, Volume 18, Issue 3, pp 520–532 | Cite as

Soil Denitrification Fluxes in a Northern Hardwood Forest: The Importance of Snowmelt and Implications for Ecosystem N Budgets

  • Jennifer L. MorseEmail author
  • Jorge Durán
  • Peter M. Groffman


Nitrogen (N) is the nutrient that most frequently limits the productivity of forest ecosystems. Understanding N cycling and forest response to altered N inputs and climate change is an ongoing research challenge. In several intensively studied forests in northeastern North America, well-characterized N inputs are not balanced by measured N losses, suggesting that an unmeasured N loss pathway such as denitrification may be important. We studied soil denitrification gas fluxes in northern hardwood forests at the Hubbard Brook long-term ecological research site in New Hampshire, USA, and found that denitrification in apparently oxic soils could account for N losses greater than half of annual atmospheric N inputs. Denitrification rates were strongly affected by elevation and season, with higher rates occurring at high elevation plots and during snowmelt. These results suggest that denitrification accounts for a major portion of the increasing amounts of “missing N” reported for this site, and that a significant amount of the anthropogenic N that enters terrestrial ecosystems in northeastern North America is returned to the atmosphere as N2. These dynamics are highly vulnerable to change, however, as soil moisture levels and conditions during snowmelt are changing rapidly along with climate.


forest soil nitrogen saturation soil respiration dinitrogen nitrous oxide elevation gradient 



We thank Don Buso, Tammy Wooster, Lisa Martel, Kate Shepard, Erica Morgan, Robin Schmidt, and James Burtis for excellent field, laboratory, and data analysis work. We thank Klaus Butterbach-Bahl and two anonymous reviewers, whose comments greatly improved this manuscript. This research was supported by the National Science Foundation (DEB #0949664 and DEB #0919047). J. D. was supported by a Fulbright fellowship of the Spanish Ministry of Education and by a FCT Research Fellowship of the Portuguese Ministry of Education and Science (SFRH/BDP/87966/2012). This research was conducted at the Hubbard Brook Experimental Forest, which is operated by the Northeastern Research Station, USDA Forest Service, Newtown Square, PA. This paper is a contribution to the Hubbard Brook Ecosystem Study.


  1. Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM. 1989. Nitrogen saturation in northern forest ecosystems. BioScience 39:378–86.CrossRefGoogle Scholar
  2. Aber JD, Ollinger SV, Fédérer CA, Reich PB, Goulden ML, Kicklighter DW, Melillo J, Lathrop RG Jr. 1995. Predicting the effects of climate change on water yield and forest production in the northeastern United States. Clim Res 5:207–22.CrossRefGoogle Scholar
  3. Aber J, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I. 1998. Nitrogen saturation in temperate forest ecosystems—hypotheses revisited. BioScience 48:921–34.CrossRefGoogle Scholar
  4. Bateman EJ, Baggs EM. 2005. Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41:379–88.CrossRefGoogle Scholar
  5. Bernal S, Hedin LO, Likens GE, Gerber S, Buso DC. 2012. Complex response of the forest nitrogen cycle to climate change. Proc Natl Acad Sci 109:3406–11.CrossRefPubMedCentralPubMedGoogle Scholar
  6. Bernhardt ES, Likens GE, Hall RO, Buso DC, Fisher SG, Burton TM, Meyer JL, McDowell WH, Mayer MS, Bowden WB, Findlay SEG, Macneale KH, Stelzer RS, Lowe WH. 2005. Can’t see the forest for the stream? In-stream processing and terrestrial nitrogen exports. BioScience 55:219–30.CrossRefGoogle Scholar
  7. Blankinship, J.C., Hart, S.C., 2012. Consequences of manipulated snow cover on soil gaseous emission and N retention in the growing season: a meta-analysis. Ecosphere 3, art1.Google Scholar
  8. Bock E, Wagner M. 2006. Oxidation of inorganic nitrogen compounds as an energy source. In: Dworkin M et al., Eds. The Prokaryotes. New York: Springer. p 457–95.CrossRefGoogle Scholar
  9. Bohlen PJ, Groffman PM, Driscoll CT, Fahey TJ, Siccama TG. 2001. Plant–soil–microbial interactions in a northern hardwood forest. Ecology 82:965–78.Google Scholar
  10. Bormann FH, Likens GE, Melillo JM. 1977. Nitrogen budget for an aggrading northern hardwood forest ecosystem. Science 196:981–3.CrossRefPubMedGoogle Scholar
  11. Bowden RD, Steudler PA, Melillo JM, Aber JD. 1990. Annual nitrous oxide fluxes from temperate forest soils in the northeastern United States. J Geophys Res Atmos 95:13997–4005.CrossRefGoogle Scholar
  12. Bowden RD, Melillo JM, Steudler PA, Aber JD. 1991. Effects of nitrogen additions on annual nitrous oxide fluxes from temperate forest soils in the northeastern United States. J Geophys Res Atmos 96:9321–8.CrossRefGoogle Scholar
  13. Brumme R, Borken W, Finke S. 1999. Hierarchical control on nitrous oxide emission in forest ecosystems. Glob Biogeochem Cycles 13:1137–48.CrossRefGoogle Scholar
  14. Buckeridge K, Cen Y-P, Layzell D, Grogan P. 2010. Soil biogeochemistry during the early spring in low arctic mesic tundra and the impacts of deepened snow and enhanced nitrogen availability. Biogeochemistry 99:127–41.CrossRefGoogle Scholar
  15. Burgin A, Groffman P. 2012. Soil O2 controls denitrification rates and N2O yield in a riparian wetland. J Geophys Res 117:G01010.Google Scholar
  16. Burgin A, Groffman P, Lewis D. 2010. Factors regulating denitrification in a riparian wetland. Soil Sci Soc Am J 74:1826–33.CrossRefGoogle Scholar
  17. Butterbach-Bahl K, Willibald G, Papen H. 2002. Soil core method for direct simultaneous determination of N2 and N2O emissions from forest soils. Plant Soil 240:105–16.CrossRefGoogle Scholar
  18. Campbell JL, Mitchell MJ, Groffman PM, Christenson LM, Hardy JP. 2005. Winter in northeastern North America: a critical period for ecological processes. Front Ecol Environ 3:314–22.CrossRefGoogle Scholar
  19. Campbell JL, Rustad LE, Boyer EW, Christopher SF, Driscoll CT, Fernandez IJ, Groffman PM, Houle D, Kiekbusch J, Magill AH, Mitchell MJ, Ollinger SV. 2009. Consequences of climate change for biogeochemical cycling in forests of northeastern North America. Can J For Res 39:264–84.CrossRefGoogle Scholar
  20. Cleavitt NL, Fahey TJ, Groffman PM, Hardy JP, Henry KS, Driscoll CT. 2008. Effects of soil freezing on fine roots in a northern hardwood forest. Can J For Res 38:82–91.CrossRefGoogle Scholar
  21. Creed IF, Spargo AT, Jones JA, Buttle JM, Adams MB, Beall FD, Booth EG, Campbell JL, Clow D, Elder K, Green MB, Grimm NB, Miniat C, Ramlal P, Saha A, Sebestyen S, Spittlehouse D, Sterling S, Williams MW, Winkler R, Yao H. 2014. Changing forest water yields in response to climate warming: results from long-term experimental watershed sites across North America. Glob Change Biol 20:3191–208.CrossRefGoogle Scholar
  22. Dittman JA, Driscoll CT, Groffman PM, Fahey TJ. 2007. Dynamics of nitrogen and dissolved organic carbon at the Hubbard Brook Experimental Forest. Ecology 88:1153–66.CrossRefPubMedGoogle Scholar
  23. Durán J, Morse JL, Groffman PM, Campbell JL, Christenson LM, Driscoll CT, Fahey TJ, Fisk MC, Mitchell MJ, Templer PH. 2014. Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests. Glob Change Biol 20:3568–77.CrossRefGoogle Scholar
  24. Fenn ME, Poth MA, Aber JD, Baron JS, Bormann BT, Johnson DW, Lemly AD, McNulty SG, Ryan DE, Stottlemyer R. 1998. Nitrogen excess in North American ecosystems: predisposing factors, ecosystem responses, and management strategies. Ecol Appl 8:706–33.CrossRefGoogle Scholar
  25. 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
  26. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ. 2003. The nitrogen cascade. BioScience 53:341–56.CrossRefGoogle Scholar
  27. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA. 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–92.CrossRefPubMedGoogle Scholar
  28. Goodale CL, Aber JD, Vitousek PM. 2003. An unexpected nitrate decline in New Hampshire streams. Ecosystems 6:0075–86.CrossRefGoogle Scholar
  29. Groffman PM. 2012. Terrestrial denitrification: challenges and opportunities. Ecol Process 1:1–11.CrossRefGoogle Scholar
  30. Groffman PM, Driscoll CT, Fahey TJ, Hardy JP, Fitzhugh RD, Tierney GL. 2001. Effects of mild winter freezing on soil nitrogen and carbon dynamics in a northern hardwood forest. Biogeochemistry 56:191–213.CrossRefGoogle Scholar
  31. Groffman PM, Altabet MA, Bohlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP, Voytek MA. 2006a. Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16:2091–122.CrossRefPubMedGoogle Scholar
  32. Groffman PM, Hardy JP, Driscoll CT, Fahey TJ. 2006b. Snow depth, soil freezing, and fluxes of carbon dioxide, nitrous oxide and methane in a northern hardwood forest. Glob Change Biol 12:1748–60.CrossRefGoogle Scholar
  33. Groffman PM, Hardy JP, Fisk MC, Fahey TJ, Driscoll CT. 2009. Climate variation and soil carbon and nitrogen cycling processes in a northern hardwood forest. Ecosystems 12:927–43.CrossRefGoogle Scholar
  34. Groffman PM, Hardy JP, Fashu-Kanu S, Driscoll CT, Cleavitt NL, Fahey TJ, Fisk MC. 2011. Snow depth, soil freezing and nitrogen cycling in a northern hardwood forest landscape. Biogeochemistry 102:223–38.CrossRefGoogle Scholar
  35. Groffman PM, Rustad L, Templer PH, Campbell JL, Christenson LM, Lany NK, Socci AM, Vadeboncoeur MA, Schaberg P, Wilson GF, Driscoll CT, Fahey TJ, Fisk MC, Goodale CL, Green MB, Hamburg SP, Johnson CE, Mitchell MJ, Morse JL, Pardo LH, Rodenhouse NL. 2012. Long-term integrated studies show complex and surprising effects of climate change in northern hardwood forests. BioScience 62:1056–66.CrossRefGoogle Scholar
  36. Hayhoe K, Wake CP, Huntington TG, Luo L, Schwartz MD, Sheffield J, Wood E, Anderson B, Bradbury J, DeGaetano A. 2007. Past and future changes in climate and hydrological indicators in the US Northeast. Clim Dyn 28:381–407.CrossRefGoogle Scholar
  37. Holtan-Hartwig L, Dörsch P, Bakken LR. 2002. Low temperature control of soil denitrifying communities: kinetics of N2O production and reduction. Soil Biol Biochem 34:1797–806.CrossRefGoogle Scholar
  38. Hothorn T, Hornik K, van de Wiel MA, Zeileis A. 2008. Implementing a class of permutation tests: the coin package. Journal of Statistical Software 28:1–23.Google Scholar
  39. Judd K, Likens G, Groffman P. 2007. High nitrate retention during winter in soils of the Hubbard Brook Experimental Forest. Ecosystems 10:217–25.CrossRefGoogle Scholar
  40. Keller M, Goreau TJ, Wofsy SC, Kaplan WA, McElroy MB. 1983. Production of nitrous oxide and consumption of methane by forest soils. Geophys Res Lett 10:1156–9.CrossRefGoogle Scholar
  41. Knowles R. 1982. Denitrification. Microbiol Rev 46:43–70.PubMedCentralPubMedGoogle Scholar
  42. Kreutzer K, Butterbach-Bahl K, Rennenberg H, Papen H. 2009. The complete nitrogen cycle of an N-saturated spruce forest ecosystem. Plant Biol 11:643–9.CrossRefPubMedGoogle Scholar
  43. Kulkarni MV, Groffman PM, Yavitt JB. 2008. Solving the global nitrogen problem: it’s a gas!. Front Ecol Environ 6:199–206.CrossRefGoogle Scholar
  44. Kulkarni MV, Burgin AJ, Groffman PM, Yavitt JB. 2014. A comparison of denitrification rates as measured using direct flux and 15N tracer methods in northeastern forest soils. Biogeochemistry 117:359–73.CrossRefGoogle Scholar
  45. Kulkarni MV, Groffman PM, Yavitt JB, Goodale CL. 2015. Complex controls of denitrification at ecosystem, landscape and regional scales in northern hardwood forests. Ecol Model. 298:39–52.Google Scholar
  46. Likens GE. 2004. Some perspectives on long-term biogeochemical research from the Hubbard Brook Ecosystem Study. Ecology 85:2355–62.CrossRefGoogle Scholar
  47. 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 Manag 196:7–28.CrossRefGoogle Scholar
  48. McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G. 2003. Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–12.CrossRefGoogle Scholar
  49. Morse JL, Bernhardt ES. 2013. Using 15N tracers to estimate N2O and N2 emissions from nitrification and denitrification in coastal plain wetlands under contrasting land-uses. Soil Biol Biochem 57:635–43.CrossRefGoogle Scholar
  50. Morse JL, Werner SF, Gillen C, Bailey SW, McGuire KJ, Groffman PM. 2014. Searching for biogeochemical hotspots in three dimensions: Soil C and N cycling in hydropedologic units in a northern hardwood forest. JGR-Biogeosciences 119:1596–607.Google Scholar
  51. Morse JL, Durán J, Beall F, Enanga EM, Creed IF, Fernandez I, Groffman PM. 2015. Soil denitrification fluxes from three northeastern North American forests across a range of nitrogen deposition. Oecologia 177:17–27.CrossRefPubMedGoogle Scholar
  52. Parkin T. 1987. Soil microsites as a source of denitrification variability. Soil Sci Soc Am J 51:1194–9.CrossRefGoogle Scholar
  53. R Development Core Team. 2009. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  54. Raciti SM, Burgin AJ, Groffman PM, Lewis DN, Fahey TJ. 2011. Denitrification in suburban lawn soils. J Environ Qual 40:1932–40.CrossRefPubMedGoogle Scholar
  55. Rustad L, Campbell J, Dukes JS, Huntington T, Fallon Lambert K, Mohan J, Rodenhouse NL. 2012. Changing climate, changing forests: the impacts of climate change on forests of the northeastern United States and eastern Canada. Newtown Square: Department of Agriculture, Forest Service, Northern Research Station. p 48.Google Scholar
  56. Schindlbacher A, Zechmeister-Boltenstern S, Butterbach-Bahl K. 2004. Effects of soil moisture and temperature on NO, NO2, and N2O emissions from European forest soils. J Geophys Res Atmos 109.Google Scholar
  57. Schlesinger WH. 2013. An estimate of the global sink for nitrous oxide in soils. Glob Change Biol 19:2929–31.CrossRefGoogle Scholar
  58. Schwarz PA, Fahey TJ, McCulloch CE. 2003. Factors controlling spatial variation of tree species abundance in a forested landscape. Ecology 84:1862–78.CrossRefGoogle Scholar
  59. Siccama TG, Fahey TJ, Johnson CE, Sherry TW, Denny EG, Girdler EB, Likens GE, Schwarz PA. 2007. Population and biomass dynamics of trees in a northern hardwood forest at Hubbard Brook. Can J For Res 37:737–49.CrossRefGoogle Scholar
  60. Soil Survey Staff. 2006. Keys to soil taxonomy. Washington, DC: US Department of Agriculture, Natural Resources Conservation Service.Google Scholar
  61. Suddick EC, Davidson EA. 2012. The role of nitrogen in climate change and the impacts of nitrogen-climate interactions on terrestrial and aquatic ecosystems, agriculture, and human health in the United States: A technical report submitted to the US National Climate Assessment. North American Nitrogen Center of the International Nitrogen Initiative (NANC-INI), Woods Hole Research Center, 149 Woods Hole Road, Falmouth, MA 02540-1644, USA.Google Scholar
  62. Swerts M, Uytterhoeven G, Merckx R, Vlassak K. 1995. Semicontinuous measurement of soil atmosphere gases with gas-flow soil core method. Soil Sci Soc Am J 59:1336–42.CrossRefGoogle Scholar
  63. Tierney GL, Fahey TJ, Groffman PM, Hardy JP, Fitzhugh RD, Driscoll CT. 2001. Soil freezing alters fine root dynamics in a northern hardwood forest. Biogeochemistry 56:175–90.CrossRefGoogle Scholar
  64. Venterea RT, Groffman PM, Verchot LV, Magill AH, Aber JD, Steudler PA. 2003. Nitrogen oxide gas emissions from temperate forest soils receiving long-term nitrogen inputs. Glob Change Biol 9:346–57.CrossRefGoogle Scholar
  65. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50.Google Scholar
  66. Wang R, Willibald G, Feng Q, Zheng XH, Liao TT, Bruggemann N, Butterbach-Bahl K. 2011. Measurement of N(2), N(2)O, NO, and CO(2) Emissions from soil with the gas-flow-soil-core technique. Environ Sci Technol 45:6066–72.CrossRefPubMedGoogle Scholar
  67. Wheeler, B., 2010. Permutation tests for linear models. The Comprehensive R Archive Network.Google Scholar
  68. Yanai RD, Vadeboncoeur MA, Hamburg SP, Arthur MA, Fuss CB, Groffman PM, Siccama TG, Driscoll CT. 2013. From missing source to missing sink: long-term changes in the nitrogen budget of a northern hardwood forest. Environ Sci Technol 47:11440–8.CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Jennifer L. Morse
    • 1
    • 2
    Email author
  • Jorge Durán
    • 1
    • 3
  • Peter M. Groffman
    • 1
  1. 1.Cary Institute of Ecosystem StudiesMillbrookUSA
  2. 2.Portland State UniversityPortlandUSA
  3. 3.Center for Functional EcologyUniversity of CoimbraCoimbraPortugal

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