Skip to main content
SpringerLink
Log in

Soil nitrogen cycling rates in low arctic shrub tundra are enhanced by litter feedbacks

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Shrub growth has increased across the Arctic in recent decades and is strongly limited by soil nitrogen (N) availability. In order to understand the role of N in controlling shrub growth, we compared N-cycling in tall birch (Betula glandulosa) and surrounding dwarf birch hummock vegetation on similar soils in a Canadian low arctic site. Stable isotope tracer analysis revealed N pools and cycling rates were ∼3 times larger and faster in the tall birch ecosystem in the late growing season, just prior to leaf senescence. Gross NH +4 -N production rates in these ecosystems correlated positively with larger pools and production rates of dissolved soil C and N, higher quality litter inputs and lower soil C. Analyses of the soil microbial community in both ecosystems indicated similar fungal dominance (epifluorescence microscopy) and similar compositions of the principal fungal or bacterial phylotypes (denaturing gradient gel electrophoresis). Together, these results strongly suggest that vegetation feedbacks associated with larger inputs of higher quality litter promote rapid soil N-cycling and enhanced shrub growth in tall birch tundra. We conclude that these litter-related feedbacks during summer may be as important as snow-shrub feedbacks in maintaining and promoting differences in shrub growth across the arctic landscape.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  CAS  Google Scholar 

  • Aerts R, van Logtestijn R, Karlsson PS (2006) Nitrogen supply differentially affects litter decomposition rates and nitrogen dynamics of sub-arctic bog species. Oecologia 146:652–658

    Article  CAS  PubMed  Google Scholar 

  • Bliss LC, Matveyeva NV (1992) In: Chapin FSI, Jefferies RL, Reynolds JF, Shaver GR, Svoboda J (eds) Circumpolar arctic vegetation. In Arctic ecosystems in a changing climate: an ecophysiological perspective. Academic, San Diego, pp 59–89

    Google Scholar 

  • Bloem J, Bolhuis PR, Veninga MR, Wieringa J (1995) Microscopic methods for counting bacteria and fungi in soil. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, San Diego, p 576

    Google Scholar 

  • Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–157

    Article  Google Scholar 

  • Bret-Harte MS, Shaver GR, Chapin FS (2002) Primary and secondary stem growth in arctic shrubs: implications for community response to environmental change. J Ecol 90:251–267

    Article  Google Scholar 

  • 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 soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Bryant JP, Swihart RK, Reichardt PB, Newton L (1994) Biogeography of woody plant-chemical defense against snowshoe hare browsing—comparison of Alaska and Eastern North-America. Oikos 70:385–395

    Article  Google Scholar 

  • Buckeridge KM, Grogan P (2008) Deepened snow alters soil microbial nutrient limitations in arctic birch hummock tundra. Appl Soil Ecol 39:210–222

    Article  Google Scholar 

  • Buckeridge KM, Jefferies RL (2007) Vegetation loss alters soil nitrogen dynamics in an Arctic salt marsh. J Ecol 95:283–293

    Article  CAS  Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • Chapin FS, Shaver GR (1981) Changes in soil properties and vegetation following disturbance of Alaskan arctic tundra. J Appl Ecol 18:605–617

    Article  Google Scholar 

  • Chapin FS III, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA (1995) Responses of arctic tundra to experimental and observed changes in climate. Ecol 76:694–711

    Article  Google Scholar 

  • Chapin FS, Sturm M, Serreze MC, McFadden JP, Key JR, Lloyd AH, McGuire AD, Rupp TS, Lynch AH, Schimel JP, Beringer J, Chapman WL, Epstein HE, Euskirchen ES, Hinzman LD, Jia G, Ping CL, Tape KD, Thompson CDC, Walker DA, Welker JM (2005) Role of land-surface changes in Arctic summer warming. Sci 310:657–660

    Article  CAS  Google Scholar 

  • Chu H, Lin XG, Fujii T, Morimoto S, Yagi K, Hu J, Zhang J (2007) Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol Biochem 39:2971–2976

    Article  CAS  Google Scholar 

  • Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071

    Article  PubMed  Google Scholar 

  • Devi N, Hagedorn F, Moiseev P, Bugmann H, Shiyatov S, Mazepa V, Rigling A (2008) Expanding forests and changing growth forms of Siberian larch at the Polar Urals treeline during the 20th century. Glob Chang Biol 14:1581–1591

    Article  Google Scholar 

  • Dijkstra P, Menyailo OV, Doucett RR, Hart SC, Schwartz E, Hungate BA (2006) C and N availability affects the N-15 natural abundance of the soil microbial biomass across a cattle manure gradient. Eur J Soil Sci 57:468–475

    Article  Google Scholar 

  • Eno CF (1960) Nitrate production in the field by incubating the soil in polyethylene bags. Proc Soil Sci Soc Am 24:277–279

    CAS  Google Scholar 

  • Fierer N, Schimel JP, Cates RG, Zou JP (2001) Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol Biochem 33:1827–1839

    Article  CAS  Google Scholar 

  • Giblin AE, Nadelhoffer KJ, Shaver GR, Laundre JA, McKerrow AJ (1991) Biogeochemical diversity along a riverside toposequence in arctic Alaska. Ecol Monogr 61:415–435

    Article  Google Scholar 

  • Goetz SJ, Bunn AG, Fiske GJ, Houghton RA (2005) Satellite-observed photosynthetic trends across boreal North America associated with climate and fire disturbance. Proc Natl Acad Sci USA 102:13521–13525

    Article  CAS  PubMed  Google Scholar 

  • Graglia E, Julkunen-Tiitto R, Shaver GR, Schmidt IK, Jonasson S, Michelsen A (2001) Environmental control and intersite variations of phenolics in Betula nana in tundra ecosystems. New Phytol 151:227–236

    Article  CAS  Google Scholar 

  • Grogan P, Jonasson S (2003) Controls on annual nitrogen cycling in the understory of a subarctic birch forest. Ecol 84:202–218

    Article  Google Scholar 

  • Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In: Bigham JM (ed) Methods of soil analysis, part 2. Microbiological and biochemical properties. Soil Sci Soc Amer, Madison, pp 985–1018

    Google Scholar 

  • Henry HAL, Jefferies RL (2003) Plant amino acid uptake, soluble N turnover and microbial N capture in soils of a grazed arctic salt marsh. J Ecol 91:000–010

    Article  CAS  Google Scholar 

  • Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522

    Article  Google Scholar 

  • IPCC (2007) Climate change 2007. Intergovernmental Panel on Climate Change, Geneva

    Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK, Nielsen EV (1999) Responses in microbes and plants to changed temperature, nutrient, and light regimes in the arctic. Ecol 80:1828–1843

    Article  Google Scholar 

  • Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143

    Article  Google Scholar 

  • Kielland K (1994) Amino-acid-absorption by arctic plants—implications for plant nutrition and nitrogen cycling. Ecol 75:2373–2383

    Article  Google Scholar 

  • Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochem 31:85–98

    Article  CAS  Google Scholar 

  • Kielland K, McFarland J, Olson K (2006) Amino acid uptake in deciduous and coniferous taiga ecosystems. Plant Soil 288:297–307

    Article  CAS  Google Scholar 

  • Kielland K, McFarland JW, Ruess RW, Olson K (2007) Rapid cycling of organic nitrogen in taiga forest ecosystems. Ecosyst 10:360–368

    Article  CAS  Google Scholar 

  • Kirkham D, Bartholomew V (1954) Equations for following nutrient transformations in soil, utilizing tracer data. Soil Sci Soc Amer Proc 18:33–34

    Article  CAS  Google Scholar 

  • Lafleur PM, Humphreys ER (2008) Spring warming and carbon dioxide exchange over low Arctic tundra in central Canada. Glob Chang Biol 14:740–756

    Article  Google Scholar 

  • Marion GM, Miller PC, Kummerow J, Oechel WC (1982) Competition for nitrogen in a tussock tundra ecosystem. Plant Soil 66:317–327

    Article  CAS  Google Scholar 

  • McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software, Gleneden Beach, p 300

    Google Scholar 

  • McFadden JP, Chapin FS, Hollinger DY (1998) Subgrid-scale variability in the surface energy balance of arctic tundra. J Geophys Res-Atmos 103:28947–28961

    Article  CAS  Google Scholar 

  • Moore JC, McCann K, de Ruiter PC (2005) Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiol 49:499–510

    Article  CAS  Google Scholar 

  • Mulvaney RL (1996) Nitrogen - Inorganic forms. In: Sparks DL (ed) Methods of soil analysis. Part 3, chemical methods. Soil Science Society of America and American Society of Agronomy, Madison, WI

  • Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nat 386:698–702

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA (1991) Effects of temperature and substrate quality on element mineralization in 6 arctic soils. Ecol 72:242–253

    Article  Google Scholar 

  • Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. In: Sparks DL (ed) Methods of soil analysis. Part 3, chemical methods. Soil Sci Soc Amer & Amer Soc Agron, Madison, pp 961–1010

    Google Scholar 

  • Nobrega S, Grogan P (2007) Deeper snow enhances winter respiration from both plant-associated and bulk soil carbon pools in birch hummock tundra. Ecosyst 10:419–431

    Article  CAS  Google Scholar 

  • Nobrega S, Grogan P (2008) Landscape and ecosystem-level controls on net carbon dioxide exchange along a natural moisture gradient in Canadian low arctic tundra. Ecosyst 11:377–396

    Article  CAS  Google Scholar 

  • Nordin A, Schmidt IK, Shaver GR (2004) Nitrogen uptake by arctic soil microbes and plants in relation to soil nitrogen supply. Ecol 85:955–962

    Article  Google Scholar 

  • Pennings SC, Siska EL, Bertness MD (2001) Latitudinal differences in plant palatability in Atlantic coast salt marshes. Ecol 82:1344–1359

    Article  Google Scholar 

  • Quested HM, Cornelissen JHC, Press MC, Callaghan TV, Aerts R, Trosien F, Riemann P, Gwynn-Jones D, Kondratchuk A, Jonasson SE (2003) Decomposition of sub-arctic plants with differing nitrogen economies: a functional role for hemiparasites. Ecol 84:3209–3221

    Article  Google Scholar 

  • Rinnan R, Baath E (2009) Differential utilization of carbon substrates by bacteria and fungi in tundra soil. Appl Environ Microbiol 75:3611–3620

    Article  CAS  PubMed  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecol 85:591–602

    Article  Google Scholar 

  • Schimel JP, Chapin FS III (1996) Tundra plant uptake of amino acid and NH4+ nitrogen in situ: plants compete well for amino acid N. Ecol 77:2142–2147

    Article  Google Scholar 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    Article  CAS  Google Scholar 

  • Schimel JP, Bilbrough C, Welker JA (2004) Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol Biochem 36:217–227

    Article  CAS  Google Scholar 

  • Shaver GR, Chapin FS III (1980) Response to fertilization by various plant growth forms in an Alaskan tundra: nutrient accumulation and growth. Ecol 61:662–675

    Article  CAS  Google Scholar 

  • Shaver GR, Chapin FS (1991) Production—biomass relationships and element cycling in contrasting arctic vegetation types. Ecol Monogr 61:1–31

    Article  Google Scholar 

  • Shaver GR, Billings WD, Chapin FS, Giblin AE, Nadelhoffer KJ, Oechel WC, Rastetter EB (1992) Global change and the carbon balance of arctic ecosystems. BioSci 42:433–441

    Article  Google Scholar 

  • Shaver GR, Canadell J, Chapin FS, Gurevitch J, Harte J, Henry G, Ineson P, Jonasson S, Melillo J, Pitelka L, Rustad L (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. BioSci 50:871–882

    Article  Google Scholar 

  • Soil Classification Working Group (1998) The Canadian system of soil classification. NRC, Ottawa

    Google Scholar 

  • Sorensen PL, Clemmensen KE, Michelsen A, Jonasson S, Strom L (2008) Plant and microbial uptake and allocation of organic and inorganic nitrogen related to plant growth forms and soil conditions at two subarctic tundra sites in Sweden. Arct Antarct Alp Res 40:171–180

    Article  Google Scholar 

  • Stark JM, Hart SC (1996) Diffusion technique for preparing salt solutions, Kjeldahl digests, and persulfate digests for nitrogen-15 analysis. Soil Sci Soc Am J 60:1846–1855

    Google Scholar 

  • Sturm M, McFadden JP, Liston GE, Chapin FS, Racine CH, Holmgren J (2001a) Snow-shrub interactions in Arctic tundra: a hypothesis with climatic implications. J Clim 14:336–344

    Article  Google Scholar 

  • Sturm M, Racine C, Tape K (2001b) Climate change—increasing shrub abundance in the Arctic. Nat 411:546–547

    Article  CAS  Google Scholar 

  • Sturm M, Schimel J, Michaelson G, Welker JM, Oberbauer SF, Liston GE, Fahnestock J, Romanovsky VE (2005) Winter biological processes could help convert arctic tundra to shrubland. BioSci 55:17–26

    Article  Google Scholar 

  • Tape K, Sturm M, Racine C (2006) The evidence for shrub expansion in Northern Alaska and the Pan-Arctic. Glob Chang Biol 12:686–702

    Article  Google Scholar 

  • Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay-rates—a microcosm test. Ecol 70:97–104

    Article  Google Scholar 

  • Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104:927–936

    Article  CAS  Google Scholar 

  • Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jonsdottir IS, Klein JA, Magnusson B, Molau U, Oberbauer SF, Rewa SP, Robinson CH, Shaver GR, Suding KN, Thompson CC, Tolvanen A, Totland O, Turner PL, Tweedie CE, Webber PJ, Wookey PA (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103:1342–1346

    Article  CAS  PubMed  Google Scholar 

  • Wallenstein MD, McMahon S, Schimel J (2007) Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiol Ecol 59:428–435

    Article  CAS  PubMed  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Sci 304:1629–1633

    Article  CAS  Google Scholar 

  • Weintraub MN, Schimel JP (2003) Interactions between carbon and nitrogen mineralization and soil organic matter chemistry in arctic tundra soils. Ecosyst 6:129–143

    Article  CAS  Google Scholar 

  • Weintraub MN, Schimel JP (2005a) Nitrogen cycling and the spread of shrubs control changes in the carbon balance of arctic tundra ecosystems. BioSci 55:408–415

    Article  Google Scholar 

  • Weintraub MN, Schimel JP (2005b) The seasonal dynamics of amino acids and other nutrients in Alaskan Arctic tundra soils. Biogeochem 73:359–380

    Article  CAS  Google Scholar 

  • Wookey PA, Aerts R, Bardgett RD, Baptist F, Brathen KA, Cornelissen JHC, Gough L, Hartley IP, Hopkins DW, Lavorel S, Shaver GR (2009) Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Glob Chang Biol 15:1153–1172

    Article  Google Scholar 

Download references

Acknowledgements

We thank the following people and institutions: Linda Cameron, Dragana Rakic, Alison Fidler, Bill Mark, Rick Doucett, and Mat Vankoughnett for laboratory assistance; Tara Zamin, Kate Edwards and two anonymous reviewers for manuscript editing; NSERC (KMB and PG), NSF (DEB 0516509- PG) and the W. Garfield Weston Foundation/ACUNS (KMB) for funding; and Steve Matthews (GNWT), Karin Clark (GNWT) and Aurora Research Institute for logistics.

Author information

Author notes

  1. Erik Zufelt

    Present address: Department of Life Sciences, Queen’s University, Kingston, ON, K7L 3N6, Canada

Authors and Affiliations

  1. Department of Biology, Queen’s University, Kingston, ON, K7L 3N6, Canada

    Kate M. Buckeridge, Erik Zufelt, Haiyan Chu & Paul Grogan

  2. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, East Beijing Road 71, Nanjing, 210008, China

    Haiyan Chu

Authors
  1. Kate M. Buckeridge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erik Zufelt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haiyan Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul Grogan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kate M. Buckeridge.

Additional information

Responsible Editor: Juha Mikola.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buckeridge, K.M., Zufelt, E., Chu, H. et al. Soil nitrogen cycling rates in low arctic shrub tundra are enhanced by litter feedbacks. Plant Soil 330, 407–421 (2010). https://doi.org/10.1007/s11104-009-0214-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-0214-8

Keywords

Search

Navigation