Ecosystems

, Volume 15, Issue 6, pp 927–939 | Cite as

Nitrogen Uptake During Fall, Winter and Spring Differs Among Plant Functional Groups in a Subarctic Heath Ecosystem

  • Klaus S. Larsen
  • Anders Michelsen
  • Sven Jonasson
  • Claus Beier
  • Paul Grogan
Article

Abstract

Nitrogen (N) is a critical resource for plant growth in tundra ecosystems, and species differences in the timing of N uptake may be an important feature regulating community composition and ecosystem productivity. We added 15N-labelled glycine to a subarctic heath tundra dominated by dwarf shrubs, mosses and graminoids in fall, and investigated its partitioning among ecosystem components at several time points (October, November, April, May, June) through to the following spring/early summer. Soil microbes had acquired 65 ± 7% of the 15N tracer by October, but this pool decreased through winter to 37 ± 7% by April indicating significant microbial N turnover prior to spring thaw. Only the evergreen dwarf shrubs showed active 15N acquisition before early May indicating that they had the highest potential of all functional groups for acquiring nutrients that became available in early spring. The faster-growing deciduous shrubs did not resume 15N acquisition until after early May indicating that they relied more on nitrogen made available later during the spring/early summer. The graminoids and mosses had no significant increases in 15N tracer recovery or tissue 15N tracer concentrations after the first harvest in October. However, the graminoids had the highest root 15N tracer concentrations of all functional groups in October indicating that they primarily relied on N made available during summer and fall. Our results suggest a temporal differentiation among plant functional groups in the post-winter resumption of N uptake with evergreen dwarf shrubs having the highest potential for early N uptake, followed by deciduous dwarf shrubs and graminoids.

Keywords

15N isotope labelling glycine cold-season plant nitrogen uptake winter temporal nitrogen uptake pattern microbial biomass 

Notes

Acknowledgments

The Abisko Scientific Research Station provided excellent logistic support during the field work. Niels Bruun, Gosha Sylvester and Karna Heinsen assisted with laboratory analyses. We thank the Danish National Research Foundation for support. The specific work was financed by the University of Copenhagen, the Royal Swedish Academy of Sciences and the Danish Natural Science Research Council.

References

  1. Allen SE. 1989. Chemical analysis of ecological material, 2nd edn. Oxford: Blackwell Scientific Publications. 368 pp.Google Scholar
  2. Bilbrough C, Welker JM, Bowman WD. 2000. Early spring nitrogen uptake by snow-covered plants: a comparison of arctic and alpine plant function under the snowpack. Arct Antarct Alp Res 32:404–11.CrossRefGoogle Scholar
  3. Brookes PC, Landman A, Pruden G, Jenkinson DS. 1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in the soil. Soil Biol Biochem 17:837–42.CrossRefGoogle Scholar
  4. Brooks PD, Williams MW, Schmidt SK. 1996. Microbial activity under alpine snowpacks, Niwot Ridge, Colorado. Biogeochemistry 32:93–113.CrossRefGoogle Scholar
  5. Brooks PD, Williams MW, Schmidt SK. 1998. Inorganic nitrogen and microbial biomass dynamics before and during spring snowmelt. Biogeochemistry 43:1–15.CrossRefGoogle Scholar
  6. Buckeridge KM, Grogan P. 2010. Deepened snow increases late thaw biogeochemical pulses in mesic low arctic tundra. Biogeochemistry 101:105–21.CrossRefGoogle Scholar
  7. Clein JS, Schimel JP. 1995. Microbial activity of tundra and taiga soils at subzero temperatures. Soil Biol Biochem 27:1231–4.CrossRefGoogle Scholar
  8. Clemmensen KE, Sørensen PL, Michelsen A, Jonasson S, Ström L. 2008. Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155:771–83.PubMedCrossRefGoogle Scholar
  9. Edwards KA, Jefferies RL. 2010. Nitrogen uptake by Carex aquatilis during the winter–spring transition in a low Arctic wet meadow. J Ecol 98:737–44.CrossRefGoogle Scholar
  10. Edwards KA, McCulloch J, Kershaw GP, Jefferies RL. 2006. Soil microbial and nutrient dynamics in a wet Arctic sedge meadow in late winter and early spring. Soil Biol Biochem 38:2843–51.CrossRefGoogle Scholar
  11. Fahnestock JT, Jones MH, Brooks PD, Walker DA, Welker JM. 1998. Winter and early spring CO2 efflux from tundra communities of northern Alaska. J Geophys Res 103:29023–7.CrossRefGoogle Scholar
  12. Fisk MC, Schmidt SK. 1995. Nitrogen mineralization and microbial biomass N dynamics in three alpine tundra communities. Soil Sci Soc Am J 59:1036–43.CrossRefGoogle Scholar
  13. Giblin AE, Nadelhoffer KJ, Shaver GR, Laundre JA, McKerrow AJ. 1991. Biogeochemical diversity along a riverside toposequence in arctic Alaska. Ecol Monogr 61:415–35.CrossRefGoogle Scholar
  14. Grogan P, Jonasson S. 2003. Controls on annual nitrogen cycling in the understory of a subarctic birch forest. Ecology 84:202–18.CrossRefGoogle Scholar
  15. Hart SC, Gunther AJ. 1989. In situ estimates of annual net nitrogen mineralization and nitrification in a subarctic watershed. Oecologia 80:284–8.Google Scholar
  16. Hobbie SE, Chapin FS. 1996. Winter regulation of tundra litter carbon and nitrogen dynamics. Biogeochemistry 35:327–38.CrossRefGoogle Scholar
  17. Hobbie JE, Hobbie EA. 2012. Amino acid cycling in plankton and soil microbes studied with radioisotopes: measured amino acids in soil do not reflect bioavailability. Biogeochemistry 107:339–60.CrossRefGoogle Scholar
  18. Jaeger C, Monson RK, Melany CF, Schmidt SK. 1999. Seasonal partitioning of nitrogen by plants and soil microorganisms in an alpine ecosystem. Ecology 80:1883–91.CrossRefGoogle Scholar
  19. Jefferies RL, Walker NA, Edwards KA, Dainty J. 2010. Is the decline of soil microbial biomass in late winter coupled to changes in the physical state of cold soils? Soil Biol Biochem 42:129–35.CrossRefGoogle Scholar
  20. Jonasson S, Havstrom M, Jensen M, Callaghan TV. 1993. In situ mineralization of nitrogen and phosphorus of arctic soils after perturbations simulating climate-change. Oecologia 95:179–86.CrossRefGoogle Scholar
  21. 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
  22. Jones MH, Fahnestock JT, Welker JM. 1999. Early and late winter CO2 efflux from arctic tundra in the Kuparuk River Watershed, Alaska, USA. Arct Antarct Alp Res 31:187–90.CrossRefGoogle Scholar
  23. Kaiser C, Meyer H, Biasi C, Rusalimova O, Barsukov P, Richter A. 2005. Storage and mineralization of carbon and nitrogen in soils of a frost-boil tundra ecosystem in Siberia. Appl Soil Ecol 29:173–83.CrossRefGoogle Scholar
  24. Kielland K, McFarland J, Olson K. 2006. Amino acid uptake in deciduous and coniferous taiga ecosystems. Plant Soil 288:297–307.CrossRefGoogle Scholar
  25. Konestabo HS, Michelsen A, Holmstrup M. 2007. Responses of springtail and mite populations to prolonged periods of soil freeze–thaw cycles in a sub-arctic ecosystem. Appl Soil Ecol 36:136–46.CrossRefGoogle Scholar
  26. Kummerow J, Ellis BA, Kummerow S, Chapin FS. 1983. Spring growth of shoots and roots in shrubs of an Alaskan muskeg. Am J Bot 70:1509–15.CrossRefGoogle Scholar
  27. Lambers H, Chapin FS, Pons TL. 1998. Plant physiological ecology. New York: Springer. 540 pp.Google Scholar
  28. Larsen KS, Jonasson S, Michelsen A. 2002. Repeated freeze–thaw cycles and their effects on biological processes in two arctic ecosystem types. Appl Soil Ecol 21:187–95.CrossRefGoogle Scholar
  29. Larsen KS, Grogan P, Jonasson S, Michelsen A. 2007a. Respiration and microbial dynamics in two sub-arctic ecosystems during winter and spring-thaw: effects of increased snow depth. Arct Antarct Alp Res 39:268–77.CrossRefGoogle Scholar
  30. Larsen KS, Ibrom A, Jonasson S, Michelsen A, Beier C. 2007b. Significance of cold-season respiration and photosynthesis in a subarctic heath ecosystem in Northern Sweden. Glob Change Biol 13:1498–508.CrossRefGoogle Scholar
  31. Lipson DA, Schmidt SK. 2004. Seasonal changes in an alpine soil bacterial community in the Colorado Rocky Mountains. Appl Environ Microb 70:2867–79.CrossRefGoogle Scholar
  32. Lipson DA, Schmidt SK, Monson RK. 1999. Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80:1623–31.CrossRefGoogle Scholar
  33. Lipson DA, Schmidt SK, Monson RK. 2000. Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass. Soil Biol Biochem 32:441–8.CrossRefGoogle Scholar
  34. McKane RB, Johnson LC, Shaver GR et al. 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71.PubMedCrossRefGoogle Scholar
  35. Oechel WC, Sveinbjörnsson B. 1978. Primary production processes in arctic bryophytes at Barrow, Alaska. In: Tietzen LL, Ed. Vegetation and production ecology of an Alaskan arctic tundra. Cambridge: Cambridge University Press. p 269–98.CrossRefGoogle Scholar
  36. Oechel WC, Vourlitis GL, Hastings SJ. 1997. Cold season CO2 emissions from arctic soils. Global Biogeochem Cycles 11:163–72.CrossRefGoogle Scholar
  37. Persson J, Hogberg P, Ekblad A, Hogberg MN, Nordgren A, Näsholm T. 2003. Nitrogen acquisition from inorganic and organic sources by boreal forest plants in the field. Oecologia 137:252–7.PubMedCrossRefGoogle Scholar
  38. Ross DJ. 1972. Effects of freezing and thawing on some grassland topsoils on oxygen uptakes and dehydrogenase activities. Soil Biol Biochem 4:115–17.CrossRefGoogle Scholar
  39. Schadt CW, Martin AP, Lipson DA, Schmidt SK. 2003. Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–61.PubMedCrossRefGoogle Scholar
  40. Schimel JP, Clein JS. 1996. Microbial response to freeze-thaw cycles in tundra and taiga soils. Soil Biol Biochem 28:1061–6.CrossRefGoogle Scholar
  41. Schimel JP, Bilbrough C, Welker JM. 2004. Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol Biochem 36:217–27.CrossRefGoogle Scholar
  42. Schmidt SK, Lipson DA. 2004. Microbial growth under the snow: Implications for nutrient allelochemical availability in temperate soils. Plant Soil 259:1–7.CrossRefGoogle Scholar
  43. Schmidt IK, Jonasson S, Michelsen A. 1999. Mineralization and microbial immobilization of N and P in arctic soils in relation to season, temperature and nutrient amendment. Appl Soil Ecol 11:147–60.CrossRefGoogle Scholar
  44. Schmidt IK, Jonasson S, Shaver GR, Michelsen A, Nordin A. 2002. Mineralization and distribution of nutrients in plants and microbes in four arctic ecosystems: responses to warming. Plant Soil 242:93–106.CrossRefGoogle Scholar
  45. Shaver GR, Chapin FS. 1980. Response to fertilization by various plant-growth forms in an Alaskan tundra—nutrient accumulation and growth. Ecology 61:662–75.CrossRefGoogle Scholar
  46. Sorensen PL, Michelsen A, Jonasson S. 2008. Nitrogen uptake during one year in subarctic plant functional groups and in microbes after long-term warming and fertilization. Ecosystems 11:223–33.CrossRefGoogle Scholar
  47. Starr G, Oberbauer S. 2003. Photosynthesis of arctic evergreens under snow: implications for tundra ecosystem carbon balance. Ecology 84:1415–20.CrossRefGoogle Scholar
  48. Tye AM, Young SD, Crout NMJ, West HM, Stapleton LM, Poulton PR, Laybourn-Parry J. 2005. The fate of N-15 added to high Arctic tundra to mimic increased inputs of atmospheric nitrogen released from a melting snowpack. Glob Change Biol 11:1640–54.CrossRefGoogle Scholar
  49. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea—how can it occur. Biogeochemistry 13:87–115.CrossRefGoogle Scholar
  50. Warren CR. 2009. Does nitrogen concentration affect relative uptake rates of nitrate, ammonium, and glycine? J Plant Nutr Soil Sci 172:224–9.CrossRefGoogle Scholar
  51. Zhou J, Chen Z, Li S. 2007. Oxidation efficiency of different oxidants of persulfate method used to determine total nitrogen and phosphorus in solutions. Commun Soil Sci Plan 34:725–34.CrossRefGoogle Scholar
  52. Zimov SA, Davidov SP, Voropaev YV, Prosiannikov SF, Semiletov IP, Chapin MC, Chapin FS. 1996. Siberian CO2 efflux in winter as a CO2 source and cause of seasonality in atmospheric CO2. Clim Change 33:111–20.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Klaus S. Larsen
    • 1
    • 2
  • Anders Michelsen
    • 1
    • 3
  • Sven Jonasson
    • 1
  • Claus Beier
    • 2
  • Paul Grogan
    • 4
  1. 1.Terrestrial Ecology Section, Department of BiologyUniversity of CopenhagenCopenhagen KDenmark
  2. 2.Department of Chemical and Biochemical EngineeringTechnical University of DenmarkKgs. LyngbyDenmark
  3. 3.Center for Permafrost (CENPERM)University of CopenhagenCopenhagen KDenmark
  4. 4.Department of BiologyQueen’s UniversityKingstonCanada

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