, Volume 18, Issue 7, pp 1179–1191 | Cite as

Soil Nitrogen Availability Affects Belowground Carbon Allocation and Soil Respiration in Northern Hardwood Forests of New Hampshire

  • Kikang Bae
  • Timothy J. FaheyEmail author
  • Ruth D. Yanai
  • Melany Fisk


Plant nutrient acquisition in forests requires respiration by roots and mycorrhizae. Belowground carbon allocation and soil respiration should thus reflect plant effort allocated to nutrient uptake, for example in conditions of different nutrient availabilities controlled by site quality or stand history. Soil respiration, belowground C allocation, and fine root biomass were measured in three sites differing in nutrient availability in the northern hardwood forests of the White Mountains of New Hampshire. Annual soil respiration and belowground C allocation measured in two stands at each site were lowest at Jeffers Brook, the site with highest nutrient availability, and higher at Hubbard Brook and Bartlett Experimental Forests. Neither soil respiration nor belowground C allocation differed significantly between mid-aged (31–41 year old) and older stands (>80 year old) within the sites, despite higher fine root (<1 mm) biomass in old stands than mid-aged stands. During the growing season, soil respiration was low where net nitrogen mineralization and net nitrification were high across an extensive sample of thirteen stands and annual belowground C allocation decreased with increasing nitrification across the six intensively studied stands. Available P was not related to soil respiration. The relationships among N availability, belowground C allocation, and soil respiration support the claim that forests allocate more C belowground in ecosystems with low availability of a limiting nutrient.


calcium fine root biomass forest age litter production mineralization nitrification phosphorus 



We thank Gavin McKellar and Corrie Blodgett for assistance with the collection of soil respiration, Braulio Quintero and Quinn Thomas for the collection of litter, Tera Ratliff and Kevan Minick for assistance with soil nutrient analyzes, Tyler Refsland, Alexis Heinz, Cindy Wood, and all summer crews for sorting fine roots. This research was supported by grants from the National Science Foundation, Biotic Systems and Resources, Ecosystem Studies and LTER programs (DEB 1114804; DEB 0949854).

Supplementary material

10021_2015_9892_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 13 kb)


  1. Aulenbach BT, Hooper RP. 2006. The composite method: an improved method for stream-water solute load estimation. Hydrol Process 20:3029–47.CrossRefGoogle Scholar
  2. Bae K. 2013. Belowground carbon fluxes respond to nutrient availability in a northern hardwood forest. PhD thesis. State University of New York, College of Environmental Science and Forestry, Syracuse, USA.Google Scholar
  3. Bloom AJ, Chapin FS, Mooney HA. 1985. Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–92.Google Scholar
  4. 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 196:43–56.CrossRefGoogle Scholar
  5. Burton A, Pregitzer K, Ruess R, Hendrick R, Allen M. 2002. Root respiration in North American forests: effects of nitrogen concentration and temperature across biomes. Oecologia 131:559–68.CrossRefGoogle Scholar
  6. Burton AJ, Jarvey JC, Jarvi MP, Zak DR, Pregitzer KS. 2011. Chronic N deposition alters root respiration-tissue N relationship in northern hardwood forests. Global Change Biol 18:258–66.CrossRefGoogle Scholar
  7. Chapin FS. 1991. Integrated responses of plants to stress. Bioscience 41:29–36.CrossRefGoogle Scholar
  8. Davidson E, Savage K, Bolstad P, Clark D, Curtis P, Ellsworth D, Hanson P, Law B, Luo Y, Pregitzer K. 2002. Belowground carbon allocation in forests estimated from litterfall and IRGA-based soil respiration measurements. Agric For Meteorol 113:39–51.CrossRefGoogle Scholar
  9. Davidson EA, Belk E, Boone RD. 1998. Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global Change Biol 4:217–27.CrossRefGoogle Scholar
  10. Ewel KC, Cropper WP Jr, Gholz HL. 1987. Soil CO2 evolution in Florida slash pine plantations. I. Changes through time. Can J For Res 17(4):325–9.CrossRefGoogle Scholar
  11. Fahey T, Siccama T, Driscoll C, Likens G, Campbell J, Johnson C, Battles J, Aber J, Cole J, Fisk M. 2005a. The biogeochemistry of carbon at Hubbard Brook. Biogeochemistry 75:109–76.CrossRefGoogle Scholar
  12. Fahey T, Tierney G, Fitzhugh R, Wilson G, Siccama T. 2005b. Soil respiration and soil carbon balance in a northern hardwood forest ecosystem. Can J For Res 35:244–53.CrossRefGoogle Scholar
  13. Fahey TJ, Battles JJ, Wilson GF. 1998. Responses of early successional northern hardwood forests to changes in nutrient availability. Ecol Monogr 68:183–212.CrossRefGoogle Scholar
  14. Finzi AC. 2009. Decades of atmospheric deposition have not resulted in widespread phosphorus limitation or saturation of tree demand for nitrogen in southern New England. Biogeochemistry 92:217–29.CrossRefGoogle Scholar
  15. Giardina CP, Ryan MG. 2002. Total belowground carbon allocation in a fast-growing Eucalyptus plantation estimated using a carbon balance approach. Ecosystems 5:487–99.CrossRefGoogle Scholar
  16. Gough CM, Vogel CS, Harrold KH, George K, Curtis PS. 2007. The legacy of harvest and fire on ecosystem carbon storage in a north temperate forest. Global Change Biol 13(9):1935–49.CrossRefGoogle Scholar
  17. Gower ST, Gholz HL, Nakane K, Baldwin VC. 1994. Production and carbon allocation patterns of pine forests. Ecol Bull 43:115–35.Google Scholar
  18. Hanson P, Edwards N, Garten C, Andrews J. 2000. Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–46.CrossRefGoogle Scholar
  19. Haynes BE, Gower ST. 1995. Belowground carbon allocation in unfertilized and fertilized red pine plantations in northern Wisconsin. Tree Physiol 15:317–25.CrossRefPubMedGoogle Scholar
  20. Janssens I, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman A, Grace J, Matteucci G. 2010. Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–22.CrossRefGoogle Scholar
  21. Lee KH, Jose S. 2003. Soil respiration, fine root production, and microbial biomass in cottonwood and loblolly pine plantations along a nitrogen fertilization gradient. For Ecol Manag 185:263–73.CrossRefGoogle Scholar
  22. Likens G, Driscoll C, Buso D, Siccama T, Johnson C, Lovett G, Fahey T, Reiners W, Ryan D, Martin C. 1998. The biogeochemistry of calcium at Hubbard Brook. Biogeochemistry 41:89–173.CrossRefGoogle Scholar
  23. Litton CM, Raich JW, Ryan MG. 2007. Carbon allocation in forest ecosystems. Global Change Biol 13:2089–109.CrossRefGoogle Scholar
  24. Lützow M, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H. 2006. Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur J Soil Sci 57:426–45.CrossRefGoogle Scholar
  25. Murphy J, Riley J. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–6.CrossRefGoogle Scholar
  26. Nave LE, Sparks JP, Le Moine J, Hardiman BS, Nadelhoffer KJ, Tallant JM, Vogel CS, Strahm BD, Curtis PS. 2014. Changes in soil nitrogen cycling in a northern temperate forest ecosystem during succession. Biogeochemistry 121(3):471–88.CrossRefGoogle Scholar
  27. Olsson P, Linder S, Giesler R, Högberg P. 2005. Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Global Change Biol 11:1745–53.CrossRefGoogle Scholar
  28. Paré D, Bernier B. 1989. Origin of the phosphorus deficiency observed in declining sugar maple stands in the Quebec Appalachians. Can J For Res 19:24–34.CrossRefGoogle Scholar
  29. Park BB, Yanai RD, Vadeboncoeur MA, Hamburg SP. 2007. Estimating root biomass in rocky soils using pits, cores, and allometric equations. Soil Sci Soc Am J 71(1):206–13.CrossRefGoogle Scholar
  30. Park BB, Yanai RD, Fahey TJ, Bailey SW, Siccama TG, Shanley JB, Cleavitt NL. 2008. Fine root dynamics and forest production across a calcium gradient in northern hardwood and conifer ecosystems. Ecosystems 11:325–41.CrossRefGoogle Scholar
  31. Phillips RP, Fahey TJ. 2007. Fertilization effects on fineroot biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytol 176:655–64. CrossRefPubMedGoogle Scholar
  32. Phillips RP, Fahey TJ. 2008. The influence of soil fertility on rhizosphere effects in northern hardwood forest soils. Soil Sci Soc Am J 72:453–61.CrossRefGoogle Scholar
  33. Raich J, Nadelhoffer K. 1989. Belowground carbon allocation in forest ecosystems: global trends. Ecology 70:1346–54.CrossRefGoogle Scholar
  34. Rastetter EB, Yanai RD, Thomas RQ, Vadeboncoeur M, Fahey TJ, Fisk MC, Kwiatkowski BL, Hamburg S. 2013. Recovery from disturbance requires resynchronization of ecosystem nutrient cycles. Ecol Appl 23(3):621–42.CrossRefPubMedGoogle Scholar
  35. Robertson GP, Sollins P, Ellis BG, Lajtha K. 1999. Exchangeable ions, pH, and cation exchange capacity. In: Robertson GP, Ed. Standard Soil Methods for Long-term Ecological Research. New York: Oxford University Press. p 106–14.Google Scholar
  36. Ryan M, Binkley D, Fownes JH. 1997. Age-related decline in forest productivity: pattern and process. Adv Ecol Res 27:213–62.CrossRefGoogle Scholar
  37. Ryzhova I, Podvezennaya M. 2008. Spatial variability of the organic carbon pool in soils of forest and steppe biogeocenoses. Eur Soil Sci 41:1260–7.CrossRefGoogle Scholar
  38. Saiz G, Byrne KA, Butterbach Bahl K, Kiese R, Blujdea V, Farrell EP. 2006. Stand age related effects on soil respiration in a first rotation Sitka spruce chronosequence in central Ireland. Global Change Biol 12:1007–20.CrossRefGoogle Scholar
  39. Sheldrick B, Wang C. 1993. Particle size distribution. In: Carter MR, Ed. Soil Sampling and Method of Analysis. Boca Raton: Lewis Publishers. p 499–511.Google Scholar
  40. Tang J, Bolstad PV, Martin JG. 2008. Soil carbon fluxes and stocks in a Great Lakes forest chronosequence. Global Change Biol 15:145–55.CrossRefGoogle Scholar
  41. Vadeboncoeur MA. 2010. Meta-analysis of fertilization experiments indicates multiple limiting nutrients in northeastern deciduous forests. Can J For Res 40(9):1766–80.CrossRefGoogle Scholar
  42. Van’t Hoff JH. 1884. Etudes de dynamique chimique. Amsterdam: F. Muller & Company.Google Scholar
  43. Vitousek PM, Farrington H. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75.CrossRefGoogle Scholar
  44. Wiseman PE, Seiler JR. 2004. Soil CO2 efflux across four age classes of plantation loblolly pine (Pinus taeda L.) on the Virginia Piedmont. For Ecol Manag 192:297–311.CrossRefGoogle Scholar
  45. Yanai R, Siccama T, Arthur M, Federer C, Friedland A. 1999. Accumulation and depletion of base cations in forest floors in the northeastern United States. Ecology 80:2774–87.CrossRefGoogle Scholar
  46. Yanai RD, Arthur MA, Acker M, Levine CR, Park BB. 2012. Variation in mass and nutrient concentration of leaf litter across years and sites in a northern hardwood forest. Can J For Res 42:1597–610.CrossRefGoogle Scholar
  47. Yanai RD, Currie WS, Goodale CL. 2003. Soil carbon dynamics after forest harvest: an ecosystem paradigm reconsidered. Ecosystems 6:197–212.CrossRefGoogle Scholar
  48. Yanai RD, Park BB, Hamburg SP. 2006. The vertical and horizontal distribution of roots in northern hardwood stands of varying age. Can J For Res 36:450–9.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Kikang Bae
    • 1
    • 2
  • Timothy J. Fahey
    • 3
    Email author
  • Ruth D. Yanai
    • 1
  • Melany Fisk
    • 4
  1. 1.Department of Forest and Natural Resources ManagementSUNY College of Environmental Science and ForestrySyracuseUSA
  2. 2.International Cooperation Division, International Affairs BureauKorea Forest ServiceDaejeonRepublic of Korea
  3. 3.Department of Natural ResourcesCornell UniversityIthacaUSA
  4. 4.Department of BiologyMiami UniversityOxfordUSA

Personalised recommendations