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

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Abstract

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.

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References

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Beaver, J. R. &; T. L. Crisman, 1989. The role of ciliated protozoa in pelagic freshwater ecosystems. Microbial. Ecol. 17: 111–136.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Canter, H. M., 1973. A new primitive protozoan devouring centric diatoms in the plankton. Zool. J. Linn. Soc. 52: 63–83.

    Google Scholar 

  • Canter, H. M., 1980. Observations on the amoeboid protozoan Asterocaelum (Proteomixida) which ingests algae. Protistologica 16: 475–483.

    Google Scholar 

  • Carlough, L. A. &; J. L. Meyer, 1991. Bacterivory by sestonic protists in a southeastern blackwater river. Limnol. Oceanogr. 36: 873–883.

    Google Scholar 

  • 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 

  • 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 

  • Dolan, J. R., 1991. Guilds of ciliate microzooplankton in the Chesapeake Bay. Estuar. coast. shelf Sci. 33: 137–152.

    Google Scholar 

  • 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 

  • 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 

  • Eisma, D., 1993. Flocculation and deflocculation of suspended matter in estuaries. Arch. Hydrobiol./Suppl. 75: 311–324.

    Google Scholar 

  • Fenchel, 1982. Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar. Ecol. Progr. Ser. 8: 225–231.

    Google Scholar 

  • Fenchel, T., 1988. Marine plankton food chains. Ann. Rev. Ecol. Syst. 19: 19–38.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Frankignoulle, M., I. Bourge &; R. Wollast, 1996. Atmospheric CO2 fluxes in a highly polluted estuary (the Scheldt). Limnol. Oceanogr. 41: 365–369.

    Google Scholar 

  • 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 

  • Gilbert, J. J. &; J. D. Jack, 1993. Rotifers as predators on small ciliates. Hydrobiologia 255/256 (Dev. Hydrobiol. 83): 247–253.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Holligan, P. M. &; W. A. Reiners, 1992. Global change. Adv. Ecol. Res. 22: 212–256.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Kerr, S. J., 1983. Colonization of blue-green algae by Vorticella (Ciliata, Peritrichida). Trans. am. microsc. Soc. 102: 38–47.

    Google Scholar 

  • 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 

  • Largier, J. L., 1993. Estuarine fronts: How important are they? Estuaries 16: 1–11.

    Google Scholar 

  • Laybourn-Parry, J., 1994. Seasonal successions of protozooplankton in freshwater ecosystems of different lattitudes. Mar. Microb. Food Webs 8: 145–162.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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.

  • 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 

  • Odum, W. E., 1988. Comparative ecology of tidal freshwater and salt marshes. Ann. Rev. Ecol. Syst. 19: 147–176.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Paffenhöfer, G.-A., 1998. Heterotrophic protozoa and small metazoa: feeding rates and prey-consumer interactions. J. Plankton Res. 20: 121–133.

    Google Scholar 

  • Patterson, D. J. &; S. Hedley, 1992. Free-living Freshwater Protozoa-A Colour Guide Wolfe, Aylesbury: 223 pp.

    Google Scholar 

  • Putt, M. &; D. K. Stoecker, 1989. An experimentally determined carbon:volume ratio for marine 'oligotrichous' ciliates. Limnol. Oceanogr. 34: 97–113.

    Google Scholar 

  • Remane, A. &; C. Schlieper, 1958. Die Biologie des Brackwassers. E. Schweizerbart'sche Verlagsbuchhändlung, Stuttgart: 348 pp.

    Google Scholar 

  • Riemann, B. &; K. Christoffersen, 1993. Microbial trophodynamics in temperate lakes. Mar. Microb. Food Webs 7: 69–100.

    Google Scholar 

  • Rothhaupt, K. O., 1990. Differences in particle size-dependent feeding efficiencies of closely related rotifer species. Limnol. Oceanogr. 35: 16–23.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Smetacek, V., 1981. The annual cycle of protozooplankton in the Kiel Bight. Mar. Biol. 63: 1–11.

    Google Scholar 

  • 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 

  • Sorokin, Y. U. &; E. B. Paveljeva, 1972. On the characteristics of the pelagic ecosystem of Dalnee lake (Kamchatka). Hydrobiologia 40: 519–552.

    Google Scholar 

  • 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 

  • Starkweather, P. L., 1980. Aspects of feeding behaviour and trophic ecology of suspension-feeding rotifers. Hydrobiologia 73: 633–72.

    Google Scholar 

  • 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 

  • 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 

  • Ter Braak, C. J. F., 1990. Update notes: CANOCO version 3.10. Agriculture Mathematics Group, Wageningen.

    Google Scholar 

  • Ter Braak, C. J. F., 1994. Canonical community ordination: Part I: Basic theory and linear methods. Ecoscience 1: 127–140.

    Google Scholar 

  • Throndsen, J., 1978. Preservation and storage. In Sournia, A. (ed.), Monographs on Oceanographic Methodology 6. Phytoplankton manual. Unesco, Norwich: 69–74.

    Google Scholar 

  • 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 

  • Utermöhl, H., 1958. Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitt. int. theor. angew. Limnol. 9: 1–38.

    Google Scholar 

  • 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 

  • 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 

  • Verity, P., 1991. Measurement and simulation of prey uptake bymarine planktonic ciliates fed plastidic and aplastidic nanoplankton. Limnol. Oceanogr. 36: 729–750.

    Google Scholar 

  • 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 

  • 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 

  • Wickham, S., 1995. Cyclops predation on ciliates: species-specific differences and functional responses. J. Plankton Res. 17: 1633–1646.

    Google Scholar 

  • 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 

  • 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 

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  1. Sect. Protistology &; Aquatic Ecology, Dept. Biology, University of Ghent, K.L. Ledeganckstraat 35, B-9000, Gent, Belgium

    Koenraad Muylaert

  2. Dept. Ecology, Free University Brussels, Pleinlaan 2, 1050, Brussel, Belgium

    Riet Van Mieghem

  3. Sect. Protistology &; Aquatic Ecology, Dept. Biology, University of Ghent, K.L. Ledeganckstraat 35, B-9000, Gent, Belgium

    Koen Sabbe & Wim Vyverman

  4. Dept. Ecology, Free University Brussels, Pleinlaan 2, 1050, Brussel, Belgium

    Micky Tackx

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Muylaert, K., Van Mieghem, R., Sabbe, K. et al. Dynamics and trophic roles of heterotrophic protists in the plankton of a freshwater tidal estuary. Hydrobiologia 432, 25–36 (2000). https://doi.org/10.1023/A:1004017018702

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