, Volume 13, Issue 8, pp 1145–1156 | Cite as

Influence of Non-nitrogenous Soil Amendments on Soil CO2 Efflux and Fine Root Production in an N-Saturated Northern Hardwood Forest

  • Yuanying Peng
  • Sean C. Thomas


Non-nitrogenous mineral nutrients may be an important constraint on forest productivity and belowground processes in many ecosystems. We measured responses of soil CO2 efflux (FCO2), fine root production, and root-free incubation soil respiration to experimental additions of non-nitrogenous mineral nutrients (phosphorus (P) + potassium (K) fertilizer, dolomitic lime, and P + K plus lime) over 2 years in a sugar-maple-dominated forest in central Ontario; this region receives some of the highest anthropogenic nitrogen (N) inputs in North America, and evidence exists for co-limitation by P, magnesium (Mg), and calcium (Ca) of the growth of dominant trees. Soil amendments, in particular P + K fertilization, reduced FCO2, fine root production and microbial respiration, with decreases in FCO2 of 28–51% in fertilized compared to control plots. Partial regression analyses indicated that soil available P had a negative effect on FCO2, fine root production, and microbial respiration, but detected no significant effects of N, Ca, or Mg. Path analysis further suggested that available P reduced both fine root production and microbial respiration, and that these effects were largely responsible for reduced FCO2. There was also a residual direct negative relationship between available P and FCO2, which may represent reduced metabolic activity of roots. The study indicates that P is a critical nutrient dominating belowground processes in an N-saturated forest ecosystem, and suggests that additions of P may enhance C sink strength in managed forests in part through reductions in soil CO2 efflux.


Acer saccharum forest management fertilization soil respiration microbial respiration fine root production phosphorus soil pH 



We thank Tomasz Gradowski for assistance with establishing the experiment and with field measurements. This research was financially supported by the Canadian National Science and Engineering Research Council (NSERC) and Ontario’s Premier’s Research Excellence Award program. Y. Peng is grateful to the University of Toronto for a Connaught scholarship.


  1. Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM. 1989. Nitrogen saturation in northern forest ecosystems—hypotheses and implications. BioScience 39:378–86.CrossRefGoogle Scholar
  2. Allen HL, Dougherty PM, Campbell RG. 1990. Manipulation of water and nutrients—practice and opportunity in Southern United States pine forests. For Ecol Manage 30:437–53.CrossRefGoogle Scholar
  3. Baggs EM. 2006. Partitioning the components of soil respiration: a research challenge. Plant Soil 284:1–5.CrossRefGoogle Scholar
  4. Ball DF. 1964. Loss-on-ignition as an estimator of organic matter and organic carbon in non-calcareous soils. J Soil Sci 15:84–92.CrossRefGoogle Scholar
  5. Bardgett RD, Usher MB, Hopkins DW. 2005. Biological diversity and function in soils. Ecological Reviews. Cambridge: Cambridge University press. p 57–73.CrossRefGoogle Scholar
  6. Binkley D, Driscoll CT, Allen HL, Schoeneberger P, McAvoy D. 1989. Acidic deposition and forest soils: context and case studies of the Southeastern United States. New York: Springer Verlag.Google Scholar
  7. Black CA. 1965. Methods of soil analysis: part I. Physical and mineralogical properties. Madison, WI: American Society of Agronomy.Google Scholar
  8. Borken R, Brumme W. 1997. Liming practice in temperate forest ecosystems and the effects on CO2, N2O and CH4 fluxes. Soil Use Manage 13:251–7.CrossRefGoogle Scholar
  9. Bowden RD, Davidson E, Savage K, Arabia C, Paul SP. 2004. Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. For Ecol Manage 196:43–56.CrossRefGoogle Scholar
  10. Bray RH, Kurtz LT. 1954. Determination of total, organic and available forms of phosphorus in soils. Soil Sci 59:39–45.CrossRefGoogle Scholar
  11. Brumme R, Beese F. 1992. Effects of liming and nitrogen fertilization on emissions of CO2 and N2O from a temperate forest. J Geophys Res 97:12851–8.Google Scholar
  12. Burton AJ, Pregitzer KS, Crawford JN, Aogg FP, Zak DR. 2004. Simulated chronic NO3 deposition reduces soil respiration in northern hardwood forests. Global Change Biol 10:1080–91.CrossRefGoogle Scholar
  13. Butnor JR, Johnsen KH, Oren R, Katul GG. 2003. Reduction of forest floor respiration by fertilization on both carbon dioxide-enriched and reference 17-year-old loblolly pine stands. Global Change Biol 9:849–61.CrossRefGoogle Scholar
  14. Campbell JL, Sun OJ, Law BE. 2004. Supply-side controls on soil respiration among Oregon forests. Global Change Biol 10:1857–69.CrossRefGoogle Scholar
  15. Chen X, Hutley LB, Eamus D. 2003. Carbon balance of a tropical savanna of northern Australia. Oecologia 137:405–16.CrossRefPubMedGoogle Scholar
  16. Chen X, Hutley LB, Eamus D. 2004. Seasonal patterns of fine-root productivity and turnover in a tropical savanna of northern Australia. J Trop Ecol 20:221–4.CrossRefGoogle Scholar
  17. Cromer RN, Jarvis PG. 1990. Growth and biomass portioning in Eucalyptus grandis seedlings in response to nitrogen supply. Aust J Plant Physiol 17:503–15.CrossRefGoogle Scholar
  18. Dralle K, Larsen JB. 1995. Growth response to different types of NPK-fertilization in Norway spruce in western Denmark. Plant Soil 168–169:501–4.CrossRefGoogle Scholar
  19. Egerton-Warburton LM, Allen EB. 2000. Shifts in the diversity of arbuscular mycorrhizal fungi along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–96.CrossRefGoogle Scholar
  20. Fenn ME, Poth MA, Aber JD, Baron JS, Bormann BT, Johnson DW, Lemly AD, McNulty S, Ryan DF, Stottlemeyer R. 1998. Nitrogen excess in North American ecosystems: predisposing factors, ecosystem responses, and management strategies. Ecol Appl 8:706–33.CrossRefGoogle Scholar
  21. Fenn ME, Baron JS, Allen EB, Rueth HM, Nydick KR, Geiser L, Bowman WD, Sickman JO, Meixner T, Johnson EW, Neitlich P. 2003. Ecological effects of nitrogen deposition in the western United States. Bioscience 53:404–20.CrossRefGoogle Scholar
  22. Fernandes SAP, Bernoux M, Cerri CC, Feigi BJ, Piccolo MC. 2002. Seasonal variation of soil chemical properties and CO2 and CH4 fluxes in unfertilized and P-fertilized pastures in an Ultisol of the Brazilian Amazon. Geoderma 107:227–341.CrossRefGoogle Scholar
  23. Fisher R, Binkley D. 2000. Ecology and management of forest soils. 3rd edn. New York: Wiley.Google Scholar
  24. Fisk MC, Fahey TJ. 2001. Microbial biomass and nitrogen cycling responses to fertilization and litter removal in young northern hardwood forests. Biogeochemistry 53:201–23.CrossRefGoogle Scholar
  25. Flanagan PW, Van Cleve K. 1983. Nutrient cycling in relation to decomposition and organic matter quality in Taiga ecosystems. Can J For Res 13:795–817.CrossRefGoogle Scholar
  26. Fox TR. 2000. Sustained productivity in intensively managed forest plantations. For Ecol Manage 138:187–202.CrossRefGoogle Scholar
  27. Foy CD, Chaney RL, White MC. 1978. The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29:511–66.CrossRefGoogle Scholar
  28. Galicia L, García-Oliva F. 2004. The effects of C, N and P additions on soil microbial activity under two remnant tree species in a tropical seasonal pasture. Appl Soil Ecol 26:31–9.CrossRefGoogle Scholar
  29. Giardina CP, Binkley D, Ryan MG, Fownes JH, Senock RS. 2004. Belowground carbon cycling in a humid tropical forest decreases with fertilization. Oecologia 139:545–50.CrossRefPubMedGoogle Scholar
  30. Gough CM, Seiler JR. 2004. Belowground carbon dynamics in loblolly pine (Pinus taeda) immediately following diammonium phosphate fertilization. Tree Physiol 24:845–51.PubMedGoogle Scholar
  31. Gradowski T, Thomas SC. 2006. Phosphorus limitation of sugar maple growth in central Ontario. For Ecol Manage 226:104–9.CrossRefGoogle Scholar
  32. Gradowski T, Thomas SC. 2008. Responses of canopy trees and saplings to P, K, and lime additions in Acer saccharum under high N deposition conditions. Tree Physiol 28:173–85.PubMedGoogle Scholar
  33. Hanson PJ, Edwards NT, Garten CT, Andrews JA. 2000. Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–46.CrossRefGoogle Scholar
  34. Harrison AF. 1989. Phosphorus distribution and cycling in European forest ecosystems. In: Tiessen H, Ed. Phosphorus cycles in terrestrial and aquatic ecosystems. Regional workshop I: Europe, SCOPE_UNEP. p 42–76.Google Scholar
  35. Haynes BE, Gower ST. 1995. Belowground carbon allocation in unfertilized and fertilized red pine plantations in northern Wisconsin. Tree Physiol 15:317–25.PubMedGoogle Scholar
  36. Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD, Guo D. 2006. Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. J Ecol 94:40–57.CrossRefGoogle Scholar
  37. Johnsen KH, Weir D, Oren R, Teskey RO, Sanchez F, Will R, Butnor J, Markewitz D, Richter D, Rials T, Allen HL, Seiler J, Ellsworth D, Maier C, Katul G, Dougherty PM. 2001. Carbon sequestration and southern pine forests. J For 99:14–21.Google Scholar
  38. Jonasson S, Michelsen A, Schmidt IK, Nielsen EV, Callaghan TV. 1996. Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: implications for plant nutrient uptake. Oecologia 106:507–15.CrossRefGoogle Scholar
  39. Kazda M. 1990. Indications of unbalanced nitrogen nutrition of Norway spruce stands. Plant Soil 128:97–101.CrossRefGoogle Scholar
  40. Keith H, Jacobsen KL, Raison RJ. 1997. Effects of soil phosphorus availability, temperature and moisture on soil respiration in Eucalyptus pauciflora forest. Plant Soil 190:127–41.CrossRefGoogle Scholar
  41. Kelly JM, Henderson GS. 1978. Effects of nitrogen and phosphorus additions on deciduous litter decomposition. Soil Sci Soc Am J 42:972–6.CrossRefGoogle Scholar
  42. Keyes MR, Grier CC. 1981. Above- and below-ground net production in 40-year-old Douglas-fir stands on low and high productivity sites. Can J For Res 11:599–605.CrossRefGoogle Scholar
  43. Kolb TE, Steiner KC, McCormick LH. 1990. Growth response of Northern red oak and yellow poplar seedlings to light, soil moisture and nutrients in relation to ecological strategy. For Ecol Manage 38:65–78.CrossRefGoogle Scholar
  44. Lamersdorf NP, Borken W. 2004. Clean rain promotes fine root growth and soil respiration in a Norway spruce forest. Global Change Biol 10:1351–2.CrossRefGoogle Scholar
  45. Lauenroth WK. 2000. Methods of estimating belowground net primary production. In: Sala OE, Jackson RB, Mooney HA, Howarth RW, Eds. Methods in ecosystem science. New York: Springer-Verlag. p 58–71.Google Scholar
  46. Lee K-H, Jose S. 2003. Soil respiration, fine root production, and microbial biomass in cottonwood and loblolly pine plantations along a nitrogen fertilization gradient. For Ecol Manage 185:263–73.CrossRefGoogle Scholar
  47. Litton CM, Raich JW, Ryan WG. 2007. Carbon allocation in forest ecosystems. Global Change Biol 13:2089–109.CrossRefGoogle Scholar
  48. Long RP, Horsley SB, Lilja PR. 1997. Impact of forest liming on growth and crown vigor of sugar maple and associated hardwoods. Can J For Res 27:1560–73.CrossRefGoogle Scholar
  49. Maier CA, Kress LW. 2000. Soil CO2 evolution and root respiration in 11-year-old loblolly pine (Pinus taeda) plantations as affected by moisture and nutrient availability. Can J For Res 30:347–59.CrossRefGoogle Scholar
  50. Matamala R, Schlesinger WH. 2000. Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem. Global Change Biol 6:967–79.Google Scholar
  51. McClaugherty CA, Aber JD, Melillo JM. 1982. The role of fine roots in the organic matter and nitrogen budgets of two forested ecosystems. Ecology 63:1481–90.CrossRefGoogle Scholar
  52. Nömmik H. 1978. Mineralization of carbon and nitrogen in forest humus as influenced by additions of phosphate and lime. Acta Agric Scand 28:221–30.Google Scholar
  53. 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
  54. Page AL, Miller RH, Kinney DR. 1982. Methods of soil analysis. Part 2. Chemical and microbiological properties. 2nd edn. Madison, WI: American Society of Agronomy Inc., Soil Science Society of America.Google Scholar
  55. Pangle RE, Seiler J. 2002. Influence of seedling roots, environmental factors and soil characteristics on soil CO2 efflux rates in a 2-year-old loblolly pine (Pinus taeda L.) plantation in the Virginia Piedmont. Environ Pollut 116:S85–96.CrossRefPubMedGoogle Scholar
  56. Pella E. 1990. Elemental organic-analysis. American Laboratory 22:28–36.Google Scholar
  57. Peng Y, Thomas SC. 2006. Soil CO2 efflux in uneven-aged managed forests: temporal patterns following harvest and effects of edaphic heterogeneity. Plant Soil 289:253–64.CrossRefGoogle Scholar
  58. Peng Y, Thomas SC, Tian D. 2008. Forest management and soil respiration: implications for carbon sequestration. Environ Rev 16:96–111.CrossRefGoogle Scholar
  59. Priess JA, Folster H. 2001. Microbial properties and soil respiration in submontane forests of Venezuelian Guyana: characteristics and response to fertilizer treatments. Soil Biol Biochem 33:503–9.CrossRefGoogle Scholar
  60. R Core Development Team. 2004. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  61. Samuelson LJ, Johnsen K, Stokes T, Lu W. 2004. Intensive management modifies soil CO2 efflux in 6-year-old Pinus taeda L. stands. For Ecol Manage 200:335–45.CrossRefGoogle Scholar
  62. SAS Institute Inc. 1999–2001. SAS online documentation, version 8. SAS Institute Inc., Cary, NC.Google Scholar
  63. Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602.CrossRefGoogle Scholar
  64. Schmid I. 2002. The influence of soil type and interspecific competition on the fine root system of Norway spruce and European beech. Basic Appl Ecol 3:339–46.CrossRefGoogle Scholar
  65. Smolander A, Kurka A, Kitunen V, Mälkönen E. 1994. Microbial biomass C and N, and respiratory activity in soil of repeatedly limed and N- and P-fertilized Norway spruce stands. Soil Biol Biochem 26:957–62.CrossRefGoogle Scholar
  66. Stevenson FJ. 1986. Cycles of soil: carbon, nitrogen sulfur, micronutrients. New York: Wiley.Google Scholar
  67. Thirukkumaran CM, Parkinson D. 2000. Microbial respiration, biomass, metabolic quotient and litter decomposition in a lodgepole pine forest floor amended with nitrogen and phosphorus fertilizers. Soil Biol Biochem 32:59–66.CrossRefGoogle Scholar
  68. Van Dick HFG, Roelofs JGM. 1988. Effects of excessive ammonium deposition on the nutritional status and condition of pine needles. Physiol Plant 73:494–501.CrossRefGoogle Scholar
  69. Vesterdal L, Raulund-Rasmussen K. 2002. Availability of nitrogen and phosphorus in Norway spruce forest floors fertilized with nitrogen and other essential nutrients. Soil Biol Biochem 34:1243–51.CrossRefGoogle Scholar
  70. Vitousek PM, Farrington H. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75.CrossRefGoogle Scholar
  71. Vose JM, Elliot KJ, Johnson DW, Walker RF, Johnson MG, Tingey DT. 1995. Effects of elevated CO2 and N fertilization on soil respiration from ponderosa pine (Pinus ponderosa) in open-top chambers. Can J For Res 25:1243–51.CrossRefGoogle Scholar
  72. Vose JM, Elliot KJ, Johnson DW, Walker RF, Tingey DT, Johnson MG. 1997. Soil respiration response to three years of elevated CO2 and N fertilization in ponderosa pine (Pinus ponderosa Doug. ex laws.). Plant Soil 190:19–28.CrossRefGoogle Scholar
  73. Walters MB, Lajzerowicz CC, Coates KD. 2006. Soil resources and the growth and nutrition of tree seedlings near harvest gap- forest edges in interior cedar-hemlock forests of British Columbia. Can J For Res 36:62–76.CrossRefGoogle Scholar
  74. Waring RH, Schlesinger WH. 1985. Forest ecosystems: concepts and management. Academic Press, Orlando.Google Scholar
  75. Williams JD. 1974. Path analysis and causal models as regression techniques. Mult Lin Regr View 8:36–61.Google Scholar
  76. Wootton JT. 1994. Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:151–65.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Faculty of ForestryUniversity of TorontoTorontoCanada

Personalised recommendations