Skip to main content
SpringerLink
Log in

Phagotrophic Phytoflagellates

  • Chapter
Advances in Microbial Ecology

Part of the book series: Advances in Microbial Ecology ((AMIE,volume 10))

Abstract

Phytoflagellates are known to be important contributors to aquatic primary production; however, their role as consumers has been largely overlooked by ecologists. This is despite the many incidental observations and laboratory studies of algal phagotrophy reported in the literature (Table I). Close phylogenetic relationships exist between the groups classically known as algae and protozoa (Margulis and Schwartz, 1982; Corliss, 1983). Mixotrophic phytoflagellates, which photosynthesize, ingest particulate matter, and absorb dissolved organic matter, illustrate the functional overlap of these groups. The apochlorotic microflagellates, in particular, have close taxonomic affinities with pigmented flagellates (Table II). This led us to propose that the pigmented forms in groups with unpigmented phagotrophs, such as the dinoflagellates, cryptophytes, coccolithophores, chrysophytes, euglenoids, and flagellated chlorophytes, had the potential for mixotrophy (Porter et al, 1985; Sanders et al, 1985; Porter, 1987).

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 74.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aaronson, S., 1973a, Digestion in phytoflagellates, in: Lysosomes in Biology and Pathology, Vol. 3 (J. T. Dingle, ed), pp. 18–37, North-Holland, Amsterdam.

    Google Scholar 

  • Aaronson, S., 1973b, Particle aggregation and phagotrophy by Ochromonas, Arch. Mikro- biol. 92:39–44.

    CAS  Google Scholar 

  • Aaronson, S., 1974, The biology and ultrastructure of phagotrophy in Ochromonas danica (Chrysophyceae: Chrysomonadida), J. Gen. Microbiol. 83:21–29.

    Google Scholar 

  • Aaronson, S., 1980, Descriptive biochemistry and physiology of the Chrysophyceae (with some comparisons to Prymesiophyceae), in: Biochemistry and Physiology of Protozoa, Vol. 3, 2nd ed. (M. Levandowsky and S. H. Hutner, eds.), pp. 117–169, Academic Press, New York.

    Google Scholar 

  • Aaronson, S., and Baker, H., 1959, A comparative biochemical study of two species of Och- romonas, J. ProtozooL 6:282–284.

    CAS  Google Scholar 

  • Antia, N. J., 1980, Nutritional physiology and biochemistry of marine Cryptomonads and Chrysomonads, in:Biochemistry and Physiology of Protozoa, Vol. 3, 2nd ed. (M. Lev- andowsky and S. H. Hutner, eds.), pp. 67–115, Academic Press, New York.

    Google Scholar 

  • Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., and Thingstad, F., 1983, The ecological role of water-column microbes in the sea. Mar. Ecol Prog. Ser. 10:257–263.

    Google Scholar 

  • Belcher, J. H., and Swale, E. M. F., 1971, The microanatomy of Phaeaster pasheri Scherffel (Chrysophyceae), Br. Phycol. J. 6:157–169.

    Google Scholar 

  • Biecheler, B., 1936, Des conditions et du mecanisme de la predation chez un dinoflagelle ä enveloppe tabulee, Peridinium gargantua n. sp., C. R. Seances Soc. Biol. Fil. 121:1054–1057.

    Google Scholar 

  • Biecheler, B., 1952, Recherches sur les peridiniens. Bull. Biol. Fr. Belg. 36:1–149.

    Google Scholar 

  • Bird, D. F., and Kalff, J., 1986, Bacterial grazing by planktonic lake algae,Science 231:493–495.

    Google Scholar 

  • Bird, D. F., and Kalff, J., 1987, Algal phagotrophy: Regulating factors and importance relative to photosynthesis inDinobryon (Chrysophyseae), Limnol. Oceanogr. 32:277–284.

    CAS  Google Scholar 

  • Bold, H. C., and Wynne, M. J., 1985, Introduction to the Algae, 2nd ed., Prentice-Hall, Englewood Cliffs, New Jersey

    Google Scholar 

  • Cole, G. T., and Wynne, M. J., 1974, Endocytosis of Microcystis aeruginosa by Ochromonas danica, J. Phycol. 10:397–410.

    Google Scholar 

  • Conrad, W., 1926, Recherches sur les flagellates de nos eaux saumatres. 2: Chrysomona- dines. Arch. Protistenkd. 56:167–231.

    Google Scholar 

  • Corliss, J. O., 1983, Consequences of creating new kingdoms of organisms. Bioscience 33:314–318.

    Google Scholar 

  • Coveney, M. F., 1982, Bacterial uptake of photosynthetic carbon from freshwater phyto- plankton, Oikos 38:8–20.

    CAS  Google Scholar 

  • Cynar, F. J., and Sieburth, J. McN., 1986, Unambiguous detection and improved quantification of phagotrophy in apochlorotic nanoflagellates using fluorescent microspheres and concomitant phase contrast and epifluorescent microscopy, Mar. Ecol Prog. Ser. 32:61–70.

    Google Scholar 

  • Daley, R. J., Morris, G. P., and Brown, S. R., 1973, Phagotrophic ingestion of a blue-green alga by Ochromonas, J. ProtozooL 20:58–61.

    Google Scholar 

  • Doddema, H., and van der Veer, J., 1983, Ochromonas monicis sp. nov., a particle feeder with bacterial endosymbionts, Cryptogamie Algologie 4:89–97.

    Google Scholar 

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

    Google Scholar 

  • Dubowsky, N., 1974, Selectivity of ingestion and digestion in the chrysomonad flagellate Ochromonas malhamensis, J. Protozool 21:295–298.

    PubMed  CAS  Google Scholar 

  • Estep, K. W., Davis, P. G., Keller, M. D., and Sieburth, J. McN., 1986, How important are oceanic algal nanoflagellates in bacterivory? Limnol Oceanogr. 31:646–650.

    Google Scholar 

  • Fenchel, T., 1980, Suspension feeding in ciliated protozoa: Functional response and particle size selection, Microb. Ecol 6:1–11.

    Google Scholar 

  • Fenchel, T., 1982a, Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar. Ecol Prog. Ser. 8:211–223.

    Google Scholar 

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

    Google Scholar 

  • Fenchel, T., 1982c, Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol Prog. Ser. 9:35–42.

    Google Scholar 

  • Fields, B. S., Shotts, E. B., Jr., Feeley, J. C., Gorman, G. W., and Martin, W. T., 1984, Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated pro- tozoam Tetrahymena pyriformis, Appl Environ. Microbiol 47:467–471.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Gantt, E., 1980, Photosynthetic cryptophytes, in: Phytoflagellates (E. R. Cox, ed.), pp. 381–405, Elsevier/North-Holland, New York.

    Google Scholar 

  • Gavaudan, P., 1931, Quelques remarques sur Chlorochromonas polymorpha, spec, nov., Botaniste 23:277–300.

    Google Scholar 

  • Geitler, L., 1948, Symbiosen zweischen Chrysomonaden und knospenden bakterienartigen Organismen sowie Beobachtungen über Organisationseigentümlichkeiten der Chrysomonaden, Öst. Bot. Z. 95:300–324.

    Google Scholar 

  • Güde, H., 1986, Loss processes influencing growth of planktonic bacterial populations in Lake Constance, J. Plank Res. 8:795–810.

    Google Scholar 

  • Harris, T. M., 1940, A contribution to the knowledge of the British freshwater Dinoflagel- lata, Proc. Linn. Soc. 152:4–33.

    Google Scholar 

  • Hibberd, D. J., 1970, Observations on the cytology and ultrastructure of Ochromonas tub- erculatus sp. nov. (Chrysophyceae), with special reference to the discobolocysts, Br. Phycol. J. 5:119–143.

    Google Scholar 

  • Hibberd, D. J., 1971, Observations on the cytology and ultrastructure of Chrysamoeba radians Klebs (Chrysophyceae), Br. Phycol. J. 6:207–223.

    Google Scholar 

  • Hofeneder, H., 1930, Ãœber die animalische Ernährung von Ceratium hirundinella O.F. Muller und über die Rolle des kernes bei dieser Zellfunktion, Arch. Protistenkd. 71:1–32.

    Google Scholar 

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

    CAS  Google Scholar 

  • Hutner, S. H., and Provasoli, L., 1951, The phytoflagellates, in: Biochemistry and Physiology of Protozoa, Vol. 1 (A. Lwofl, ed.), pp. 27–128, Academic Press, New York.

    Google Scholar 

  • Hutner, S. H., Provasoli, L., and Filfus, J., 1953. Nutrition of some phagotrophic freshwater chrysomonads, Ann, N. Y. Acad Sei. 56:852–862.

    CAS  Google Scholar 

  • Kimura, B., and Ishida, Y., 1985, Photophagotrophy in Uroglena americana, Chrysophyceae, Jpn. J. Limnol. 46:315–318.

    Google Scholar 

  • Klaveness, D., 1982, TheCryptomonas-Caulobacterconsorimm: Facultative ectocommen- salism with possible taxonomic consequences?, Nord. J. Bot. 2:183–188.

    Google Scholar 

  • Kochert, G., and Olson, L. W., 1970, Endosymbiotic bacteria in Volvox carteri, Trans. Am. Microscop. Soc. 89:475–478.

    Google Scholar 

  • Kofoid, C. A., and Swezy, O., 1921, The free-living unarmored dinoflagellata, Mem. Univ. Calif. 5:1–562.

    Google Scholar 

  • Korshikov, A. A., 1928, Studies on the chrysomonads. L Arch. Protistenkd. 67:253–290.

    Google Scholar 

  • Kuhl, A., 1974, Phosphorus, in:Algal Physiology and Biochemistry (W. D. P. Stewart, ed.), pp. 636–654, University of California Press, Berkeley.

    Google Scholar 

  • Larsson, U., and Hagström, A., 1979, Phytoplankton exudate release as an energy source for the growth of pelagic bacteria, Mar. Biol. 52:199–206.

    Google Scholar 

  • Lauterborn, V. R., 1906, Eine neue Chrysomonadinen-Gattung(Palatinella cyrptophora nov. gen. nov. spec.), Zool. Anz, 30:423–428.

    Google Scholar 

  • Laval-Peuto, M., and Febvre, M., 1986, On plastid symbiosis in Tontonia appendiculari- formis (Cilophora, Oligotrichina), BioSystems 19:137–158.

    PubMed  CAS  Google Scholar 

  • Lee, R. E., 1980, Phycology, Cambridge University Press, Cambridge.

    Google Scholar 

  • Leedale, G. F., 1967, Euglenoid Flagellates, Prentice-Hall, Englewood Cliffs, New Jersey.

    Google Scholar 

  • Leedale, G. F., 1969, Observations on endonuclear bacteria in euglenid flagellates, Ost. Bot. Z. 116:279–294.

    Google Scholar 

  • Leedale, G. F., and Hibberd, D. J., 1985, Class 1. Phytomastigophorea Calkins, 1909, in: Illustrated Guide to the Protozoa (J. J. Lee, S. H. Hutner, and E. C. Bovee, eds.), pp. 18–105, Society of Protozoologists, Lawrence, Kansas.

    Google Scholar 

  • Lessard, E. J., and Swift, E., 1985, Species-specific grazing rates of heterotrophic dinoflag- ellates in oceanic waters, measured with a dual-label radioisotope technique. Mar. Biol. 87:289–296.

    Google Scholar 

  • Loeblich, A. R., III, 1967, Aspects of the physiology and biochemistry of Pyrrhophyta,Phyte 5:216–235.

    Google Scholar 

  • MacKinnon, D. L., and Hawes, R. S. J., 1961, Introduction to the Study of Protozoa, Oxford University Press, Oxford.

    Google Scholar 

  • Manton, L, 1972, Observations on the biology and micro-anatomy of Chrysochromulina megacylindra Leadbeater, Br. Phycol. J. 7:235–248.

    Google Scholar 

  • Margulis, L., 1981, Symbiosis in Cell Evolution, Freeman, San Francisco.

    Google Scholar 

  • Margulis, L., and Schwartz, K. V., 1982, Five Kingdoms, Freeman, San Francisco.

    Google Scholar 

  • McManus, G. B., and Fuhrman, J. A., 1986, Photosynthetic pigments in the ciliate Laboea strobila from Long Island Sound, USA, J. Plank. Res. 8:317–327.

    Google Scholar 

  • Meyer, D. H., and S. Aaronson, 1973, Evidence for the secretion by Ochromonas danica of an acid hydrolase into its environment, J. Phycol. 9(Suppl.):20.

    Google Scholar 

  • Müeller, M., Röhlich, P., and Törö, I., 1965, Studies on the feeding and digestion of protozoa. VII. Ingestion of polystyrene latex particles and its early effect on acid phosphatase in Paramecium multinucleatum and Tetrahymena pyriformis, J. Protozool. 12:27–34.

    Google Scholar 

  • Myers, J., and Graham, J., 1956, The role of photosynthesis in the physiology of Ochromonas, J. Cell. Comp. Physiol. 47:397–414.

    CAS  Google Scholar 

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

    Google Scholar 

  • Parke, M., and Adams, I., 1960, The motile Crystallolithus hyalinus Gaardner and Markali) and the non-motile phases in the life history of Coccolithus pelagicus (Wallich) Schiller, J. Mar. Biol. Assoc. U. K. 39:263–274.

    Google Scholar 

  • Parke, M., Manton, I., and Clarke, B., 1955, Studies on marine flagellates. II. Three new species of Chrysochromulina, J. Mar. Biol. Assoc. 34:579–609.

    Google Scholar 

  • Parke, M., Manton, I., and Clarke, B., 1956, Studies on marine flagellates. III. Three further species of Chrysochromulina, J. Mar. Biol. Assoc. 35:387–414.

    Google Scholar 

  • Parke, M., Manton, L, and Clarke, B., 1958, Studies on marine flagellates. IV. Morphology and microanatomy of a new species ofChrysochromulina, J. Mar. Biol. Assoc. 37:209–228.

    Google Scholar 

  • Parke, M., Manton, I., and Clarke, B., 1959, Studies on marine flagellates. V. Morphology and microanatomy of Chrysochromulina strobilus sp. nov., J. Mar. Biol. Assoc. 38:169–188.

    Google Scholar 

  • Pascher, A., 1911, Cyrtophora, eine neue tentakeltragende Chrysomonade aus Franzensbad und ihre Verwandten, Ber. Deutsch. Bot. Ges. 29:112–125.

    Google Scholar 

  • Pascher, A., 1943, Zur Kenntnis verschiedener Ausbildungen der planktontischen Dinob- ryen, Int. Rev. Gesamten. Hydrobiol. 43:110–123.

    Google Scholar 

  • Pienaar, R. N., and Norris, R. E. 1979, The ultrastructure of the flagellate Chrysochromulina spinifera (Fournier) comb. nov. (Prymnesiophyceae) with special reference to scale production, Phycologia 18:99–108.

    Google Scholar 

  • Pitelka, D. R., 1963, Electron-Microscopic Structure of Protozoa, Pergamon Press, Oxford.

    Google Scholar 

  • Pomeroy, L. R., 1974, The ocean’s food web, a changing paradigm, Bioscience 24:499–504.

    Google Scholar 

  • Porter, K. G., 1973, Selective grazing and differential digestion of algae by Zooplankton, Nature, 244:179–180.

    Google Scholar 

  • Porter, K. G., 1987, Phagotrophic phytoflagellates in microbial food webs,Hydrobiologia, in press. (Special volume, The Role of Microorganisms in Aquatic Food Webs [T. Herman, ed.])

    Google Scholar 

  • Porter, K. G., Sherr, E. B., Sherr, B. E, Pace, M., and Sanders, R. W., 1985, Protozoa in planktonic food webs, J. ProtozooL 32:409–415.

    Google Scholar 

  • Pratt, J. R. and Caims, J., Jr., 1985, Functional groups in the protozoa: Roles in differing ecosystems, J. ProtozooL 32:415–423.

    Google Scholar 

  • Pringsheim, E. G., 1952, On the nutrition of Ochromonas, Q. J. Microscop. Sei. 93:71–96.

    Google Scholar 

  • Pringsheim, E. G., 1963, Farblose Algen, G. Fischer, Jena.

    Google Scholar 

  • Provasoli, L., 1958, Nutrition and ecology of protozoa and algae, Annu. Rev. Microbiol. 12:279–308.

    PubMed  CAS  Google Scholar 

  • Rapport, D. J., Berger, J., and Reid, D. W. B., 1972, Determination of food preference of Stentor coeruleus, Biol. Bull. 142:103–109.

    Google Scholar 

  • Ricketts, T. R., 1971, Endocytosis in Tetrahymena pyriformis, Exp. Cell. Res. 66:49–58.

    PubMed  CAS  Google Scholar 

  • Sanders, R. W., and Porter, K. G., 1986, Use of metabolic inhibitors to estimate protozoo- plankton grazing and bacterial production in a monomictic lake with an anaerobic hypolimnion, Appl. Environ. Microbiol, 52:101–107.

    PubMed  CAS  Google Scholar 

  • Sanders, R. W., Porter, K. G., and McDonough, R. J., 1985, Bacterivory by ciliates, micro- flagellates and mixotrophic algae: Factors influencing particle ingestion, Eos 66:1314.

    Google Scholar 

  • Schiller, J., 1952, Neue Mikrophyton aus dem Neusiedler See und benachbarter gebiete, Öst. Bot. Z. 99:100–117.

    Google Scholar 

  • Schuster, F. L., Hershenov, B., and Aaronson, S., 1968, Ultrastructural observations on aging of stationary cultures and feeding in Ochromonas, J. ProtozooL 15:335–346.

    CAS  Google Scholar 

  • Sherr, B. F., Sherr, E. B., and Berman, T., 1983, Grazing, growth, and ammonium excretion rates of a heterotrophic microflagellate fed with four species of bacteria, Appl Environ. Microbiol 45:1196–1201.

    Google Scholar 

  • Sieburth, J. McN., and Davis, P. G., 1982, The role of heterotrophic nanoplankton in the grazing and nuturing of planktonic bacteria in the Sargasso and Caribbean Sea, Ann. Inst. Oceanogr. 58 (Suppl.):285–296.

    Google Scholar 

  • Skuja, H., 1948, Taxonomie des Phytoplanktons einiger Seen in Uppland, Schweden, Symb. Bot. UpsaL 9:1–399.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Stoltze, H. J., Lui, N. S. T., Anderson, O. R., and Roels, O. A., 1969, The influence of the mode of nutrition on the digestive system of Ochromonas malhamensis, J. Cell BioL 43:90–104.

    Google Scholar 

  • Swale, E. M. F., 1969, A study of the nannoplankton flagellate Pedinella hexacostata Vysot- skii by light and electron microscopy, Br. Phycol J. 4:65–86.

    Google Scholar 

  • Taylor, F. J. R., 1982, Symbioses in marine microplankton, Ann. Inst. Oceanogr. Paris 58(S):61–90.

    Google Scholar 

  • Taylor, G. T., Iturriaga, R., and Sullivan, C. W., 1985, Interactions of bactivorous grazers and heterotrophic bacteria with dissolved organic matter. Mar. Ecol Prog. Ser. 23:129–141.

    Google Scholar 

  • Tsekos, I., 1973, Licht- und electronenmikroskopische Untersuchunger über die Stoffaufnahme durch Poterioochromonas stipulata, Protoplasma 77:397–409.

    CAS  Google Scholar 

  • Uhlig, G., and SahUng, G., 1985, Blooming and red tide phenomenon in Noctiluca scintil- lans, Bull Mar. Sci 37:780.

    Google Scholar 

  • Vysotskiii, A. V., 1888 (1887), Mastigophora i Rhizopoda, naigenyya v ’Veisovom’ i, R(e)pnom ’ozerakh’, Tr. Obshch. Ispyt. Prir. Imp. Khar’kov. Univ. 21:119–140.

    Google Scholar 

  • Wawrik, E, 1970, Mixotrophie bei Cryptomonas borealisSkn)2L, Arch. Protistenkd. 112:312–313.

    Google Scholar 

  • Wright, R. T., and Coffin, R. B., 1984, Measuring microzooplankton grazing by its impact on bacterial production, Microb. Ecol. 10:137–150.

    Google Scholar 

  • Wujek, D. E., 1969, Ultrastructure of flagellated chrysophytes. L Dinobryon, Cytologia 34:71–79.

    Google Scholar 

  • Wujek, D. W., 1976, Ultrastructure of flagellated chrysophytes. II. Uroglena and Uroglen- opsis, Cytologia 41:665–670.

    Google Scholar 

  • Wujek, D. E., 1978, Ultrastructure of flagellated chrysophytes. III. Mallomonas caudata, Trans. Kans. Acad Sei. 81:327–335.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Georgia, Athens, Georgia, 30602, USA

    Robert W. Sanders & Karen G. Porter

Authors
  1. Robert W. Sanders
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen G. Porter
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. University of New South Wales, Kensington, New South Wales, Australia

    K. C. Marshall

Rights and permissions

Reprints and permissions

Copyright information

© 1988 Plenum Press, New York

About this chapter

Cite this chapter

Sanders, R.W., Porter, K.G. (1988). Phagotrophic Phytoflagellates. In: Marshall, K.C. (eds) Advances in Microbial Ecology. Advances in Microbial Ecology, vol 10. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5409-3_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-5409-3_5

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-5411-6

  • Online ISBN: 978-1-4684-5409-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation