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Net transfer of carbon between ectomycorrhizal tree species in the field

Nature volume 388, pages 579582 (07 August 1997) | Download Citation

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Abstract

Different plant species can be compatible with the same species of mycorrhizal fungi1,2 and be connected to one another by a common mycelium3,4. Transfer of carbon3,4,5, nitrogen6,7 and phosphorus8,9 through interconnecting mycelia has been measured frequently in laboratory experiments, but it is not known whether transfer is bidirectional, whether there is a net gain by one plant over its connected partner, or whether transfer affects plant performance in the field10,11. Laboratory studies using isotope tracers show that the magnitude of one-way transfer can be influenced by shading of ‘receiver’ plants3,5, fertilization of ‘donor’ plants with phosphorus12, or use of nitrogen-fixing donor plants and non-nitrogen-fixing receiver plants13,14, indicating that movement may be governed by source–sink relationships. Here we use reciprocal isotope labelling in the field to demonstrate bidirectional carbon transfer between the ectomycorrhizal tree species Betula papyrifera and Pseudotsuga menziesii, resulting in net carbon gain by P. menziesii. Thuja plicata seedlings lacking ectomycorrhizae absorb small amounts of isotope, suggesting that carbon transfer between B. papyrifera and P. menziesii is primarily through the direct hyphal pathway. Net gain by P. menziesii seedlings represents on average 6% of carbon isotope uptake through photosynthesis. The magnitude of net transfer is influenced by shading of P. menziesii, indicating that source–sink relationships regulate such carbon transfer under field conditions.

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References

  1. 1.

    , & in Mycorrhizal Functioning: An Integrative Plant–Fungal Progess(ed. Allen, M. F.) 357–423 (Chapman and Hall, New York, (1992)).

  2. 2.

    , , & Biology of the ectomycorrhizal genus, Rhizopogon. II. Patterns of host-fungus specificity following spore inoculation of diverse hosts grown in monoculture and dual culture. New Phytol. 126, 677–690 (1994).

  3. 3.

    & Direct transfer of carbon between plants connected by vesicular–arbuscular mycorrhizal mycelium. Nature 307, 53–56 (1984).

  4. 4.

    , , & The structure and function of ectomycorrhizal roots with special reference to their role in forming interplant connections and providing pathways for assimulate and water transport. Plant Soil 71, 433–443 (1983).

  5. 5.

    & The structure and function of the vegetative mycelium of ectomycorrhizal plants. I. Translocation of 14C-labeled carbon between plants interconnected by a common mycelium. New Phytol. 103, 143–156 (1986).

  6. 6.

    , , & Nitrogen translocation between Alnus glutinosa (L.) Gaertn. seedlings inoculated with Frankia sp. and Pinus contorta Doug. ex Loud seedlings connected by a common ectomycorrhizal mycelium. New Phytol. 130, 231–242 (1993).

  7. 7.

    , , & Nutrient transfer between the root zones of soybean and maize plants connected by a common mycorrhizal mycelium. Physiologia Plantarum 82, 423–432 (1991).

  8. 8.

    & Rates of phosphorus transfer within and between ryegrass (Lolium perenne) plants. Funct. Ecol. 7, 242–248 (1993).

  9. 9.

    & Vesicular-arbascular mycorrhiza in natural vegetation systems III. Nutrient transfer between plants with mycorrhizal connections. New Phytol. 90, 277–284 (1982).

  10. 10.

    Mycorrhizal links between plants: their functioning and ecological significance. Adv. Ecol. Res. 18, 243–270 (1988).

  11. 11.

    & in Mycorrhizal Functioning: An Integrative Plant–Fungal Process(ed. Allen, M. F.) 301–332 (Chapman and Hall, New York, (1992)).

  12. 12.

    & Nutrient transport between ryegrass plants differing in nutrient status. Oecologia 70, 128–131 (1986).

  13. 13.

    & Transfer of symbiotically fixed nitrogen from berseem (Trifolium alexandrium L.) to maize via vesicular arbuscular mycorrhizal hyphae. New Phytol. 125, 447–454 (1992).

  14. 14.

    & Nitrogen fixation by Alnus incana and nitrogen transfer from A. incana to Pinus sylvestris influenced by macronutrients and ectomycorrhiza. New Phytol. 131, 453–459 (1995).

  15. 15.

    , & in The Ecology of Mixed-Species Stands of Trees(eds Cannell, M. G. R., Malcom, D. C. & Robertson, P. A.) 151–179 (Cambridge Univ. Press, (1992)).

  16. 16.

    , , , & Bootstrapping in ecosystems. Bioscience 39, 230–237.

  17. 17.

    in Biodiversity and Ecosystem Function(eds Schulze, E.-D. & Mooney, H. A.) 181–209 (Springer, Berlin, (1994)).

  18. 18.

    Dynamics and Structure of Plant Communities(Princeton Univ. Press, NJ, (1988)).

  19. 19.

    & in Biodiversity and Ecosystem Function(eds Schulze, E.-D. & Mooney, H. A.) 497–510 (Springer, Berlin, (1994)).

  20. 20.

    thesis, Oregon State Univ.((1995)).

  21. 21.

    Carbon gain by plants in natural environments. Bioscience 37, 21–28 (1987).

  22. 22.

    & Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol. 114, 1–38 (1990).

  23. 23.

    & Carbon transfer associated with assimilation of organic nitrogen sources by silver birch (Betula pendula Roth.). Trees 3, 17–23 (1989).

  24. 24.

    , & Transport of carbon among connected ramets of Eichhornia crassipes (Pontederiaceae) at normal and high levels of CO2. Am. J. Bot. 78, 1459–1466 (1991).

  25. 25.

    , , & Carbon transfer between C3 and C4 plants linked by a common mycorrhizal network, quantified using stable carbon isotopes. Soil Biol. Biochem. 28, 471–477 (1996).

  26. 26.

    & Effect of clipping, benomyl, and genet on 14C transfer between mycorrhizal plants. Oikos 71, 246–252 (1994).

  27. 27.

    , & Productivity and sustainability influence biodiversity in grassland ecosystems. Nature 379, 718–720 (1996).

  28. 28.

    , , , & Ectomycorrhizal mediation of competition between coniferous tree species. New Phytol. 112, 501–511 (1989).

  29. 29.

    in Carbon Isotope Techniques(eds Coleman, D. C. & Fry, B.) 155–170 (Academic, San Diego, (1991)).

  30. 30.

    & in Carbon Isotope Techniques(eds Coleman, D. C. & Fry, B.) 11–37 (Academic, San Diego, (1991)).

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Acknowledgements

We thank B. Danielson and C. Y. Li for review of the experiment designs; J. Smith and D. McKay for help with identification of ectomycorrhizal morphotypes and assistance in the greenhouse; C. Weicker and C. Gordon for assistance in the field; B. Zimonick, A. Vyse and P. G. Comeau for help and support; the staff at the Kamloops Forest Region of the British Columbia Ministry of Forests and Forestry Science Laboratory at Oregon State University for assistance; and S. Smith and R. Finlay for comments on the manuscript. This work was supported by the British Columbia Ministry of Forests and the Canada-British Columbia Partnership Agreement on Forest Resource Development (FRDA II).

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Affiliations

  1. *Kamloops Forest Region, British Columbia Ministry of Forests, Kamloops, British Columbia V2C 2T7, Canada

    • Suzanne W. Simard
  2. †Forest Science Department, Oregon State University, Corvallis, Oregon 97331, USA

    • David A. Perry
  3. §Crop and Soil Science Department, Oregon State University, Corvallis, Oregon 97331, USA

    • David D. Myrold
  4. ‡Biology Department, Okanagan University College, Kelowna, British Columbia V1V 1V7, Canada

    • Melanie D. Jones
    •  & Daniel M. Durall
  5. United States Department of Agriculture, Forest Service, Pacific Northwest Research Station, Corvallis, Oregon 97331, USA

    • Randy Molina

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Correspondence to Suzanne W. Simard.

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https://doi.org/10.1038/41557

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