Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-25T07:15:09.937Z Has data issue: false hasContentIssue false
  • English
  • Français

Mycorrhizas and nutrient cycling in sand dune ecosystems

Published online by Cambridge University Press:  05 December 2011

D. J. Read
D. J. Read
Affiliation:
Department of Animal and Plant Sciences, The University of Sheffield, Sheffield S10 2TN, U.K.
Get access

Synopsis

The extent of occurrence, the form and the function of mycorrhizal infection are shown to change with successional development across coastal sand dune systems. The interrelationships between these changes and the prevailing physico-chemical conditions are explored and clear patterns are recognised in terms of both type and function of the infection. The periodically disturbed and nutritionally enriched high tide line is colonised by non-mycorrhizal ruderal species. There follows a sequence of plant communities, each characterised by the presence of a dominant mycorrhizal type and a distinctive nutritional limitation. In the foredunes, pioneer grasses are normally infected with vesicular-arbuscular (VA) mycorrhizal fungi. Plants such as Ammophila, Leymus and Uniola, all of which have extensive root systems, appear, when fully grown, to be only facultatively mycorrhizal. However, experimental evidence suggests that infection is important for the early growth of such plants and it is suggested that in these, as in many other dune species, mycorrhizas may be essential at critical stages in the life cycle, most notably during the phase of seedling establishment. Here, phosphorus (P) is the most important growth-limiting nutrient. The extensive mycelial network of VA hyphae not only facilitates capture of this element but also provides the aggregation of sand grains necessary for dune stabilisation. In semi-fixed dune pastures, as sand inputs are reduced, productivities are low and species diversity increased. Phosphate limitation persists and the majority of the characteristic species show VA infection. Experimental studies using microcosms of dune sand containing an assemblage of species typical of such communities suggest that the maintenance of the species richness is dependent upon mycorrhizal fungi which produce a large absorptive mycelial network into which the roots of germinating seedlings become incorporated as they are infected. Accumulation of organic matter in dune-slacks leads to reduction of pH. Nitrification is inhibited, ammonium becomes the major mineral nitrogen (N) source and N replaces P as the key growth-limiting element. Here plants with ecto-mycorrhizal infection predominate. Salix repens produces a shrub layer enriched with litter in which a guild of species interconnected by a common mycorrhizal mycelium occurs. The functional basis of this guild structure is explored, the ability of some of its mycorrhizal fungi to mobilise nutrients from organic macro-molecules being seen as a vital attribute. Where organic matter accumulation and base depletion are most strongly developed in the oldest parts of the succession, plants with ericoid mycorrhizas become important. The ability of their mycorrhizal fungi to liberate N and P from acidic organic complexes, as well as to assimilate or exclude, and hence detoxify, organic acids and metal ions facilitates vigorous growth of ericaceous species in soil conditions which are inimical to plants important earlier in the succession. Since the attributes of each mycorrhizal type are relevant to a specific suite of edaphic properties the formation of appropriate symbiotic associations is likely to be a prerequisite for successional change. It is concluded that mutualism contributes significantly to fitness in the sand dune ecosystems, the further understanding of which will be dependent upon more effective collaboration between the microbiological and ecological disciplines.

Type
Research Article
Information
Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences , Volume 96: Coastal Sand Dunes , 1989 , pp. 89 - 110
Copyright
Copyright © Royal Society of Edinburgh 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, L. K. & Robson, A. D. 1985. Formation of external hyphae in soil by four species of vesiculararbuscular mycorrhizal fungi. New Phytologist 99, 245–255.CrossRefGoogle Scholar
Abuzinadah, R. A. & Read, D. J. 1986a. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. I. Utilization of peptides and proteins by ectomycorrhizal fungi. New Phytologist 103, 481–493.CrossRefGoogle Scholar
Abuzinadah, R. A. & Read, D. J. 1986b. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. III. Protein utilization by Betula, Picea and Pinus in mycorrhizal association with Hebeloma crustuliniforme. New Phytologist 103, 507–514.CrossRefGoogle Scholar
Abuzinadah, R. A. & Read, D. J. 1989a. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. IV. The utilisation of peptides by birch (Betula pendula) infected with different mycorrhizal fungi. New Phytologist 112, 55–60.Google Scholar
Abuzinadah, R. A. & Read, D. J. 1989b. Carbon transfer associated with assimilation of organic nitrogen sources by silver birch (Betula pendula Roth.). Trees 3, 17–23.Google Scholar
Alexander, I. J. 1983. The significance of ectomycorrhizas in the nitrogen cycle. In Nitrogen as an Ecological Factor, eds. Lee, J. A., McNeill, S. & Rorison, I. H., pp. 69–93. Oxford: Blackwell Scientific.Google Scholar
Allen, E. B. & Allen, M. F. 1988. Facilitation of succession by the non-mycotrophic colonizer Salsola kali (Chenopodiaceae) on a harsh site: effects of mycorrhizal fungi. American Journal of Botany 75, 257–266.CrossRefGoogle Scholar
Allen, M. F. 1982. Influence of vesicular-arbuscular mycorrhizae on water movement through Bouteloua gracilis. New Phytologist 91, 191–196.Google Scholar
Allen, M. F. & Boosalis, M. G. 1983. Effects of two species of VA mycorrhizal fungi on drought tolerance of winter wheat. New Phytologist 93, 66–76.CrossRefGoogle Scholar
Allen, M. F., Allen, E. B. & Friese, C. F. 1989. Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular-arbuscular mycorrhizal fungi. New Phytologist 111, 45–49.CrossRefGoogle Scholar
Allen, M. F., Sexton, J.C., Moore, T.S. & Christensen, M. 1981. Comparative water relations and photosynthesis of mycorrhizal and non-mycorrhizal Bouteloua gracilis. New Phytologist 88, 683–693.CrossRefGoogle Scholar
Asai, T. 1934. Uber das Vorkommen und die Bedeutung der Wurzel-pilze in den Landpflanzen. Japanese Journal of Botany 7, 107–150.Google Scholar
Baylis, G. T. S. 1975. The magnolioid mycorrhiza and mycotrophy in root systems derived from it. In Endomycorrhizas, eds Sanders, F. E., Mosse, B. & Tinker, P. B., pp. 373–389. London: Academic Press.Google Scholar
Birch, C. P. D. 1986. Development of VA mycorrhizal infection in seedlings in semi-natural grassland turf. In Physiological and Genetical Aspects of Mycorrhizae, eds Gianinazzi-Pearson, V. & Gianinazzi, S., pp. 233–239. Paris: INRA.Google Scholar
Björkman, E. 1960. Monotropa hypopitys L. – an epiparasite on tree roots. Physiologia Plantarum 13, 308–329.CrossRefGoogle Scholar
Boullard, B. 1958. Les mycorrhizes des especes de contact marin et de contact salin. Revue de Mycologie 23, 282–317.Google Scholar
Bradley, R., Burt, A. J. & Read, D. J. 1981. Mycorrhizal infection and resistance to heavy metal toxicity in Calluna vulgaris. Nature, London 292, 335–337.CrossRefGoogle Scholar
Bradley, R., Burt, A. J. & Read, D. J. 1982. The biology of mycorrhiza in the Ericaceae. VIII. The role of mycorrhizal infection in heavy metal resistance. New Phytologist 91, 197–209.CrossRefGoogle Scholar
Brown, J. C. 1958. Soil fungi of some British sand dunes in relation to soil types and succession. Journal of Ecology 46, 641–664.Google Scholar
Castellano, M. A. & Trappe, J. M. 1985. Mycorrhizal associations of five species of Monotropoideae in Oregon. Mycologia 77, 499–502.CrossRefGoogle Scholar
Cowles, H. C. 1899. The ecological relations of the vegetation on the sand dunes of Lake Michigan. Botanical Gazette 27, 95–117.Google Scholar
Daft, M. J. & Nicolson, T. H. 1966. Effect of Endogone mycorrhiza on plant growth. New Phytologist 65, 343–350.CrossRefGoogle Scholar
Dominik, T. 1951. Badanie mykotrofizmo roslinnosci wydm nadmorskich i srodladowych. Acta Sociatas Botanischen Gesellshaft 21, 125–164.Google Scholar
Duddridge, J. A. & Read, D. J. 1982. An ultrastructural analysis of the development of mycorrhizas in Monotropa hypopitys. New Phytologist 92, 203–214.Google Scholar
Ellenburg, H. 1988. Vegetation Ecology of Central Europe. Cambridge: Cambridge Universtiy Press.Google Scholar
Ernst, W. H. O., van Duin, W. E. & Oolbecking, G. T. 1984. Vesicular arbuscular myckorrhiza in dune vegetation. Acta Botanica Neerlandica 33, 151–160.CrossRefGoogle Scholar
Forster, S. M. 1979. Microbial aggregation of sand in an embryo dune system. Soil Biology and Biochemistry 11, 537–543.Google Scholar
Forster, S. M. & Nicolson, T. H. 1981. Microbial aggregation of sand in a maritime dune succession. Soil Biology and Biochemistry 13, 205–208.CrossRefGoogle Scholar
Francis, R. & Read, D. J. 1984. Direct transfer of carbon between plants connected by vesiculararbuscular mycorrhizal mycelium. Nature 30, 53–56.Google Scholar
Frank, A. B. 1885. Ueber die auf Wurzelsymbiose beruhende Ernahrung gewisser Baume durch Unterirdische Pilze. Bericht der Deutschen Botanischen Gesellschaft 3, 128–145.Google Scholar
Frank, A. B. 1948. Die Bedeutung der Mykorrhiza-pilze fur die gemeine Kiefer. Forstwissenschatliche Zentralblatt 16, 1852–1890.Google Scholar
Fries, N. 1944. Beobactungen uber die thamniscophage Mycorrhiza einiger Halophyten. Botanisker Notiser 2, 255–264.Google Scholar
Friese, C. F. 1984. The distribution of VAM fungi in a sand dune. MS Thesis, University of Rhode Island, Kingston, R.I.Google Scholar
Gemma, J. N., Koske, R. E. & Carreiro, M. 1989. Seasonal dynamics of selected VA mycorrhizal fungi in a sand dune. Mycological Research 92, 317–321.Google Scholar
Gemma, J. N., & Koske, R. E. 1989. Field inoculation of American beachgrass (Ammophila breviligulata) with VA mycorrhizal fungi. Journal of Environmental Management (in press).Google Scholar
Gimingham, C. H. 1972. Ecology of Heathlands. London: Chapman & Hall.Google Scholar
Giovannetti, M. & Nicolson, T. H. 1983. Vesicular-arbuscular mycorrhizas in Italian sand dunes. Transactions of the British Mycological Society 80, 552–557.CrossRefGoogle Scholar
Good, R. 1935. Contributions towards a survey of the plants and animals of South Haven Peninsula, Studland Heath, Dorset. II General ecology of the flowering plants and ferns. Journal of Ecology 23, 361–405.CrossRefGoogle Scholar
Gorham, E. 1958. Soluble salts in dune sands from Blakeney Point in Norfolk. Journal of Ecology 46, 373–379.CrossRefGoogle Scholar
Grime, J. P. 1979. Plant Strategies and Vegetation Processes. London: John Wiley.Google Scholar
Grime, J. P., Mackey, J. M. I., Hillier, S. H. & Read, D. J. 1987. Floristic diversity in a model system using experimental microcosms. Nature, London 328, 420–422.CrossRefGoogle Scholar
Grubb, P. J. & Suter, M. B. 1971. The mechanism of acidification of soil by Calluna & Ulex and the significance for conservation. In The Scientific Management of Animal and Plant Communities for Conservation, eds Duffey, E. & Watt, S. S., pp. 115–132.Google Scholar
Harley, J. L. & Harley, E. L. 1987. A check-list of mycorrhiza in the British flora. New Phytologist 105, 1–102.CrossRefGoogle Scholar
Harley, J. L. & Smith, S. E. 1983. Mycorrhizal Symbiosis. London: Academic Press.Google Scholar
Jalal, M. A. F. & Read, D. J. 1983. The organic acid composition of Calluna heathland soil with special reference to phyto- and fungi-toxicity. I. Isolation and identification of organic acids. Plant and Soil 70, 257–272.Google Scholar
Jehne, W. & Thompson, C. H. 1981. Endomycorrhizae in plant colonisation in coastal sand dunes at Cooloola, Queensland. Australian Journal of Ecology 6, 221–230.Google Scholar
Koske, R. E. 1975. Endogone spores in Australian sand dunes. Canadian Journal of Botany 53, 668–672.Google Scholar
Koske, R. E. 1981. A preliminary study of interactions between species of vesicular-arbuscular mycorrhizal fungi in a sand dune. Transactions of the British Mycological Society 76, 411–416.Google Scholar
Koske, R. E. 1987. Ecology of VAM & VAMF in sand dunes. In Mycorrhizae in the Next Decade: Practical Application and Research Priorities, eds Sylvia, D. M., Hung, L. L. & Graham, J. H. Gainesville: University of Florida.Google Scholar
Koske, R. E. & Halvorson, W. L. 1981. Ecological studies of vesicular-arbuscular mycorrhizae in a barrier sand dune. Canadian Journal of Botany 59, 1413–1422.Google Scholar
Koske, R. E. & Polson, W. R. 1984. Are VA mycorrhizae required for sand dune stabilisation? Bio-Science 34, 420–424.Google Scholar
Leake, J. R. 1987. Metabolism of phyto- and fungitoxic phenolic acids by the ericoid mycorrhizal fungus. In Mycorrhizae in the Next Decade: Practical Application and Research Priorities, eds Sylvia, D. M., Hung, L. L. & Graham, J. H., p. 332. Gainesville: University of Florida.Google Scholar
Leake, J. R. & Read, D. J. 1989a. The biology of mycorrhiza in the Ericaceae XIII. Some characteristics of the extra-cellular proteinase activity of the ericoid endophyte Hymenoscyphus ericae. New Phytologist 112, 69–76.CrossRefGoogle Scholar
Leake, J. R. & Read, D. J. 1989b. The effects of phenolic compounds on nitrogen mobilisation by ericoid mycorrhizal systems. In Proceedings of the Second European Conference on Mycorrhizas, ed. Mejstrik, V. (in press).Google Scholar
Murdock, C. L., Jacobs, J. A. & Gerdemann, J. W. 1967. Utilisation of phosphorus sources of different availability by mycorrhizal and non-mycorrhizal maize. Plant and Soil 27, 329–334.CrossRefGoogle Scholar
Nicolson, T. H. 1959. Mycorrhiza in the Gramineae I. Vesicular-arbuscular endophytes, with special reference to the external phase. Transactions of the British Mycological Society 42, 421–438.Google Scholar
Nicolson, T. H. 1960a. Mycorrhiza in the Gramineae II. Development in different habitats, particularly sand dunes. Transactions of the British Mycological Society 43, 132–145.CrossRefGoogle Scholar
Nicolson, T. H. 1960b. Vesicular-arbusculare Mycorrhiza bei den Gramineen – morphologische und ökologische Aspekte. In Mycorrhiza, eds Rawald, W.B., Lyr, H. pp. 57–67. Jena: Gustav Fischer.Google Scholar
Nicolson, T. H. 1967. Vesicular-arbuscular mycorrhiza – a universal plant symbiosis. Science Progress 55, 561–581.Google Scholar
Nicolson, T. H. & Johnston, C. 1979. Mycorrhiza in the Gramineae III. Glomus fasciculatus as the endophyte of pioneer grasses in maritime sand dunes. Transactions of the British Mycological Society 72, 261–268.CrossRefGoogle Scholar
Powell, C. L. 1975. Potassium uptake by endotrophic mycorrhizas. In Endomycorrhizas, eds Sanders, F. E., Mosse, B. & Tinker, P. B., pp. 460–468. London: Academic Press.Google Scholar
Puppi, G., Tabacchini, P., Riess, S. & Sanvito, A. 1986. Seasonal patterns in mycorrhizal association in a maritime sand dune system. In Physiological and Genetical Aspects of Mycorrhizae, eds Gianinazzi-Pearson, V. & Gianninazzi, S., pp. 245–251. Paris: INRA.Google Scholar
Read, D. J. 1987. In support of Frank's organic nitrogen theory. Angewandt Botanik 61, 25–37.Google Scholar
Read, D. J. 1983. The biology of mycorrhiza in the Ericales. Canadian Journal of Botany 61, 985–1004.Google Scholar
Read, D. J. 1984. The structure and function of the vegetative mycelium of mycorrhizal roots. In The Ecology and Physiology of the Fungal Mycelium, eds Jennings, D. H. & Rayner, A. D. M., pp. 215–240. Cambridge: Cambridge University Press.Google Scholar
Read, D. J., Francis, R. & Finlay, R. D. 1985. Mycorrhizal mycelia and nutrient cycling in plant communities. In Ecological Interactions in Soil: Plants, Microbes and Animals, eds Fitter, A. H., Atkinson, D., Read, D. J. & Usher, M. B., British Ecological Society Special Publication 4, pp. 193–217. Oxford: Blackwell Scientific.Google Scholar
Read, D. J., Leake, J. R. & Langdale, A. R. 1989. The nitrogen nutrition of mycorrhizal fungi and their host plants. In Nitrogen, Phosphorus and Sulphur Utilisation by Fungi, eds Boddy, L., Marchant, R. & Read, D. J., pp. 181–204. Cambridge: Cambridge University Press.Google Scholar
Read, D. J. & Bajwa, R. 1985. Some nutritional aspects of the biology of ericaceous mycorrhizas. Proceedings of the Royal Society of Edinburgh 85B, 317–332.Google Scholar
Read, D. J. & Stribley, D. P. 1975. Some mycological aspects of the biology of mycorrhiza in the Ericaceae. In Endomycorrhizas, eds Sanders, F. E. & Tinker, P. B., pp. 105–117. London: Academic Press.Google Scholar
Rix, K. & Newman, E. I. 1985. Evidence for rapid cycling of phosphorus from dying roots to living plants. Oikos 45, 174–180.Google Scholar
Salisbury, E. J. 1922. The soils of Blakeney Point: a study of soil reaction and succession in relation to plant cover. Annals of Botany 36, 391–431.Google Scholar
Salisbury, E. J. 1925. Note on the edaphic succession in some dune soils with special reference to the time factor. Journal of Ecology 13, 322–328.Google Scholar
Salisbury, E. J. 1952. Downs and Dunes – their Plant Life and its Environment. London: G. Bell.Google Scholar
Stahl, E. 1900. Der Sinn der Mycorhizen bildung. Eine vergleichend-biologische Studie. Jahrbuch für Wissenschaftliche Botanik 34, 539–668.Google Scholar
Sutton, J. C. & Sheppard, B. R. 1976. Aggregation of sand-dune soil by endomycorrhizal fungi. Canadian Journal of Botany 54, 326–333.Google Scholar
Sylvia, D. M. 1986. Spatial and temporal distribution of vesicular-arbuscular mycorrhizal fungi associated with Uniola paniculala in Florida foredunes. Mycologia 78, 734–740.CrossRefGoogle Scholar
Tansley, A. G. 1939. The British Islands and their Vegetation. Cambridge: Cambridge University Press.Google Scholar
Tisdall, J. M. & Oades, J. M. 1979. Stabilisation of soil aggregates by the root systems of rye grass. Australian Journal of Soil Research 17, 429–441.CrossRefGoogle Scholar
Virginia, R., Jenkins, M. B. & Jarrell, W. M. 1986. Depth of root symbiont occurrence in soils. Biology and Fertility of Soils 2, 127–130.Google Scholar
Webley, D. M., Eastwood, D. J. & Gimingham, C. H. 1952. Development of soil microflora in relation to plant succession on sand dunes including the “rhizosphere” flora associated with colonising species. Journal of Ecology 40, 168–178.Google Scholar
Willis, A. J. 1963. Braunton Burrows: the effects on the vegetation of the addition of mineral nutrients to the dune soils. Journal of Ecology 51, 353–374.CrossRefGoogle Scholar
Willis, A. J. 1985. Dune water and nutrient regimes – their ecological relevance. In Sand Dunes and Their Management, ed. Doody, P. Peterborough: Nature Conservancy Council Publication No. 13.Google Scholar
Willis, A. J. 1989. Coastal sand dunes as biological systems. Proceedings of the Royal Society of Edinburgh 96B, 17–36.Google Scholar
Wilson, K. 1960. The time factor in the development of dune soils at South Haven Peninsula, Dorset. Journal of Ecology 48, 341–359.CrossRefGoogle Scholar