Plant Ecology

, Volume 172, Issue 1, pp 133–141

Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology

  • Eileen V. Carey
  • Marilyn J. Marler
  • Ragan M. Callaway


Invasive exotic weeds pose one of the earth's most pressing environmental problems. Although many invaders completely eliminate native plant species from some communities, ecologists know little about the mechanisms by which these exotics competitively exclude other species. Mycorrhizal fungi radically alter competitive interactions between plants within natural communities, and a recent study has shown that arbuscular mycorrhizal (AM) fungi provide a substantial competitive advantage to spotted knapweed, Centaurea maculosa, a noxious perennial plant that has spread throughout much of the native prairie in the northwestern U.S. Here we present evidence that this advantage is potentially due to mycorrhizally mediated transfer of carbon from a native bunchgrass, Festuca idahoensis, to Centaurea. Centaurea maculosa, Festuca idahoensis (Idaho fescue, C3), and Bouteloua gracilis (blue gramma, C4) were grown in the greenhouse either alone or with Centaurea in an incomplete factorial design with and without AM fungi. Centaurea biomass was 87–168% greater in all treatments when mycorrhizae were present in the soil (P < 0.0001). However, Centaurea biomass was significantly higher in the treatment with both mycorrhizae and Festuca present together than in any other treatment combination (P < 0.0001). This high biomass was attained even though Centaurea photosynthetic rates were 14% lower when grown with Festuca and mycorrhizae together than when grown with Festuca without mycorrhizae. Neither biomass nor photosynthetic rates of Centaurea were affected by competition with the C4 grass Bouteloua either with or without mycorrhizae. The stable isotope signature of Centaurea leaves grown with Festuca and mycorrhizae was more similar to that of Festuca, than when Centaurea was grown alone with mycorrhizae (P = 0.06), or with Festuca but without mycorrhizae (P = 0.09). This suggests that carbon was transferred from Festuca to the invasive weed. We estimated that carbon transferred from Festuca by mycorrhizae contributed up to 15% of the aboveground carbon in Centaurea plants. Our results indicate that carbon parasitism via AM soil fungi may be an important mechanism by which invasive plants out compete their neighbors, but that this interaction is highly species-specific.

Arbuscular mycorrhizae Bouteloua gracilis Carbon transfer Centaurea maculosa Festuca idahoensis Invasive weeds 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen E.B. and Allen M.F. 1990. The mediation of competition by mycorrhizae in successional and patchy environments. In: Grace J.B. and Tilman G.D. (eds), Perspectives on Plant Competition. Academic Press, New York, pp. 367-389.Google Scholar
  2. Allen E.B. and Allen M.F. 1984. Competition between plants of different successional stages: mycorrhizae as regulators. Canadian Journal of Botany 62: 2625-2629.Google Scholar
  3. Allen M.F., Smith W.K., Moore T.S. and Christensen M. 1981. Comparative water relations and photosynthesis of mycorrhizal and non-mycorrhizal Bouteloua gracilis H.B.K. Lag ex Steud. New Phytologist 88: 683-693.Google Scholar
  4. Bergelson J.M. and Crawly M.J. 1988. Mycorrhizal infection and plant species diversity. Nature 344: 202.Google Scholar
  5. Caldwell M.M., Eissenstaat D.M., Richards J.H. and Allen M.F. 1985. Competition for phosphorus: differential uptake from dual-isotope labeled soil interspaces between shrub and grass. Science 217: 941-943.Google Scholar
  6. Chiariello N., Hickman J.C. and Mooney H.A. 1982. Endomycorrhizal role for interspecific transfer of phosphorus in a community of annual plants. Science 217: 941-943.Google Scholar
  7. DeLucia E.H., Callaway R.M., Thomas E.M. and Schlesinger W.H. 1997. Mechanisms of P acquisition for ponderosa pine under different climatic regimes. Annals of Botany 79: 11-120.Google Scholar
  8. Ehleringer J.R. and Osmond C.B. 1991. Stable Isotopes. In: Pearcy R.W., Ehleringer J.R., Mooney H.A. and Rundel P.W. (eds), Plant Physiological Ecology: Field Methods and Instrumentation. Chapman and Hall, New York, pp. 281-300.Google Scholar
  9. Fitter A.H., Graves J.D., Watkins N.K., Robinson D. and Scrimgeour C. 1998. Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Functional Ecology 12: 406-412.Google Scholar
  10. Francis R. and Read D.J. 1994. The contributions of mycorrhizal fungi to the determination of plant community structure. Plant and Soil 159: 11-25.Google Scholar
  11. Goodwin J. 1992. The role of mycorrhizal fungi in competitive interactions among native bunchgrasses and alien weeds: a review and synthesis. Northwest Science 66: 251260.Google Scholar
  12. Graves J.D., Watkins N.K., Fitter A.H., Robinson D. and Scrimgeour C. 1997. Intraspecific transfer of carbon between plants linked by a common mycorrhizal network. Plant and Soil 192: 153-159.Google Scholar
  13. Griffith D. and Lucey J.R. 1991. Economic evaluation of spotted knapweed (Centaurea maculosa) control using picloram. Journal of Range Management 44: 43-47.Google Scholar
  14. Grime J.P., Mackey J.M.L., Hillier S.H. and Read D.J. 1987. Floristic diversity in a model system using experimental microcosms. Nature 328: 420-422.Google Scholar
  15. Hartnett D.C., Hetrick B.A.D., Wilson G.W.T. and Gibson D.J. 1993. Mycorrhizal influence of intra-and inter-specific neighbor interactions among co-occurring prairie grasses. Journal of Ecology 81: 787-795.Google Scholar
  16. Hays R., Reid C.P.P., St. John T.V. and Coleman C.D. 1982. Effects of nitrogen and phosphorus on blue gramma growth and mycorrhizal infection. Oecologia 54: 260-265.Google Scholar
  17. Hetrick B.A.D., Wilson G.W.T. and Hartnett D.C. 1989. Relationship between mycorrhizal dependence and competitive ability of two tallgrass prairie grasses. Canadian Journal of Botany 67: 2608-2615.Google Scholar
  18. Hetrick B.A.D., Wilson G.W.T. and Todd T.C. 1990. Differential responses of C3 and C4 grasses to mycorrhizal symbiosis, phosphorus fertilization, and soil microorganisms. Canadian Journal of Botany 68: 461-467.Google Scholar
  19. Klironomos J. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67-70.PubMedGoogle Scholar
  20. Koide R.T. and Li M. 1990. On host regulation of the vesiculararbuscular mycorrhizal symbiosis. New Phytologist 114: 59-74.Google Scholar
  21. Leake J.R. 1994. The biology of myco-heterotrophic ('saprophytic') plants. New Phytologist 127: 171-216.Google Scholar
  22. Marler M.J., Zabinski C.A. and Callaway R.M. 1999a. Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80: 1180-1186.Google Scholar
  23. Marler M.J., Zabinski C.A., Wojtowicz T. and Callaway R.M. 1999b. Mycorrhizae and fine root dynamics of Centaurea maculosa and native bunchgrasses in western Montana. Northwest Science 73: 217-224.Google Scholar
  24. McGonigle T.P., Miller M.H., Evans D.G., Fairchild G.L. and Swan J.A. 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115: 495-501.Google Scholar
  25. Moora M. and Zobel M. 1996. Effect of arbuscular mycorrhiza on inter-and intraspecific competition of two grassland species. Oecologia 108: 70-84.Google Scholar
  26. Press M.C., Shah N., Tuohy J.M. and Stewart G.R. 1987. Carbon isotope ratios demonstrate carbon flux from C-4 host to C-3 parasite. Plant Physiology 85: 1143-1145.Google Scholar
  27. Robinson D. and Fitter A. 1999. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. Journal of Experimental Botany 50: 9-13.Google Scholar
  28. Simard S.W., Perry D.A., Jones M.D., Myrold D.D., Durall D.M. and Molina R. 1997. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388: 579-582.Google Scholar
  29. Walter L.E.F., Hartnett D.C., Hetrick B.A.D. and Schwab A.P. 1996. Interspecific nutrient transfer in a tallgrass prairie plant community. American Journal of Botany 83: 180-184.Google Scholar
  30. Waters J.R. and Borowicz V.A. 1995. Effect of clipping benomyl and get on 14C transfer between mycorrhizal plants. Oikos 71: 246-252.Google Scholar
  31. Watkins N.K., Fitter A.H., Graves J.D. and Robinson D. 1996. Carbon transfer between C3 and C4 plants linked by a common mycorrhizal network, quantified using stable carbon isotopes. Soil Biology and Biochemistry 28: 471-477.Google Scholar
  32. Watson A.K. and Renney A.J. 1974. The biology of Canadian weeds. 6. Centaurea diffusa and C. maculosa. Canadian Journal of Plant Science 54: 687-701.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Eileen V. Carey
    • 1
  • Marilyn J. Marler
    • 1
  • Ragan M. Callaway
    • 1
  1. 1.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  2. 2.Department of Forest ResourcesUniversity of MinnesotaSt. PaulUSA

Personalised recommendations