Skip to main content
Log in

Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters, measured with a dual-label radioisotope technique

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

A dual-isotope method was developed to measure grazing rates and food preferences of individual species of heterotrophic dinoflagellates from natural populations, collected from the Slope, Gulf Stream, and Sargasso Sea and from a transect from Iceland to New England, in 1983. The isotope method measures the grazing rates of microzooplankton which cannot be separated in natural populations on the basis of size. Tritiated-thymidine and 14C-bicarbonate were used to label natural heterotrophic and autotrophic food, respectively. Nine oceanic dinoflagellate species in the genera Protoperidinium, Podolampas, and Diplopsalis fed on both heterotrophic and autotrophic food particles with clearance rates of 0.4 to 8.0 μl cell-1 h-1, based on 3H incorporation, and 0.0 to 28.3 μl cell-1 h-1, based on 14C incorporation. Two dinoflagellate species, Protoperidinium ovatum and Podolampas palmipes, fed only on 3H-labelled food particles. Several species of dinoflagellates fed on bacteria (<1 μm) which had been prelabelled with 3H-thymidine. The clearance rates of heterotrophic dinoflagellates and ciliates were similar and within the range of tintinnid ciliate clearance rates reported in the literature. As heterotrophic dinoflagellates and ciliates can have comparable abundances in oceanic waters, we conclude that heterotrophic dinoflagellates may have an equally important impact as microheterotrophic grazers of phytoplankton and bacteria in oceanic waters.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Anraku, M.: Influence of the Cape Cod Canal on the hydrography and on the copepods in Buzzards Bay and Cape Cod Bay, Massachusetts. II. Respiration and feeding. Limnol. Oceanogr. 9, 195–206 (1964)

    Google Scholar 

  • Barker, H. A.: The culture and physiology of the marine dinoflagellates. Arch. Mikrobiol. 6, 157–181 (1935)

    Google Scholar 

  • Beers, J. R., F. M. H. Reid and G. L. Stewart: Seasonal abundance of the microplankton population in the North Pacific Central Gyre. Deep-Sea Res. 29, 227–245 (1982)

    Article  Google Scholar 

  • Biecheler, B.: Recherches sur les Peridiniens. Bull. biol. Fr. Belg. 36 (Suppl.), 1–149 (1952)

    Google Scholar 

  • Blackbourn, D. J.: The feeding biology of tintinnid Protozoa and some other inshore microzooplankton, 224 pp. Ph.D. thesis, University of British Columbia 1974

  • Bursa, A. S.: The annual oceanographic cycle at Igloolik in the Canadian Arctic. II. The phytoplankton. J. Fish. Res. Bd Can. 18, 563–615 (1961)

    Google Scholar 

  • Cachon, P. J. et M. Cachon: Le système stomatopharyngien de Kofoidinium Pavillard. Comparisons avec celui divers Peridiniens libres et parasites. Protistologica 10, 217–222 (1974)

    Google Scholar 

  • Capriulo, G. M.: Feeding of field collected tintinnid micro-zooplankton on natural food. Mar. Biol. 71, 73–86 (1982)

    Google Scholar 

  • Capriulo, G. M. and E. J. Carpenter: Grazing by the 35 to 202 μm micro-zooplankton in Long Island Sound. Mar. Biol. 56, 319–326 (1980)

    Google Scholar 

  • Capriulo, G. M. and D. V. Ninivaggi: A comparison of the feeding activities of field collected tintinnids and copepods fed identical natural particle assemblages. Annls Inst. océanogr., Paris (N.S.) 58 (Suppl.), 325–334 (1982)

    Google Scholar 

  • Conover, R. J.: Oceanography of Long Island Sound, 1952–1954. VI. Biology of Acartia tonsa and A. clausii. Bull. Bingham oceanogr. Coll. 15, 156–233 (1956)

    Google Scholar 

  • Conover, R. J.: Feeding interactions of the pelagic zone. Rapp. P. v. Réun. Cons. perm. int. Explor. Mer 173, 66–76 (1978)

    Google Scholar 

  • Cuhel, R. and J. Waterbury: Biochemical composition and shortterm nutrient incorporation patterns in a unicellular marine cyanobacterium, Synechococcus (WH 7803). Limnol. Oceanogr. 29, 370–373 (1984)

    Google Scholar 

  • Daro, M. H.: A simplified 14C method for grazing measurements on natural plankton populations. Helgoländer wiss. Meeresunters. 31, 241–248 (1978)

    Google Scholar 

  • Davis, P. G.: Bacterivorous flagellates in marine waters, 164 pp. Ph.D. thesis, University of Rhode Island 1982

  • Davis, P. G. and J. McN. Sieburth: Differentiation of phototrophic and heterotrophic nanoplankton populations in marine waters by epifluorescence microscopy. Annls Inst. océanogr., Paris (N.S.) 58 (Suppl.), 249–260 (1982)

    Google Scholar 

  • Davis, P. G. and J. McN. Sieburth: Estuarine and oceanic microflagellate predation of actively growing bacteria: estimation by frequency of dividing-divided bacteria. Mar. Ecol. Prog. Ser. 19, 237–246 (1984)

    Google Scholar 

  • Deevey, G. B. and A. L. Brooks: Copepods of the Sargasso Sea off Bermuda: species composition, and vertical and seasonal distribution between the surface and 2 000 m. Bull. mar. Sci. 27, 256–291 (1977)

    Google Scholar 

  • Dodge, J. D. and R. M. Crawford: The morphology and fine structure of Ceratium hirundinella (Dinophyceae). J. Phycol. 6, 137–149 (1970)

    Google Scholar 

  • Dodge, J. D. and B. Hart-Jones: The vertical and seasonal distribution of dinoflagellates in the North Sea. Botanica mar. 17, 113–117 (1974)

    Google Scholar 

  • Donaghay, P. L. and L. F. Small: Food selection capabilities of the estuarine copepod Acartia clausi. Mar. Biol. 52, 137–146 (1979)

    Google Scholar 

  • Droop, M. R.: Phagotrophy in Oxyrrhis marina. Nature, Lond. 172, 250–252 (1953)

    Google Scholar 

  • Elbrächter, M.: On the taxonomy of unarmored dinophytes (Dinophyta) from the Northwest African upwelling region. “Meteor” ForschErgebn. (Ser. D) 30, 1–22 (1979)

    Google Scholar 

  • Fenchel, T.: Suspension feeding in ciliated Protozoa: functional response and particle size selection. Microb. Ecol. 6, 1–11 (1980a)

    Google Scholar 

  • Fenchel, T.: Relation between particle size selection and clearance in suspension feeding ciliates. Limnol. Oceanogr. 25, 735–740 (1980b)

    Google Scholar 

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

    Google Scholar 

  • Frey, L. C. and E. F. Stoermer: Dinoflagellate phagotrophy in the upper Great Lakes. Trans. Am. microsc. Soc. 99, 439–444 (1980)

    Google Scholar 

  • Frost, B. W.: Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17, 805–815 (1972)

    Google Scholar 

  • Fuhrman, J. A.: Influence of method on the apparent size distribution of bacterioplankton cells: epifluorescence microscopy compared to scanning electron microscopy. Mar. Ecol. Prog. Ser. 5, 103–106 (1982)

    Google Scholar 

  • Fuhrman, J. A. and F. Azam: Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar. Biol. 66, 109–120 (1982)

    Google Scholar 

  • Gaines, G. and F. J. R. Taylor: Extracellular digestion in marine dinoflagellates. J. Plankton Res. 6, 1057–1061 (1984)

    Google Scholar 

  • Hargis, J. R.: Comparison of techniques for measuring zooplankton filtration rates. Limnol. Oceanogr. 22, 942–944 (1977)

    Google Scholar 

  • Heinbokel, J. F.: Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar. Biol. 47, 177–189 (1978)

    Google Scholar 

  • Hollibaugh, J. T., J. A. Fuhrman and F. Azam: Radioactive labelling of natural assemblages of bacterioplankton for use in trophic studies. Limnol. Oceanogr. 25, 172–181 (1980)

    Google Scholar 

  • Kimor, B.: The role of phagotrophic dinoflagellates in marine ecosystems. Kieler Meeresforsch. (Sondbd) 5, 164–173 (1981)

    Google Scholar 

  • Kofoid, C. A. and O. Swezy: The free-living unarmoured dinoflagellata. Mem. Univ. Calif. 5, 1–538 (1921)

    Google Scholar 

  • Lee, R. E.: Saprophytic and phagocytic isolates of the colorless heterotrophic dinoflagellate Gyrodinium lebouriae Herdman. J. mar. biol. Ass. U.K. 57, 303–315 (1977)

    Google Scholar 

  • Lefèvre, J. and J. R. Grall: On the relationship of Noctiluca swarming off the western coast of Brittany with hydrological features and plankton characteristics of the environment. J. exp. mar. Biol. Ecol. 4, 287–306 (1970)

    Article  Google Scholar 

  • Lessard, E. J.: Oceanic heterotrophic dinoflagellates: distribution, abundance, and role as microzooplankton, 146 pp. Ph.D. dissertation, University of Rhode Island 1984

  • Marlowe, C. J. and C. B. Miller: Patterns of vertical distribution and migration of zooplankton at Ocean Station “P”. Limnol. Oceanogr. 20, 824–844 (1975)

    Google Scholar 

  • Morey-Gaines, G. and M. Elbrächter: Heterotrophic nutrition. In: The biology of dinoflagellates. Ed. by F. J. R. Taylor. Oxford: Blackwell Scientific. (In press)

  • Morey-Gaines, G. and R. Ruse: Encystment and reproduction of the predatory dinoflagellate, Polykrikos kofoidi Chatton (Gymnodiniales). Phycologia 19, 230–236 (1980)

    Google Scholar 

  • Mullin, M.: Some factors affecting the feeding of marine copepods of the genera Calanus. Limnol. Oceanogr. 8, 239–250 (1963)

    Google Scholar 

  • Norris, D. R.: Possible phagotrophic feeding in Ceratium lunula Schimper. Limnol. Oceanogr. 14, 448–449 (1969)

    Google Scholar 

  • Paasche, E. and S. Kristiansen: Ammonium regeneration by microzooplankton in the Oslofjord. Mar. Biol. 69, 55–63 (1982)

    Google Scholar 

  • Rivkin, R. and H. Seliger: Liquid scintillation counting for 14C uptake of single cells isolated from natural samples. Limnol. Oceanogr. 26, 780–784 (1981)

    Google Scholar 

  • Roman, M. R. and P. A. Rublee: A method to determine in situ zooplankton grazing rates on natural particle assemblages. Mar. Biol. 65, 303–309 (1981)

    Google Scholar 

  • Runge, J. A.: Effect of hunger and season on the feeding behaviour of Calanus pacificus. Limnol. Oceanogr. 25, 134–145 (1980)

    Google Scholar 

  • Schütt, F.: Die Peridineen der Plankton-Expedition. I. Teil, Studien über die Zellen der Peridineen, Ergebn. Atlant. Ozean Planktonexped. Humboldt-Stift. 4, 1–170 (1895)

    Google Scholar 

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

    Google Scholar 

  • Spero, H. J.: Phagotrophy in Gymnodinium fungiforme (Pyrrophya): the peduncle as an organelle of ingestion. J. Phycol. 18, 356–360 (1982)

    Google Scholar 

  • Spero, H. J. and M. D. Montescue: Phagotrophic feeding and its importance to the life cycle of the holozoic dinoflagellate, Gymnodinium fungiforme. J. Phycol. 17, 43–51 (1981)

    Google Scholar 

  • Spittler, P.: Feeding experiments with tintinnids. Oikos (Suppl.) 15, 128–132 (1973)

    Google Scholar 

  • Stoecker, D., R. R. L. Guillard and R. M. Kavee: Selective predation by Favella ehrenbergii (Tintinnia) on and among dinoflagellates. Biol. Bull. mar. biol. Lab., Woods Hole 160, 136–145 (1981)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J. M. Lawrence, Tampa

Partially supported by a grant from the National Science Foundation, OCE-81-17744

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lessard, E.J., Swift, E. Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters, measured with a dual-label radioisotope technique. Mar. Biol. 87, 289–296 (1985). https://doi.org/10.1007/BF00397808

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00397808

Keywords

Navigation