Phagotrophic Phytoflagellates

  • Robert W. Sanders
  • Karen G. Porter
Part of the Advances in Microbial Ecology book series (AMIE, volume 10)


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).


Clearance Rate Grazing Rate Food Vacuole Fluorescent Microsphere Ceratium Hirundinella 
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  1. 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
  2. Aaronson, S., 1973b, Particle aggregation and phagotrophy by Ochromonas, Arch. Mikro- biol. 92:39–44.Google Scholar
  3. Aaronson, S., 1974, The biology and ultrastructure of phagotrophy in Ochromonas danica (Chrysophyceae: Chrysomonadida), J. Gen. Microbiol. 83:21–29.Google Scholar
  4. 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
  5. Aaronson, S., and Baker, H., 1959, A comparative biochemical study of two species of Och- romonas, J. ProtozooL 6:282–284.Google Scholar
  6. 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
  7. 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
  8. Belcher, J. H., and Swale, E. M. F., 1971, The microanatomy of Phaeaster pasheri Scherffel (Chrysophyceae), Br. Phycol. J. 6:157–169.Google Scholar
  9. 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
  10. Biecheler, B., 1952, Recherches sur les peridiniens. Bull. Biol. Fr. Belg. 36:1–149.Google Scholar
  11. Bird, D. F., and Kalff, J., 1986, Bacterial grazing by planktonic lake algae,Science 231:493–495.Google Scholar
  12. Bird, D. F., and Kalff, J., 1987, Algal phagotrophy: Regulating factors and importance relative to photosynthesis inDinobryon (Chrysophyseae), Limnol. Oceanogr. 32:277–284.Google Scholar
  13. Bold, H. C., and Wynne, M. J., 1985, Introduction to the Algae, 2nd ed., Prentice-Hall, Englewood Cliffs, New JerseyGoogle Scholar
  14. Cole, G. T., and Wynne, M. J., 1974, Endocytosis of Microcystis aeruginosa by Ochromonas danica, J. Phycol. 10:397–410.Google Scholar
  15. Conrad, W., 1926, Recherches sur les flagellates de nos eaux saumatres. 2: Chrysomona- dines. Arch. Protistenkd. 56:167–231.Google Scholar
  16. Corliss, J. O., 1983, Consequences of creating new kingdoms of organisms. Bioscience 33:314–318.Google Scholar
  17. Coveney, M. F., 1982, Bacterial uptake of photosynthetic carbon from freshwater phyto- plankton, Oikos 38:8–20.Google Scholar
  18. 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
  19. 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
  20. 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
  21. Dodge, J. D., and Crawford, R. M., 1970, The morphology and fine structure of Ceratium hirundinella (Dinophyceae), J. Phycol 6:137–149.Google Scholar
  22. Dubowsky, N., 1974, Selectivity of ingestion and digestion in the chrysomonad flagellate Ochromonas malhamensis, J. Protozool 21:295–298.PubMedGoogle Scholar
  23. 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
  24. Fenchel, T., 1980, Suspension feeding in ciliated protozoa: Functional response and particle size selection, Microb. Ecol 6:1–11.Google Scholar
  25. Fenchel, T., 1982a, Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar. Ecol Prog. Ser. 8:211–223.Google Scholar
  26. Fenchel, T., 1982b, Ecology of heterotrophic microflagellates. IL Bioenergetics and growth. Mar. Ecol Prog Ser. 8:225–231.Google Scholar
  27. Fenchel, T., 1982c, Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol Prog. Ser. 9:35–42.Google Scholar
  28. 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.PubMedGoogle Scholar
  29. Gaines, G., and Taylor, F. J. R., 1984, Extracellular digestion in marine dinoflagellates, J. Plank. Res. 6:1057–1061.Google Scholar
  30. Gantt, E., 1980, Photosynthetic cryptophytes, in: Phytoflagellates (E. R. Cox, ed.), pp. 381–405, Elsevier/North-Holland, New York.Google Scholar
  31. Gavaudan, P., 1931, Quelques remarques sur Chlorochromonas polymorpha, spec, nov., Botaniste 23:277–300.Google Scholar
  32. Geitler, L., 1948, Symbiosen zweischen Chrysomonaden und knospenden bakterienartigen Organismen sowie Beobachtungen über Organisationseigentümlichkeiten der Chrysomonaden, Öst. Bot. Z. 95:300–324.Google Scholar
  33. Güde, H., 1986, Loss processes influencing growth of planktonic bacterial populations in Lake Constance, J. Plank Res. 8:795–810.Google Scholar
  34. Harris, T. M., 1940, A contribution to the knowledge of the British freshwater Dinoflagel- lata, Proc. Linn. Soc. 152:4–33.Google Scholar
  35. 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
  36. Hibberd, D. J., 1971, Observations on the cytology and ultrastructure of Chrysamoeba radians Klebs (Chrysophyceae), Br. Phycol. J. 6:207–223.Google Scholar
  37. Hofeneder, H., 1930, Über 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
  38. 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.Google Scholar
  39. 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
  40. Hutner, S. H., Provasoli, L., and Filfus, J., 1953. Nutrition of some phagotrophic freshwater chrysomonads, Ann, N. Y. Acad Sei. 56:852–862.Google Scholar
  41. Kimura, B., and Ishida, Y., 1985, Photophagotrophy in Uroglena americana, Chrysophyceae, Jpn. J. Limnol. 46:315–318.Google Scholar
  42. Klaveness, D., 1982, TheCryptomonas-Caulobacterconsorimm: Facultative ectocommen- salism with possible taxonomic consequences?, Nord. J. Bot. 2:183–188.Google Scholar
  43. Kochert, G., and Olson, L. W., 1970, Endosymbiotic bacteria in Volvox carteri, Trans. Am. Microscop. Soc. 89:475–478.Google Scholar
  44. Kofoid, C. A., and Swezy, O., 1921, The free-living unarmored dinoflagellata, Mem. Univ. Calif. 5:1–562.Google Scholar
  45. Korshikov, A. A., 1928, Studies on the chrysomonads. L Arch. Protistenkd. 67:253–290.Google Scholar
  46. Kuhl, A., 1974, Phosphorus, in:Algal Physiology and Biochemistry (W. D. P. Stewart, ed.), pp. 636–654, University of California Press, Berkeley.Google Scholar
  47. 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
  48. Lauterborn, V. R., 1906, Eine neue Chrysomonadinen-Gattung(Palatinella cyrptophora nov. gen. nov. spec.), Zool. Anz, 30:423–428.Google Scholar
  49. Laval-Peuto, M., and Febvre, M., 1986, On plastid symbiosis in Tontonia appendiculari- formis (Cilophora, Oligotrichina), BioSystems 19:137–158.PubMedGoogle Scholar
  50. Lee, R. E., 1980, Phycology, Cambridge University Press, Cambridge.Google Scholar
  51. Leedale, G. F., 1967, Euglenoid Flagellates, Prentice-Hall, Englewood Cliffs, New Jersey.Google Scholar
  52. Leedale, G. F., 1969, Observations on endonuclear bacteria in euglenid flagellates, Ost. Bot. Z. 116:279–294.Google Scholar
  53. 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
  54. 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
  55. Loeblich, A. R., III, 1967, Aspects of the physiology and biochemistry of Pyrrhophyta,Phyte 5:216–235.Google Scholar
  56. MacKinnon, D. L., and Hawes, R. S. J., 1961, Introduction to the Study of Protozoa, Oxford University Press, Oxford.Google Scholar
  57. Manton, L, 1972, Observations on the biology and micro-anatomy of Chrysochromulina megacylindra Leadbeater, Br. Phycol. J. 7:235–248.Google Scholar
  58. Margulis, L., 1981, Symbiosis in Cell Evolution, Freeman, San Francisco.Google Scholar
  59. Margulis, L., and Schwartz, K. V., 1982, Five Kingdoms, Freeman, San Francisco.Google Scholar
  60. 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
  61. 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
  62. 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
  63. Myers, J., and Graham, J., 1956, The role of photosynthesis in the physiology of Ochromonas, J. Cell. Comp. Physiol. 47:397–414.Google Scholar
  64. Norris, D. R., 1969, Possible phagotrophic feeding in Ceratium lunula Schimper, Limnol. Oceanogr. 14:448–449.Google Scholar
  65. 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
  66. 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
  67. 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
  68. 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
  69. 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
  70. Pascher, A., 1911, Cyrtophora, eine neue tentakeltragende Chrysomonade aus Franzensbad und ihre Verwandten, Ber. Deutsch. Bot. Ges. 29:112–125.Google Scholar
  71. Pascher, A., 1943, Zur Kenntnis verschiedener Ausbildungen der planktontischen Dinob- ryen, Int. Rev. Gesamten. Hydrobiol. 43:110–123.Google Scholar
  72. 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
  73. Pitelka, D. R., 1963, Electron-Microscopic Structure of Protozoa, Pergamon Press, Oxford.Google Scholar
  74. Pomeroy, L. R., 1974, The ocean’s food web, a changing paradigm, Bioscience 24:499–504.Google Scholar
  75. Porter, K. G., 1973, Selective grazing and differential digestion of algae by Zooplankton, Nature, 244:179–180.Google Scholar
  76. 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
  77. 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
  78. Pratt, J. R. and Caims, J., Jr., 1985, Functional groups in the protozoa: Roles in differing ecosystems, J. ProtozooL 32:415–423.Google Scholar
  79. Pringsheim, E. G., 1952, On the nutrition of Ochromonas, Q. J. Microscop. Sei. 93:71–96.Google Scholar
  80. Pringsheim, E. G., 1963, Farblose Algen, G. Fischer, Jena.Google Scholar
  81. Provasoli, L., 1958, Nutrition and ecology of protozoa and algae, Annu. Rev. Microbiol. 12:279–308.PubMedGoogle Scholar
  82. 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
  83. Ricketts, T. R., 1971, Endocytosis in Tetrahymena pyriformis, Exp. Cell. Res. 66:49–58.PubMedGoogle Scholar
  84. 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.PubMedGoogle Scholar
  85. 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
  86. Schiller, J., 1952, Neue Mikrophyton aus dem Neusiedler See und benachbarter gebiete, Öst. Bot. Z. 99:100–117.Google Scholar
  87. 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.Google Scholar
  88. 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
  89. 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
  90. Skuja, H., 1948, Taxonomie des Phytoplanktons einiger Seen in Uppland, Schweden, Symb. Bot. UpsaL 9:1–399.Google Scholar
  91. 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
  92. 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
  93. 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
  94. 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
  95. Taylor, F. J. R., 1982, Symbioses in marine microplankton, Ann. Inst. Oceanogr. Paris 58(S):61–90.Google Scholar
  96. 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
  97. Tsekos, I., 1973, Licht- und electronenmikroskopische Untersuchunger über die Stoffaufnahme durch Poterioochromonas stipulata, Protoplasma 77:397–409.Google Scholar
  98. Uhlig, G., and SahUng, G., 1985, Blooming and red tide phenomenon in Noctiluca scintil- lans, Bull Mar. Sci 37:780.Google Scholar
  99. 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
  100. Wawrik, E, 1970, Mixotrophie bei Cryptomonas borealisSkn)2L, Arch. Protistenkd. 112:312–313.Google Scholar
  101. Wright, R. T., and Coffin, R. B., 1984, Measuring microzooplankton grazing by its impact on bacterial production, Microb. Ecol. 10:137–150.Google Scholar
  102. Wujek, D. E., 1969, Ultrastructure of flagellated chrysophytes. L Dinobryon, Cytologia 34:71–79.Google Scholar
  103. Wujek, D. W., 1976, Ultrastructure of flagellated chrysophytes. II. Uroglena and Uroglen- opsis, Cytologia 41:665–670.Google Scholar
  104. Wujek, D. E., 1978, Ultrastructure of flagellated chrysophytes. III. Mallomonas caudata, Trans. Kans. Acad Sei. 81:327–335.Google Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Robert W. Sanders
    • 1
  • Karen G. Porter
    • 1
  1. 1.Department of ZoologyUniversity of GeorgiaAthensUSA

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