Hydrobiologia

, Volume 255, Issue 1, pp 231–246 | Cite as

Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates) — a review

  • Hartmut Arndt
Article

Abstract

Recent investigations have shown that processes within the planktonic microbial web are of great significance for the functioning of limnetic ecosystems. However, the general importance of protozoans and bacteria as food sources for rotifers, a major component of planktonic habitats, has seldom been evaluated. Results of feeding experiments and the analysis of the food size spectrum of rotifers suggest that larger bacteria, heterotrophic flagellates and small ciliates should be a common part of the food of most rotifer species. About 10–40 per cent of rotifers' food can consist of heterotrophic organisms of the microbial web. Field experiments have indicated that rotifer grazing should generally play a minor role in bacteria consumption compared to feeding by coexisting protozoans. However, according to recent experiments regarding food selection, rotifers should be efficient predators on protozoans. Laboratory experiments have revealed that even nanophagous rotifers can feed on ciliates. Preliminary microcosm and chemostat experiments have indicated that rotifers, due to their relatively low community grazing rates compared to the growth rates of bacteria and protozoans, should generally not be able (in contrast to some cladocerans) to suppress the microbial web via grazing, though they may structure it. Filter-feeding nanophagous rotifers (e.g. brachionids) seem to be significant feeders on the smaller organisms of the microbial web (bacteria, flagellates, small ciliates), whereas grasping species (e.g. synchaetids and asplanchnids) seem to be efficient predators on larger organisms (esp. ciliates). Another important role of rotifers is their feedback effect on the microbial web. Rotifers provide degraded algae, bacteria and protozoans to the microbial web and may promote microbial activity. Additional experimental work is necessary for a better understanding of the function of rotifers in aquatic ecosystems.

Key words

rotifers feeding bacteria ciliates heterotrophic flagellates microbial web 

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References

  1. Alekperov, K. & V. I. Kryuchkov, 1981. Planktonic infusoria of the Kura hatchery ponds. Hydrobiol. J. 17: 18–22.Google Scholar
  2. Arndt, H., H. Güde, M. Macek & K. O. Rothhaupt, 1992. Chemostats used to model the microbial food web: evidence for the feedback effect of herbivorous metazoans. Arch. Hydrobiol. Beih. Ergebn. Limnol. 37: 187–194.Google Scholar
  3. Arndt, H., G. Jost & N. Wasmund, 1990. Dynamics of pelagic ciliates in eutrophic estuarine waters: importance of functional groups among ciliates and responses to bacterial and phytoplankton production. Arch. Hydrobiol. Beih. Ergebn. Limnol. 34: 239–245.Google Scholar
  4. Arndt, H. & J. Mathes, 1991. Large heterotrophic flagellates form a significant part of protozooplankton biomass in lakes and rivers. Ophelia 33: 225–234.Google Scholar
  5. Arndt, H. & B. Nixdorf, 1991. Spring clear-water phase in a eutrpphic lake: Control by herbivorous zooplankton enhanced by grazing on components of the microbial web. Verh. int. Ver. Limnol. 24: 879–883.Google Scholar
  6. Arndt, H., C. Schröder & W. Schnese, 1990. Rotifers of the genus Synchaeta — an important component of the zooplankton in the coastal waters of the southern Baltic. Limnologica 21: 233–235.Google Scholar
  7. 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. Mar. Ecol. Prog. Ser. 10: 257–263.Google Scholar
  8. Berninger, U.-G., B. J. Finlay & P. Kuuppo-Leinikki, 1991. Protozoan control of bacterial abundances in freshwater. Limnol. Oceanogr. 36: 139–147.Google Scholar
  9. Bogdan, K. G. & J. J. Gilbert, 1982. Seasonal patterns of feeding by natural populations of Keratella, Polyarthra, and Bosmina: Clearance rates, selectivities, and contributions to community grazing. Limnol. Oceanogr. 27: 918–934.Google Scholar
  10. Bogdan, K. G. & J. J. Gilbert, 1987. Quantitative comparison of food niches in some freshwater zooplankton. A multitracer approach. Oecologia 72: 331–340.Google Scholar
  11. Bogdan, K. G., J. J. Gilbert & P. L. Starkweather, 1980. In situ clearance rates of planktonic rotifers. In H. J. Dumont & J. Green (eds), Rotatoria. Developments in Hydrobiology I. Dr W. Junk Publishers, The Hague: 73–77. Reprinted from Hydrobiologia 73.Google Scholar
  12. Boon, P. I. & R. J. Shiel, 1990. Grazing on bacteria by zooplankton in Australian billabongs. Aust. J. mar. Freshwat. Res. 41: 247–257.Google Scholar
  13. Buikema, A. L., Jr., J. Cairns Jr., P. C. Edmunds & T. H. Krakauer, 1977. Culturing and ecology studies of the rotifer, Polyarthra vulgaris. U.S. Envir. Protection Agency, Ecol. Res. Ser., EPA-600/3-77-051, 50 pp.Google Scholar
  14. Buikema, A. L., Jr., J. D. Miller & W. H. Yongue Jr., 1978. Effects of algae and protozoans on the dynamics of Polyarthra vulgaris. Verh. int. Ver. Limnol. 20: 2395–2399.Google Scholar
  15. Burckhardt, R., 1986. Zur Bedeutung von planktischen Ciliaten als Nahrung für Metazooplankton des Zingster Stromes. Diploma thesis, University of Rostock.Google Scholar
  16. Burckhardt, R. & H. Arndt, 1987. Untersuchungen zur Konsumtion von Ciliaten durch Metazooplankter des Barther Boddens (südliche Ostsee). Wiss. Z. Univ. Rostock, math.-nat. R. 36: 22–26.Google Scholar
  17. Christoffersen, K., B. Riemann, L. R. Hansen, A. Klysner & H. B. Sörensen, 1990. Qualitative importance of the microbial loop and plankton community structure in a eutrophic lake during a bloom of cyanobacteria. Microb. Ecol. 20: 253–272.Google Scholar
  18. DeBiase, A. E., R. W. Sanders & K. G. Porter, 1990. Relative nutritional value of ciliate protozoa and algae as food for Daphina. Microb. Ecol. 19: 199–210.Google Scholar
  19. Dodson, S. I., 1984. Ecology and behaviour of a free-swimming, tube-dwelling rotifer Cephalodella forficula. Freshwat. Biol. 14: 329–334.Google Scholar
  20. Dolan, J. R. & C. L. Gallegos, 1991. Trophic coupling of rotifers, microflagellates, and bacteria during fall months in the Rhode River Estuary. Mar. Ecol. Prog. Ser. 77: 147–156.Google Scholar
  21. Ejsmont-Karabin, J., 1974. Studies on the feeding of planktonic polyphage Asplanchna priodonta GOSSE (Rotatoria). Ekol. pol. 22: 311–317.Google Scholar
  22. Fenchel, T., 1987. Ecology of Protozoa: The Biology of Freeliving Phagotrophic Protists. Science Tech Publishers, Madison, Wisconsin.Google Scholar
  23. Garreau, F., C. Rougier & R. Pourriot, 1988. Exploitation des ressources alimentaires par le predateur planctonique Asplanchna girodi De GUERNE 1888 (Rotiferes) dans un lac de sabliere. Arch. Hydrobiol. 112: 91–106.Google Scholar
  24. Geller, W., R. Berberovic, U. Gaedke, H. Müller, H.-R. Pauli, M. M. Tilzer & T. Weisse, 1991. Relations among the components of autotrophic and heterotrophic plankton during the seasonal cycle 1987 in Lake Constance. Verh. int. Ver. Limnol. 24: 831–836.Google Scholar
  25. Gilbert, J. J., 1976. Polymorphism in the rotifer Asplanchna sieboldi: biomass, growth, and reproductive rate of the saccate and campanulate morphotype. Ecology 57: 542–551.Google Scholar
  26. Gilbert, J. J., 1980. Observations on the susceptibility of some protists and rotifers to predation by Asplanchna girodi. In H. J. Dumont & J. Green (eds), Rotatoria. Developments in Hydrobiology I. Dr W. Junk Publishers, The Hague: 87–91. Reprinted from Hydrobiologia 73.Google Scholar
  27. Gilbert, J. J. & K. G. Bogdan, 1981. Selectivity of Polyarthra and Keratella for flagellate and aflagellate cells. Verh. int. Ver. Limnol. 21: 1515–1521.Google Scholar
  28. Gilbert, J. J. & J. D. Jack, 1993. Rotifers as predators on small ciliates. Hydrobiologia 255/256: 247–253.Google Scholar
  29. Güde, H., 1988. Direct and indirect influences of crustacean zooplankton on bacterioplankton of Lake Constance. Hydrobiologia 159: 63–73.Google Scholar
  30. Güde, H., 1989. The role of grazing on bacteria in plankton succession. In U. Sommer (ed.), Plankton Ecology: Succession in Plankton Communities. Springer-Verlag, Berlin, Heidelberg, New York: 337–364.Google Scholar
  31. Hessen, D. O. & T. Andersen, 1990. Bacteria as a source of phosphorus for zooplankton. Hydrobiologia 206: 217–223.Google Scholar
  32. Higashihara, T., T. Fukuoka, T. Abe, I. Mizuhara, O. Imado & R. Hirano, 1983. Culture of the rotifer Brachionus plicatilis using a microbial flock produced from alcohol fermentation slop. Bull. Jpn. Soc. Sci. Fish. 49: 1001–1014.Google Scholar
  33. Hollowday, E. D., 1949. On the capture of plankton Rotifera as food by the heliozoan Actinosphaerium eichhorni. J. Quekett Microscopical Club ser. 4: 362–363.Google Scholar
  34. Hollowday, E.D., 1979. The capture and ingestion of the plankton rotifer Asplanchna priodonta GOSSE by the holotrichous ciliate Trachelius. Microscopy 35: 535–538.Google Scholar
  35. Jacobs, J., 1974. Quantitative measurement of food selection. A modification of the forage ratio and Ivlev's electivity index. Oecologia 14: 413–417.Google Scholar
  36. Jürgens, K. & H. Güde, 1991. Seasonal changes in the grazing impact of phagotrophic flagellates on bacteria in Lake Constance. Mar. Microb. Food Webs 5: 27–37.Google Scholar
  37. Jumars, P. A., D. L. Penry, J. A. Baross, M. J. Perry & B. W. Frost, 1989. Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep Sea Research 36: 483–495.Google Scholar
  38. Koste, W., 1970. Über die sessilien Rotatorien einer Moorblänke in Nordwestdeutschland. Arch. Hydrobiol. 68: 96–125.Google Scholar
  39. Koste, W., 1973. Das Rädertier-Porträt. Ein merkwürdiges festsitzendes Rädertier: Cupelopagis vorax. Mikrokosmos 62: 101–106.Google Scholar
  40. Koste, W., 1973. Rotatoria. Die Rädertiere Mitteleuropas. Gebrüder Borntraeger, Berlin, Stuttgart.Google Scholar
  41. Kreiskott, H., 1958. Natürliche und experimentelle Blockierung der Eiablage bei Epiphanes senta (EHRENBERG). Arch. Hydrobiol. 54: 393–403.Google Scholar
  42. Lampert, W., 1978. Release of dissolved organic carbon by grazing zooplankton. Limnol. Oceanogr. 23: 831–834.Google Scholar
  43. Maly, E. J., 1969. A laboratory study of the interaction between the predatory rotifer Asplanchna and Paramecium. Ecology 50: 59–73.Google Scholar
  44. Matsuyama, M. & E. Shirouzu, 1978. Importance of photosynthetic sulfur bacteria, Chromatium sp., as an organic matter producer in Lake Kaiike. Jap. J. Limnol. 39: 103–111.Google Scholar
  45. Nauwerck, A., 1963. Die Beziehungen zwischen Zooplankton und Phytoplankton im See Erken. Symb. Bot. Upsal. 175: 1–163.Google Scholar
  46. Nixdorf, B. & H. Arndt, 1992. Seasonal changes in carbon dynamics in a eutrophic lake including the microbial web. Arch. Hydrobiol. Beih. Ergebn. Limnol. in press.Google Scholar
  47. Ooms-Wilms, A. L., 1991. Ingestion of fluorescently labelled bacteria by rotifers and cladocerans in Lake Loosdrecht as measures of bacterivory: preliminary results. Mem. Ist. ital. Idrobiol. 48: 269–278.Google Scholar
  48. Pace, M. L., G. B. McManus & S. E. G. Findlay, 1990. Planktonic community structure determines the fate of bacterial production in a temperate lake. Limnol. Oceanogr. 35: 795–808.Google Scholar
  49. Pernie, G. L., D. Scavia, M. L. Pace & H. J. Carrick, 1990. Micrograzer impact and substrate limitation of bacterioplankton in Lake Michigan. Can. J. Fish. aquat. Sci. 47: 1836–1841.Google Scholar
  50. Pilarska, J., 1972. The dynamics of growth of experimental populations of the rotifer Brachionus rubens EHRENBG. Pol. Arch. Hydrobiol. 19: 265–277.Google Scholar
  51. Porter, K. G., E. B. Sherr, B. F. Sherr, M. Pace & R. W. Sanders, 1985. Protozoa in planktonic food webs. J. Protozool. 32: 409–415.Google Scholar
  52. Porter, K. G., H. Paerl, R. Hodson, M. pace, J. Priscu, B. Riemann, D. Scavia & J. Stockner, 1988. Microbial interactions in lake food webs. In S. R. Carpenter (ed.), Complex Interactions in Lake Communities. Springer-Verlag, New York: 209–227.Google Scholar
  53. Pourriot, R., 1965. Recherches sur l'écologie des rotifés. Vie et Milieu Suppl. 21: 1–224.Google Scholar
  54. Pourriot, R., 1977. Food and feeding habits of Rotifera. Arch. Hydrobiol. Beih. Ergebn. Limnol. 8: 243–260.Google Scholar
  55. Rainer, H., 1968. Urtiere, Protozoa; Wurzelfüßler, Rhizopoda; Sonnentierchen, Heliozoa. In M. Dahl & F. Peus (eds), Die Tierwelt Deutschlands. Gustav Fischer Verlag, Jena.Google Scholar
  56. Reguera, B., 1984. The effect of ciliate contamination in mass cultures of the rotifer, Brachionus plicatilis O. F. MÜLLER. Aquaculture 40: 103–108.Google Scholar
  57. Ricci, C., 1984. Culturing of some bdelloid rotifers. Hydrobiologia 112: 45–51.Google Scholar
  58. Riemann, B., N. O. G. Jorgensen, W. Lampert & J. A. Fuhrman, 1986. Zooplankton induced changes in dissolved free amino acids and in production rates of freshwater bacteria. Microb. Ecol. 12: 247–258.Google Scholar
  59. Robertson, J. R. & G. W. Salt, 1981. Responses in growth, mortality, and reproduction to variable food levels by the rotifer, Asplanchna girodi. Ecology 62: 1585–1596.Google Scholar
  60. Rothhaupt, K. O., 1990a. Changes of the functional responses of the rotifers Brachionus rubens and Brachionus calyciflorus with particle sizes. Limnol. Oceanogr. 35: 24–32.Google Scholar
  61. Rothhaupt, K.O., 1990b. Differences in particle size-dependent feeding efficiencies of cloesely related rotifer species. Limnol. Oceanogr. 35: 16–23.Google Scholar
  62. Ruttner-Kolisko, A., 1980. The abundance and distribution of Filinia terminalis in various types of lakes as related to temperature, oxygen, and food. In H. J. Dumont & J. Green (eds), Rotatoria. Developments in Hydrobiology I. Dr W. Junk Publishers, The Hague: 169–175. Reprinted from Hydrobiologia 73.Google Scholar
  63. Sanders, R. W. & K. G. Porter, 1990. Bacterivorous flagellates as food resources for the freshwater crustacean zooplankter Daphnia ambigua. Limnol. Oceanogr. 35: 188–191.Google Scholar
  64. 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. Limnol. Oceanogr. 34: 673–687.Google Scholar
  65. Scott, J. M., 1987. Further nutritional studies on the marine rotifer Encentrum linnhei. In L. May, R. Wallace & A. Herzig (eds), Rotifer Symposium IV. Developments in Hydrobiology 42. Dr W. Junk Publishers, Dordrecht: 303–306. Reprinted from Hydrobiologia 147.Google Scholar
  66. Sorokin, Y. I. & E. B. Paveljeva, 1972. On the quantitative characteristics of the pelagic ecosystems of Dalnee Lake (Kamchatka). Hydrobiologia 40: 519–552.Google Scholar
  67. Spittler, P., 1976. Beiträge zur Kenntnis der Nahrungsauswahl von Zooplanktern eutropher Küstengewässer. Wiss. Z. Univ. Rostock, math.-nat. R. 25: 305–310.Google Scholar
  68. Starkweather, P. L., 1980. Behavioral determinants of diet quantity and diet quality in Brachionus calyciflorus. In W. C. H. Kerfoot (ed.), Evolution and Ecology of Zooplankton Communities. University Press of New England, Hanover, New Hampshire and London: 151–157.Google Scholar
  69. Starkweather, P. L., J. J. Gilbert & T. M. Frost, 1979. Bacterial feeding by the rotifer Brachionus calyciflorus: Clearance and ingestion rates, behaviour and population dynamics. Oecologia 44: 26–30.Google Scholar
  70. Stemberger, R. S., 1981. A general approach to the culture of planktonic rotifers. Can. J. Fish. Aquat. Sci. 38: 721–724.Google Scholar
  71. Stockner, J. G., 1988. Phototrophic picoplankton: An overview from marine and freshwater ecosystems. Limnol. Oceanogr. 33: 765–775.Google Scholar
  72. Stoecker, D. K. & J. M. Capuzzo, 1990. Predation on Protozoa: its importance to zooplankton. J. Plankton Res. 12: 891–908.Google Scholar
  73. Vadstein, O., G. Øie & Y. Olsen, 1993. Particle size dependent feeding by the rotifer Brachionus plicatilis. Hydrobiologia 255/256: 261–267.Google Scholar
  74. Weisse, T., 1991. The annual cycle of heterotrophic freshwater nanoflagellates: role of bottom-up versus top-down control. J. Plankton Res. 13: 167–185.Google Scholar
  75. Weisse, T. & H. Müller, 1990. Significance of heterotrophic nanoflagellates and ciliates in large lakes: evidence from Lake Constance. In M. M. Tilzer & C. Serruya (eds), Large Lakes. Springer-Verlag, Berlin: 540–555.Google Scholar
  76. 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. Limnol. Oceanogr. 35: 781–794.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Hartmut Arndt
    • 1
  1. 1.Max-Planck-Institut für LimnologiePlönGermany

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