, Volume 138, Issue 3, pp 419–425 | Cite as

Species-specific measurements of ectomycorrhizal turnover under N-fertilization: combining isotopic and genetic approaches

  • Kathleen K. TresederEmail author
  • C. A. Masiello
  • J. L. Lansing
  • M. F. Allen
Ecosystems Ecology


Ectomycorrhizal fungi play a significant role in the transfer of nutrients between plant and soil pools. Here we combine natural abundance 14C measurements with restriction fragment length polymorphism (RFLP) to study the effects of nitrogen fertilization on the residence time of carbon within ectomycorrhizal species. We show that the carbon in ectomycorrhizal fungi turns over every 4–5 years, indicating that these fungi are relatively long-lived. Moreover, ectomycorrhizal fungi responded in a species-specific way to fertilization. Cenococcum geophilum contained younger carbon on average in nitrogen-fertilized plots than in control plots, even though turnover rates of the community as a whole did not shift significantly. Our results suggest that the response of ectomycorrhizal fungi to N availability is complex, and alterations in tissue turnover within this microbial pool may vary depending on community structure.


Anthropogenic nitrogen deposition  Pinus edulis Radiocarbon RFLP Community composition 



We thank I. Levin and S. Leavitt for access to atmospheric data; Sevilleta Long-term Ecological Research Center for use of field sites and equipment; Lawrence Livermore National Laboratory for radiocarbon analyses of samples; and J. Borneman (University of California Riverside) and A. Denton (University of Alaska Fairbanks) for advice and technical assistance with the genetic analyses. This work was funded by NSF Cross-site (DEB 9996211), Biocomplexity (DEB 9981548), and LTER III (DEB 0080529) grants to M.F.A.; an NSF Ecosystems grant to K.K.T. (DEB 010776); a Mellon Foundation grant to K.K.T.; and a Center for Accelerated Mass Spectrometry minigrant from Lawrence Livermore National Laboratory to K.K.T., C.A.M., and M.F.A.


  1. Abuzinadah RA, Read DJ (1989) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. 4. The utilization of peptides by birch ( Betula pendula L) infected with different mycorrhizal fungi. New Phytol 112:55–60Google Scholar
  2. Agerer R (2002) Colour atlas of ectomycorrhizae. Einhorn, Schwabisch GmundGoogle Scholar
  3. Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, CambridgeGoogle Scholar
  4. Baar J, Stanton NL (2000) Ectomycorrhizal fungi challenged by saprotrophic basidiomycetes and soil microfungi under different ammonium regimes in vitro. Mycol Res 104:691–697CrossRefGoogle Scholar
  5. Baum C, Makeschin F (2000) Effects of nitrogen and phosphorus fertilization on mycorrhizal formation of two poplar clones ( Populus trichocarpa and P. tremula × tremuloides). J Plant Nutr Soil Sci 163:491–497Google Scholar
  6. Baum C, Weih M, Verwijst T, Makeschin F (2002) The effects of nitrogen fertilization and soil properties on mycorrhizal formation of Salix viminalis. For Ecol Manage 160:35–43CrossRefGoogle Scholar
  7. Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–393Google Scholar
  8. Chen CL, Chang HM (1985) Chemistry of lignin degradation. In: Higuchi T (ed) Biosynthesis and biodegradation of wood components. Academic Press, Orlando, Fla., pp 535–556Google Scholar
  9. Dickie IA, Avis PG, McLaughlin DJ, Reich P (2003) Good-Enough RFLP Matcher (GERM) program. Mycorrhiza 13:171–172PubMedGoogle Scholar
  10. Finlay R, Soderstrom B (1992) Mycorrhiza and carbon flow to the soil. In: Allen MF (ed) Mycorrhizal functioning: An integrative plant-fungal process. Chapman and Hall, New York, pp 134–162Google Scholar
  11. Fransson PMA, Taylor AFS, Finlay RD (2001) Elevated atmospheric CO2 alters root symbiont community structure in forest trees. New Phytol 152:431–442CrossRefGoogle Scholar
  12. Gardes M, White TJ, Fortin JA, Bruns TD, Taylor JW (1991) Identification of indigenous and introduced symbiotic fungi in ectomycorrhizae by amplification of nuclear and mitochondrial ribosomal DNA. Can J Bot 69:180–190Google Scholar
  13. Gaudinski JB, Trumbore SE, Davidson EA, Zheng SH (2000) Soil carbon cycling in a temperate forest: radiocarbon-based estimates of residence times, sequestration rates and partitioning of fluxes. Biogeochemistry 51:33–69CrossRefGoogle Scholar
  14. Gaudinski JB, Trumbore SE, Davidson EA, Cook AC, Markewitz D, Richter DD (2001) The age of fine-root carbon in three forests of the eastern United States measured by radiocarbon. Oecologia 129:420–429Google Scholar
  15. Gehring CA, Theimer TC, Whitham TG, Keim P (1998) Ectomycorrhizal fungal community structure of pinyon pines growing in two environmental extremes. Ecology 79:1562–1572Google Scholar
  16. Goodman DM, Durall DM, Trofymow JA, Berch SM (1996) A manual of concise descriptions of North American ectomycorrhizae. Mycologue, VictoriaGoogle Scholar
  17. Harley JL (1969) Ecology of ectotrophic mycorrhizas. In: Polunin N (ed) The biology of mycorrhiza. Leonard Hill, London, pp 150–162Google Scholar
  18. Harris D, Paul EA (1987) Carbon requirements of vesicular-arbuscular mycorrhizae. In: Safir GR (ed) Ecophysiology of VA mycorrhizae. CRC, Boca Raton, Florida, pp 93–105Google Scholar
  19. Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soybean- Rhizobium-Glomus associations. New Phytol 101:427–440Google Scholar
  20. Hobbie EA, Weber NS, Trappe JM, van Klinken GJ (2002) Using radiocarbon to determine the mycorrhizal status of fungi. New Phytol 156:129–136CrossRefGoogle Scholar
  21. Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10:1855–1871PubMedGoogle Scholar
  22. Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83Google Scholar
  23. Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002a) In situ (CO2)-13C pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334Google Scholar
  24. Johnson D, Leake JR, Read DJ (2002b) Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of 14C. Soil Biol Biochem 34:1521–1524CrossRefGoogle Scholar
  25. Karen O, Nylund JE (1997) Effects of ammonium sulfate on the community structure and biomass of ectomycorrhizal fungi in a Norway spruce stand in southwestern Sweden. Can J Bot 75:1628–1642Google Scholar
  26. Kucey RMN, Paul EA (1982) Carbon flow, photosynthesis, and N2 fixation in mycorrhizal and nodulated faba beans ( Vicia faba L.). Soil Biol Biochem 14:407–412CrossRefGoogle Scholar
  27. Lansing JL (2003) Comparing arbuscular and ectomycorrhizal fungal communities in seven North American forests and their response to nitrogen fertilization. Ph.D. dissertation. Department of Land, Air, and Water Resources. University of California Davis, Davis, CaliforniaGoogle Scholar
  28. Levin I, Kromer B (1997) 14CO2 records from Schauinsland. In: Trends: a compendium of data on global change. Carbon Dioxide Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, TennesseeGoogle Scholar
  29. Levin I, et al (1994) Δ14CO2 record from Vermunt. In: Trends: a compendium of data on global change. Carbon Dioxide Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, TennesseeGoogle Scholar
  30. Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115Google Scholar
  31. Majdi H, Nylund J-E (1996) Does liquid fertilization affect fine root dynamics and lifespan of mycorrhizal short roots? Plant Soil 185:305–309Google Scholar
  32. Majdi H, Damm E, Nylund JE (2001) Longevity of mycorrhizal roots depends on branching order and nutrient availability. New Phytol 150:195–202CrossRefGoogle Scholar
  33. Orlov A (1957) Observations on absorbing roots of spruce ( Picea excelsa Link) in natural conditions. Bot J USSR 42:1172–1181Google Scholar
  34. Orlov A (1960) Growth and changes with age of feeder roots of Picea excelsa Link. Bot J USSR 45:888–896Google Scholar
  35. Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309Google Scholar
  36. Read DJ (1991a) Mycorrhizas in ecosystems. Experientia 47:376–391Google Scholar
  37. Read DJ (1991b) Mycorrhizas in ecosystems—nature’s response to the “Law of the minimum”. In: Hawksworth DL (ed) Frontiers in mycology. CAB International, Regensburg, pp 101–130Google Scholar
  38. Rygiewicz PT, Johnson MG, Ganio LM, Tingey DT, Storm MJ (1997) Lifetime and temporal occurrence of ectomycorrhizae on Ponderosa pine ( Pinus ponderosa Laws) seedlings grown under varied atmospheric CO2 and nitrogen levels. Plant Soil 189:275–287CrossRefGoogle Scholar
  39. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San DiegoGoogle Scholar
  40. Sokal RR, Rohlf FJ (1995) Biometry, 3 edn. Freeman, New YorkGoogle Scholar
  41. SPSS (2000) Systat 10. SPSS, ChicagoGoogle Scholar
  42. Stuiver M, Polach HA (1977) Reporting of 14C data. Radiocarbon 19:355–363Google Scholar
  43. Termorshuizen AJ (1993) The influence of nitrogen fertilizers on ectomycorrhizas and their fungal carpophores in young stands of Pinus sylvestris. For Ecol Manage 57:179–189CrossRefGoogle Scholar
  44. Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200Google Scholar
  45. Treseder KK, Allen MF (2002) Direct N and P limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–515CrossRefGoogle Scholar
  46. Treseder KK, Davidson DW, Ehleringer JR (1995) Absorption of ant-provided carbon dioxide and nitrogen by a tropical epiphyte. Nature 375:137–139Google Scholar
  47. Vogel JS, Nelson DE, Southon JR (1987) 14C background levels in an accelerator mass spectrometry system. Radiocarbon 29:323–333Google Scholar
  48. Vogt KA, Grier CC, Edmonds RL, Meier CE (1982) Mycorrhizal role in net primary production and nutrient cycling in Abies amabilis (Dougl.) Forbes ecosystems in western Washington. Ecology 63:370–380Google Scholar
  49. White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Kathleen K. Treseder
    • 1
    • 5
    Email author
  • C. A. Masiello
    • 1
    • 2
    • 6
  • J. L. Lansing
    • 1
    • 3
  • M. F. Allen
    • 1
    • 4
  1. 1.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  2. 2.Lawrence Livermore National LaboratoryLivermoreUSA
  3. 3.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA
  4. 4.Center for Conservation BiologyUniversity of CaliforniaRiversideUSA
  5. 5.Department of Ecology and Evolutionary Biology and Department of Earth System ScienceUniversity of CaliforniaIrvineUSA
  6. 6.Department of GeographyUC Santa BarbaraSanta BarbaraUSA

Personalised recommendations