, Volume 16, Issue 6, pp 980–1001 | Cite as

Nitrogen Addition Increases Carbon Storage in Soils, But Not in Trees, in an Eastern U.S. Deciduous Forest

  • Gary M. LovettEmail author
  • Mary A. Arthur
  • Kathleen C. Weathers
  • Ross D. Fitzhugh
  • Pamela H. Templer


Forest ecosystems in most industrialized and agricultural regions receive elevated rates of atmospheric nitrogen (N) deposition from air pollution. To evaluate the effects of excess N deposition on carbon (C) and N cycling, we experimentally added N (as NH4NO3) to naturally-occurring, single-species plots of five different tree species that are common in the Northern Hardwood forests of northeastern North America: sugar maple (Acer saccharum Marsh), American beech (Fagus grandifolia Ehrh.), yellow birch (Betula alleghaniensis Britton), eastern hemlock (Tsuga canadensis (L.) Carr), and northern red oak (Quercus rubra L.). The experiment was performed in the Catskill Mountains of southeastern New York State, USA, and used a paired-plot design with six replicate plots per species. After 6 years of treatment, most species showed increases in foliar N concentrations in N-treated plots, but only for maple and birch were those increases statistically significant. No significant effects of the N treatment were observed on woody biomass increment or aboveground net primary production (ANPP) for any species. In the oak plots, the N treatment increased acorn production in mast years. In the soils, the N treatment was associated with a significant decline in potential N mineralization and nitrification rates in the mineral horizon but not in the forest floor, and in the mineral horizon the effect of the N treatment varied among species. The N treatment caused a significant increase in C stock, N stock and C:N ratio in the forest floor, with the largest effect in the hemlock plots. Nitrate leaching increased significantly in treated plots compared to controls. Dissolved organic carbon (DOC) in soil solution was unaffected by the N treatment, but the variation in DOC across plots was correlated with the C stock in the forest floor. These results suggest that the ANPP of these forests is not limited by N availability, but that excess N may cause accumulations of C in the forest floor, particularly in hemlock stands, perhaps through inhibition of decomposition rates or by altering phenolic chemistry of the litter. The magnitude, and sometimes the direction of the N treatment responses varied among species, suggesting that predictions of forest responses to elevated N deposition should take into account spatial and temporal variation in tree species composition.

Key words

forest nitrogen deposition carbon nitrogen fertilization Catskill mountains 



We thank the US Department of Agriculture National Research Initiative, the National Science Foundation (DEB9981503 and DEB0444895), the USDA Forest Service Northeastern States Research Cooperative, and the A.W. Mellon Foundation for support for this work. We are grateful to the many students and research assistants who have helped with this work over the years, especially Chuck Schirmer, Jake Griffin, Brent Mellen, Jessica Hancock, Greg Abernathy, Miriam Osredkar, Margaret Ward, and Milinda Hamilton. We thank Dr. Jack Schultz for analysis of phenolic concentrations in litter.


  1. Aber JD, Ollinger SV, Driscoll CT. 1997. Modeling nitrogen saturation in forest ecosystems in response to land use and atmospheric deposition. Ecol Model 101:61–78.CrossRefGoogle Scholar
  2. Appel HM, Govenor HL, D’Ascenzo M, Siska E, Schultz JC. 2001. Limitations of Folin assays of foliar phenolics in ecological studies. J Chem Ecol 27:761–78.PubMedCrossRefGoogle Scholar
  3. Batesmith EC. 1977. Astringency of leaves. 1. Astringent tannins of Acer species. Phytochemistry 16:1421–6.CrossRefGoogle Scholar
  4. Bedison JE, McNeil BE. 2009. Is the growth of temperate forest trees enhanced along an ambient nitrogen deposition gradient? Ecology 90:1736–42.PubMedCrossRefGoogle Scholar
  5. Berg B, Dise N. 2004. Calculating the long-term stable nitrogen sink in northern European forests. Acta Oecol: Intl J Ecol 26:15–21.CrossRefGoogle Scholar
  6. Berg B, McClaugherty C, De Santo AV, Johnson D. 2001. Humus buildup in boreal forests: effects of litter fall and its N concentration. Can J For Res/Rev Can Rech For 31:988–98.CrossRefGoogle Scholar
  7. Callahan HS, Del Fierro K, Patterson AE, Zafar H. 2008. Impacts of elevated nitrogen inputs on oak reproductive and seed ecology. Glob Chang Biol 14:285–93.CrossRefGoogle Scholar
  8. Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF. 2000. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–65.CrossRefGoogle Scholar
  9. Christenson LM, Lovett GM, Weathers KC, Arthur MA. 2009. The influence of tree species, nitrogen fertilization, and soil C to N ratio on gross soil nitrogen transformations. Soil Sci Soc Am J 73:638–46.CrossRefGoogle Scholar
  10. Crowley KF, McNeil BE, Lovett GM, Canham CD, Driscoll CT, Rustad LE, Denny E, Hallett RA, Arthur MA, Boggs JL, Goodale CL, Kahl JS, McNulty SG, Ollinger SV, Pardo LH, Schaberg PG, Stoddard JL, Weand MP, Weathers KC. 2012. Do nutrient limitation patterns shift from nitrogen toward phosphorus with increasing nitrogen deposition across the northeastern United States? Ecosystems 15:940–57.CrossRefGoogle Scholar
  11. Dail DB, Hollinger DY, Davidson EA, Fernandez I, Sievering HC, Scott NA, Gaige E. 2009. Distribution of nitrogen-15 tracers applied to the canopy of a mature spruce-hemlock stand, Howland, Maine, USA. Oecologia 160:589–99.PubMedCrossRefGoogle Scholar
  12. de Vries W, Solberg S, Dobbertin M, Sterba H, Laubhahn D, Reinds GJ, Nabuurs GJ, Gundersen P, Sutton MA. 2008. Ecologically implausible carbon response? Nature 451:E1–3.PubMedCrossRefGoogle Scholar
  13. de Vries W, Solberg S, Dobbertin M, Sterba H, Laubhann D, van Oijen M, Evans C, Gundersen P, Kros J, Wamelink GWW, Reinds GJ, Sutton MA. 2009. The impact of nitrogen deposition on carbon sequestration by European forests and heathlands. For Ecol Manage 258:1814–23.CrossRefGoogle Scholar
  14. DeForest JL, Zak DR, Pregitzer KS, Burton AJ. 2004. Atmospheric nitrate deposition and the microbial degradation of cellobiose and vanillin in a northern hardwood forest. Soil Biol Biochem 36:965–71.CrossRefGoogle Scholar
  15. Dise NB, Wright RF. 1995. Nitrogen leaching from European forests in relation to nitrogen deposition. For Ecol Manage 71:153–61.CrossRefGoogle Scholar
  16. Driese KL, Reiners WA, Lovett GM, Simkin SM. 2004. A vegetation map for the Catskill Park, NY, derived from multi-temporal landsat imagery and GIS data. Northeast Nat 11:421–42.CrossRefGoogle Scholar
  17. Driscoll CT, Whitall D, Aber J, Boyer E, Castro M, Cronan C, Goodale CL, Groffman P, Hopkinson C, Lambert K, Lawrence G, Ollinger S. 2003. Nitrogen pollution in the northeastern United States: sources, effects, and management options. Bioscience 53:357–74.CrossRefGoogle Scholar
  18. Evans C, Goodale C, Caporn S, Dise N, Emmett B, Fernandez I, Field C, Findlay S, Lovett G, Meesenburg H, Moldan F, Sheppard L. 2008. Does elevated nitrogen deposition or ecosystem recovery from acidification drive increased dissolved organic carbon loss from upland soil? A review of evidence from field nitrogen addition experiments. Biogeochemistry 91:13–35.CrossRefGoogle Scholar
  19. Federer CA. 1995. Brook 90: a simulation model for evaporation, soil water, and streamflow. Version 3.25. USDA Forest Service, Durham, NH.Google Scholar
  20. Finzi AC, Van Breemen N, Canham CC. 1998. Canopy tree-soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8:440–6.Google Scholar
  21. Fitzhugh RD, Driscoll CT, Groffman PM, Tierney GL, Fahey TJ, Hardy JP. 2001. Effects of soil freezing disturbance on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem. Biogeochemistry 56:215–38.CrossRefGoogle Scholar
  22. Gee GW, Bauder JW. 1986. Particle size analysis. Agron Monogr 9:383–411.Google Scholar
  23. Hagerman AE, Klucher KM. 1986. Tannin–protein interactions. In: Cody V, Middleton E, Harborne J, Eds. Plant flavonoids in biology and medicine: biochemical pharmacological and structure activity relationships. New York: Alan R. Liss. p 67–76.Google Scholar
  24. Hancock JE, Arthur MA, Weathers KC, Lovett GM. 2008. Carbon cycling along a gradient of beech bark disease impact in the Catskill Mountains, New York. Can J For Res/Rev Can Rech For 38:1267–74.CrossRefGoogle Scholar
  25. Hartzfeld PW, Forkner R, Hunter MD, Hagerman AE. 2002. Determination of hydrolyzable tannins (gallotannins and ellagitannins) after reaction with potassium iodate. J Agric Food Chem 50:1785–90.PubMedCrossRefGoogle Scholar
  26. Holland EA, Braswell BH, Lamarque JF, Townsend A, Sulzman J, Muller JF, Dentener F, Brasseur G, Levy 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: Atmospheres 102:15849–66.CrossRefGoogle Scholar
  27. Huttunen L, Aphalo PJ, Lehto T, Niemela P, Kuokkanen K, Kellomaki S. 2009. Effects of elevated temperature, elevated CO2 and fertilization on quality and subsequent decomposition of silver birch leaf litter. Soil Biol Biochem 41:2414–21.CrossRefGoogle Scholar
  28. Hyvonen R, Persson T, Andersson S, Olsson B, Agren GI, Linder S. 2008. Impact of long-term nitrogen addition on carbon stocks in trees and soils in northern Europe. Biogeochemistry 89:121–37.CrossRefGoogle Scholar
  29. Institute SAS. 1989. SAS/STAT User’s Guide, Version 6. Cary, NC: SAS Institute, Inc.Google Scholar
  30. Iverson LR, Prasad AM, Matthews SN, Peters M. 2008. Estimating potential habitat for 134 eastern US tree species under six climate scenarios. For Ecol Manage 254:390–406.CrossRefGoogle Scholar
  31. Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G, Papale D, Piao SL, Schulze ED, Tang J, Law BE. 2010. Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–22.CrossRefGoogle Scholar
  32. Jenkins JC, Chojnacky DC, Heath LS, Birdsey RA. 2004. Comprehensive database of diameter-based biomass regressions for North American tree species. Newtown Square, PA: USDA Forest Service, Northeastern Research Station.Google Scholar
  33. Johnson DW. 1992. Nitrogen retention in forest soils. J Environ Qual 21:1–12.CrossRefGoogle Scholar
  34. Jones CG, Ostfeld RS, Richard MP, Schauber EM, Wolff JO. 1998. Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease. Science 279:1023–6.PubMedCrossRefGoogle Scholar
  35. King JS, Pregitzer KS, Zak DR, Kubiske ME, Holmes WE. 2001. Correlation of foliage and litter chemistry of sugar maple, Acer saccharum, as affected by elevated CO2 and varying N availability, and effects on decomposition. Oikos 94:403–16.CrossRefGoogle Scholar
  36. Kraus TEC, Dahlgren RA, Zasoski RJ. 2003. Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil 256:41–66.CrossRefGoogle Scholar
  37. Lewis GP, Likens GE. 2000. Low stream nitrate concentrations associated with oak forests on the Allegheny High Plateau of Pennsylvania. Wat Resour Res 36:3091–4.CrossRefGoogle Scholar
  38. Liu LL, Greaver TL. 2010. A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–28.PubMedCrossRefGoogle Scholar
  39. Long ZT, Pendergast TH, Carson WP. 2007. The impact of deer on relationships between tree growth and mortality in an old-growth beech-maple forest. For Ecol Manage 252:230–8.CrossRefGoogle Scholar
  40. Lovett GM, Arthur MA, Weathers KC, Griffin JM. 2010. Long-term changes in forest carbon and nitrogen cycling caused by an introduced pest/pathogen complex. Ecosystems 13:1188–200.CrossRefGoogle Scholar
  41. Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD. 2006. Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405.CrossRefGoogle Scholar
  42. Lovett GM, Goodale CL. 2011. A new conceptual model of nitrogen saturation based on experimental nitrogen addition to an oak forest. Ecosystems 14:615–31.CrossRefGoogle Scholar
  43. Lovett GM, Lindberg SE. 1993. Atmospheric deposition and canopy interactions of nitrogen in forests. Can J For Res/Rev Can Rech For 23:1603–16.CrossRefGoogle Scholar
  44. Lovett GM, Mitchell MJ. 2004. Sugar maple and nitrogen cycling in the forests of eastern North America. Front Ecol Environ 2:81–8.CrossRefGoogle Scholar
  45. Lovett GM, Rueth H. 1999. Soil nitrogen transformations in beech and maple stands along a nitrogen deposition gradient. Ecol Appl 9:1330–44.CrossRefGoogle Scholar
  46. Lovett GM, Weathers KC, Arthur MA. 2002. Control of N loss from forested watersheds by soil carbon:nitrogen ratio and tree species composition. Ecosystems 5:712–18.CrossRefGoogle Scholar
  47. Lovett GM, Weathers KC, Arthur MA, Schultz JC. 2004. Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry 67:289–308.CrossRefGoogle Scholar
  48. Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P. 2004. Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA. For Ecol Manage 196:7–28.CrossRefGoogle Scholar
  49. 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 447:848–50.PubMedCrossRefGoogle Scholar
  50. McDowell WH, Magill AH, Aitkenhead-Peterson JA, Aber JD, Merriam JL, Kaushal SS. 2004. Effects of chronic nitrogen amendment on dissolved organic matter and inorganic nitrogen in soil solution. For Ecol Manage 196:29–41.CrossRefGoogle Scholar
  51. McIntosh RP. 1972. Forests of the Catskill Mountains, New York. Ecol Monogr 42:143–61.CrossRefGoogle Scholar
  52. McNulty SG, Boggs J, Aber JD, Rustad L, Magill A. 2005. Red spruce ecosystem level changes following 14 years of chronic N fertilization. For Ecol Manage 219:279–91.CrossRefGoogle Scholar
  53. Nadelhoffer KJ, Emmet B, Gundersen P, Kjonaas OJ, Koopmans CJ, Schlepp P, Tietema A, Wright RF. 1999. Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–8.CrossRefGoogle Scholar
  54. Nave LE, Vance ED, Swanston CW, Curtis PS. 2009. Impacts of elevated N inputs on north temperate forest soil C storage, C/N, and net N-mineralization. Geoderma 153:231–40.CrossRefGoogle Scholar
  55. Nowacki GJ, Abrams MD. 2008. The demise of fire and “Mesophication” of forests in the eastern United States. Bioscience 58:123–38.CrossRefGoogle Scholar
  56. Ollinger SV, Smith ML, Martin ME, Hallett RA, Goodale CL, Aber JD. 2002. Regional variation in foliar chemistry and N cycling among forests of diverse history and composition. Ecology 83:339–55.Google Scholar
  57. Ostfeld RS, Jones CG, Wolff JO. 1996. Of mice and mast: ecological connections in eastern deciduous forests. Bioscience 46:323–30.CrossRefGoogle Scholar
  58. Ostfeld RS, Keesing F. 2000. Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15:232–7.PubMedCrossRefGoogle Scholar
  59. Pregitzer KS, Burton AJ, Zak DR, Talhelm AF. 2008. Simulated chronic nitrogen deposition increases carbon storage in Northern Temperate forests. Glob Chang Biol 14:142–53.Google Scholar
  60. Rich JL. 1934. Glacial geology of the Catskill Mountains. New York State Museum Bull 299:1–180.Google Scholar
  61. Ross DS, Wemple BC, Jamison AE, Fredriksen G, Shanley JB, Lawrence GB, Bailey SW, Campbell JL. 2009. A cross-site comparison of factors influencing soil nitrification rates in northeastern USA forested watersheds. Ecosystems 12:158–78.CrossRefGoogle Scholar
  62. Schultz JC, Baldwin IT. 1982. Oak leaf quality declines in response to defoliation by gypsy-moth larvae. Science 217:149–50.PubMedCrossRefGoogle Scholar
  63. Stoddard JL, Murdoch PS. 1991. Catskill Mountains. In: Charles DF, Ed. Acidic deposition and aquatic ecosystems: regional case studies. New York: Springer. p 237–71.CrossRefGoogle Scholar
  64. Sutton MA, Simpson D, Levy PE, Smith RI, Reis S, van Oijen M, de Vries W. 2008. Uncertainties in the relationship between atmospheric nitrogen deposition and forest carbon sequestration. Glob Chang Biol 14:2057–63.CrossRefGoogle Scholar
  65. Swain T, Hillis WE. 1959. The phenolic constituents of Prunus domestica. I. The quantitative analysis of phenolic constituents. J Sci Food Agric 10:63–8.CrossRefGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. Templer PH, Mack MC, Chapin FSIII, Christenson LM, Compton JE, Crook HD, Currie WS, Curtis C, Dail B, D’Antonio CM, Emmett BA, Epstein H, Goodale CL, Gundersen P, Hobbie SE, Holland K, Hooper DU, Hungate BA, Lamontagne S, Nadelhoffer KJ, Osenberg CW, Perakis SS, Schleppi P, Schimel J, Schmidt IK, Sommerkorn M, Spoelstra J, Tietema A, Wessel WW, Zak DR. 2012. Sinks for nitrogen inputs in terrestrial ecosystems: a meta-analysis of enriched 15N field tracer studies. Ecology 93(8):1816–29.PubMedCrossRefGoogle Scholar
  68. Thomas RQ, Canham CD, Weathers KC, Goodale CL. 2010. Increased tree carbon storage in response to nitrogen deposition in the US. Nat Geosci 3:13–17.CrossRefGoogle Scholar
  69. Thornton PE, Doney SC, Lindsay K, Moore JK, Mahowald N, Randerson JT, Fung I, Lamarque JF, Feddema JJ, Lee YH. 2009. Carbon–nitrogen interactions regulate climate–carbon cycle feedbacks: results from an atmosphere–ocean general circulation model. Biogeosciences 6:2099–120.CrossRefGoogle Scholar
  70. Tornes LA. 1979. Soil survey of Ulster County. Syracuse, NY: USDA Soil Conservation Service.Google Scholar
  71. 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 6:806–14.CrossRefGoogle Scholar
  72. VanSoest PJ, Robertson JB, Lewis BA. 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–97.CrossRefGoogle Scholar
  73. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115.CrossRefGoogle Scholar
  74. Waldrop MP, Zak DR, Sinsabaugh RL, Gallo M, Lauber C. 2004. Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–7.CrossRefGoogle Scholar
  75. Wallace ZP, Lovett GM, Hart JE, Machona B. 2007. Effects of nitrogen saturation on tree growth and death in a mixed-oak forest. For Ecol Manage 243:210–18.CrossRefGoogle Scholar
  76. Weand MP, Arthur MA, Lovett GM, McCulley RL, Weathers KC. 2010a. Effects of tree species and N additions on forest floor microbial communities and extracellular enzyme activities. Soil Biology & Biochemistry 42:2161–73.CrossRefGoogle Scholar
  77. Weand MP, Arthur MA, Lovett GM, Sikora F, Weathers KC. 2010b. The phosphorus status of northern hardwoods differs by species but is unaffected by nitrogen fertilization. Biogeochemistry 97:159–81.CrossRefGoogle Scholar
  78. Weathers KC, Lovett GM, Likens GE, Lathrop R. 2000. The effect of landscape features on deposition to Hunter Mountain, Catskill Mountains, New York. Ecol Appl 10:528–40.CrossRefGoogle Scholar
  79. Weathers KC, Simkin SM, Lovett GM, Lindberg SE. 2006. Empirical modeling of atmospheric deposition in mountainous landscapes. Ecol Appl 16:1590–607.PubMedCrossRefGoogle Scholar
  80. Zimmer M. 1999. The fate and effects of ingested hydrolyzable tannins in Porcellio scaber. J Chem Ecol 25:611–28.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Gary M. Lovett
    • 1
    Email author
  • Mary A. Arthur
    • 2
  • Kathleen C. Weathers
    • 1
  • Ross D. Fitzhugh
    • 3
  • Pamela H. Templer
    • 4
  1. 1.Cary Institute of Ecosystem StudiesMillbrookUSA
  2. 2.Department of ForestryUniversity of KentuckyLexingtonUSA
  3. 3.Department of Plant BiologyUniversity of IllinoisUrbanaUSA
  4. 4.Department of BiologyBoston UniversityBostonUSA

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