Submerged Leaf Surfaces as a Microbial Habitat

  • Raymond Goulder
  • John H. Baker
Part of the Brock/Springer Series in Contemporary Bioscience book series (BROCK/SPRINGER)


The economic importance of plant pathogens in the phyllosphere of terrestrial crop plants has encouraged research on the microbial ecology of aerial leaf surfaces. The present volume and the four previous volumes (Preece and Dickinson, 1971; Dickinson and Preece, 1976; Blakeman, 1981; Fokkema and van den Heuvel, 1986) are quite narrowly restricted to the aerial phyllosphere. Information on the microbiology of submerged leaf surfaces is, in contrast, scattered in ecological, microbiological, and freshwater journals and is probably not well known to students of the aerial phyllosphere. The microbial community at submerged leaf surfaces is of ecological importance in many fresh waters. Submerged leaf surfaces are sites of primary and secondary production by microalgae and bacteria which can rival that of phytoplankton and bacterioplankton in the water column. The community serves as food for grazing invertebrates and protozoa, it contributes to biopurification of organically-polluted watercourses, and can be a substantial source of planktonic microorganisms. We, therefore, make no apology for devoting the bulk of this review to submerged, freshwater, leaf surfaces, except for our concluding comparison of the aerial and aquatic phylloplane.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Al-Hadithi, S.A. and Goulder, R. 1989a. Physiological state of epiphytic bacteria on submerged stems of the reed Phragmites australis compared with planktonic bacteria in gravel-pit ponds. Journal of Applied Bacteriology 66:107–117.Google Scholar
  2. Al-Hadithi, S.A. and Goulder, R. 1989b. A note on the physiological state of epiphytic bacteria compared with planktonic bacteria in two organically-enriched watercourses. Journal of Applied Bacteriology 67:293–297.Google Scholar
  3. Allanson, B.R. 1973. The fine structure of the periphyton of Chara sp. and Potamogeton natans from Wytham Pond, Oxford, and its significance to the macrophyte-periphyton metabolic model of R G Wetzel and H L Allen. Freshwater Biology 3:535–542.CrossRefGoogle Scholar
  4. Allen, H.L. and Ocevski, B.T. 1982. Comparative seasonal uptake of glucose and acetate by epiphytic bacteria on the surfaces of three species of macrophyte in the littoral zone of Lake Ohrid, Yugoslavia. Archiv für Hydrobiologie 93:423–445.Google Scholar
  5. Andrews, J.H., Kenerley, C.M., and Nordheim, E.V. 1980. Positional variation in phylloplane microbial populations within an apple tree canopy. Microbial Ecology 6:71–84.CrossRefGoogle Scholar
  6. Austin, B., Goodfellow, M., and Dickinson, C.H. 1978. Numerical taxonomy of phylloplane bacteria isolated from Lolium perenne. Journal of General Microbiology 104:139–155.Google Scholar
  7. Baker, J.H. 1988. Epiphytic bacteria, pp. 171–191 in Austin, B. (editor), Methods in Aquatic Microbiology. John Wiley & Sons, New York.Google Scholar
  8. Baker, J.H. and Farr, I.S. 1977. Origins, characterization and dynamics of suspended bacteria in two chalk streams. Archiv für Hydrobiologie 80:308–326.Google Scholar
  9. Baker, J.H. and Farr, I.S. 1987. Importance of dissolved organic matter produced by duckweed (Lemna minor) in a southern English river. Freshwater Biology 17:324–330.CrossRefGoogle Scholar
  10. Baker, J.H. and Orr, D.R. 1986. Distribution of epiphytic bacteria on freshwater plants. Journal of Ecology 74:155–165.CrossRefGoogle Scholar
  11. Baldock, B.M., Baker, J.H., and Sleigh, M.A. 1983. Abundance and productivity of protozoa in chalk streams. Holarctic Ecology 6:238–246.Google Scholar
  12. Beckett, P.M., Armstrong, W., Justin, S.H.F.W., and Armstrong, J. 1988. On the relative importance of convective and diffusive gas flows in plant aeration. New Phytologist 110:463–468.CrossRefGoogle Scholar
  13. Birkby, K.M. and Preece, T.F. 1987. The ligules of green leaves of cock’s-foot grass, Dactylis glomerata L., are a micro-habitat for bacteria and fungi. Journal of Applied Bacteriology 63:505–511.Google Scholar
  14. Blakeman, J.P. (editor). 1981. Microbial Ecology of the Phylloplane. Academic Press, London.Google Scholar
  15. Bownik, L.J. 1970. The periphyton of the submerged macrophytes of Mikolajskie Lake. Ekologia Polska 18:503–520.Google Scholar
  16. Burkholder, J.M. and Wetzel, R.G. 1989. Microbial colonization on natural and artificial macrophytes in a phosphorus-limited, hardwater lake. Journal of Phy-cology 25:55–65.Google Scholar
  17. Burrage, S.W. 1971. The micro-climate at the leaf surface, pp. 91–101 in Preece, T.F. and Dickinson, C.H. (editors), Ecology of Leaf Surface Micro-organisms. Academic Press, London.Google Scholar
  18. Burrage, S.W. 1976. Aerial microclimate around plant surfaces, pp. 173–184 in Dickinson, C.H. and Preece, T.F. (editors), Microbiology of Aerial Plant Surfaces. Academic press, London.Google Scholar
  19. Buscemi, P.A. 1958. Littoral oxygen depletion produced by a cover of Elodea canadensis. Oikos 9:239–245.CrossRefGoogle Scholar
  20. Carignan, R. and Kalff, J. 1982. Phosphorus release by submerged macrophytes: significance to epiphyton and phytoplankton. Limnology and Oceanography 27:419–427.CrossRefGoogle Scholar
  21. Cattaneo, A. 1978. The microdistribution of epiphytes on the leaves of natural and artificial macrophytes. British Phycological Journal 13:183–188.CrossRefGoogle Scholar
  22. Cattaneo, A. and Kalff, J. 1979. Primary production of algae growing on natural and artificial aquatic plants: a study of interactions between epiphytes and their substrate. Limnology and Oceanography 24:1031–1037.CrossRefGoogle Scholar
  23. Corpe, W.A. and Rheem, S. 1989. Ecology of methy lo trophic bacteria on living leaf surfaces. FEMS Microbiology Ecology 62:243–250.CrossRefGoogle Scholar
  24. Costerton, J.W., Cheng, K.-J., Geesey, G.G., Ladd, T.I., Nickel, J.C., Dasgupta, M., and Marrie, T.J. 1987. Bacterial biofilms in nature and disease. Annual Review of Microbiology 41:435–464.PubMedCrossRefGoogle Scholar
  25. Dale, H.M. and Gillespie, T.J. 1977. The influence of submersed aquatic plants on temperature gradients in shallow water bodies. Canadian Journal of Botany 55:2216–2225.CrossRefGoogle Scholar
  26. Dickinson, C.H. and Preece, T.F. (editors). 1976. Microbiology of Aerial Plant Surfaces. Academic Press, London.Google Scholar
  27. Dickinson, C.H., Austin, B., and Goodfellow, M. 1975. Quantitative and qualitative studies of phylloplane bacteria from Lolium perenne. Journal of General Microbiology 91:157–166.Google Scholar
  28. Edmonds, R.L. (editor). 1979. Aerobiology, The Ecological Systems Approach. Dow-den, Hutchinson & Ross, Stroudsburg, Pennsylvania.Google Scholar
  29. Eminson, D. and Moss, B. 1980. The composition and ecology of periphyton communities in freshwaters. I. The influence of host type and external environment on community composition. British Phycological Journal 15:429–446.CrossRefGoogle Scholar
  30. Fokkema, N.J. and Schippers, B. 1986. Phyllosphere versus rhizosphere as environments for saprophytic colonization, pp. 137–159 in Fokkema, N.J. and van den Heuvel, J. (editors), Microbiology of the Phyllosphere. Cambridge University Press, Cambridge, UK.Google Scholar
  31. Fokkema, N.J. and van den Heuvel, J. (editors). 1986. Microbiology of the Phyllosphere. Cambridge University Press, Cambridge, UK.Google Scholar
  32. Fontaine, T.D. and Nigh, D.G. 1983. Characteristics of epiphyte communities on natural and artificial submersed lotie plants: substrate effects. Archiv für Hydrobiologie 96:293–301.Google Scholar
  33. Fry, J.C. and Davies, A.R. 1985. An assessment of methods for measuring volumes of planktonic bacteria, with particular reference to television image analysis. Journal of Applied Bacteriology 58:105–112.Google Scholar
  34. Fry, J.C. and Humphrey, N.C.B. 1978. Techniques for the study of bacteria epiphytic on aquatic macrophytes. pp. 1–29 in Lovelock, D.W. and Davies, R. (editors), Techniques for the Study of Mixed Populations. Society for Applied Bacteriology, Technical Series No. 11. Academic Press, London.Google Scholar
  35. Fry, J.C. and Zia, T. 1982. A method for estimating viability of aquatic bacteria by slide culture. Journal of Applied Bacteriology 53:189–198.Google Scholar
  36. Fry, J.C, Goulder, R., and Rimes, C.A. 1985. A note on the efficiency of stomaching for the quantitative removal of epiphytic bacteria from submerged aquatic plants. Journal of Applied Bacteriology 58:113–115.Google Scholar
  37. Fuhrman, J.A. and Azam, F. 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Marine Biology 66:109–120.CrossRefGoogle Scholar
  38. Godfrey, B.E.S. 1976. Leachates from aerial parts of plants and their relation to plant surface microbial populations, pp. 433–439 in Dickinson, C.H. and Preece, T.F. (editors), Microbiology of Aerial Plant Surfaces. Academic Press, London.Google Scholar
  39. Goodfellow, M., Austin, B., and Dawson, D. 1976. Classification and identification of phylloplane bacteria using numerical taxonomy, pp. 275–292 in Dickinson, C.H. and Preece, T.F. (editors), Microbiology of Aerial Plant Surfaces. Academic Press, London.Google Scholar
  40. Goulder, R. 1969. Interactions between the rates of production of a freshwater macrophyte and phytoplankton in a pond. Oikos 20:300–309.CrossRefGoogle Scholar
  41. Goulder, R. 1970. Day-time variations in the rates of production by two natural communities of submerged freshwater macrophytes. Journal of Ecology 58:521–528.CrossRefGoogle Scholar
  42. Goulder, R. 1980. Seasonal variation in heterotrophic activity and population density of planktonic bacteria in a clean river. Journal of Ecology 68:349–363.CrossRefGoogle Scholar
  43. Goulder, R. 1984. Downstream increase in the abundance and heterotrophic activity of suspended bacteria in an intermittent calcareous headstream. Freshwater Biology 14:611–619.CrossRefGoogle Scholar
  44. Goulder, R. 1990. Extracellular enzyme activities associated with epiphytic microbiota on submerged stems of the reed Phragmites australis. FEMS Microbiology Ecology 73:323–330.CrossRefGoogle Scholar
  45. Grace, J. and Collins, M.A. 1976. Spore liberation from leaves by wind. pp. 185–198 in Dickinson, C.H. and Preece, T.F. (editors), Microbiology of Aerial Plant Surfaces. Academic Press, London.Google Scholar
  46. Gregory, P.H. 1971. The leaf as a spore trap. pp. 239–243 in Preece, T.F. and Dickinson, C.H. (editors), Ecology of Leaf Surface Micro-organisms. Academic Press, London.Google Scholar
  47. Gregory, P.H. 1973. The Microbiology of the Atmosphere, 2nd edition. Leonard Hill Books, Aylesbury.Google Scholar
  48. Haines, D.W., Rogers, K.H., and Rogers, F.E.J. 1987. Loose and firmly attached epiphyton: their relative contributions to algal and bacterial carbon productivity in a Phragmites marsh. Aquatic Botany 29:169–176.CrossRefGoogle Scholar
  49. Hickman, M. 1971. The standing crop and primary productivity of the epiphyton attached to Equisetum fluviatile L. in Priddy Pool, North Somerset. British Phycological Journal 6:51–59.CrossRefGoogle Scholar
  50. Hickman, M. and Klarer, D.M. 1973. Methods for measuring the primary productivity and standing crops of an epiphytic algal community attached to Scirpus validus Vahl. Internationale Revue der Gesamten Hydrobiologie 58:893–901.CrossRefGoogle Scholar
  51. Hirano, S.S. and Upper, C.D. 1986. Temporal, spatial, and genetic variability of leaf-associated bacterial populations, pp. 235–251 in Fokkema, N.J. and van den Heuvel, J. (editors), Microbiology of the Phyllosphere. Cambridge University Press, Cambridge, UK.Google Scholar
  52. Hoppe, H.-G. in press. Microbial extracellular enzyme activity: a new key parameter in aquatic ecology. In Chróst, R.J. (editor), Microbial Enzymes in Aquatic Environments. Springer-Verlag, New York.Google Scholar
  53. Hossell, J.C. and Baker, J.H. 1979a. Epiphytic bacteria of the freshwater plant Ranunculus penicillatus: enumeration, distribution and identification. Archiv für Hydrobiologie 86:322–337.Google Scholar
  54. Hossell, J.C. and Baker, J.H. 1979b. A note on the enumeration of epiphytic bacteria by microscopic methods with particular reference to two freshwater plants. Journal of Applied Bacteriology 46:87–92.Google Scholar
  55. Hough, R.A. and Wetzel, R.G. 1975. The release of dissolved organic carbon from submersed aquatic macrophytes: diel, seasonal, and community relationships. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 19:939–948.Google Scholar
  56. Jenkerson, C.G. and Hickman, M. 1986. Interrelationships among the epipelon, epiphyton and phytoplankton in a eutrophic lake. Internationale Revue der Gesamten Hydrobiologie 71:557–579.CrossRefGoogle Scholar
  57. Jensen, V. 1971. The bacterial flora of beech leaves, pp. 463–469 in Preece, T.F., and Dickinson, C.H. (editors), Ecology of Leaf Surface Micro-organisms. Academic Press, London.Google Scholar
  58. Jones, J.G. 1970. Studies on freshwater bacteria: effect of medium composition and method on estimates of bacterial population. Journal of Applied Bacteriology 33:679–686.PubMedGoogle Scholar
  59. Kinkel, L.L., Andrews, J.H., and Nordheim, E.V. 1989. Fungal immigration dynamics and community development on apple leaves. Microbial Ecology 18:45–58.CrossRefGoogle Scholar
  60. Kjelleberg, S., Hermansson, M., and Marden, P. 1987. The transient phase between growth and non-growth of heterotrophic bacteria, with emphasis on the marine environment. Annual Review of Microbiology 41:25–49.PubMedCrossRefGoogle Scholar
  61. Kudryavtsev, V.M. 1984. Bacteria on vascular aquatic plants. Hydrobiological Journal 19:50–55.Google Scholar
  62. Leben, C. 1965. Influence of humidity on the migration of bacteria on cucumber seedlings. Canadian Journal of Microbiology 11:671–676.PubMedCrossRefGoogle Scholar
  63. Lindemann, J., Constantinidou, H.A., Barchet, W.R., and Upper, C.D. 1982. Plants as sources of airborne bacteria, including ice nucleation-active bacteria. Applied and Environmental Microbiology 44:1059–1063.PubMedGoogle Scholar
  64. Lindow, S.E., Knudsen, G.R., Seidler, R.J., Walter, M.V., Lambou, V.W., Amy, P.S., Schmedding, D., Prince, V., and Hern, S. 1988. Aerial dispersal and epiphytic survival of Pseudomonas syringae during a pretest for the release of genetically engineered strains into the environment. Applied and Environmental Microbiology 54:1557–1563.PubMedGoogle Scholar
  65. Lorch, H.-J. and Ottow, J.C.G. 1985. Use of bacteria attached to submerged macrophytes and glass slides as indicators of an increasing water pollution. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 22:2297–2303.Google Scholar
  66. Lorch, H.-J. and Ottow, J.C.G. 1986. Scanning electron microscopy of bacteria and diatoms attached to a submerged macrophyte in an increasingly polluted stream. Aquatic Botany 26:377–384.CrossRefGoogle Scholar
  67. Madsen, T.V. and Warncke, E. 1983. Velocities of currents around and within submerged aquatic vegetation. Archiv für Hydrobiologie 97:389–394.Google Scholar
  68. Meulemans, J.T. 1988. Seasonal changes in biomass and production of periphyton growing upon reed in Lake Maarsseveen. Archiv für Hydrobiologie 112: 21–42.Google Scholar
  69. Monteith, J.L. and Unsworth, M.H. 1990. Principles of Environmental Physics, 2nd edition. Edward Arnold, London.Google Scholar
  70. Morin, J.O. 1986. Initial colonization of periphyton on natural and artificial apices of Myriophyllum heterophyllum Michx. Freshwater Biology 16:685–694.CrossRefGoogle Scholar
  71. Morin, J.O. and Kimball, K.D. 1983. Relationship of macrophyte-mediated changes in the water column to periphyton composition and abundance. Freshwater Biology 13:403–414.CrossRefGoogle Scholar
  72. Moss, B. 1981. The composition and ecology of periphyton communities in freshwaters. II. Inter-relationships between water chemistry, phytoplankton populations and periphyton populations in a shallow lake and associated experimental reservoirs (‘Lund tubes’). British Phycological Journal 16:59–76.CrossRefGoogle Scholar
  73. Preece, T.F. and Dickinson, C.H. (editors). 1971. Ecology of Leaf Surface Microorganisms. Academic Press, London.Google Scholar
  74. Prins, H.B.A. and Elzenga, J.T.M. 1989. Bicarbonate utilization: function and mechanism. Aquatic Botany 34:59–83.CrossRefGoogle Scholar
  75. Ramsay, A.J. 1974. The use of autoradiography to determine the proportion of bacteria metabolizing in an aquatic habitat. Journal of General Microbiology 80:363–373.Google Scholar
  76. Raskin, I. and Kende, H. 1983. How does deep water rice solve its aeration problem. Plant Physiology 72:447–454.PubMedCrossRefGoogle Scholar
  77. Raskin, I. and Kende, H. 1985. Mechanism of aeration in rice. Science 228:327–329.PubMedCrossRefGoogle Scholar
  78. Rimes, C.A. and Goulder, R. 1985. A note on the attachment rate of suspended bacteria to submerged aquatic plants in a calcareous stream. Journal of Applied Bacteriology 59:389–392.Google Scholar
  79. Rimes, C.A. and Goulder, R. 1986a. Temporal variation in density of epiphytic bacteria on submerged vegetation in a calcareous stream. Letters in Applied Microbiology 3:17–21.CrossRefGoogle Scholar
  80. Rimes, C.A. and Goulder, R. 1986b. Quantitative observations on the ability of epiphytic bacteria to contribute to the populations of suspended bacteria in two dissimilar headstreams. Freshwater Biology 16:301–311.CrossRefGoogle Scholar
  81. Rimes, C.A. and Goulder, R. 1986c. Suspended bacteria in calcareous and acid headstreams; abundance, heterotrophic activity and downstream change. Freshwater Biology 16:633–651.CrossRefGoogle Scholar
  82. Rimes, C.A. and Goulder, R. 1987. Relations between suspended bacteria, epiphytic bacteria and submerged vegetation over the spring growing season in a calcareous headstream. Freshwater Biology 17:291–305.CrossRefGoogle Scholar
  83. Rogers, K.H. and Breen, C.M. 1981. Effects of epiphyton on Potamogeton crispus L. leaves. Microbial Ecology 7:351–363.CrossRefGoogle Scholar
  84. Sand-Jensen, K. 1989. Environmental variables and their effect on photosynthesis of aquatic plant communities. Aquatic Botany 34:5–25.CrossRefGoogle Scholar
  85. Sand-Jensen, K. and Sondergaard, M. 1981. Phytoplankton and epiphyte development and their shading effect on submerged macrophytes in lakes of different nutrient status. Internationale Revue der Gesamten Hydrobiologie 66:529–552.CrossRefGoogle Scholar
  86. Sand-Jensen, K., Revsbech, N.P., and Jorgensen, B.B. 1985. Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Marine Biology 89:55–62.CrossRefGoogle Scholar
  87. Sand-Jensen, K., Jeppesen, E., Nielsen, K., Van der Bijl, L., Hjermind, L., Nielsen, L.W., and Iversen, T.M. 1989a. Growth of macrophytes and ecosystem consequences in a lowland Danish stream. Freshwater Biology 22:15–32.CrossRefGoogle Scholar
  88. Sand-Jensen, K., Borg, D., and Jeppesen, E. 1989b. Biomass and oxygen dynamics of the epiphyte community in a Danish lowland stream. Freshwater Biology 22:431–443.CrossRefGoogle Scholar
  89. Silvester, N.R. and Sleigh, M.A. 1985. The forces on microorganisms at surfaces in flowing water. Freshwater Biology 15:433–448.CrossRefGoogle Scholar
  90. Smith, C.S., Chand, T., Harris, R.F., and Andrews, J.H. 1989. Colonization of a submersed aquatic plant, Eurasian water milfoil (Myriophyllum spicatum), by fungi under controlled conditions. Applied and Environmental Microbiology 55:2326–2332.PubMedGoogle Scholar
  91. Steemann Nielsen, E. 1952. The use of radio- active carbon (C14) for measuring organic production in the sea. Journal du Conseil Permanent International pour l’Exploration de la Mer. 18:117–140.Google Scholar
  92. Stott, M.A. 1971. Studies on the physiology of some leaf saprophytes, pp. 203–210 in Preece, T.F. and Dickinson, C.H. (editors), Ecology of Leaf Surface Microorganisms. Academic Press, London.Google Scholar
  93. Tabor, P.S. and Neihof, R.A. 1982. Improved method for determination of respiring individual microorganisms in natural waters. Applied and Environmental Microbiology 43:1249–1255.PubMedGoogle Scholar
  94. Tukey, H.B. 1971. Leaching of substances from plants, pp. 67–80 in Preece, T.F. and Dickinson, C.H. (editors), Ecology of Leaf Surface Micro-organisms. Academic Press, London.Google Scholar
  95. Van Outryve, M.F., Gosselé, F., and Swings, J. 1989. The bacterial microflora of witloof chicory (Cichorium intybus L. var. foliosum Hegi) leaves. Microbial Ecology 18:175–186.CrossRefGoogle Scholar
  96. Westlake, D.F. 1964. Light extinction, standing crop and photosynthesis within weed beds. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 15:415–425.Google Scholar
  97. Westlake, D.F. 1966. The light climate for plants in rivers, pp. 99–119 in Bainbridge, R., Evans, G.C., and Rackham, O. (editors), Light as an Ecological Factor. Black-well Scientific Publications, Oxford.Google Scholar
  98. Westlake, D.F. 1967. Some effects of low-velocity currents on the metabolism of aquatic macrophytes. Journal of Experimental Botany 18:187–205.CrossRefGoogle Scholar
  99. Wetzel, R.G. 1983 Limnology, 2nd edition. W.B. Saunders Company, Philadelphia.Google Scholar
  100. Wright, R.T. and Hobbie, J.E. 1966. Use of glucose and acetate by bacteria and algae in aquatic ecosystems. Ecology 47:447–464.CrossRefGoogle Scholar
  101. Zimmermann, R., Iturriaga, R., and Becker-Birck, J. 1978. Simultaneous determination of the total number of aquatic bacteria and the number thereof involved in respiration. Applied and Environmental Microbiology 36:926–935.PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1991

Authors and Affiliations

  • Raymond Goulder
  • John H. Baker

There are no affiliations available

Personalised recommendations