Patterns of nitrogen and carbon stable isotope ratios in macrofungi, plants and soils in two old-growth conifer forests

New Phytologist

Volumn 164, Issue 2, 2004, Pages 317-335

  Trudell, Steven A ^a   Rygiewicz, Paul T ^b   Edmonds, Robert L ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

13C; 15N; Ectomycorrhizal fungi; Macrofungi; Nutrient cycling; Saprotrophic fungi; Stable isotopes

Indexed keywords

CARBON ISOTOPE; CONIFEROUS FOREST; FUNGUS; NITROGEN ISOTOPE; OLD-GROWTH FOREST;

NORTH AMERICA; OLYMPIC NATIONAL PARK; UNITED STATES; WASHINGTON [UNITED STATES];

CONIFEROPHYTA; FUNGI;

EID: 4344617672     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2004.01162.x     Document Type: Article

References (67)

1. Abraham W-R, Hesse C, Pelz O. 1998. Ratios of carbon isotopes in microbial lipids as an indicator of substrate usage. Applied and Environmental Microbiology 64: 4202-4209.
2. Abuzinadah RA, Read DJ. 1986. 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.
3. Aerts R, Chapin FS III. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30: 1-67.
4. Agerer R. 1990. Studies on ectomycorrhizae XXIV: ectomycorrhizae of Chroogomphus helveticus and C. rutilus (Gomphidiaceae, Basidiomycetes) and their relationship to those of Suillus and Rhizopogon. Nova Hedwigia 50: 1-63.
5. Agerer R. 2001. Exploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11: 107-114.
6. Bending GD, Read DJ. 1995. The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. Foraging behaviour and translocation of nutrients from exploited organic matter. New Phytologist 130: 401-409.
7. Boddy L. 1999. Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91: 13-32.
8. Cairney JWG. 1999. Intraspecific physiological variation: implications for understanding functional diversity in ectomycorrhizal fungi. Mycorrhiza 9: 125-135.
9. Chapela IH, Osher LJ, Horton TR, Henn MR. 2001. Ectomycorrhizal fungi introduced with exotic pine plantations induce soil carbon depletion. Soil Biology and Biochemistry 33: 1733-1740.
10. Dickie IA, Xu B, Koide RT. 2002. Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytologist 156: 527-535.
11. Edmonds RL, Blew RD, Marra JL, Blew J, Barg AK, Murray G, Thomas TB. 1998. Vegetation patterns, hydrology, and water chemistry in small watersheds in the Hoh River Valley, Olympic National Park. Scientific Monograph NPSD/NRUSGS/NRSM-98/02. Washington, DC, USA: US Department of the Interior, National Park Service.
12. Emmerton KS, Callaghan TV, Jones HE, Leake JR, Michelsen A, Read DJ. 2001. Assimilation and isotopic fractionation of nitrogen by mycorrhizal fungi. New Phytologist 151: 503-511.
13. 15N in forests across a nitrogen deposition gradient. Forest Ecology and Management 101: 9-18.
14. Erland S, Taylor AFS. 2002. Diversity of ecto-mycorrhizal fungal communities in relation to the abiotic environment. In: van der Heijden MGA, Sanders IR, eds. Mycorrhizal Ecology. Ecological Studies 157. Berlin, Germany: Springer-Verlag, 163-200.
15. 15N abundance in plant foliage from Great Smoky Mountains National Park. Canadian Journal of Forest Research 24: 1636-1645.
16. Gebauer G, Dietrich P. 1993. Nitrogen isotope ratios in different compartments of a mixed stand of spruce, larch and beech trees and of understorey vegetation including fungi. Isotopenpraxis in Environmental and Health Studies 29: 35-44.
17. 15N natural abundance in fruit bodies of different functional groups of fungi in relation to substrate utilization. New Phytologist 142: 93-101.
18. Griffith GW, Easton GL, Jones AW. 2002. Ecology and diversity of waxcap (Hygrocybe spp.) fungi. Botanical Journal of Scotland 54: 7-22.
19. Grime JP. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111: 1169-1194.
20. 15N natural abundance patterns of field-collected fungi from three kinds of ecosystems. Rapid Communications in Mass Spectrometry 10: 974-978.
21. 4-derived sucrose. Applied and Environmental Microbiology 66: 4180-4186.
22. 15N isotopic fractionation in forest fungi and the roots of the saprotrophic-mycorrhizal divide. Oecologia 128: 480-487.
23. Henn MR, Chapela IH. 2004. Isotopic fractionation during ammonium assimilation by basidiomycete fungi and its implications for natural nitrogen isotope patterns. New Phytologist 162: 771-781.
24. 13C pattern and physiological process. Applied and Environmental Microbiology 68: 4956-4964.
25. Hitchcock CL, Cronquist A. 1973. Flora of the Pacific Northwest: an illustrated manual. Seattle, WA, USA: University of Washington Press.
26. Hobbie EA, Colpaert JV. 2003. Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phytologist 157: 115-126.
27. Hobbie EA, Macko SA, Shugart HH. 1999a. Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118: 353-360.
28. Hobbie EA, Macko SA, Shugart HH. 1999b. Interpretation of nitrogen isotope signatures using the NIFTE model. Oecologia 120: 405-415.
29. 15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122: 273-283.
30. Hobbie EA, Weber NS, Trappe JM. 2001. Mycorrhizal vs saprotrophic starus of fungi: the isotopic evidence. New Phytologist 150: 601-610.
31. 15N abundance of surface soils, roots and mycorrhizas in profiles of European forest soils. Oecologia 108: 207-214.
32. Högberg P, Högberg MN, Quist ME, Ekblad A, Näsholm T. 1999a. Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris. New Phytologist 142: 569-576.
33. 13C abundance reveals trophic status of fungi and host-origin of carbon in mycorrhizal fungi in mixed forests. Proceedings of the National Academy of Sciences, USA 96: 8534-8539.
34. Horwath WR, Idol TW, Southworth D, Lindahl A, Snyder S, Allen MF. 2002. Comparison of nitrogen isotope signatures of mycorrhizal and non-mycorrhizal fungi associated with oaks. Mycological Society of America annual meeting abstracts. Inoculum 53: 33-34.
35. Jennings DH. 1995. The physiology of fungal nutrition. Cambridge, UK: Cambridge University Press.
36. Klironomos JN, Hart MM. 2001. Animal nitrogen swap for plant carbon. Nature 410: 651-652.
37. 15N abundance of field-collected fungi and their ecological implications. New Phytologist 144: 323-330.
38. Kohzu A, Tateishi T, Yamada A, Koba K, Wada E. 2000. Nitrogen isotope fractionation during nitrogen transport from ectomycorrhizal fungi, Suillus granulatus, to the host plant, Pinus densiflora. Soil Science and Plant Nutrition 46: 733-739.
39. Kuyper TW, Landeweert R. 2002. Vertical niche differentiation by hyphae of ectomycorrhizal fungi in soil. New Phytologist 156: 323-325.
40. Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E. 2003. Molecular identification of ectomycorrhizal mycelium in soil horizons. Applied and Environmental Microbiology 69: 327-333.
41. Leake JR. 2001. Is diversity of ectomycorrhizal fungi important for ecosystem function? New Phytologist 152: 1-3.
42. Lilleskov EA, Hobbie EA, Fahey TJ. 1997. Natural abundance nitrogen isotopes: a potential tool for exploring diversity of nitrogen utilization in ectomycorrhizal fungal communities. In: Flores HE, Lynch JP, Eissenstat D, eds. Radical biology: advances and perspectives on the function of plant roots. Rockville, MD, USA: American Society of Plant Physiologists, 523-525.
43. Lilleskov EA, Hobbie EA, Fahey TJ. 2002. Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytologist 154: 219-231.
44. Lindahl BO, Taylor AFS, Finlay RD. 2002. Defining nutritional constraints on carbon cycling in boreal forests - towards a less 'phytocentric' perspective. Plant and Soil 242: 123-135.
45. Maser C, Anderson RG, Cromack K Jr, Williams JT, Martin RE. 1979. Dead and down woody material. In: Thomas JW, ed. Wildlife habitat in managed forests: the Blue Mountains of Oregon. Handbook no. 553. Washington, DC, USA: US Department of Agriculture.
46. Miller OK Jr. 1982. Taxonomy of ecto- and ectendomycorrhizal fungi. In: Schenck NC, ed. Methods and principles of mycorrhizal research. St Paul, MN, USA: American Phytopathological Society Press, 91-101.
47. Molina R, Massicotte H, Trappe JM. 1992. Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. In: Allen MF, ed. Mycorrhizal functioning: an integrative plant-fungal process. New York, NY, USA: Chapman & Hall, 357-423.
48. Nadelhoffer KJ, Fry B. 1988. Controls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter. Soil Science Society of America Journal 52: 1633-1640.
49. Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P. 1998. Boreal forest plants take up organic nitrogen. Nature 392: 914-916.
50. Näsholm T, Huss-Danell K, Högberg P. 2000. Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81: 1155-1161.
51. O'Dell TE, Ammirati JF, Schreiner EG. 1999. Species richness and abundance of ectomycorrhizal basidiomycete sporocarps on a moisture gradient in the Tsuga heterophylla zone. Canadian Journal of Botany 77: 1699-1711.
52. Pérez-Moreno J, Read DJ. 2000. Mobilization and transfer of nutrients from litter to tree seedlings via the vegetative mycelium of ectomycorrhizal plants. New Phytologist 145: 301-309.
53. Pérez-Moreno J, Read DJ. 2001a. Exploitation of pollen by mycorrhizal mycelial systems with special reference to nutrient recycling in boreal forests. Proceedings of the Royal Society of London, Series B 268: 1329-1335.
54. Pérez-Moreno J, Read DJ. 2001b. Nutrient transfer from soil nematodes to plants: a direct pathway provided by the mycorrhizal mycelial network. Plant, Cell & Environment 24: 1219-1226.
55. Peterson BJ, Fry B. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293-320.
56. Read DJ. 2002. Towards ecological relevance: progress and pitfalls in the path towards an understanding of mycorrhizal functions in nature. In: van der Heijden MGA, Sanders IR, eds. Mycorrhizal ecology. Ecological Studies 157. Berlin, Germany: Springer, 3-29.
57. Read DJ, Pérez-Moreno J. 2003. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytologist 157: 475-492.
58. 15N as an integrator of the nitrogen cycle. Trends in Ecology and Evolution 16: 153-162.
59. Rosling A, Landeweert R, Lindahl BD, Larsson K-H, Kuyper TW, Taylor AFS, Finlay RD. 2003. Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytologist 159: 775-783.
60. Singer R. 1986. The agaricales in modern taxonomy, 4th edn. Koenigstein, Germany: Koeltz Scientific Books.
61. 15N abundance in fruit bodies of ectomycorrhizal fungi from boreal forests. New Phytologist 136: 713-720.
62. Taylor AFS, Martin F, Read DJ. 2000. Fungal diversity in ectomycorrhizal communities of Norway spruce (Picea abies [L.] Karst.) and beech (Fagus sylvatica L.) along north-south transects in Europe. In: Schulze E-D, ed. Carbon and nitrogen cycling in European forest ecosystems. Ecological Studies 142. Berlin, Germany: Springer, 344-365.
63. 15N abundance of ectomycorrhizal and saprotrophic fungal sporocarps. New Phytologist 159: 757-774.
64. Trudell SA, Edmonds RL. 2004. Macrofungus communities correlate with moisture and nitrogen abundance in two old-growth conifer forests, Olympic National Park, Washington, USA. Canadian Journal of Botany 82: 781-800.
65. Trudell SA, Rygiewicz PT, Edmonds RL. 2001. Nitrogen stable isotope ratios in sporocarps of ectomycorrhizal fungi: influence of phylogenetic and environmental factors. Phytopathology 91: S125.
66. Trudell SA, Rygiewicz PT, Edmonds RL. 2003. Nitrogen and carbon stable isotope abundances support the myco-heterotrophic nature and host-specificity of certain achlorophyllous plants. New Phytologist 160: 391-401.
67. 15N abundance of soils. In: Boutton TW, Yamasaki S, eds. Mass spectrometry of soils. New York, NY, USA: Marcel Dekker, 205-223.