Advertisement

Biogeochemistry

, Volume 95, Issue 2–3, pp 355–371 | Cite as

Controls of nitrogen isotope patterns in soil profiles

  • Erik A. Hobbie
  • Andrew P. Ouimette
Article

Abstract

To determine the dominant processes controlling nitrogen (N) dynamics in soils and increase insights into soil N cycling from nitrogen isotope (δ15N) data, patterns of 15N enrichment in soil profiles were compiled from studies on tropical, temperate, and boreal systems. The maximum 15N enrichment between litter and deeper soil layers varied strongly with mycorrhizal fungal association, averaging 9.6 ± 0.4‰ in ectomycorrhizal systems and 4.6 ± 0.5‰ in arbuscular mycorrhizal systems. The 15N enrichment varied little with mean annual temperature, precipitation, or nitrification rates. One main factor controlling 15N in soil profiles, fractionation against 15N during N transfer by mycorrhizal fungi to host plants, leads to 15N-depleted plant litter at the soil surface and 15N-enriched nitrogen of fungal origin at depth. The preferential preservation of 15N-enriched compounds during decomposition and stabilization is a second important factor. A third mechanism, N loss during nitrification and denitrification, may account for large 15N enrichments with depth in less N-limited forests and may account for soil profiles where maximum δ15N is at intermediate depths. Mixing among soil horizons should also decrease differences among soil horizons. We suggest that dynamic models of isotope distributions within soil profiles that can incorporate multiple processes could provide additional information about the history of nitrogen movements and transformations at a site.

Keywords

Nitrogen isotopes Soil horizons Isotopic fractionation Modeling Mycorrhizal fungi Soil mixing Denitrification 

Notes

Acknowledgments

We thank Ben Houlton and two anonymous reviewers for useful comments on an earlier version of the manuscript. This work was suported by NSF grant DEB-0614266.

Supplementary material

10533_2009_9328_MOESM1_ESM.xls (68 kb)
(XLS 67 kb)

References

  1. Amundson R, Austin AT, Schuur EAG et al (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem Cycles 17:1031–1041. doi: 10.1029/2002GB001903 CrossRefGoogle Scholar
  2. Azcon-Aquilar GR, Handley LL, Scrimgeour CM (1998) The δ15N of lettuce and barley are affected by AM status and external concentration of N. New Phytol 138:19–26. doi: 10.1046/j.1469-8137.1998.00883.x CrossRefGoogle Scholar
  3. Baisden WT, Amundson R, Brenner DL et al (2002a) A multiisotope C and N modeling analysis of soil organic matter turnover and transport as a function of soil depth in a California annual grassland soil chronosequence. Global Biogeochem Cycles 16:26Google Scholar
  4. Baisden WT, Amundson R, Cook AC, Brenner DL (2002b) Turnover and storage of C and N in five density fractions from California annual grassland surface soils. Global Biogeochem Cycles 16:16Google Scholar
  5. Barton L, McLay CDA, Schipper LA, Smith CT (1999) Annual denitrification rates in agricultural and forest soils: a review. Aust J Soil Res 37:1073–1093. doi: 10.1071/SR99009 CrossRefGoogle Scholar
  6. Billings SA (2006) Soil organic matte dynamics and land use change at a grassland/forest ecotone. Soil Biol Biochem 38:2934–2943. doi: 10.1016/j.soilbio.2006.05.004 CrossRefGoogle Scholar
  7. Billings SA, Richter DD (2006) Changes in stable isotopic signatures of soil nitrogen and carbon during 40 years of forest development. Oecologia 148:325–333. doi: 10.1007/s00442-006-0366-7 CrossRefGoogle Scholar
  8. Bird JA, Torn (2006) Fine roots versus needles: a comparison of 13C and 15 N dynamics in a ponderosa pine forest soil. Biogeochemistry 79:361–382. doi: 10.1007/s10533-005-5632-y CrossRefGoogle Scholar
  9. Boeckx P, Paulino L, Oyarzun C et al (2005) Soil δ15N patterns in old-growth forests of southern Chile as integrator for N-cycling. Isotopes Environ Health Stud 41:249–259. doi: 10.1080/10256010500230171 CrossRefGoogle Scholar
  10. Bohlen PJ, Pelletier DM, Groffman PM et al (2004) Influence of earthworm invasion on redistribution and retention of soil carbon and nitrogen in northern temperate forests. Ecosystems (N Y, Print) 7:13–27. doi: 10.1007/s10021-003-0127-y CrossRefGoogle Scholar
  11. Caner L, Zeller B, Dambrine E et al (2004) Origin of the nitrogen assimilated by soil fauna living in decomposing beech litter. Soil Biol Biochem 36:1861–1872. doi: 10.1016/j.soilbio.2004.05.007 CrossRefGoogle Scholar
  12. Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44CrossRefGoogle Scholar
  13. Clarholm M (1981) Protozoan grazing of bacteria in soil—impact and importance. Microb Ecol 7:343–350. doi: 10.1007/BF02341429 CrossRefGoogle Scholar
  14. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil-nitrogen. Soil Biol Biochem 17:181–187. doi: 10.1016/0038-0717(85)90113-0 CrossRefGoogle Scholar
  15. Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology, 2nd edn. Academic Press, New YorkGoogle Scholar
  16. DeRuiter PC, Moore JC, Zwart KB et al (1993) Simulation of nitrogen mineralization in the belowground food webs of 2 winter-wheat fields. J Appl Ecol 30:95–106. doi: 10.2307/2404274 CrossRefGoogle Scholar
  17. Dominguez J, Bohlen PJ, Parmelee RW (2004) Earthworms increase nitrogen leaching to greater soil depths in row crop agroecosystems. Ecosystems (N Y, Print) 7:672–685. doi: 10.1007/s10021-004-0150-7 CrossRefGoogle Scholar
  18. Emmett BA, Kjonaas OJ, Gundersen P et al (1998) Natural abundance of 15N in forests across a nitrogen deposition gradient. For Ecol Manag 101:9–18CrossRefGoogle Scholar
  19. Evans RD, Belnap J (1999) Long-term consequences of disturbance on nitrogen dynamics in an arid ecosystem. Ecology 80:150–160Google Scholar
  20. Frey SD, Six J, Elliott ET (2003) Reciprocal tansfer of carbon and nitrogen by decomposer fungi at the soil-litter interface. Soil Biol Biochem 35:1001–1004. doi: 10.1016/S0038-0717(03)00155-X CrossRefGoogle Scholar
  21. Gabet EJ, Reichman OJ, Seabloom EW (2003) The effects of bioturbation on soil processes and sediment transport. Annu Rev Earth Planet Sci 21:249–273. doi: 10.1146/annurev.earth.31.100901.141314 CrossRefGoogle Scholar
  22. Garten CT (1993) Variation in foliar 15N abundance and the availability of soil nitrogen on Walker Branch watershed. Ecology 74:2098–2113. doi: 10.2307/1940855 CrossRefGoogle Scholar
  23. Garten CT, van Miegroet H (1994) Relationships between soil nitrogen dynamics and natural 15N abundance in plant foliage from Great Smoky Mountains National Park. Can J Res 24:1636–1645. doi: 10.1139/x94-212 CrossRefGoogle Scholar
  24. Gavito ME, Olsson PA (2003) Allocation of plant carbon to foraging and storage in arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 45:181–187. doi: 10.1016/S0168-6496(03)00150-8 CrossRefGoogle Scholar
  25. Goldberg SD, Knorr KH, Gebauer G (2008) N2O concentration and isotope signature along profiles provide deeper insight into the fate of N2O in soils. Isotopes Environ Health Stud 41:377–391. doi: 10.1080/10256010802507433 CrossRefGoogle Scholar
  26. Guo DL, Li H, Mitchell RJ, Han WX, Hendricks JJ, Fahey TJ, Hendrick RL (2008) Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytol 177:443-456CrossRefGoogle Scholar
  27. Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ 15:965–985. doi: 10.1111/j.1365-3040.1992.tb01650.x CrossRefGoogle Scholar
  28. Handley LL, Daft MJ, Wilson J et al (1993) Effects of the ecto- and VA-mycorrhizal fungi Hydnagium carneum and Glomus clarum on the 15 N and 13C values of Eucalyptus globulus and Ricinus communis. Plant Cell Environ 16:375–382. doi: 10.1111/j.1365-3040.1993.tb00883.x CrossRefGoogle Scholar
  29. Handley LL, Austin AT, Robinson D et al (1999a) The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Aust J Plant Physiol 26:185–199CrossRefGoogle Scholar
  30. Handley LL, Azcon R, Lozano JMR, Scrimgeour CM (1999b) Plant δ15N associated with arbuscular mycorrhization, drought and nitrogen deficiency. Rapid Commun Mass Spectrom 13:1320–1324. doi: 10.1002/(SICI)1097-0231(19990715)13:13<1320::AID-RCM607>3.0.CO;2-M CrossRefGoogle Scholar
  31. Haubert D, Haggblom MM, Langel R et al (2006) Trophic shift of stable isotopes and fatty acids in Collembola on bacterial diets. Soil Biol Biochem 38:2004–2007. doi: 10.1016/j.soilbio.2005.11.031 CrossRefGoogle Scholar
  32. Hedin LO, von Fischer JC, Ostrom NE et al (1998) Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil-stream interfaces. Ecology 79:684–703Google Scholar
  33. Hobbie EA, Colpaert JV (2003) Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phytol 157:115–126. doi: 10.1046/j.1469-8137.2003.00657.x CrossRefGoogle Scholar
  34. Hobbie EA, Hobbie JE (2008) Natural abundance of 15N in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems (N Y, Print) 11:815–830. doi: 10.1007/s10021-008-9159-7 CrossRefGoogle Scholar
  35. Hobbie EA, Macko SA, Shugart HH (1999) Interpretation of nitrogen isotope signatures using the NIFTE model. Oecologia 120:405–415. doi: 10.1007/s004420050873 CrossRefGoogle Scholar
  36. Hobbie EA, Macko SA, Williams M (2000) Correlations between foliar δ15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122:273–283. doi: 10.1007/PL00008856 CrossRefGoogle Scholar
  37. 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 146:258–268. doi: 10.1007/s00442-005-0208-z CrossRefGoogle Scholar
  38. Högberg P (1990) 15N natural abundance as a possible marker of the ectomycorrhizal habit of trees in mixed African woodlands. New Phytol 115:483-486CrossRefGoogle Scholar
  39. Högberg P (1997) 15N natural abundance in soil-plant systems. New Phytol 137:179–203. doi: 10.1046/j.1469-8137.1997.00808.x CrossRefGoogle Scholar
  40. Högberg P, Hogbom L, Schinkel H et al (1996) 15N abundance of surface soils, roots and mycorrhizas in profiles of European forest soils. Oecologia 108:207–214Google Scholar
  41. Houlton BZ, Sigman DM, Hedin LO (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci USA 103:8745–8750. doi: 10.1073/pnas.0510185103 CrossRefGoogle Scholar
  42. Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci 104:8902–8906CrossRefGoogle Scholar
  43. Hübner H (1986) Isotope effects of nitrogen in the soil and biosphere. In: Fritz P, Fontes PC (eds) Handbook of environmental isotope geochemistry, vol 2. Elsevier, Amsterdam, pp 361–425Google Scholar
  44. Johnson D, Leake JR, Read DJ (2002) Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of 14C. Soil Biol Biochem 34:1521–1524. doi: 10.1016/S0038-0717(02)00126-8 CrossRefGoogle Scholar
  45. Jones DL, Kielland K (2002) Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34:209–219. doi: 10.1016/S0038-0717(01)00175-4 CrossRefGoogle Scholar
  46. Kaste JM, Heimsath AM, Bostick BC (2007) Short-term soil mixing quantified with fallout radionuclides. Geology 35:243–246. doi: 10.1130/G23355A.1 CrossRefGoogle Scholar
  47. Kendall C (1998) Tracing nitrogen sources and cycling in catchments. In: Kendall C, McDonnell J (eds) Isotope tracers in catchment hydrology. Elsevier, Amsterdam, pp 519–578Google Scholar
  48. Kerley SJ, Jarvis SC (1997) Variation in 15N natural abundance of soil, humic fractions and plant materials in a disturbed and an undisturbed grassland. Biol Fert Soil 24:147–152CrossRefGoogle Scholar
  49. Kitayama K, Iwamoto K (2001) Patterns of natural 15N abundance in the leaf-to-soil continuum of tropical rain forests differing in N availability on Mount Kinabalu, Borneo. Plant Soil 229:203–212. doi: 10.1023/A:1004853915544 CrossRefGoogle Scholar
  50. Koba K, Tokuchi N, Yoshioka T et al (1998) Natural abundance of 15N in a forest soil. Soil Sci Soc Am J 62:778–781Google Scholar
  51. Kramer MG, Sollins P, Sletten RS, Swart PK (2003) N isotope fractionation and measures of organic matter alteration during decomposition. Ecology 84:2021–2025. doi: 10.1890/02-3097 CrossRefGoogle Scholar
  52. Kramer MG, Sollins P, Sletten RS (2004) Soil carbon dynamics across a windthrow disturbance sequence in southeast Alaska. Ecology 85:2230–2244. doi: 10.1890/02-4098 CrossRefGoogle Scholar
  53. Ledgard SF, Freney JR, Simpson JR (1984) Variations in natural enrichment of 15N in the profiles of some Australian pasture soils. Aust J Soil Res 22:155–164. doi: 10.1071/SR9840155 CrossRefGoogle Scholar
  54. Lee KE, Foster RC (1991) Soil fauna and soil structure. Aust J Soil Res 29:745–775. doi: 10.1071/SR9910745 CrossRefGoogle Scholar
  55. Lindahl BD, Ihrmark K, Boberg J et al (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 160:255–272Google Scholar
  56. Mariotti A, Pierre D, Vedy JC et al (1980) The abundance of natural nitrogen 15 in the organic matter of soils along an altitudinal gradient (Chablais, Haute Savoie, France). Catena 7:293–300Google Scholar
  57. Mariotti A, Germon JC, Hubert P et al (1981) Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62:413–430. doi: 10.1007/BF02374138 CrossRefGoogle Scholar
  58. Martinelli LA, Piccolo MC, Townsend AR et al (1999) Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65Google Scholar
  59. Melillo JM, Aber JD, Linkins AE et al (1989) Carbon and nitrogen dynamics along the decay continuum—plant litter to soil organic matter. Plant Soil 115:189–198. doi: 10.1007/BF02202587 CrossRefGoogle Scholar
  60. Michelsen A, Schmidt IK, Jonasson S et al (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. doi: 10.1007/BF00328791 CrossRefGoogle Scholar
  61. 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 115:406–418. doi: 10.1007/s004420050535 CrossRefGoogle Scholar
  62. Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning. Chapman and Hall, New York, pp 357–423Google Scholar
  63. Moore JC, McCann K, de Ruiter PC (2005) Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia (Jena) 49:499–510. doi: 10.1016/j.pedobi.2005.05.008 CrossRefGoogle Scholar
  64. Nadelhoffer KF, Fry B (1988) Controls on natural 15N and 13C abundances in forest soil organic-matter. Soil Sci Soc Am J 52:1633–1640Google Scholar
  65. Nadelhoffer KJ, Colman BP, Currie WS et al (2004) Decadal-scale fates of 15N tracers added to oak and pine stands under ambient and elevated N inputs at the Harvard Forest (USA). For Ecol Manag 196:89–107CrossRefGoogle Scholar
  66. Nardoto GB (2005) Abundância natural de 15N na Amazônia e Cerrado—implicações para a ciclagem de nitrogênio. PhD thesis, Universidade de São PauloGoogle Scholar
  67. 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. Springer, Berlin, pp 93–115Google Scholar
  68. Pardo LH, Hemond HF, Montoya JP et al (2002) Response of the natural abundance of 15N in forest soils and foliage to high nitrate loss following clear-cutting. Can J Res 32:1126–1136. doi: 10.1139/x02-041 CrossRefGoogle Scholar
  69. Pardo LH, Templer PH, Goodale CL et al (2006) Regional assessment of N saturation using foliar and root δ15N. Biogeochemistry 80:143–171. doi: 10.1007/s10533-006-9015-9 CrossRefGoogle Scholar
  70. Pardo LH, Hemond HF, Montoya JP, Pett-Ridge J (2007) Natural abundance 15N in soil and litter across a nitrate-output gradient in New Hampshire. For Ecol Manag 251:217–230CrossRefGoogle Scholar
  71. Perez T, Trumbore SE, Tyler SC et al (2000) Isotopic variability of N2O emissions from tropical forest soils. Global Biogeochem Cycles 14:525–535. doi: 10.1029/1999GB001181 CrossRefGoogle Scholar
  72. Ponsard S, Arditi R (2000) What can stable isotopes (δ15N and δ13C) tell about the food web of soil macro-invertebrates? Ecology 81:852–864Google Scholar
  73. Pörtl K, Zechmeister-Boltenstern S, Wanek W et al (2007) Natural 15N abundance of soil N pools and N2O reflect the nitrogen dynamics of forest soils. Plant Soil 295:79–94. doi: 10.1007/s11104-007-9264-y CrossRefGoogle Scholar
  74. Quideau SA, Graham RC, Feng X, Chadwick OA (2003) Natural isotopic distribution in soil surface horizons differentiated by vegetation. Soil Sci Soc Am J 67:1544–1550Google Scholar
  75. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391. doi: 10.1007/BF01972080 CrossRefGoogle Scholar
  76. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162. doi: 10.1016/S0169-5347(00)02098-X CrossRefGoogle Scholar
  77. Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602. doi: 10.1890/03-8002 CrossRefGoogle Scholar
  78. Schmidt S, Stewart GR (1997) Waterlogging and fire impacts on nitrogen availability and utilization in a subtropical wet heathland (wallum). Plant Cell Environ 20:1231–1241. doi: 10.1046/j.1365-3040.1997.d01-20.x CrossRefGoogle Scholar
  79. Schuur EAG, Matson PA (2001) Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431–442. doi: 10.1007/s004420100671 CrossRefGoogle Scholar
  80. Shearer G, Kohl DH (1986) N2-fixation in field settings—estimations based on natural 15N abundance. Aust J Plant Physiol 13:699–756Google Scholar
  81. Silfer JA, Engel MH, Macko SA (1992) Kinetic fractionation of stable carbon and nitrogen isotopes during peptide bond hydrolysis: experimental evidence and geochemical implications. Chem Geol 101:211–221Google Scholar
  82. Silver WL, Neff J, McGroddy M et al (2000) Effects of soil texture on belowground carbon and nutrient storage in a lowland Amazonian forest ecosystem. Ecosystems (N Y, Print) 3:193–209. doi: 10.1007/s100210000019 CrossRefGoogle Scholar
  83. Sollins P, Swanston C, Kleber M et al (2006) Organic C and N stabilization in a forest soil: evidence from sequential density fractionation. Soil Biol Biochem 38:3313–3324. doi: 10.1016/j.soilbio.2006.04.014 CrossRefGoogle Scholar
  84. Stehfest E, Bouwman L (2006) N2O and NO emission from agricultural fields and soils under natural vegetation: summarizing available measurement data and modeling of global annual emissions. Nutr Cycl Agroecosyst 74:207–228. doi: 10.1007/s10705-006-9000-7 CrossRefGoogle Scholar
  85. Taylor AFS, Alexander I (2005) The ectomycorrhizal symbiosis: life in the real world. Mycologist 19:102–112. doi: 10.1017/S0269915XO5003034 CrossRefGoogle Scholar
  86. Tiessen H, Karamanos RE, Stewart JWB, Selles F (1984) Natural nitrogen-15 abundance as an indicator of soil organic matter transformations in native and cultivated soils. Soil Sci Soc Am J 48:312–315CrossRefGoogle Scholar
  87. Vervaet H, Boeckx P, Unamuno V et al (2002) Can δ15N profiles in forest soils predict NO3 loss and net N mineralization rates? Biol Fertil Soils 36:143–150. doi: 10.1007/s00374-002-0512-2 CrossRefGoogle Scholar
  88. Wada E, Imaizumi R, Takai Y (1984) Natural abundance of 15N in soil organic-matter with special reference to paddy soils in Japan–biogeochemical implications on the nitrogen-cycle. Geochem J 18:109–123Google Scholar
  89. Wallenda T, Kottke I (1998) Nitrogen deposition and ectomycorrhizas. New Phytol 139:169–187CrossRefGoogle Scholar
  90. Wallenda T, Stober C, Högbom L (2000) Nitrogen uptake processes in roots and mycorrhizas. In: Schulze E-D et al (eds) Carbon and nitrogen physiology in forest ecosystems. Springer, Berlin, pp 122–143Google Scholar
  91. Yoo K, Amundson R, Heimsath AM, Dietrich WE (2005) Process-based model linking pocket gopher (Thomomys bottae) activity to sediment transport and soil thickness. Geology 33:917–920. doi: 10.1130/G21831.1 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Complex Systems Research CenterUniversity of New HampshireDurhamUSA

Personalised recommendations