, Volume 21, Issue 8, pp 1564–1579 | Cite as

Decomposition of Senesced Leaf Litter is Faster in Tall Compared to Low Birch Shrub Tundra

  • Casper T. Christiansen
  • Michelle C. Mack
  • Jennie DeMarco
  • Paul Grogan


Many Low Arctic tundra regions are currently undergoing a vegetation shift towards increasing growth and groundcover of tall deciduous shrubs due to recent climate warming. Vegetation change directly affects ecosystem carbon balance, but it can also affect soil biogeochemical cycling through physical and biological feedback mechanisms. Recent studies indicate that enhanced snow accumulation around relatively tall shrubs has negligible physical effect on litter decomposition rates. However, these investigations were no more than 3 years, and therefore may be insufficient to detect differences in inherently slow biogeochemical processes. Here, we report a 5-year study near Daring Lake, Canada, comparing Betula neoalaskana foliar litter decay rates within unmanipulated and snowfenced low-stature birch (height: ~ 0.3 m) plots to test the physical effect of experimentally deepened snow, and within tall birch (height: ~ 0.8 m) plots to test the combined physical and biological effects, that is, deepened snow plus strong birch dominance. Having corrected for carbon gain by the colonizing decomposers, actual litter carbon loss increased by approximately 25% in the tall birch relative to both low birch sites. Decay of lignin-like acid unhydrolizable litter residues also accelerated in the tall birch site, and a similar but lower magnitude response in the snowfenced low birch site indicated that physical effects of deepened snow were at least partially responsible. In contrast, deepened snow alone did not affect litter carbon loss. Our findings suggest that a combination of greater litter inputs, altered soil microbial community, enhanced soil nutrient pools, and warmer winter soils together promote relatively fast decomposition of recalcitrant litter carbon in tall birch shrub environments.


Arctic Betula climate warming deepened snow litter decomposition deciduous shrubs long-term investigation 



We are thankful for lab assistance from Yvette Chirinian, Olivia RoDee, and Samantha Miller. We also thank Mike Treberg and Robbie Hember for constructing the snowfences, and Karin Clark and Steve and Louise Matthews for logistical support at the Daring Lake TERS. Many helpful comments from two anonymous reviewers greatly improved the manuscript. This work was financed by NSERC and the Department of Environment and Natural Resources in the Government of the Northwest Territories. C.T.C. was financed by an Ontario Trillium scholarship from the Ontario Ministry of Training, Colleges and Universities. M.C.M. and J.D.’s participation was funded by NSF Grants DEB-0516041 and OPP-6767545.

Supplementary material

10021_2018_240_MOESM1_ESM.docx (3.1 mb)
Supplementary material 1 (DOCX 3158 kb)


  1. Aerts R, Callaghan TV, Dorrepaal E, van Logtestijn RSP, Cornelissen JHC. 2012. Seasonal climate manipulations have only minor effects on litter decomposition rates and N dynamics but strong effects on litter P dynamics of sub-arctic bog species. Oecologia 170:809–19.CrossRefGoogle Scholar
  2. Ågren GI, Wetterstedt JAM. 2007. What determines the temperature response of soil organic matter decomposition? Soil Biol Biochem 39:1794–8.CrossRefGoogle Scholar
  3. Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Ann Rev Plant Biol 54:519–46.CrossRefGoogle Scholar
  4. Bokhorst S, Metcalfe DB, Wardle DA. 2013. Reduction in snow depth negatively affects decomposers but impact on decomposition rates is substrate dependent. Soil Biol Biochem 62:157–64.CrossRefGoogle Scholar
  5. Buckeridge KM, Banerjee S, Siciliano SD, Grogan P. 2013. The seasonal pattern of soil microbial community structure in mesic Low Arctic tundra. Soil Biol Biochem 65:338–47.CrossRefGoogle Scholar
  6. Buckeridge KM, Cen YP, Layzell DB, Grogan P. 2010a. Soil biogeochemistry during the early spring in Low Arctic mesic tundra and the impacts of deepened snow and enhanced nitrogen availability. Biogeochemistry 99:127–41.CrossRefGoogle Scholar
  7. Buckeridge KM, Grogan P. 2008. Deepened snow alters soil microbial nutrient limitations in Arctic birch hummock tundra. Appl Soil Ecol 39:210–22.CrossRefGoogle Scholar
  8. Buckeridge KM, Grogan P. 2010. Deepened snow increases late thaw biogeochemical pulses in mesic Low Arctic tundra. Biogeochemistry 101:105–21.CrossRefGoogle Scholar
  9. Buckeridge KM, Zufelt E, Chu HY, Grogan P. 2010b. Soil nitrogen cycling rates in Low Arctic shrub tundra are enhanced by litter feedbacks. Plant Soil 330:407–21.CrossRefGoogle Scholar
  10. Chapin FS, Fetcher N, Kielland K, Everett KR, Linkins AE. 1988. Productivity and nutrient cycling of Alaskan tundra: enhancement by flowing soil water. Ecology 69:693–702.CrossRefGoogle Scholar
  11. Chapin FS, Moilanen L. 1991. Nutritional controls over nitrogen and phosphorus resorption from Alaskan birch leaves. Ecology 72:709–15.CrossRefGoogle Scholar
  12. Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA. 1995. Responses of Arctic tundra to experimental and observed changes in climate. Ecology 76:694–711.CrossRefGoogle Scholar
  13. Chapin FS, Shaver GR, Mooney HA. 2002. Principles of terrestrial ecosystem ecology. New York, USA: Springer. p 529.Google Scholar
  14. 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. Science 310:657–60.CrossRefGoogle Scholar
  15. Christiansen CT, Haugwitz MS, Priemé A, Nielsen CS, Elberling B, Michelsen A, Grogan P, Blok D. 2017. Enhanced summer warming reduces fungal decomposer diversity and litter mass loss more strongly in dry than in wet tundra. Global Change Biol 23:406–20.CrossRefGoogle Scholar
  16. Chu H, Grogan P. 2010. Soil microbial biomass, nutrient availability and nitrogen mineralization potential among vegetation-types in a low arctic tundra landscape. Plant Soil 329:411–20.CrossRefGoogle Scholar
  17. Chu HY, Neufeld JD, Walker VK, Grogan P. 2011. The influence of vegetation type on the dominant soil bacteria, archaea, and fungi in a Low Arctic tundra landscape. Soil Sci Soc Am 75:1756–65.CrossRefGoogle Scholar
  18. Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins FM, Hyvonen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Steinweg JM, Wallenstein MD, Wetterstedt JAM, Bradford MA. 2011. Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Global Change Biol 17:3392–404.CrossRefGoogle Scholar
  19. DeMarco J, Mack MC, Bret-Harte MS. 2011. The effects of snow, soil microenvironment, and soil organic matter quality on N availability in three Alaskan Arctic plant communities. Ecosystems 14:804–17.CrossRefGoogle Scholar
  20. DeMarco J, Mack MC, Bret-Harte MS. 2014a. Effects of Arctic shrub expansion on biophysical vs. biogeochemical drivers of litter decomposition. Ecology 95:1861–75.CrossRefGoogle Scholar
  21. DeMarco J, Mack MC, Bret-Harte MS, Burton M, Shaver GR. 2014b. Long-term experimental warming and nutrient additions increase productivity in tall deciduous shrub tundra. Ecosphere 5:72.CrossRefGoogle Scholar
  22. Deslippe JR, Hartmann M, Mohn WW, Simard SW. 2011. Long-term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra. Global Change Biol 17:1625–36.CrossRefGoogle Scholar
  23. Elberling B, Brandt KK. 2003. Uncoupling of microbial CO2 production and release in frozen soil and its implications for field studies of Arctic C cycling. Soil Biol Biochem 35:263–72.CrossRefGoogle Scholar
  24. Elmendorf SC, Henry GHR, Hollister RD, Bjork RG, Boulanger-Lapointe N, Cooper EJ, Cornelissen JHC, Day TA, Dorrepaal E, Elumeeva TG, Gill M, Gould WA, Harte J, Hik DS, Hofgaard A, Johnson DR, Johnstone JF, Jonsdottir IS, Jorgenson JC, Klanderud K, Klein JA, Koh S, Kudo G, Lara M, Levesque E, Magnusson B, May JL, Mercado-Diaz JA, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Onipchenko VG, Rixen C, Schmidt NM, Shaver GR, Spasojevic MJ, Porhallsdottir PE, Tolvanen A, Troxler T, Tweedie CE, Villareal S, Wahren CH, Walker X, Webber PJ, Welker JM, Wipf S. 2012. Plot-scale evidence of tundra vegetation change and links to recent summer warming. Nat Clim Change 2:453–7.CrossRefGoogle Scholar
  25. Epstein HE, Raynolds MK, Walker DA, Bhatt US, Tucker CJ, Pinzon JE. 2012. Dynamics of aboveground phytomass of the circumpolar Arctic tundra during the past three decades. Environ Res Lett 7:015506.CrossRefGoogle Scholar
  26. Erhagen B, Öquist M, Sparrman T, Haei M, Ilstedt U, Hedenström M, Schleucher J, Nilsson MB. 2013. Temperature response of litter and soil organic matter decomposition is determined by chemical composition of organic material. Global Change Biol 19:3858–71.CrossRefGoogle Scholar
  27. Forbes BC, Fauria MM, Zetterberg P. 2010. Russian Arctic warming and ‘greening’ are closely tracked by tundra shrub willows. Global Change Biol 16:1542–54.CrossRefGoogle Scholar
  28. Goetz SJ, Bunn AG, Fiske GJ, Houghton RA. 2005. Satellite-observed photosynthetic trends across boreal North America associated with climate and fire disturbance. Proc Nat Acad Sci 102:13521–5.CrossRefGoogle Scholar
  29. Grogan P. 2012. Cold season respiration across a Low Arctic landscape: the influence of vegetation type, snow depth, and interannual climatic variation. Arct Antarct Alp Res 44:446–56.CrossRefGoogle Scholar
  30. Hartley IP, Garnett MH, Sommerkorn M, Hopkins DW, Fletcher BJ, Sloan VL, Phoenix GK, Wookey PA. 2012. A potential loss of carbon associated with greater plant growth in the European Arctic. Nat Clim Change 2:875–9.CrossRefGoogle Scholar
  31. Hernández DL, Hobbie SE. 2010. The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil 335:397–411.CrossRefGoogle Scholar
  32. Higuchi T. 1990. Lignin biochemistry: biosynthesis and biodegradation. Wood Sci Technol 24:23–63.CrossRefGoogle Scholar
  33. Hobbie SE. 1996. Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–22.CrossRefGoogle Scholar
  34. Hobbie SE, Chapin FS. 1996. Winter regulation of tundra litter carbon and nitrogen dynamics. Biogeochemistry 35:327–38.CrossRefGoogle Scholar
  35. Hobbie SE, Schimel JP, Trumbore SE, Randerson JR. 2000. Controls over carbon storage and turnover in high-latitude soils. Global Change Biol 6:196–210.CrossRefGoogle Scholar
  36. Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70.Google Scholar
  37. Jia GS, Epstein HE, Walker DA. 2006. Spatial heterogeneity of tundra vegetation response to recent temperature changes. Global Change Biol 12:42–55.CrossRefGoogle Scholar
  38. Jonasson S, Michelsen A, Schmidt IK, Nielsen EV. 1999. Responses in microbes and plants to changed temperature, nutrient, and light regimes in the Arctic. Ecology 80:1828–43.CrossRefGoogle Scholar
  39. Ju J, Masek JG. 2016. The vegetation greenness trend in Canada and US Alaska from 1984–2012 Landsat data. Remote Sens Environ 176:1–16.CrossRefGoogle Scholar
  40. Kögel-Knabner I. 2002. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–62.CrossRefGoogle Scholar
  41. Kuo S. 1996. Phosphorus. Sparks DL editor. Methods of soil analysis. Part 3: Chemical methods. Madison, WI, USA: Soil Science Society of America and American Society of Agronomy, pp 869–919.Google Scholar
  42. Kuzyakov Y, Friedel JK, Stahr K. 2000. Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–98.CrossRefGoogle Scholar
  43. Littell RC, Milliken GA, Stroup WW, Wolfinger RD. 1996. SAS© system for mixed models. Cary, North Carolina: SAS Institute Inc. pp 1–633.Google Scholar
  44. Manzoni S, Jackson RB, Trofymow JA, Porporato A. 2008. The global stoichiometry of litter nitrogen mineralization. Science 321:684–6.CrossRefGoogle Scholar
  45. Manzoni S, Trofymow JA, Jackson RB, Porporato A. 2010. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106.CrossRefGoogle Scholar
  46. McLaren JR, Buckeridge KM, Weg MJ, Shaver GR, Schimel JP, Gough L. 2017. Shrub encroachment in Arctic tundra: Betula nana effects on above-and belowground litter decomposition. Ecology 98:1361–76.CrossRefGoogle Scholar
  47. McMahon SK, Wallenstein MD, Schimel JP. 2009. Microbial growth in Arctic tundra soil at -2 degrees C. Environ Microbiol Reports 1:162–6.CrossRefGoogle Scholar
  48. McMahon SK, Wallenstein MD, Schimel JP. 2011. A cross-seasonal comparison of active and total bacterial community composition in Arctic tundra soil using bromodeoxyuridine labeling. Soil Biol Biochem 43:287–95.CrossRefGoogle Scholar
  49. Mikan CJ, Schimel JP, Doyle AP. 2002. Temperature controls of microbial respiration in Arctic tundra soils above and below freezing. Soil Biol Biochem 34:1785–95.CrossRefGoogle Scholar
  50. Moore TR. 1984. Litter decomposition in a Subarctic spruce-lichen woodland, Eastern Canada. Ecology 65:299–308.CrossRefGoogle Scholar
  51. Myers-Smith IH, Elmendorf SC, Beck PSA, Wilmking M, Hallinger M, Blok D, Tape KD, Rayback SA, Macias-Fauria M, Forbes BC, Speed JDM, Boulanger-Lapointe N, Rixen C, Levesque E, Schmidt NM, Baittinger C, Trant AJ, Hermanutz L, Collier LS, Dawes MA, Lantz TC, Weijers S, Jorgensen RH, Buchwal A, Buras A, Naito AT, Ravolainen V, Schaepman-Strub G, Wheeler JA, Wipf S, Guay KC, Hik DS, Vellend M. 2015. Climate sensitivity of shrub growth across the tundra biome. Nat Clim Change 5:887–91.CrossRefGoogle Scholar
  52. Myers-Smith IH, Forbes BC, Wilmking M, Hallinger M, Lantz T, Blok D, Tape KD, Macias-Fauria M, Sass-Klaassen U, Levesque E, Boudreau S, Ropars P, Hermanutz L, Trant A, Collier LS, Weijers S, Rozema J, Rayback SA, Schmidt NM, Schaepman-Strub G, Wipf S, Rixen C, Menard CB, Venn S, Goetz S, Andreu-Hayles L, Elmendorf S, Ravolainen V, Welker J, Grogan P, Epstein HE, Hik DS. 2011. Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6:045509.CrossRefGoogle Scholar
  53. Myers-Smith IH, Hik DS. 2013. Shrub canopies influence soil temperatures but not nutrient dynamics: an experimental test of tundra snow–shrub interactions. Ecol Evol 3:3683–700.CrossRefGoogle Scholar
  54. Nobrega S, Grogan P. 2007. Deeper snow enhances winter respiration from both plant-associated and bulk soil carbon pools in birch hummock tundra. Ecosystems 10:419–31.CrossRefGoogle Scholar
  55. 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. Ecosystems 11:377–96.CrossRefGoogle Scholar
  56. Öquist MG, Sparrman T, Klemedtsson L, Drotz SH, Grip H, Schleucher J, Nilsson M. 2009. Water availability controls microbial temperature responses in frozen soil CO2 production. Global Change Biol 15:2715–22.CrossRefGoogle Scholar
  57. Osono T. 2007. Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–74.CrossRefGoogle Scholar
  58. Parker TC, Subke J-A, Wookey PA. 2015. Rapid carbon turnover beneath shrub and tree vegetation is associated with low soil carbon stocks at a Subarctic treeline. Global Change Biol 21:2070–81.CrossRefGoogle Scholar
  59. Parkinson JA, Allen SE. 1975. Wet oxidation procedure suitable for determination of nitrogen and mineral nutrients in biological-material. Commun Soil Sci Plant Anal 6:1–11.CrossRefGoogle Scholar
  60. Preston CM, Trofymow JA, Niu J, Sayer BG. 1997. 13C nuclear magnetic resonance spectroscopy with cross-polarization and magic-angle spinning investigation of the proximate-analysis fractions used to assess litter quality in decomposition studies. Can J Bot 75:1601–13.CrossRefGoogle Scholar
  61. Ryan MG, Melillo JM, Ricca A. 1990. A comparison of methods for determining proximate carbon fractions of forest litter. Can J For Res 20:166–71.CrossRefGoogle Scholar
  62. Saiz-Jimenez C. 1996. Chapter 1—The chemical structure of humic substances: recent advances. In: Piccolo A, Ed. Humic substances in terrestrial ecosystems. Amsterdam: Elsevier Science. p 1–44.Google Scholar
  63. Schadt CW, Martin AP, Lipson DA, Schmidt SK. 2003. Seasonal dynamics of previously unknown fungal lineages in tundra soils. Science 301:1359–61.CrossRefGoogle Scholar
  64. Schimel JP, Bilbrough C, Welker JA. 2004. Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol Biochem 36:217–27.CrossRefGoogle Scholar
  65. Schimel JP, Weintraub MN. 2003. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–63.CrossRefGoogle Scholar
  66. Schreeg LA, Mack MC, Turner BL. 2013. Nutrient-specific solubility patterns of leaf litter across 41 lowland tropical woody species. Ecology 94:94–105.CrossRefGoogle Scholar
  67. Semenchuk PR, Elberling B, Amtorp C, Winkler J, Rumpf S, Michelsen A, Cooper EJ. 2015. Deeper snow alters soil nutrient availability and leaf nutrient status in High Arctic tundra. Biogeochemistry 124:81–94.CrossRefGoogle Scholar
  68. Shaver GR, Bret-Harte SM, Jones MH, Johnstone J, Gough L, Laundre J, Chapin FS. 2001. Species composition interacts with fertilizer to control long-term change in tundra productivity. Ecology 82:3163–81.CrossRefGoogle Scholar
  69. Sørensen MV, Strimbeck R, Nystuen KO, Kapas RE, Enquist BJ, Graae BJ. 2017. Draining the pool? Carbon storage and fluxes in three Alpine plant communities. Ecosystems: 1–15.Google Scholar
  70. Sturm M, McFadden JP, Liston GE, Chapin FS, Racine CH, Holmgren J. 2001. Snow-shrub interactions in Arctic tundra: a hypothesis with climatic implications. J Clim 14:336–44.CrossRefGoogle Scholar
  71. 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. Bioscience 55:17–26.CrossRefGoogle Scholar
  72. Tape K, Sturm M, Racine C. 2006. The evidence for shrub expansion in Northern Alaska and the Pan-Arctic. Global Change Biol 12:686–702.CrossRefGoogle Scholar
  73. Tremblay B, Levesque E, Boudreau S. 2012. Recent expansion of erect shrubs in the Low Arctic: evidence from Eastern Nunavik. Environ Res Lett 7:035501.CrossRefGoogle Scholar
  74. Vankoughnett MR, Grogan P. 2014. Nitrogen isotope tracer acquisition in low and tall birch tundra plant communities: a 2 year test of the snow–shrub hypothesis. Biogeochemistry 118:291–306.CrossRefGoogle Scholar
  75. Vankoughnett MR, Grogan P. 2016. Plant production and nitrogen accumulation above-and belowground in low and tall birch tundra communities: the influence of snow and litter. Plant Soil 408:195–210.CrossRefGoogle Scholar
  76. Walker DA, Raynolds MK, Daniels FJA, Einarsson E, Elvebakk A, Gould WA, Katenin AE, Kholod SS, Markon CJ, Melnikov ES, Moskalenko NG, Talbot SS, Yurtsev BA, Team C. 2005. The circumpolar Arctic vegetation map. J Veg Sci 16:267–82.CrossRefGoogle Scholar
  77. Walker MD, Walker DA, Welker JM, Arft AM, Bardsley T, Brooks PD, Fahnestock JT, Jones MH, Losleben M, Parsons AN, Seastedt TR, Turner PL. 1999. Long-term experimental manipulation of winter snow regime and summer temperature in Arctic and Alpine tundra. Hydrol Process 13:2315–30.CrossRefGoogle Scholar
  78. Wallenstein MD, McMahon S, Schimel J. 2007. Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiology Ecology 59:428–35.CrossRefGoogle Scholar
  79. Wickings K, Grandy AS, Reed SC, Cleveland CC. 2012. The origin of litter chemical complexity during decomposition. Ecol Lett 15:1180–8.CrossRefGoogle Scholar
  80. Wilmking M, Harden J, Tape K. 2006. Effect of tree line advance on carbon storage in NW Alaska. J Geophys Res Biogeosci 111:G02023.CrossRefGoogle Scholar
  81. Zamin TJ, Bret-Harte MS, Grogan P. 2014. Evergreen shrubs dominate responses to experimental summer warming and fertilization in Canadian mesic Low Arctic tundra. J Ecol 102:749–66.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Casper T. Christiansen
    • 1
    • 2
  • Michelle C. Mack
    • 3
  • Jennie DeMarco
    • 4
  • Paul Grogan
    • 1
  1. 1.Department of BiologyQueen’s UniversityKingstonCanada
  2. 2.Uni Research ClimateBjerknes Centre for Climate ResearchBergenNorway
  3. 3.Center for Ecosystem Science and Society and Department of Biological SciencesNorthern Arizona UniversityFlagstaffUSA
  4. 4.Department of BiologyUniversity of FloridaGainesvilleUSA

Personalised recommendations