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Natural Abundance of 15N in Nitrogen-Limited Forests and Tundra Can Estimate Nitrogen Cycling Through Mycorrhizal Fungi: A Review

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Abstract

The hyphae of ectomycorrhizal and ericoid mycorrhizal fungi proliferate in nitrogen (N)-limited forests and tundra where the availability of inorganic N is low; under these conditions the most common fungal species are those capable of protein degradation that can supply their host plants with organic N. Although it is widely understood that these symbiotic fungi supply N to their host plants, the transfer is difficult to quantify in the field. A novel approach uses the natural 15N:14N ratios (expressed as δ15N values) in plants, soils, and mycorrhizal fungi to estimate the fraction of N in symbiotic trees and shrubs that enters through mycorrhizal fungi. This calculation is possible because mycorrhizal fungi discriminate against 15N when they create compounds for transfer to plants; host plants are depleted in 15N, whereas mycorrhizal fungi are enriched in 15N. The amount of carbon (C) supplied to these fungi can be stoichiometrically calculated from the fraction of plant N derived from the symbiosis, the N demand of the plants, the fungal C:N ratio, and the fraction of N retained in the fungi. Up to a third of C allocated belowground, or 20% of net primary production, is used to support ectomycorrhizal fungi. As anthropogenic N inputs increase, the C allocation to fungi decreases and plant δ15N increases. Careful analyses of δ15N patterns in systems dominated by ectomycorrhizal and ericoid mycorrhizal symbioses may reveal the ecosystem-scale effects of alterations in the plant–mycorrhizal symbioses caused by shifts in climate and N deposition.

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References

  • 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 Phytol 103:481–93.

    Article  CAS  Google Scholar 

  • Abuzinadah RA, Read DJ. 1989. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. IV. The utilization of peptides by birch (Betula pendula L.) infected with different mycorrhizal fungi. New Phytol 112:55–60

    Google Scholar 

  • Aerts R 2002. The role of various types of mycorrhizal fungi in nutrient cycling and plant competition. In: van der Heijden MGA, Sanders I, Eds. Mycorrhizal ecology. Berlin: Springer Verlag. pp 117–33.

    Google Scholar 

  • Ågren GI, Bosatta E 1996. Theoretical ecosystem ecology. Cambridge: Cambridge University Press. 250p.

    Google Scholar 

  • Amundson R, Austin AT, Schuurr EAG, You K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT 2003. Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem Cycles 17(1):1031.

    Article  CAS  Google Scholar 

  • Azcon-Aquilar C, Handley LL, Scrimgeour CM 1998. The 15N of lettuce and barley are affected by AM status and external concentration of N. New Phytol 138:19–26.

    Article  Google Scholar 

  • Benjdia M, Rikirsch E, Muller T, Morel M, Corratge C, Zimmermann S, Chalot M, Frommer WB, Wipf D 2006. Peptide uptake in the ectomycorrhizal fungus Hebeloma cylindrosporum: characterization of two di- and tripeptide transporters (HcPTR2A and B). New Phytol 170:401–10.

    Article  PubMed  CAS  Google Scholar 

  • Bidartondo MI, Ek H, Wallander H, Söderström B 2001. Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151:543–50.

    Article  CAS  Google Scholar 

  • Bird JA, Torn MS 2006. Fine roots versus needles: a comparison of 13C and 15N dynamics in a ponderosa pine forest soil. Biogeochemistry 79:53–67.

    Article  Google Scholar 

  • Bol R, Ostle NJ, Chenu CC, Petzke KJ, Werner RA, Balesdent J 2004. Long term changes in the distribution and δ15N values of individual soil amino acids in the absence of plant and fertiliser inputs. Isotopes Environ Health Stud 40:243–56.

    Article  PubMed  CAS  Google Scholar 

  • Chalot M, Blaudez D, Brun A 2006. Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11:263–6.

    Article  PubMed  CAS  Google Scholar 

  • Chalot M, Brun A 1998. Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44.

    Article  PubMed  CAS  Google Scholar 

  • Clarkson DT 1985. Factors affecting mineral nutrient acquisition by plants. Annu Rev Plant Physiol 36:77–115.

    Article  CAS  Google Scholar 

  • Clemmensen KE, Michelsen A, Jonasson S, Shaver GR 2006. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol 171:391–404.

    Article  PubMed  Google Scholar 

  • Coleman DC, Crossley DA Jr, Hendrix PF 2004. Fundamentals of soil ecology, 2nd edition. New York: Academic Press. 408p.

    Google Scholar 

  • Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J 2005. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol 167:309–19.

    Article  PubMed  CAS  Google Scholar 

  • Dijkstra P, Ishizu A, Doucett R, Hart SC, Schwartz E, Menyailo OV, Hungate BA 2006. 13C and 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38:3257–66.

    Article  CAS  Google Scholar 

  • Emmerton KS, Callaghan TV, Jones HE, Leake JR, Michelsen A, Read DJ 2001a. Assimilation and isotopic fractionation of nitrogen by mycorrhizal and nonmycorrhizal subarctic plants. New Phytol 151:513–24.

    Article  CAS  Google Scholar 

  • Emmerton KS, Callaghan TV, Jones HE, Leake JR, Michelsen A, Read DJ 2001b. Assimilation and isotopic fractionation of nitrogen by mycorrhizal fungi. New Phytol 151:503–11.

    Article  CAS  Google Scholar 

  • Emmett BA, Kjonaas OJ, Gundersen P, Koopmans C, Tietema A, Sleep D 1998. Natural abundance of 15N in forests across a nitrogen deposition gradient. For Ecol Manage 101:9–18.

    Article  Google Scholar 

  • Fry B 2006. Stable isotope ecology. New York: Springer-Verlag. 308p.

    Google Scholar 

  • Goericke R, Montoya JP, Fry B 1994. Physiology of isotopic fractionation in algae and cyanobacteria. In: Lajtha K, Michener RH, Eds. Stable isotopes in ecology and environmental science. London: Blackwell Publishing. pp 187–221.

    Google Scholar 

  • Handley LL, Austin AT, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S, Stewart GR 1999a. The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Aust J Plant Physiol 26:185–99.

    Article  Google Scholar 

  • Handley LL, Azcón R, Lozano JMR, Scrimgeour CM. 1999b. Plant δ15N associated with arbuscular mycorrhization, drought and nitrogen deficiency. Rapid Commun Mass Spectrom 13:1320–4

  • Handley LL, Daft MJ, Wilson J, Scrimgeour CM, Ingleby K, Sattar MA 1993. Effects of the ecto- and VA-mycorrhizal fungi Hydnagium carneum and Glomus clarum on the 15N and 13C values of Eucalyptus globulus and Ricinus communis. Plant Cell Environ 16:375–82.

    Article  CAS  Google Scholar 

  • Hendricks JJ, Mitchell RJ, Gren KM, Crocker TL, Yarbrough JG 2004. Assessing the 15N concentration of plant-available soil nitrogen. Commun Soil Sci Plant Anal 35:1207–17.

    Article  CAS  Google Scholar 

  • Hendricks JJ, Mitchell RJ, Kuehn KA, Pecot SD, Sims SE 2006. Measuring external mycelia production of ectomycorrhizal fungi in the field: the soil matrix matters. New Phytol 171:179–86.

    Article  PubMed  CAS  Google Scholar 

  • Henn MR, Chapela IH 2001. Ecophysiology of 13C and 15N isotopic fractionation in forest fungi and the roots of the saprotrophic-mycorrhizal divide. Oecologia 128:480–7.

    Article  Google Scholar 

  • Henn MR, Chapela IH 2004. Isotopic fractionation during ammonium assimilation by basidiomycete fungi and its implications for natural nitrogen isotope patterns. New Phytol 162:771–81.

    Article  CAS  Google Scholar 

  • Hobbie EA 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563–9.

    Article  PubMed  Google Scholar 

  • Hobbie EA, Colpaert JV 2003. Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phytol 157:115–26.

    Article  CAS  Google Scholar 

  • Hobbie JE, Hobbie EA 2006. 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in arctic tundra. Ecology 87:816–22.

    Article  PubMed  Google Scholar 

  • Hobbie EA, Jumpponen A, Trappe J 2005. Foliar and fungal 15N:14N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models. Oecologia 146:258–68.

    Article  PubMed  Google Scholar 

  • Hobbie EA, Macko SA, Shugart HH 1999a. Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–60.

    Article  Google Scholar 

  • Hobbie EA, Macko SA, Shugart HH 1999b. Interpretation of nitrogen isotope signatures using the NIFTE model. Oecologia 120:405–15.

    Article  Google Scholar 

  • Hobbie EA, Macko SA, Williams M 2000. Correlations between foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122:273–83.

    Article  Google Scholar 

  • Hobbie EA, Olszyk DM, Rygiewicz PT, Johnson MG, Tingey DT 2001. Foliar nitrogen levels and natural abundance 15N reveal mycorrhizal-plant partitioning and recycling of nitrogen during development under climate change. Tree Physiol 21:1113–22.

    PubMed  CAS  Google Scholar 

  • Hobbie EA, Sanchez FS, Rygiewicz PT 2004. Carbon use, nitrogen use, and isotopic fractionation of ectomycorrhizal and saprotrophic fungi in natural abundance and 13C-labelled cultures. Mycol Res 108:725–36.

    Article  PubMed  CAS  Google Scholar 

  • Hobbie EA, Wallander H 2006. Integrating ectomycorrhizal fungi into quantitative frameworks of forest carbon and nitrogen cycling. In: Gadd GM, Ed. Fungi in biogeochemical cycles. Cambridge: Cambridge University Press. pp 98–128.

    Google Scholar 

  • Högberg P 1990. 15N natural abundance as a possible marker of the ectomycorrhizal habit of the trees in mixed African woodlands. New Phytol 115:483–6.

    Article  Google Scholar 

  • Högberg P, Högberg MN, Quist ME, Ekblad A, Näsholm T 1999. Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris. New Phytol 142:69–576.

    Article  Google Scholar 

  • Högberg P, Högbom L, Schinkel H, Högberg M, Johannisson C, Wallmark H 1996. 15N abundance of surface soils, roots and mycorrhizas in profiles of European forest soils. Oecologia 108:207–14.

    Google Scholar 

  • Högberg P, Read DJ 2006. Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–54.

    Article  PubMed  Google Scholar 

  • Horton TR, Bruns TD 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol Ecol 10:1855–71.

    Article  PubMed  CAS  Google Scholar 

  • Ingestad T, Ågren GI 1988. Nutrient-uptake and allocation at steady-state nutrition. Physiol Plant 72:450–9.

    Article  CAS  Google Scholar 

  • Jackson RB, Mooney HA, Schulze ED 1997. A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci 94:7362–6.

    Article  PubMed  CAS  Google Scholar 

  • Jennings DH 1995. The physiology of fungal nutrition. Cambridge: Cambridge University Press. 642p.

    Google Scholar 

  • Jin H, Pfeffer PE, Douds DD, Piotrowski E, Lammers PJ, Shachar-Hill Y 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168:687–96.

    Article  PubMed  CAS  Google Scholar 

  • Johnston CA, Groffman P, Breshears DD, Cardon ZG, Currie W, Emanuel W, Guadinski J, Jackson RB, Lajtha K, Nadelhoffer K, Nelson D, Post WM, Tetallack G, Wielopolski L 2004. Carbon cycling in soil. Front Ecol Environ 2:522–8.

    Article  Google Scholar 

  • Jones DL, Hodge A 1999. Biodegradation kinetics and sorption reactions of three differently charged amino acids in soil and their effects on plant organic nitrogen availability. Soil Biol Biochem 31:1331–42.

    Article  CAS  Google Scholar 

  • Jones DL, Shannon D, Junvee-Fortune T, Farrarc J 2005a. Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biol Biochem 37:179–81.

    Article  CAS  Google Scholar 

  • Jones DL, Healy JR, Willett VB, Farrar JF, Hodge A 2005b. Dissolved organic nitrogen uptake by plants—an important N uptake pathway? Soil Biol Biochem 37:413–23.

    Article  CAS  Google Scholar 

  • Kerley SJ, Read DJ 1995. The biology of mycorrhizae in the Ericaceae. 18. Chitin degradation by Hymenoscyphus ericae and transfer of chitin-nitrogen to the host-plant. New Phytol 131:369–75.

    Article  CAS  Google Scholar 

  • 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 Sci Plant Nutr 46:733–9.

    Google Scholar 

  • Kohzu A, Yoshioka T, Ando T, Takahashi M, Koba K, Wada E 1999. Natural 13C and 15N abundance of field-collected fungi and their ecological implications. New Phytol 144:323–30.

    Article  Google Scholar 

  • Kuzyakov Y, Friedel JK, Stahr K 2000. Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–98.

    Article  CAS  Google Scholar 

  • Landeweert R, Leeflang P, Smit E, Kuyper T 2005. Diversity of an ectomycorrhizal fungal community studied by a root tip and total soil DNA approach. Mycorrhiza 15:1–6.

    Article  PubMed  Google Scholar 

  • 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 Phytol 154:219–31.

    Article  CAS  Google Scholar 

  • Lindahl BD, Finlay RD, Cairney JWG 2005. Enzymatic activities of mycelia in mycorrhizal fungal communities. In: Dighton J, White JF, Oudemans P, Eds. The fungal community. Boca Raton: Taylor & Francis. pp 331–48.

    Google Scholar 

  • Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD 2007. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–20.

    Article  PubMed  CAS  Google Scholar 

  • Lindahl BD, Taylor AFS 2004. Occurrence of N-acetylhexosaminidase-encoding genes in ectomycorrhizal basidiomycetes. New Phytol 164:193–9.

    Article  CAS  Google Scholar 

  • Lipson DA, Monson RK 1998. Plant-microbe competition for soil amino acids in the alpine tundra: effects of freeze-thaw and dry-rewet events. Oecologia 113:406–14.

    Article  Google Scholar 

  • Lodge DJ 1987. Nutrient concentrations, percentage moisture and density of field-collected fungal mycelia. Soil Biol Biochem 19:727–33.

    Article  Google Scholar 

  • Macko SA, Fogel Estep ML, Engel MH, Hare PE 1986. Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochim Cosmochim Acta 50:2143–6.

    Article  CAS  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71.

    Article  PubMed  CAS  Google Scholar 

  • Michelsen A, Quarmby C, Sleep D, Jonasson S 1998. Vascular plant 15N natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115:406–18.

    Article  Google Scholar 

  • Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D 1996. Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105:53–63.

    Article  Google Scholar 

  • Michelsen A, Sprent JI 1994. The influence of vesicular-arbuscular mycorrhizal fungi on the nitrogen fixation of nursery-grown Ethiopian acacias estimated by the 15N natural abundance method. Plant Soil 160:249–57.

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ, Fry B 1994. Nitrogen isotope studies in forest ecosystems. In: Lajtha K, Michener RH, Eds. Stable isotopes in ecology and environmental science. London: Blackwell Publishing. pp 22–44.

    Google Scholar 

  • Nadelhoffer KJ, Giblin AE, Shaver GR, Linkins AE 1992. Microbial processes and plant nutrient availability in Arctic soils. In: Chapin FS III, Jefferies RL, Reynolds JF, Shaver GR, Svoboda J, Chu EW, Eds. Arctic ecosystems in a changing climate. New York: Academic Press. pp 281–300.

    Google Scholar 

  • Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P 1998. Boreal forest plants take up organic nitrogen. Nature 392:914–6.

    Article  Google Scholar 

  • Nordin A, Högberg P, Näsholm T 2001. Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–32.

    Article  Google Scholar 

  • Olsson PA, Jakobsen I, Wallander H 2002. Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment. In: van der Heijden MGA, Sanders I, Eds. Mycorrhizal ecology. Berlin: Springer Verlag. pp 93–115.

    Google Scholar 

  • Persson J, Högberg P, Ekblad A, Högberg MN, Nordgren A, Näsholm T. 2003. Nitrogen acquisition from inorganic and organic sources by boreal forest plants in the field. Oecologia 137:252–7

    Google Scholar 

  • Portl K, Zechmeister-Boltenstern S, Wanek W, Ambus P, Berger TW 2007. Natural 15N abundance of soil N pools and N2O reflect the nitrogen dynamics of forest soils. Plant Soil 295:79–94.

    Article  CAS  Google Scholar 

  • Pritsch K, Raidl S, Marksteiner E, Blaschke H, Agerer R, Schloter M, Hartmann A 2004. A rapid and highly sensitive method for measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferone-labelled fluorogenic substrates in a microplate system. J Microbiol Methods 58:233–41.

    Article  PubMed  CAS  Google Scholar 

  • Read DJ, Perez-Moreno J 2003. Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–92.

    Article  Google Scholar 

  • Riemann L, Azam F 2002. Widespread N-acetyl-D-glucosamine uptake among pelagic marine bacteria and its ecological implications. Appl Environ Microbiol 68:5554–62.

    Article  PubMed  CAS  Google Scholar 

  • Roberts P, Bol R, Jones DL 2007. Free amino sugar reactions in soil in relation to soil carbon and nitrogen cycling. Soil Biol Biochem 39:3081–92.

    Article  CAS  Google Scholar 

  • Rosling A, Landeweert R, Lindahl BD, Larsson KH, Kuyper TW, Taylor AFS, Finlay RD 2003. Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159:775–83.

    Article  CAS  Google Scholar 

  • Schimel JP, Bennett J 2004. Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85:591–602.

    Article  Google Scholar 

  • Schmidt S, Handley LL, Sangtiean T 2006. Effects of nitrogen source and ectomycorrhizal association on growth and δ15N of two subtropical Eucalyptus species from contrasting ecosystems. Funct Plant Biol 33:367–79.

    Article  CAS  Google Scholar 

  • Schmidt S, Stewart GR 1997. Waterlogging and fire impacts on nitrogen availability and utilization in a subtropical wet heathland (wallum). Plant Cell Environ 20:1231–41.

    Article  Google Scholar 

  • Schmidt S, Stewart GR 2003. δ15N values of tropical savanna and monsoon forest species reflect root specialisations and soil nitrogen status. Oecologia 134:569–77.

    PubMed  CAS  Google Scholar 

  • Schwartz E, Blazewicz S, Doucett R, Hungate BA, Hart SC, Dijkstra P 2007. Natural abundance δ15N and δ13C of DNA extracted from soil. Soil Biol Biochem 39:3101–7.

    Article  CAS  Google Scholar 

  • Simard SW, Jones MD, Durall DM 2002. Carbon and nutrient fluxes within and between mycorrhizal plants. In: van der Heijden MGA, Sanders I, Eds. Mycorrhizal ecology. Berlin: Springer Verlag. pp 33–61.

    Google Scholar 

  • Smith SE, Smith FA 1990. Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol 114:1–38.

    Article  CAS  Google Scholar 

  • Taylor AFS, Alexander I 2005. The ectomycorrhizal symbiosis: life in the real world. Mycologist 19:102–12.

    Article  Google Scholar 

  • Taylor AFS, Fransson PMA 2007. Natural abundance of 15N and 13C in saprotrophic fungi: what can they tell us? In: Gadd G, Watkinson SC, Dyer P, Eds. Fungi in the environment. Cambridge: Cambridge University Press. pp. 141–58.

    Google Scholar 

  • Taylor AFS, Fransson PMA, Högberg P, Högberg MN, Plamboeck AH 2003. Species level patterns in 13C and 15N abundance of ectomycorrhizal and saprotrophic fungal sporocarps. New Phytol 159:757–74.

    Article  CAS  Google Scholar 

  • 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. New York: Springer-Verlag. pp 343–65.

    Google Scholar 

  • Trudell SA, Edmonds RL 2004. Macrofungus communities correlate with moisture and nitrogen abundance in two old-growth conifer forests, Olympic National Park, Washington, USA. Can J Bot 82:781–800.

    Article  CAS  Google Scholar 

  • 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 Phytol 160:391–401.

    Article  CAS  Google Scholar 

  • van Dam D, van Breemen N 1995. NICCCE: a model for cycling of nitrogen and carbon isotopes in coniferous forest ecosystems. Ecol Model 79:255–75.

    Article  CAS  Google Scholar 

  • Wallander H, Nilsson LO, Hagerberg D, Bååth E 2001. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–60.

    Article  CAS  Google Scholar 

  • Wallenda T, Kottke I 1998. Nitrogen deposition and ectomycorrhizas. New Phytol 139:169–87.

    Article  CAS  Google Scholar 

  • Wheeler CT, Tilak M, Scrimgeour CM, Hooker JE, Handley LL 2000. Effects of symbiosis with Frankia and arbuscular mycorrhizal fungus on the natural abundance of 15N in four species of Casuarina. J Exp Bot 51:287–97.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by NSF OPP-0612598 and NSF DEB-0614266. Comments on the manuscript by Erik Lilleskov and two anonymous reviewers are gratefully acknowledged.

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Hobbie, E.A., Hobbie, J.E. Natural Abundance of 15N in Nitrogen-Limited Forests and Tundra Can Estimate Nitrogen Cycling Through Mycorrhizal Fungi: A Review. Ecosystems 11, 815–830 (2008). https://doi.org/10.1007/s10021-008-9159-7

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