, Volume 160, Issue 3, pp 589–599 | Cite as

Distribution of nitrogen-15 tracers applied to the canopy of a mature spruce-hemlock stand, Howland, Maine, USA

  • David Bryan Dail
  • David Y. Hollinger
  • Eric A. Davidson
  • Ivan Fernandez
  • Herman C. Sievering
  • Neal A. Scott
  • Elizabeth Gaige
Global Change Ecology - Original Paper


In N-limited ecosystems, fertilization by N deposition may enhance plant growth and thus impact C sequestration. In many N deposition–C sequestration experiments, N is added directly to the soil, bypassing canopy processes and potentially favoring N immobilization by the soil. To understand the impact of enhanced N deposition on a low fertility unmanaged forest and better emulate natural N deposition processes, we added 18 kg N ha−1 year−1 as dissolved NH4NO3 directly to the canopy of 21 ha of spruce-hemlock forest. In two 0.3-ha subplots, the added N was isotopically labeled as 15NH4 + or 15NO3 (1% final enrichment). Among ecosystem pools, we recovered 38 and 67% of the 15N added as 15NH4 + and 15NO3 , respectively. Of 15N recoverable in plant biomass, only 3–6% was recovered in live foliage and bole wood. Tree twigs, branches, and bark constituted the most important plant sinks for both NO3 and NH4 +, together accounting for 25–50% of 15N recovery for these ions, respectively. Forest floor and soil 15N retention was small compared to previous studies; the litter layer and well-humified O horizon were important sinks for NH4 + (9%) and NO3 (7%). Retention by canopy elements (surfaces of branches and boles) provided a substantial sink for N that may have been through physico-chemical processes rather than by N assimilation as indicated by poor recoveries in wood tissues. Canopy retention of precipitation-borne N added in this particular manner may thus not become plant-available N for several years. Despite a large canopy N retention potential in this forest, C sequestration into new wood growth as a result of the N addition was only ~16 g C m−2 year−1 or about 10% above the current net annual C sequestration for this site.


Nitrogen-15 Nitrate Ammonium Nitrogen deposition Carbon sequestration Forest elemental cycling 



We thank the International Paper Company, and GMO, LLC for providing access to the research site in Howland, Maine. We also thank our technical support staff; Mr. John Lee, Ms. Holly Hughes, Mr. Charles Rodrigues and George Sharard, and undergraduates; Mr. David Dunston, Ms. Nell Burger and Ms. Gretchen Miles; Department of Energy (DOE) SURE program interns who worked on this project. This research was supported by the Office of Science (BER), U.S. Department of Energy Terrestrial Carbon Program, under Interagency Agreement no. DE-AI02-00ER63028 and through the Northeast Regional Center of the National Institute for Global Environmental Change under Cooperative Agreement nos. DE-FC02-03ER63613, DE-FC-03-90ER61010, and DE-FG02-00ER63002; and through the National Institute for Climatic Change Research agreement no. DE-FG02-06ER64157 and National Science Foundation (NSF) award no. 0223188. Financial support does not constitute an endorsement by the DOE or NSF of the views expressed in this article. This experiment was in compliance with the current laws of the state of Maine and the United States of America.


  1. Aber JD, Magill A, McNulty SG, Boone RD, Nadelhoffer KJ, Downs M, Hallett R (1995) Forest biogeochemistry and primary production altered by nitrogen saturation. Water Air Soil Pollut (Hist Arch) 85(3):1665–1670. doi: 10.1007/BF00477219 CrossRefGoogle Scholar
  2. Arthur MA, Fahey TJ (1993) Controls on soil solution chemistry in a subalpine forest in North-Central Colorado. Soil Sci Soc Am J 57:1122–1130Google Scholar
  3. Bowden RD, Geballe GT, Bowden WB (1989) Foliar uptake of 15N from simulated cloud water by red spruce (Picea rubens) seedlings. Can J For Res 19:382–386. doi: 10.1139/cjfr-19-3-382 CrossRefGoogle Scholar
  4. Boxman AW, van Dam D, van Dijk HFG, Hogervorst RF, Koopmans CJ (1995) Ecosystem response to reduced nitrogen and sulphur inputs into two coniferous forest stands in the Netherlands. For Ecol Manage 71:7–29CrossRefGoogle Scholar
  5. Boyce RL, Friedland AJ, Chamberlain CP, Poulson SR (1996) Direct canopy nitrogen uptake from 15N-labeled wet deposition by mature red spruce. Can J For Res 26:1539–1547. doi: 10.1139/cjfr-26-9-1539 CrossRefGoogle Scholar
  6. Brix H (1981) Effects of nitrogen fertilizer source and application rates on foliar nitrogen concentration, photosynthesis, and growth of Douglas-fir. Can J For Res 11:775–780. doi: 10.1139/cjfr-11-4-775 CrossRefGoogle Scholar
  7. Bubb KA, Xu ZH, Simpson JA, Safligna PG (1999) Growth response to fertilisation and recovery of 15N-labelled fertiliser by young hoop pine plantations of subtropical Australia. Nutr Cycl Agroecosyst 54(1):81–92CrossRefGoogle Scholar
  8. Buchmann N, Schultze E-D, Gebauer G (1995) 15N-ammonium and 15N-nitrate uptake of a 15-year-old Picea abies plantation. Oecologia 102:361–370. doi: 10.1007/BF00329803 CrossRefGoogle Scholar
  9. Buchmann N, Gebauer G, Schulze E-D (1996) Partitioning of 15N-labeled ammonium and nitrate among soil, litter, below- and above-ground biomass of trees and understory in a 15-year-old Picea abies plantation. Biogeochemistry 33:1–23. doi: 10.1007/BF00000967 CrossRefGoogle Scholar
  10. Cole DW (1981) Nitrogen uptake and translocation by forest ecosystems. In: Clark FE (ed) Terrestrial nitrogen cycles. Ecol Bull 33:219–232Google Scholar
  11. Cole D, Rapp M (1981) Elemental cycling in forest ecosystems. In: Reichle D (ed) Dynamic properties of forest ecosystems. International Biological Programme, vol 23. Cambridge University Press, Cambridge, pp 341–409Google Scholar
  12. Currie WS, Nadelhoffer KJ, Aber JD (2004) Redistributions of 15N highlight turnover and replenishment of mineral soil organic N as a long-term control on forest C balance. For Ecol Manage 196:109–127CrossRefGoogle Scholar
  13. Dominé F, Shepson PB (2002) Air-snow interactions and atmospheric chemistry. Science 297(5586):1506–1510PubMedCrossRefGoogle Scholar
  14. Eilers J, Brumme R, Matzner E (1992) Uptake of labelled N by spruce trees. For Ecol Manage 51:239–249CrossRefGoogle Scholar
  15. Emmett BA, Brittain SA, Hughes S, Görres J, Kennedy V, Norris D, Rafarel R, Reynolds B, Stevens PA (1995) Nitrogen additions (NaNO3 and NH4NO3) at Aber Forest, Wales. I. Response of throughfall and soil water chemistry. For Ecol Manage 71:45–59. doi: 10.1016/0378-1127(94)06083-U CrossRefGoogle Scholar
  16. Fenn ME, Poth MA, Aber JD, Baron JS, Bormann BT, Johnson DW, Lemly DA, McNulty SG, Ryan DF, Stottlemyer R (1998) Nitrogen excess in North American ecosystems: predisposing factors, ecosystem responses, and management strategies. Ecol Appl 8(3):706–733. doi: 10.2307/2641261 CrossRefGoogle Scholar
  17. Fernandez IJ, Lawrence GB, Richards KJ (1990) Characteristics of foliar chemistry in a commercial spruce-fir stand of northern New England USA. Plant Soil 125:288–292. doi: 10.1007/BF00010668 CrossRefGoogle Scholar
  18. Friedland AJ, Miller EK, Battles JJ, Thorne JF (1991) Nitrogen deposition, distribution and cycling in a subalpine spruce-fir forest in the Adirondacks, New York, USA. Biogeochemistry 14(1):31–55. doi: 10.1007/BF00000885 CrossRefGoogle Scholar
  19. Gaige E, Dail DB, Hollinger DY, Davidson EA, Lee JT, Fernandez IF, Sievering H, Rodrigues C, Hughes H, White A, Halteman W (2007) Changes in canopy processes following whole-forest canopy nitrogen fertilization of a mature spruce-hemlock forest. Ecosystems. doi: 10.1007/s10021-007-9081-4
  20. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland C, Green P, Holland E, Karl DM, Michaels AF, Porter JH, Townsend A, Vorosmarty C (2004) Nitrogen cycles: past, present and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  21. Hättenschwiler S, Körner C (1998) Biomass allocation and canopy development in spruce model ecosystems under elevated CO2 and increased N deposition. Oecologia 113:104–114. doi: 10.1007/s004420050358 CrossRefGoogle Scholar
  22. Holland EA, Braswell BH, Lamarque J-F, Townsend A, Sulzman J, Müller J-F, Dentener F, Brasseur G, Levy II H, Penner JE, Roelofs GJ (1997) Variations in the predicted spatial distribution of atmospheric nitrogen deposition and their impact on carbon uptake by terrestrial ecosystems. J Geophys Res 102(D13):15,849–15,866. doi: 10.1029/96JD03164
  23. Hollinger DY, Goltz SM, Davidson EA, Lee JT, Tu K, Valentine HT (1999) Seasonal patterns and environmental control of carbon dioxide and water vapor exchange in an ecotonal boreal forest. Glob Change Biol 5:891–902CrossRefGoogle Scholar
  24. Hollinger DY, Aber J, Dail B, Davidson EA, Goltz SM, Hughes H, Leclerc MY, Lee JT, Richardson AD, Rodrigues C, Scott NA, Achuatavarier D, Walsh J (2004) Spatial and temporal variability in forest–atmosphere CO2 exchange. Glob Change Biol 10:1689–1706CrossRefGoogle Scholar
  25. Jenkins JC, Chojnacky DC, Heath LS, Birdsey RA (2003) National-scale biomass estimators for United States tree species. For Sci 49:12–35Google Scholar
  26. Jenkinson D, Goulding K, Powlson D (1999) Comment: nitrogen deposition and carbon sequestration. I. Nature 400:629CrossRefGoogle Scholar
  27. Johnson DW, Lindberg S (eds) (1992) Atmospheric deposition and forest nutrient cycling. Springer, New York, p 486Google Scholar
  28. Kahl JS, Norton SA, Fernandez IJ, Nadelhoffer KJ, Driscoll CT, Aber JD (1993) Experimental inducement of nitrogen saturation at the watershed scale. Environ Sci Technol 27:565–568. doi: 10.1021/es00040a017 CrossRefGoogle Scholar
  29. Lang GE, Reiners WA, Heier RK (1976) Potential alteration of precipitation chemistry by epiphytic lichens. Oecologia 25:229–241. doi: 10.1007/BF00345100 CrossRefGoogle Scholar
  30. Lawrence GB, Fernandez IJ (1991) Biogeochemical effects of acidic deposition on a low elevation spruce-fir stand in Howland, Maine. Can J For Res 21:867–875. doi: 10.1139/cjfr-21-6-867 CrossRefGoogle Scholar
  31. Magnani F, Mencuccini M, Borghetti M, Berbigier P, Berninger F, Delzon S, Grelle A, Hari P, Jarvis PG, Kolari P, Kowalski AS, Lankreijer H, Law BE, Lindroth A, Loustau D, Manca G, Moncrieff JB, Rayment M, Tedeschi V, Valentini R, Grace J (2007) The human footprint in the carbon cycle of temperate and boreal forests. Nature 447:849–851. doi: 10.1038/nature05847 CrossRefGoogle Scholar
  32. McLaughlin JW, Fernandez I, Richards K (1996) Atmospheric deposition to a low-elevation spruce-fir forest, Maine, USA. J Environ Qual 25:248–259CrossRefGoogle Scholar
  33. McNulty SG, Aber JD (1993) Effects of chronic nitrogen additions on nitrogen cycling in a high-elevation spruce-fir stand. Can J For Res 23:1252–1263CrossRefGoogle Scholar
  34. Meyer MM, Tukey HB (1965) Nitrogen, phosphorus, and potassium plant reserves and the spring growth of Taxus and Forsythia. Proc Am Soc Hortic Sci 87:537–544Google Scholar
  35. Nadelhoffer KJ, Fry B (1994) In: Lajtha K, Michener R (eds) Stable isotopes in ecology. Blackwell, Oxford, pp 22–44Google Scholar
  36. Nadelhoffer KJ, Downs MR, Fry B, Aber JD, Magill AH, Melillo JM (1995) The fate of 15N-labelled nitrate additions to a northern hardwood forest in eastern Maine, USA. Oecologia 103:292–301. doi: 10.1007/BF00328617 CrossRefGoogle Scholar
  37. Nadelhoffer KJ, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans CJ, Schleppi P, Tietema A, Wright RF (1999a) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148. doi: 10.1038/18205 CrossRefGoogle Scholar
  38. Nadelhoffer KJ, Downs MR, Fry B (1999b) Sinks for N-15 enriched additions to an oak forest and a red pine plantation. Ecol Appl 9:72–86. doi: 10.1139/cjfr-23-7-1252 CrossRefGoogle Scholar
  39. Nadelhoffer KJ, Downs MR, Fry B, Magill AH, Aber JD (1999c) Controls on N retention and exports in a forested watershed. Environ Monit Assess 55:187–210. doi: 10.1023/A:1006190222768 CrossRefGoogle Scholar
  40. Nadelhoffer KJ, Colman BP, Currie WS, Magill A, Aber JD (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 Manage 196:89–107. doi: 10.1016/j.foreco.2004.03.014 CrossRefGoogle Scholar
  41. Nixon SW, Ammerman JW, Atkinson LP, Berounsky VM, Billen G, Boicourt WC, Boyton WR, Church TM, Ditoro DM, Elmgren R, Garber JH, Giblin AE, Jahnke RA, Owens PJ, Pilson MEQ, Seitzinger SP (1996) The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry 35:141–180. doi: 10.1007/BF02179826 CrossRefGoogle Scholar
  42. Pepper DA, Del Grosso RE, McMurtrie RE, Parton WJ (2005) Simulated carbon sink response of shortgrass steppe, tallgrass prairie and forest ecosystems to rising [CO2], temperature and nitrogen input. Glob Biogeochem Cycl 19:GB1004. doi: 0.1029/2004GB002226
  43. Piatek KB, Mitchell MJ, Silva SR, Kendall C (2005) Sources of nitrate in snowmelt discharge: evidence from water chemistry and stable isotopes of nitrate. Water Air Soil Pollut 154(1):13–35. doi: 10.1007/s11270-005-4641-8 CrossRefGoogle Scholar
  44. Pregitzer KS, Dickmann DI, Hendrick R, Nguyen PV (1990) Whole-tree carbon and nitrogen partitioning in young hybrid poplars. Tree Physiol 7:79–92PubMedGoogle Scholar
  45. Pregitzer KS, Burton AJ, Zak DR, Talhelm AF (2008) Simulated chronic nitrogen deposition increases carbon storage in northern temperate forests. Glob Chang Biol 14:142–153Google Scholar
  46. Proe MF, Millard P (1995) Effect of N supply upon the seasonal partitioning of N and P uptake in young Sitka spruce (Picea sitchensis). Can J For Res 25:1704–1709. doi: 10.1139/cjfr-25-10-1704 CrossRefGoogle Scholar
  47. Reiners WA, Olson RK (1984) Effects of canopy components on throughfall chemistry: an experimental analysis. Oecologia 63:320–330. doi: 10.1007/BF00390660 CrossRefGoogle Scholar
  48. Schindler D, Bayley S (1993) The biosphere as an increasing sink for atmospheric carbon: estimates from increased nitrogen deposition. Glob Biogeochem Cycl 7:717–733CrossRefGoogle Scholar
  49. Schleppi P, Bucher-Wallin I, Siegwolf R, Saurer M, Muller N, Bucher JB (1999) Simulation of increased nitrogen deposition to a montane forest ecosystem: partitioning of the added 15 N. Water Air Soil Pollut 116:129–134. doi: 10.1023/A:1005206927764 CrossRefGoogle Scholar
  50. Scott N, Rodrigues CA, Hughes H, Lee JT, Davidson EA, Dail DB, Malerba P, Hollinger DY (2004) Changes in carbon storage and net carbon exchange one year after an initial shelterwood harvest at Howland Forest, ME. Environ Manage 33(1):S9–S22CrossRefGoogle Scholar
  51. Sievering H (1999) Comment: nitrogen deposition and carbon sequestration. II. Nature 400:629–630. doi: 10.1038/23176 CrossRefGoogle Scholar
  52. Sievering H, Fernandez I, Lee J, Hom J, Rustad L (2000) Forest canopy uptake of atmospheric nitrogen deposition at eastern US conifer sites: carbon storage implications? Glob Biogeochem Cycl 14:1153–1160. doi: 10.1029/1999GB001250 Google Scholar
  53. Sievering H, Kelly T, McConville G, Seibold C, Turnipseed A (2001) Nitric acid dry deposition to conifer forests: Niwot Ridge spruce-fir-pine study. Atmos Environ 35:3851–3859CrossRefGoogle Scholar
  54. Tamm CO (1991) Nitrogen in terrestrial ecosystems: questions of productivity, vegetational changes, and ecosystem stability. Ecol Stud 81. doi: 10.2307/2260680
  55. Templer PH, Lovett GM, Weathers KC, Findlay SE, Dawson TE (2005) Influence of tree species on forest nitrogen retention in the Catskill mountains, New York, USA. Ecosystems 8:1–16. doi: 10.1007/s10021-004-0230-8 CrossRefGoogle Scholar
  56. Townsend AR, Braswell BH, Holland EA, Penner JE (1996) Spatial and temporal patterns in terrestrial carbon storage due to deposition of fossil fuel nitrogen. Ecol Appl 6:806–814CrossRefGoogle Scholar
  57. UNEP and WHRC (2007) Reactive nitrogen in the environment: too much or too little of a good thing. In: Davidson EA, Arden-Clarke C, Braun E (eds) The United Nations Environment Programme, ParisGoogle Scholar
  58. USDA Forest Service FIA program. http://fia.fs.fed.us/program-features/basic-forest-inventory. Accessed January 2009)
  59. USEPA (2004) CASTNET/NADP program, Howland, Maine, USA. http://www.epa.gov/castnet/sites/how132.html. Accessed January 2009)
  60. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  61. Vose JM, Swank WT (1990) Preliminary estimates of foliar absorption of 15N-labeled nitric acid vapor (NHO3) by mature eastern white pine (Pinus strobes). Can J For Res 20:857–860CrossRefGoogle Scholar
  62. Wetzel S, Greenwood JS (1989) Proteins as a potential nitrogen storage compound in bark and leaves of several softwoods. Trees 3:149–153CrossRefGoogle Scholar
  63. Wright RF, Tietema A (1995) Ecosystem response to 9 years of nitrogen addition at Songndal, Norway. For Ecol Manage 71:133–142CrossRefGoogle Scholar
  64. Young HE, Ribe JH, Wainwright K (1980) Weight tables for tree and shrub species in Maine. University of Maine Life Sciences and Agricultural Experimental Station. Miscellaneous report 230. University of Maine, Orono, p 84Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • David Bryan Dail
    • 1
  • David Y. Hollinger
    • 2
  • Eric A. Davidson
    • 3
  • Ivan Fernandez
    • 1
  • Herman C. Sievering
    • 4
  • Neal A. Scott
    • 5
  • Elizabeth Gaige
    • 1
  1. 1.The University of MaineOronoUSA
  2. 2.USDA-Forest ServiceWashingtonUSA
  3. 3.The Woods Hole Research CenterFalmouthUSA
  4. 4.University of ColoradoDenverUSA
  5. 5.Queen’s UniversityKingstonCanada

Personalised recommendations