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Biogeochemistry

, Volume 121, Issue 2, pp 305–316 | Cite as

Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests

  • S. D. FreyEmail author
  • S. Ollinger
  • K. Nadelhoffer
  • R. Bowden
  • E. Brzostek
  • A. Burton
  • B. A. Caldwell
  • S. Crow
  • C. L. Goodale
  • A. S. Grandy
  • A. Finzi
  • M. G. Kramer
  • K. Lajtha
  • J. LeMoine
  • M. Martin
  • W. H. McDowell
  • R. Minocha
  • J. J. Sadowsky
  • P. H. Templer
  • K. Wickings
Biogeochemistry Letters

Abstract

The terrestrial biosphere sequesters up to a third of annual anthropogenic carbon dioxide emissions, offsetting a substantial portion of greenhouse gas forcing of the climate system. Although a number of factors are responsible for this terrestrial carbon sink, atmospheric nitrogen deposition contributes by enhancing tree productivity and promoting carbon storage in tree biomass. Forest soils also represent an important, but understudied carbon sink. Here, we examine the contribution of trees versus soil to total ecosystem carbon storage in a temperate forest and investigate the mechanisms by which soils accumulate carbon in response to two decades of elevated nitrogen inputs. We find that nitrogen-induced soil carbon accumulation is of equal or greater magnitude to carbon stored in trees, with the degree of response being dependent on stand type (hardwood versus pine) and level of N addition. Nitrogen enrichment resulted in a shift in organic matter chemistry and the microbial community such that unfertilized soils had a higher relative abundance of fungi and lipid, phenolic, and N-bearing compounds; whereas, N-amended plots were associated with reduced fungal biomass and activity and higher rates of lignin accumulation. We conclude that soil carbon accumulation in response to N enrichment was largely due to a suppression of organic matter decomposition rather than enhanced carbon inputs to soil via litter fall and root production.

Keywords

Nitrogen deposition Soil carbon Temperate forest Terrestrial carbon sink 

Notes

Acknowledgments

We thank Michelle Day, Stephanie Juice, Melissa Knorr, Rich MacLean, April Melvin, and Marissa Weiss for assistance with sample collection and analysis. This work was supported by the National Science Foundation Long-term Ecological Research (LTER) Program.

Supplementary material

10533_2014_4_MOESM1_ESM.docx (4.2 mb)
Supplementary material 1 (DOCX 4349 kb)

References

  1. Bauer GA, Bazzaz FA, Minocha R, Long S, Magill A, Aber J, Berntson GM (2004) Effects of chronic N additions on tissue chemistry, photosynthetic capacity, and carbon sequestration potential of a red pine (Pinus resinosa Ait.) stand in the NE United States. For Ecol Manag 196:173–186CrossRefGoogle Scholar
  2. Boden TA, Marland G, Andres RJ (2012) Global, regional, and national fossil-fuel CO2 emissions. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge. doi: 10.3334/CDIAC/00001_V2012 Google Scholar
  3. Bowden RD, Davidson E, Savage K, Arabia C, Steudler P (2004) Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. For Ecol Manag 196:43–56CrossRefGoogle Scholar
  4. Brzostek ER, Edward R, Finzi AC (2011) Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils. Ecology 92:892–902Google Scholar
  5. Burton AJ, Jarvey JC, Jarvi MP, Zak DR, Pregitzer KS (2012) Chronic N deposition alters root respiration-tissue N relationship in northern hardwood forests. Glob Chang Biol 18:258–266CrossRefGoogle Scholar
  6. Currie WS, Aber JD, McDowell WH, Boone RD, Magill AH (1996) Vertical transport of dissolved organic C and N under long-term N amendments in pine and hardwood forests. Biogeochemistry 35:471–505CrossRefGoogle Scholar
  7. Cusack DF, Silver WL, Torn MS, McDowell WH (2011) Effects of nitrogen additions on above- and belowground carbon dynamics in two tropical forests. Biogeochemistry 104:203–225CrossRefGoogle Scholar
  8. de Vries W, Reinds GJ, Gundersen P, Sterba H (2006) The impact of nitrogen deposition on carbon sequestration in European forests and forest soils. Glob Chang Biol 12:1151–1173CrossRefGoogle Scholar
  9. 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 Manag 258:1814–1823CrossRefGoogle Scholar
  10. Deng F, Chen JM (2011) Recent global CO2 flux inferred from atmospheric CO2 observations and its regional analyses. Biogeosciences 8:3263–3281CrossRefGoogle Scholar
  11. Denman KL et al (2007) In: Solomon S et al (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 499–587Google Scholar
  12. Evans CD, Goodale CL, Caporn SJM, Dise NB, Emmett BA, Fernandez IJ, Field CD, Findlay SEG, Lovett GM, Meesenburg H, Moldan F, Sheppard LJ (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 91:13–35CrossRefGoogle Scholar
  13. Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171CrossRefGoogle Scholar
  14. 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 320:889–892CrossRefGoogle Scholar
  15. Goodale CL, Apps MJ, Birdsey RA, Field CB, Heath LS, Houghton RA, Jenkins JC, Kohlmaier GH, Kurz W, Liu S, Nabuurs GJ, Nilsson S, Shvidenko AZ (2002) Forest carbon sinks in the northern hemisphere. Ecol Appl 12:891–899CrossRefGoogle Scholar
  16. Guckert JB, Antworth CP, Nichols PD (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Ecol 31:147–158Google Scholar
  17. Hogberg P, Fan H, Quist M, Binkley D, Tamm CO (2006) Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob Chang Biol 12:489–499CrossRefGoogle Scholar
  18. Holland EA, Braswell BH, Sulzman J, Lamarque JF (2004) Nitrogen deposition onto the United States and Western Europe. Data set. http://www.daac.ornl.gov from Oak Ridge National Laboratory Distributed Active Archive Center, Oak Ridge, Tennessee, USA. Accessed 8 June 2014
  19. Hyvönen R, Persson T, Andersson S, Olsson B, Ågren GI, Linder, S (2008) Impact of long-term nitrogen addition on carbon stocks in trees and soils in northern Europe. Biogeochemistry 89:121–137Google Scholar
  20. Hyvönen R, Ågren GI, Linder S, Persson T, Cotrufo MF, Ekblad A, Freeman M, Grelle A, Janssens IA, Jarvis PG, Kellomäki S, Lindroth A, Loustau D, Lundmark T, Norby RJ, Oren R, Pilegaard K, Ryan MG, Sigurdsson BD, Strömgren M, van Oijen M, Wallin G (2007) The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytol 173:463–480CrossRefGoogle Scholar
  21. Janssens IA, Dieleman W, Luyssaert S, Subke J-A, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G, Papale D, Piao SL, Schulze E-D, Tang J, Law BE (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322CrossRefGoogle Scholar
  22. Kamble PN, Rousk J, Frey SD, Bååth E (2013) Bacterial growth and growth-limiting nutrients following chronic nitrogen additions to a hardwood forest soil. Soil Biol Biochem 59:32–37CrossRefGoogle Scholar
  23. Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257CrossRefGoogle Scholar
  24. Laubhann D, Sterba H, Reinds GJ, de Vries W (2009) The impact of atmospheric deposition and climate on forest growth in European monitoring plots: an individual tree growth model. For Ecol Manag 258:1751–1761CrossRefGoogle Scholar
  25. Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828CrossRefGoogle Scholar
  26. Lovett GM, Goodale CL (2011) A new conceptual model of nitrogen saturation based on experimental nitrogen addition to an oak forest. Ecosystems 14:615–631Google Scholar
  27. Lovett GM, Arthur MA, Weathers KC, Fitzhugh RD, Templer PH (2013) Nitrogen addition increases carbon storage in soils, but not in trees, in an eastern US deciduous forest. Ecosystems 16:980–1001CrossRefGoogle Scholar
  28. Magill AH, Aber JD (1998) Long-term effects of experimental nitrogen additions on foliar litter decay and humus formation in forest ecosystems. Plant Soil 203:301–311CrossRefGoogle Scholar
  29. Magill AH, Aber JD, Hendricks JJ, Bowden RD, Melillo JM, Steudler P (1997) Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition. Ecol Appl 7:402–415CrossRefGoogle Scholar
  30. 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 196:7–28CrossRefGoogle Scholar
  31. Myneni RB, Dong J, Tucker CJ, Kaufmann RK, Kauppi PE, Liski J, Zhou L, Alexeyev V, Hughes MK (2001) A large carbon sink in the woody biomass of Northern forests. Proc Natl Acad Sci 98:14784–14789CrossRefGoogle Scholar
  32. Nadelhoffer KJ, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans CJ, Schleppi P, Tietema A, Wright RF (1999) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148CrossRefGoogle Scholar
  33. 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 Manag 196:89–107CrossRefGoogle Scholar
  34. 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 153:231–240CrossRefGoogle Scholar
  35. Ollinger SV, Aber JD, Lovett GM, Millham SE, Lathrop RG, Ellis SE (1993) A spatial model of atmospheric deposition for the Northeastern US. Ecol Appl 3:459–472CrossRefGoogle Scholar
  36. Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao S, Rautiainen A, Sitch S, Hayes D (2011) A large and persistent carbon sink in the world’s forests. Science 333:993–998CrossRefGoogle Scholar
  37. Peterjohn WT, Melillo JM, Steudler PA, Newkirk KM (1994) Responses of trace gas fluxes and N availability to experimentally elevated soil temperatures. Ecol Appl 4:617–625Google Scholar
  38. Pinder RW, Davidson EA, Goodale CL, Greaver TL, Herrick JD, Liu L (2012) Climate change impacts of US reactive nitrogen. Proc Nat Acad Sci 109:7671–7675CrossRefGoogle Scholar
  39. Pregitzer KS, Burton AJ, Zak DR, Talhelm AF (2008) Simulated chronic N deposition increases carbon storage in northern temperate forests. Glob Chang Biol 14:142–153Google Scholar
  40. Schimel DS, House JI, Hibbard KA, Bousquet P, Ciais P, Peylin P, Braswell BH, Apps MJ, Baker D, Bondeau A, Canadell J, Churkina G, Cramer W, Denning AS, Field CB, Friedlingstein P, Goodale C, Heimann M, Houghton RA, Melillo JM, Moore B, Murdiyarso D, Noble I, Pacala SW, Prentice IC, Raupach MR, Rayner PJ, Scholes RJ, Steffen WL, Wirth C (2001) Recent patterns and mechanisms of carbon exchange by terrestrial ecosystems. Nature 414:169–172CrossRefGoogle Scholar
  41. Smithwick EAH, Eissenstat DM, Lovett GM, Bowden RD, Rustad LE, Driscoll CT (2013) Root stress and nitrogen deposition: consequences and research priorities. New Phytol 197:712–719CrossRefGoogle Scholar
  42. Solberg S, Dobbertin M, Reinds GJ, Lange H, Andreassen K, Fernandez PG, Hildingsson A, de Vries W (2009) Analyses of the impact of changes in atmospheric deposition and climate on forest growth in European monitoring plots: a stand growth approach. For Ecol Manag 258:1735–1750CrossRefGoogle Scholar
  43. Sutton MA (2008) Uncertainties in the relationship between atmospheric nitrogen deposition and forest carbon sequestration. Glob Chang Biol 14:2057–2063CrossRefGoogle Scholar
  44. Talhelm AF, Pregitzer KS, Burton AJ (2011) No evidence that chronic nitrogen additions increase photosynthesis in mature sugar maple forests. Ecol Appl 21:2413–2424CrossRefGoogle Scholar
  45. Templer PH, Mack MC, Chapin FS, Christenson LM, Compton JE, Crook HD, Currie WS, Curtis CJ, Dail DB, D’Antonio CM, Emmett BA, Epstein HE, 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 93:1816–1829CrossRefGoogle Scholar
  46. Thomas RQ, Canham CD, Weathers KC, Goodale CL (2010) Increased tree carbon storage in response to nitrogen deposition in the US. Nat Geosci 3:13–17CrossRefGoogle Scholar
  47. Thomas RQ, Bonan GB, Goodale CL (2013a) Insights into mechanisms governing forest carbon response to nitrogen deposition: a model-data comparison using observed responses to nitrogen addition. Biogeosciences 10:3869–3887CrossRefGoogle Scholar
  48. Thomas RQ, Zaehle S, Templer PH, Goodale CL (2013b) Global patterns of nitrogen limitation: confronting two global biogeochemical models with observations. Glob Chang Biol 19:2986–2998CrossRefGoogle Scholar
  49. Tonitto C, Goodale CL, Weiss MS, Frey SD, Ollinger SV (2013) The effect of nitrogen addition on soil organic matter dynamics: a model analysis of the Harvard Forest Chronic Nitrogen Amendment Study and soil carbon response to anthropogenic nitrogen deposition. Biogeochemistry. doi: 10.1007/s10533-013-9887-4 Google Scholar
  50. Turlapati SA, Minocha R, Bhiravarasa PS, Tisa LS, Thomas WK, Minocha SC (2013) Chronic N-amended soils exhibit an altered bacterial community structure in Harvard Forest, MA, USA. FEMS Microbiol Ecol 83:478–493CrossRefGoogle Scholar
  51. Whittinghill KA, Currie WS, Zak DR, Burton AJ, Pregitzer KS (2012) Anthropogenic N deposition increases soil C storage by decreasing the extent of litter decay: analysis of field observations with an ecosystem model. Ecosystems 15:450–461CrossRefGoogle Scholar
  52. Wickings K, Grandy AS, Reed S, Cleveland C (2011) Management intensity alters decomposition via biological pathways. Biogeochemistry 104:365–379Google Scholar
  53. Zak DR, Holmes WE, Burton AJ, Pregitzer KS, Talhelm AF (2008) Simulated atmospheric NO3 deposition increases soil organic matter by slowing decomposition. Ecol Appl 18:2016–2027CrossRefGoogle Scholar
  54. Zak DR, Pregitzer KS, Burton AJ, Edwards IP, Kellner H (2011) Microbial responses to a changing environment: implications for the future functioning of terrestrial ecosystems. Fungal Ecol 4:386–395CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • S. D. Frey
    • 1
    Email author
  • S. Ollinger
    • 1
    • 2
  • K. Nadelhoffer
    • 3
  • R. Bowden
    • 4
  • E. Brzostek
    • 5
  • A. Burton
    • 6
  • B. A. Caldwell
    • 7
  • S. Crow
    • 8
  • C. L. Goodale
    • 9
  • A. S. Grandy
    • 1
  • A. Finzi
    • 10
  • M. G. Kramer
    • 11
  • K. Lajtha
    • 7
  • J. LeMoine
    • 3
  • M. Martin
    • 2
  • W. H. McDowell
    • 1
  • R. Minocha
    • 12
  • J. J. Sadowsky
    • 1
  • P. H. Templer
    • 10
  • K. Wickings
    • 1
  1. 1.Department of Natural Resources and the EnvironmentUniversity of New HampshireDurhamUSA
  2. 2.Earth Systems Research CenterUniversity of New HampshireDurhamUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  4. 4.Department of Environmental ScienceAllegheny CollegeMeadvilleUSA
  5. 5.Department of GeographyIndiana UniversityBloomingtonUSA
  6. 6.School of Forest Resources and Environmental ScienceMichigan Technological UniversityHoughtonUSA
  7. 7.Department of Forest ScienceOregon State UniversityCorvallisUSA
  8. 8.Department of Natural Resources and Environmental ManagementUniversity of Hawai’i MānoaHonoluluUSA
  9. 9.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  10. 10.Department of BiologyBoston UniversityBostonUSA
  11. 11.Soil and Water Science DepartmentUniversity of FloridaGainesvilleUSA
  12. 12.USDA Forest ServiceNorthern Research StationDurhamUSA

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