, Volume 432, Issue 1–3, pp 25–36 | Cite as

Dynamics and trophic roles of heterotrophic protists in the plankton of a freshwater tidal estuary

  • Koenraad MuylaertEmail author
  • Riet Van Mieghem
  • Koen Sabbe
  • Micky Tackx
  • Wim Vyverman


Freshwater tidal estuaries comprise the most upstream reaches of estuaries and are often characterised by the presence of dense bacterial and algal populations which provide a large food source for bacterivorous and algivorous protists. In 1996, the protistan community in the freshwater tidal reaches of the Schelde estuary was monitored to evaluate whether these high food levels are reflected in a similarly high heterotrophic protistan biomass. Protistan distribution patterns were compared to those of metazoan zooplankton to evaluate the possible role of top-down regulation of protists by metazoans. Apart from the algivorous sarcodine Asterocaelum, which reached high densities in summer, heterotrophic protistan biomass was dominated by ciliates and, second in importance, heterotrophic nanoflagellates (HNAN). HNAN abundance was low (annual average 2490 cells ml−1) and did not display large seasonal variation. It is hypothesised that HNAN were top-down controlled by oligotrich ciliates throughout the year and by rotifers in summer. Ciliate abundance was generally relatively high (annual average 65 cells ml−1) and peaked in winter (maximum 450 cells ml−1). The decline of ciliate populations in summer was ascribed to grazing by rotifers, which developed dense populations in that season. In winter, ciliate populations were probably regulated `internally' by carnivorous ciliates (haptorids and Suctoria). Our observations suggest that, in this type of productive ecosystems, the microbial food web is mainly top-down controlled rather than regulated by food availability.

heterotrophic nanoflagellates ciliates rotifers bacteria microbial food web tidal river estuary Schelde 


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  1. Albright, L. J., E. B. Sherr, B. F. Sherr &; R. D. Fallon, 1987. Grazing of ciliated protozoa on free and particle-attahed bacteria. Mar. Ecol. Progr. Ser. 38: 125–129.Google Scholar
  2. Anderson, O. R. &; A. Rogerson, 1995. Annual abundances and growth potential of Gymnamoebae in the Hudson Estuary with comparative data from the Firth of Clyde. Eur. J. Protistol. 31: 223–233.Google Scholar
  3. Arndt, H., 1993a. A critical review of the importance of rhizopods (naked and testate amoebae) and actinopods (heliozoa) in lake plankton. Mar. Microb. Food Webs 7: 3–29.Google Scholar
  4. Arndt, H., 1993b. Rotifers as predators on components of the microbial food web (bacteria, heterotrophic flagellates, ciliates)-a review. Hydrobiologia 255/256 (Dev. Hydrobiol. 83): 231–246.Google Scholar
  5. Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil &; F. Thingstadt, 1983. The ecological role of water column microbes in the sea. Mar. Ecol. Progr. Ser. 10: 257–263.Google Scholar
  6. Bailey-Watts, A. E. &; J. W. G. Lund, 1973. Observations on a diatom bloom in Loch Leven, Scotland. Biol. J. Linn. Soc. 5: 235–253.Google Scholar
  7. Basu, B. K. &; F. R. Pick, 1997. Factors related to heterotrophic bacterial and flagellate abundance in temperate rivers. Aquat. Microb. Ecol. 12: 123–129.Google Scholar
  8. Beaver, J. R. &; T. L. Crisman, 1989. The role of ciliated protozoa in pelagic freshwater ecosystems. Microbial. Ecol. 17: 111–136.Google Scholar
  9. Berninger, U.-G., S. A. Wickham &; B. J. Findlay, 1993. Trophic coupling within the microbial food web: a study with fine temporal resolution in a eutrophic freshwater ecosystem. Freshwat. Biol. 30: 419–432.Google Scholar
  10. Børsheim, K. Y., 1984. Clearance rates on bacteria-sized particles by freshwater ciliates measured with monodispersed fluorescent latex beads. Oecologia 63: 286–288.Google Scholar
  11. Børsheim, K. Y. &; G. Bratbak, 1987. Cell volume to carbon conversion factors for a bacterivorous Monas sp. enriched from seawater. Mar. Ecol. Progr. Ser. 36: 171–175.Google Scholar
  12. Canter, H. M., 1973. A new primitive protozoan devouring centric diatoms in the plankton. Zool. J. Linn. Soc. 52: 63–83.Google Scholar
  13. Canter, H. M., 1980. Observations on the amoeboid protozoan Asterocaelum (Proteomixida) which ingests algae. Protistologica 16: 475–483.Google Scholar
  14. Carlough, L. A. &; J. L. Meyer, 1991. Bacterivory by sestonic protists in a southeastern blackwater river. Limnol. Oceanogr. 36: 873–883.Google Scholar
  15. Cole, J. J., N. F. Caraco &; B. L. Peierls, 1992. Can phytoplankton maintain a positive carbon balance in a turbid, freshwater, tidal estuary? Limnol. Oceanogr. 37: 1608–1617.Google Scholar
  16. De Sève, M. A., 1993. Diatoms bloom in the tidal freshwater zone of a turbid and shallow estuary, Rupert Bay (James Bay, Canada). Hydrobiologia 269/270: 225–233.Google Scholar
  17. Dolan, J. R., 1991. Guilds of ciliate microzooplankton in the Chesapeake Bay. Estuar. coast. shelf Sci. 33: 137–152.Google Scholar
  18. Dolan, J. R. &; D. W. Coats, 1990. Seasonal abundances of planktonic ciliates and microflagellates in mesohaline Chesapeake Bay waters. Estuar. coast. shelf Sci. 31: 157–175.Google Scholar
  19. Dolan, J. R. &; C. L. Gallegos, 1991. Trophic coupling of rotifers, microflagellates, and bacteria during fall months in the Rhode River Estuary. Mar. Ecol. Progr. Ser. 77: 147–156.Google Scholar
  20. Eisma, D., 1993. Flocculation and deflocculation of suspended matter in estuaries. Arch. Hydrobiol./Suppl. 75: 311–324.Google Scholar
  21. Fenchel, 1982. Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar. Ecol. Progr. Ser. 8: 225–231.Google Scholar
  22. Fenchel, T., 1988. Marine plankton food chains. Ann. Rev. Ecol. Syst. 19: 19–38.Google Scholar
  23. Findlay, S., M. Pace &; D. Fisher, 1996. Spatial and temporal variability in the lower food web of the tidal freshwater Hudson River. Estuaries 19: 866–873.Google Scholar
  24. Findlay, S., M. L. Pace, D. Lints, J. J. Cole, N. F. Caraco &; B. Peierls, 1991. Weak coupling of bacterial and algal production in a hetertrophic ecosystem: The Hudson River estuary. Limnol. Oceanogr. 36: 268–278.Google Scholar
  25. Foissner, W. &; H. Berger, 1996. A user-friendly guide to the ciliates (Protzoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes and waste waters, with notes on their ecology. Freshwat. Biol. 35: 375–482.Google Scholar
  26. Frankignoulle, M., I. Bourge &; R. Wollast, 1996. Atmospheric CO2 fluxes in a highly polluted estuary (the Scheldt). Limnol. Oceanogr. 41: 365–369.Google Scholar
  27. Gasol, J. M., 1994. A framework for the assessment of top-down vs bottom-up control of heterotrophic nanoflagellate abundance. Mar. Ecol. Progr. Ser. 113: 291–300.Google Scholar
  28. Gilbert, J. J. &; J. D. Jack, 1993. Rotifers as predators on small ciliates. Hydrobiologia 255/256 (Dev. Hydrobiol. 83): 247–253.Google Scholar
  29. Goossen, N. K., P. Van Rijswijk &; U. Brockmann, 1995. Comparison of heterotrophic bacterial production rates in early spring in the turbid estuaries of the Scheldt and the Elbe. Hydrobiologia 311: 31–42.Google Scholar
  30. Goossen, N. K., P. Van Rijswijk, J. Kromkamp &; J. Peene, 1997. Regulation of annual variation in heterotrophic bacterial production in the Schelde estuary (SW Netherlands). Aquat. Microbiol. Ecol. 12: 223–232.Google Scholar
  31. Heinbokel, J. F., D. W. Coats, K. W. Henderson &; M. A. Tyler, 1988. Reproduction rates and secondary production of three species of the rotifer genus Synchaeta in the estuarine Potomac River.J. Plankton Res. 10: 659–674.Google Scholar
  32. Heip, C. H. R., N. K. Goosen, P. M. J. Herman, J. Kromkamp, J. J. Middelburg &; K. Soetaert, 1995. Production and consumption of biological particles in temperate tidal estuaries. Oceanogr. Mar. Biol. Ann. Rev. 33: 1–149.Google Scholar
  33. Holligan, P. M. &; W. A. Reiners, 1992. Global change. Adv. Ecol. Res. 22: 212–256.Google Scholar
  34. Jongman, R. H. G., C. J. F. Ter Braak &; O. F. R. van Tongeren, 1987. Data analysis in community and landscape ecology. Pudoc, Wageningen: 299 pp.Google Scholar
  35. Jonsson, P. R., 1986. Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar. Ecol. Progr. Ser. 33: 265–277.Google Scholar
  36. Jürgens, K., S. A. Wickham, K. O. Rothhaupt &; B. Santer, 1996. Feeding rates of macro-and microzooplankton on heterotrophic nanoflagellates. Limnol. Oceanogr. 41: 1833–1839.Google Scholar
  37. Kerr, S. J., 1983. Colonization of blue-green algae by Vorticella (Ciliata, Peritrichida). Trans. am. microsc. Soc. 102: 38–47.Google Scholar
  38. Kobayashi, T., P. Gibbs, P. I. Dixon &; R. S. Shiel, 1996. Grazing by a river zooplankton community: Importance of microzooplankton. Mar. Freshwat. Res. 47: 1025–1036.Google Scholar
  39. Largier, J. L., 1993. Estuarine fronts: How important are they? Estuaries 16: 1–11.Google Scholar
  40. Laybourn-Parry, J., 1994. Seasonal successions of protozooplankton in freshwater ecosystems of different lattitudes. Mar. Microb. Food Webs 8: 145–162.Google Scholar
  41. Laybourn-Parry, J., A. Rogerson &; W. Crawford, 1992. Temporal patterns of protozooplankton abundance in te Clyde and Loch Striven. Estuar. coast. shelf Sci. 35: 533–543.Google Scholar
  42. Laybourn-Parry, J., M. Walton, J. Young, R. I. Jones &; A. Shine, 1994. Protozooplankton and bacterioplankton in a large oligotrophic lake-Loch Ness, Scotland. J. Plankton Res. 16: 1655–1670.Google Scholar
  43. Lovejoy, C., W. F. Vincent, J. J. Frenette &; J. J. Dodson, 1993. Microbial gradients in a turbid estuary: Application of a new method for protozoan community analysis. Limnol. Oceanogr. 38: 1295–1303.Google Scholar
  44. Meire, P., T. Ysebaert, M. Hoffmann, E. Van Den Balck, K. Devos, R. Samanya, N. Deregge, J. Van Waeyenberge, A. Anselin, G. Rossaert &; E. Kuijken, 1994. Ecologisch onderzoek in de Zeeschelde door het Instituut vor Natuurbehoud: onderbouwing van natuurherstel en natuurontwikkeling. Biol. Jaarb. Dodonaea 62: 27–47.Google Scholar
  45. Montagnes, D. J. S, 1996. Growth responses of planktonic ciliates in the genera Strobilidium and Strombidium. Mar. Ecol. Progr. Ser. 130: 241–254.Google Scholar
  46. Muylaert, K., A. Van Kerkvoorde, W. Vyverman &; K. Sabbe, 1997. Structural characteristics of phytoplankton assemblages in tidal and non-tidal freshwater systems: a case-study from the Schelde basin. Freshwat. Biol. 38: 263–276.Google Scholar
  47. Muylaert, K., K. Sabbe &; W. Vyverman. Spatial and temporal dynamics of phytoplankton communities in a freshwater tidal estuary (Schelde, Belgium). Estuar. coast. Shelf Sci. 50: 673-687.Google Scholar
  48. Nakano, S., N. Ishii, P. M. Manage &; Z. Kabawata, 1998. Trophic roles of heterotrophic nanoflagellates and ciliates among planktonic organisms in a hypereutrophic pond. Aquat. Microb. Ecol. 16: 153–161.Google Scholar
  49. Odum, W. E., 1988. Comparative ecology of tidal freshwater and salt marshes. Ann. Rev. Ecol. Syst. 19: 147–176.Google Scholar
  50. Ooms-Willems, A. L., G. Postema &; R. D. Gulati, 1995. Evaluation of bacterivory of Rotifera based on measurements of in situ ingestion of fluorescent particles, including some comparisons with Cladocera. J. Plankton Res. 17: 1057–1077.Google Scholar
  51. Pace, M. L., E. G. S. Findlay &; D. Lints, 1992. Zooplankton in advective environments: the Hudson River community and a comparitive analysis. Can. J. Fish. aquat. Sci. 49: 1060–1069.Google Scholar
  52. 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
  53. Paffenhöfer, G.-A., 1998. Heterotrophic protozoa and small metazoa: feeding rates and prey-consumer interactions. J. Plankton Res. 20: 121–133.Google Scholar
  54. Patterson, D. J. &; S. Hedley, 1992. Free-living Freshwater Protozoa-A Colour Guide Wolfe, Aylesbury: 223 pp.Google Scholar
  55. Putt, M. &; D. K. Stoecker, 1989. An experimentally determined carbon:volume ratio for marine 'oligotrichous' ciliates. Limnol. Oceanogr. 34: 97–113.Google Scholar
  56. Remane, A. &; C. Schlieper, 1958. Die Biologie des Brackwassers. E. Schweizerbart'sche Verlagsbuchhändlung, Stuttgart: 348 pp.Google Scholar
  57. Riemann, B. &; K. Christoffersen, 1993. Microbial trophodynamics in temperate lakes. Mar. Microb. Food Webs 7: 69–100.Google Scholar
  58. Rothhaupt, K. O., 1990. Differences in particle size-dependent feeding efficiencies of closely related rotifer species. Limnol. Oceanogr. 35: 16–23.Google Scholar
  59. Sanders, R. W. &; S. A. Wickham, 1993. Planktonic protozoa and metazoa: Predation, food quality and population control. Mar. Microb. Food Webs 7: 197–223.Google Scholar
  60. Sanders, R.W., D. A. Caron &; U. G. Berninger, 1992. Relationships between bacteria and heterotrophic nanoplankton in marine and fresh waters-an inter-ecosystem comparison. Mar. Ecol. Progr. Ser. 86: 1–14.Google Scholar
  61. Sanders, R. W., D. A. Leeper, C. H. King &; K. G. Porter, 1994. Grazing by rotifers and crustacean zooplankton on nanoplanktonic protists. Hydrobiologia 288: 167–181.Google Scholar
  62. 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
  63. Schuchardt B., U. Haesloop &; M. Schirmer, 1993. The tidal freshwater reach of the Weser estuary: Riverine or estuarine? Neth. J. Aquat. Ecol. 27: 215–226.Google Scholar
  64. Sheldon, R. W., P. Nival &; F. Rassoulzadegan, 1986. An experimental investigation of a flagellate-ciliate-copepod food chain with some observations relevant to the linear biomass hypothesis. Limnol. Oceanogr. 31: 184–188.Google Scholar
  65. Sherr, E. B. &; B. F. Sherr, 1994. Bacterivory and herbivory: key roles of phagotrophic protists in pelagic food webs. Microb. Ecol. 28: 223–235.Google Scholar
  66. Sherr, B. F., E. B. Sherr &; C. Pedrós-Alió, 1989. Simultaneous measurements of bacterioplankton production and protozoan herbivory in estuarine water. Mar. Ecol. Progr. Ser. 54: 209–219.Google Scholar
  67. Sherr, E. B., D. A. Caron &; B. F. Sherr, 1993. Staining of heterotrophic protists for visualisation via epifluorescence microscopy. In Kemp, P. F., B. F. Sherr, E. B. Sherr &; J. J. Cole (eds), Aquatic Microbial Ecology. Lewis Publishers, Boca Raton: 213–227.Google Scholar
  68. Shiah, F.-K. &; H. W. Ducklow, 1994. Temperature and substrate regulation of bacterial abundance, production and specific growth rate in Chesapeake Bay, U.S.A. Mar. Ecol. Progr. Ser. 103: 297–308.Google Scholar
  69. Sime-Ngando, T., M. Gosselin, S. Roy &; J.-P. Chanut, 1995. Significance of planktonic ciliated protozoa in the Lower St. Lawrence estuary: Comparison with bacterial, phytoplankton and particulate organic carbon. Aquat. Microbiol. Ecol. 9: 243–258.Google Scholar
  70. Smayda, T. J., 1978. From phytoplankters to biomass. In Sournia, A. (ed.), Monographs on Oceanographic Methodology 6. Phytoplankton manual. Unesco, Norwich: 273–279.Google Scholar
  71. Smetacek, V., 1981. The annual cycle of protozooplankton in the Kiel Bight. Mar. Biol. 63: 1–11.Google Scholar
  72. Soetaert, K. &; P. M. J. Herman, 1995. Carbon flows in the Westerschelde estuary (The Netherlands) evaluated by means of an ecosystem model (MOSES). Hydrobiologia 311: 247–266.Google Scholar
  73. Sorokin, Y. U. &; E. B. Paveljeva, 1972. On the characteristics of the pelagic ecosystem of Dalnee lake (Kamchatka). Hydrobiologia 40: 519–552.Google Scholar
  74. Soto, Y., M. Bianchi, J. Martinez &; J. V. Rego, 1993. Seasonal evolution of microplanktonic communities in the estuarine front ecosystem of the Rhône River plume (North-western Mediterranean Sea). Estuar. coast. Shelf Sci. 37: 1–13.Google Scholar
  75. Starkweather, P. L., 1980. Aspects of feeding behaviour and trophic ecology of suspension-feeding rotifers. Hydrobiologia 73: 633–72.Google Scholar
  76. Taverniers, E., 1997. Zeescheldebekken: De afvoer ven de Schelde in 1996. Ministerie van de Vlaamse Gemeenschap, Departement Leefmilieu en Infrastructuur, Administratie Waterwegen en Zeewezen, Afdeling Maritieme Schelde, Antwerpen.Google Scholar
  77. Ter Braak, C. J. F., 1987. CANOCO-a FORTRAN program for canonical community ordination by (partial) (detrended) (canonical) correspondence analysis, principal component analysis and redundancy analysis (version 2.1). Agriculture Mathematics Group, Wageningen.Google Scholar
  78. Ter Braak, C. J. F., 1990. Update notes: CANOCO version 3.10. Agriculture Mathematics Group, Wageningen.Google Scholar
  79. Ter Braak, C. J. F., 1994. Canonical community ordination: Part I: Basic theory and linear methods. Ecoscience 1: 127–140.Google Scholar
  80. Throndsen, J., 1978. Preservation and storage. In Sournia, A. (ed.), Monographs on Oceanographic Methodology 6. Phytoplankton manual. Unesco, Norwich: 69–74.Google Scholar
  81. Tranvik, L. J., K. G. Porter &; J. M. Sieburth, 1989. Occurrence of bacterivory in Cryptomonas, a common fresh-water phytoplankter. Oecologia 78: 473–476.Google Scholar
  82. Utermöhl, H., 1958. Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitt. int. theor. angew. Limnol. 9: 1–38.Google Scholar
  83. Vacqué, D. &; M. L. Pace, 1992. Grazing on bacteria by flagellates and cladocerans in lakes of contrasting food-web structure. J. Plankton Res. 14: 307–321.Google Scholar
  84. Vacqué, D., M. L. Pace, S. Findlay &; D. Lints, 1992. Fate of bacterial production in a heterotrophic ecosystem: Grazing by protists and metazoans in the Hudson estuary. Mar. Ecol. Progr. Ser. 89: 155–163.Google Scholar
  85. Verity, P., 1991. Measurement and simulation of prey uptake bymarine planktonic ciliates fed plastidic and aplastidic nanoplankton. Limnol. Oceanogr. 36: 729–750.Google Scholar
  86. Weisse, T., 1991a. The annual cycle of heterotrophic freshwater nanoflagellates: role of bottom-up versus top-down controll. J. Plankton Res. 13: 167–185.Google Scholar
  87. Weisse, T., 1991b. The microbial food web and its sensitivity to eutrophication and contaminant enrichment: A cross-system overview. Int Rev. ges. Hydrobiol. 76: 327–337.Google Scholar
  88. Wickham, S., 1995. Cyclops predation on ciliates: species-specific differences and functional responses. J. Plankton Res. 17: 1633–1646.Google Scholar
  89. Wollast, R. J., 1983. Interactions in estuaries and coastal waters. In Bolin, B. &; R. B. Cook (ed.), The Major Biogeochemical Cycles and their Interactions. John Wiley and Sons, New York: 385–407.Google Scholar
  90. Zimmermann, H., 1996. Interactions between planktonic protozoans and metazoans after the spring bloom of phytoplankton in a eutrophic lake, the Belauer See, in the Bornhövener Seenkette, North Germany. Acta Protozool. 35: 215–221.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Koenraad Muylaert
    • 1
    Email author
  • Riet Van Mieghem
    • 2
  • Koen Sabbe
    • 3
  • Micky Tackx
    • 4
  • Wim Vyverman
    • 3
  1. 1.Sect. Protistology &; Aquatic Ecology, Dept. BiologyUniversity of GhentGentBelgium
  2. 2.Dept. EcologyFree University BrusselsBrusselBelgium
  3. 3.Sect. Protistology &; Aquatic Ecology, Dept. BiologyUniversity of GhentGentBelgium
  4. 4.Dept. EcologyFree University BrusselsBrusselBelgium

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