) Seasonal changes in abundeance of heterotrophic nanoflagellates and their consumption of bacteria in Lake Biwa with special reference to trophic interactions with Daphia galeata. Arch Hydrobiol 142: 21–34

    Google Scholar 

  26. Nielsen, TG, Kiorboe, T (1994) Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 2. Ciliates. Limnol Oceanogr 39: 508–519

    Google Scholar 

  27. Niemi, M, Kuparinen, J, Uusi-Rauva, A, Korhonen, K (1983) Preparation of algal samples for liquid scintillation counting. Hydrobiologia 106: 149–159

    Article  CAS  Google Scholar 

  28. Nixdorf, B, Arndt, H (1993) Seasonal changes in the plankton dynamics of a Eutrophic Lake including the microbial web. Int Rev Gesamten Hydrobiol 78: 403–410

    Google Scholar 

  29. Nõges, P, Tuvikene, L, Nõges, T, Kisand, A (1999) Primary production, sedimentation and resuspension in large shallow Lake Võrtsjärv. Aquat Sci 61: 168–182

    Article  Google Scholar 

  30. Nõges, T, Nõges, P, Haberman, J, Kisand, V, Kangur, K, Kangur, A, Järvalt, A (1998) Food web structure in the shallow eutrophic Lake Võrtsjärv. Limnologica 28: 115–128

    Google Scholar 

  31. Porter, KG, Feig, YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25: 943–948

    Google Scholar 

  32. Porter, KG, McDonough, R (1984) The energetic cost of response to blue-green-algal filaments by Cladocerans. Limnol Oceanogr 29: 365–369

    Article  Google Scholar 

  33. Putt, M, Stoecker, DK (1989) An experimentally determined carbon: volume ratio for marine ‘oligotrichous’ ciliates from estuarine and coastal waters. Limnol Oceanogr 34: 1097–1103

    Google Scholar 

  34. Rothhaupt, KO, Güde, H (1996) Influence of metazoan zooplankton on the microbial community before and after the onset of the spring clear-water phase in Lake Constance (Bodensee). Arch Hydrobiol Ergebn Limnol 48: 21–30

    Google Scholar 

  35. Sanders, RW, Porter, KG, Bennett, SJ, DeBiase, AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34: 673–687

    Google Scholar 

  36. Schelske, CL, Carrick, HJ, Aldridge, FJ (1995) Can wind-driven resuspension of meroplankton affect phytoplankton dynamics? J North Am Benthol Soc 14: 616–630

    Article  Google Scholar 

  37. Sherr, EB, Sherr, BF (2002) Significance of predation by protists in aquatic microbial food webs. Anton van Leeuwenhoek Int J G 81: 293–308

    Article  CAS  Google Scholar 

  38. Šimek, K, Babenzien, D, Bitl, T, Koschel, R, Macek, M, Nedoma, J, Vrba, J (1998) Microbial food webs in an artificially divided acidic bog lake. Int Rev Hydrobiol 83: 3–18

    Google Scholar 

  39. Šimek, K, Bobkova, J, Macek, M, Nedoma, J, Psenner, R (1995) Ciliate grazing on picoplankton in a eutrophic reservoir during the summer phytoplankton maximum: a study at the species and community level. Limnol Oceanogr 40: 1077–1090

    Article  Google Scholar 

  40. Šimek, K, Macek, J, Seda, J, Vyhnalek, V (1990) Possible food chain relationships between bacterioplankton, protozoans, and cladocerans in a reservoir. Int Rev Gesamten Hydrobiol 75: 583–596

    Google Scholar 

  41. Simon, M, Azam, F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201–213

    CAS  Google Scholar 

  42. Sommaruga, R, Psenner, R (1993) Nanociliates of the order Prostomatida: their relevance in the microbial food web of a mesotrophic lake. Aquat Sci 55: 179–187

    Article  Google Scholar 

  43. Zingel, P (1999) Pelagic ciliated protozoa in a shallow eutrophic lake: community structure and seasonal dynamics. Arch Hydrobiol 146: 495–511

    Google Scholar 

  44. Zingel, P, Paaver, T (2005) Quick springtime changes in community structure of pelagic ciliated protozoa. Arch Hydrobiol 163: 525–537

    Article  Google Scholar 

  45. Tadonleke, RD, Planas, D, Lucotte, A (2005) Microbial food webs in boreal humic lakes and reservoirs: ciliates as a major factor related to the dynamics of the most active bacteria. Microb Ecol 49: 325–341

    Article  PubMed  CAS  Google Scholar 

  46. Utermöhl, H (1958) Zur Vervollkommung der quaatitativen Phytoplanktonmethodik. Mitt Int Ver Theor Angew Limnol 9: 1–38

    Google Scholar 

  47. Weisse, T (1990) Trophic interactions among heterotrophic microplankton, nanoplankton, and bacteria in Lake Constance. Hydrobiol 191: 111–122

    Article  Google Scholar 

  48. Weisse, T, Frahm, A (2001) Species-specific interactions between small planktonic ciliates (Urotricha spp.) and rotifers (Keratella spp.). J Plankton Res 23: 1329–1338

    Article  Google Scholar 

  49. Worden, AZ, Nolan, JK, Palenik, B (2004) Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnol Oceanogr 49: 168–179

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Mark Dopson who made valuable language revision on the manuscript. This study was funded by grants to Tiina Nõges from the Estonian Ministry of Education (0362480s03) and by Estonian Science Foundation grants 4080 and 5738, and to Veljo Kisand from the Hanse Advanced Institute and EU Marie Curie MERG-CT-6-2005-014873. Data collection in state monitoring program was supported by Estonian Ministry of Environment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Veljo Kisand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zingel, P., Agasild, H., Nõges, T. et al. Ciliates are the Dominant Grazers on Pico- and Nanoplankton in a Shallow, Naturally Highly Eutrophic Lake. Microb Ecol 53, 134–142 (2007). https://doi.org/10.1007/s00248-006-9155-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9155-4

Keywords

Navigation