Soils of northern latitude tundra ecosystems have accumulated large amounts of carbon that might be released as CO2 when temperature rises and the tree-line moves north. We aim to investigate the potential CO2 flux changes at a subarctic tundra heath under changing climate.
We measured daytime ecosystem respiration and photosynthesis at a subarctic heath over a full year under ambient conditions and in factorial long-term (13 years) increased summer temperature and leaf litter addition plots, and in additional short-term (2 years) summer warming plots.
Under ambient conditions the ecosystem was a daytime sink of CO2 in the five warmest months, but a net daytime source in the cold season. Thirteen years of summer warming by 1 °C at soil surface increased CO2 emissions, as daytime respiration increased by 37% and photosynthesis by 29% over the year. Short-term warming likewise increased fluxes. Litter addition also increased the emission of CO2 as ecosystem respiration rose by 21% but photosynthesis remained unchanged. Both warming and litter addition significantly enhanced the amount of green biomass.
This study suggests that in a changed climate subarctic ecosystems will act as a positive feedback source of atmospheric CO2. It shows the significance of CO2 fluxes outside the growing season and demonstrates a cold-season long- but not short-term legacy effect of increased summer warming on CO2 emission.
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Abisko Scientific Research Station (2016) Temperature and precipitation data 1913–2015. Available from: http://polar.se/abisko. Accessed 13 Nov 2012
Arndal MF, Illeris L, Michelsen A, Albert K, Tamstorf M, Hansen BU (2009) Seasonal variation in gross ecosystem production, plant biomass, and carbon and nitrogen pools in five high arctic vegetation types. Arct Antarct Alp Res 41:164–173
Belshe EF, Schuur EG, Bolker BM (2013) Tundra ecosystems observed to be CO2 sources due to differential amplification of the carbon cycle. Ecol Lett 16:1307–1315
Bengtson P, Barker J, Grayston SJ (2012) Evidence of a strong coupling between root exudation, C and N availability, and stimulated SOM decomposition caused by rhizosphere priming effects. Ecol Evol 2:1843–1852
Boelman NT, Stieglitz M, Rueth HM, Sommerkorn M, Griffin KL, Shaver GR, Gamon JA (2003) Response of NDVI, biomass, and ecosystem gas exchange to long-term warming and fertilization in wet sedge tundra. Oecologia 135:414–421
Brooks PD, Grogan P, Templer PH, Groffman P, Öquist MG, Schimel J (2011) Carbon and nitrogen cycling in snow-covered environments. Geogr Compass 5:682–699
Campioli M, Leblans N, Michelsen A (2012) Twenty-two years of warming, fertilisation and shading of subarctic heath shrubs promote secondary growth and plasticity but not primary growth. PLoS One 7(4):e34842
Christiansen CT, Schmidt NM, Michelsen A (2012) High arctic dry heath CO2 exchange during the early cold season. Ecosystems 15:1083–1092
Collins M, Knutti R, Arblaster J (2013) Long-term climate change: projections, commitents and irreversibility Climate Change 2013: The Physical Science Basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM). Cambridge University Press, Cambridge , United Kingdom and New York, NY, USA
Crowther TW, Todd-Brown KEO, Rowe CW, Wieder WR, Carey JC, Machmuller MB, Snoek BL, Fang S, Zhou G, Allison SD, Blair JM, Bridgham SD, Burton AJ, Carrillo Y, Reich PB, Clark JS, Classen AT, Dijkstra FA, Elberling B, Emmett BA, Estiarte M, Frey SD, Guo J, Harte J, Jiang L, Johnson BR, Kröel-Dulay G, Larsen KS, Laudon H, Lavallee JM, Luo Y, Lupascu M, Ma LN, Marhan S, Michelsen A, Mohan J, Niu S, Pendall E, Peñuelas J, Pfeifer-Meister L, Poll C, Reinsch S, Reynolds LL, Schmidt IK, Sistla S, Sokol NW, Templer PH, Treseder KK, Welker JM, Bradford MA (2016) Quantifying global soil carbon losses in response to warming. Nature 540:104–108
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173
DeMarco J, Mack MC, Bret-Harte MS (2014a) Effects of arctic shrub expansion on biophysical vs. biogeochemical drivers of litter decomposition. Ecology 95:1861–1875
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
Elmendorf SC, Henry GHR, Hollister RD, Björk 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, Jónsdóttir IS, Jorgenson JC, Klanderud K, Klein JA, Koh S, Kudo G, Lara M, Lévesque E, Magnússon B, May JL, Mercado-Dı´az JA, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Onipchenko VG, Rixen C, Martin Schmidt N, Shaver GR, Spasojevic MJ, Þórhallsdóttir ÞE, 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 Chang 2:453–457
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-Atmos 103:29023–29027
Grogan P, Chapin FS (1999) Arctic soil respiration: effects of climate and vegetation depend on season. Ecosystems 2:451–459
Grogan P, Jonasson S (2005) Temperature and substrate controls on intra-annual variation in ecosystem respiration in two subarctic vegetation types. Glob Chang Biol 11:465–475
Grogan P, Jonasson S (2006) Ecosystem CO2 production during winter in a Swedish subarctic region: the relative importance of climate and vegetation type. Glob Chang Biol 12:1479–1495
Grogan P, Illeris L, Michelsen A, Jonasson S (2001) Respiration of recently-fixed plant carbon dominates mid-winter ecosystem CO2 production in sub-arctic heath tundra. Clim Chang 50:129–142
Hartley IP, Garnett M, Sommerkorn M, Hopkins DW, Fletcher BJ, Sloan VL, Wookey PA (2012) A potential loss of carbon associated with greater plant growth in the European Arctic. Nat Clim Chang 2:875–879
Hicks-Pries CE, van Logtestijn RSP, Schuur EAG, Natali SM, Cornelissen JHC, Aerts R, Dorrepaal E (2015) Decadal warming causes a consistent and persistent shift from heterotrophic to autotrophic respiration in contrasting permafrost ecosystems. Glob Chang Biol 21:4508–4519
Hicks-Pries CE, Bird JA, Castanha C, Hatton PJ, Torn MS (2017) Long term decomposition: the influence of litter type and soil horizon on retention of plant carbon and nitrogen in soils. Biogeochemistry 134:5–16
Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522
Hugelius G, Strauss J, Zubrzycki S, Harden JW, Schuur EAG, Ping CL, Schirrmeister L, Grosse G, Michaelson GJ, Koven CD, O'Donnell JA, Elberling B, Mishra U, Camill P, Yu Z, Palmtag J, Kuhry P (2014) Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11:6573–6593
Illeris L, Christensen TR, Mastepanov M (2004a) Moisture effects on temperature sensitivity of CO2 exchange in a subarctic heath ecosystem. Biogeochemistry 70:315–330
Illeris L, Konig SM, Grogan P, Jonasson S, Michelsen A, Ro-Poulsen H (2004b) Growing-season carbon dioxide flux in a dry subarctic heath: responses to long-term manipulations. Arct Antarct Alp Res 36:456–463
Lafleur PM, Humphreys ER, St Louis VL, Myklebust MC, Papakyriakou T, Poissant L, Barker JD, Pilote M, Swystun KA (2012) Variation in peak growing season net ecosystem production across the Canadian Arctic. Environ Sci Technol 46:7971–7977
Larsen KS, Grogan P, Jonasson S, Michelsen A (2007a) Respiration and microbial dynamics in two subarctic ecosystems during winter and spring thaw: effects of increased snow depth. Arct Antarct Alp Res 39:268–276
Larsen KS, Ibrom A, Beier C, Jonasson S, Michelsen A (2007b) Ecosystem respiration depends strongly on photosynthesis in a temperate heath. Biogeochemistry 85:201–213
Larsen KS, Ibrom A, Jonasson S, Michelsen A, Beier C (2007c) Significance of cold-season respiration and photosynthesis in a subarctic heath ecosystem in northern Sweden. Glob Chang Biol 13:1498–1508
Leffler AJ, Klein ES, Oberbauer SF, Welker JM (2016) Coupled long-term summer warming and deeper snow alters species composition and stimulates gross primary productivity in tussock tundra. Oecologia 181:287–297
Lett S, Michelsen A (2014) Seasonal variation in nitrogen fixation and effects of climate change in a subarctic heath. Plant Soil 379:193–204
Lund M, Falk JM, Friborg T, Mbufong HN, Sigsgaard C, Soegaard H, Tamstorf MP (2012) Trends in CO2 exchange in a high Arctic tundra heath, 2000-2010. J Geophys Res Biogeosci 117:G02001
Mauritz M, Bracho R, Celis G, Hutchings J, Natali SM, Pegoraro E, Salmon VG, Schädel C, Webb EE, Schuur EAG (2017) Nonlinear CO2 flux response to 7 years of experimentally induced permafrost thaw. Glob Chang Biol 23:3646–3666
McMichael CE, Hope AS, Stow DA, Fleming JB, Vourlitis G, Oechel W (1999) Estimating CO2 exchange at two sites in Arctic tundra ecosystems during the growing season using a spectral vegetation index. Int J Remote Sens 20:683–698
Metcalfe DB, Hermans TDG, Ahlstrand J, Becker M, Berggren M, Bjork RG, Bjorkman MP, Blok D, Chaudhary N, Chisholm C, Classen AT, Hasselquist NJ, Jonsson M, Kristensen JA, Kumordzi BB, Lee H, Mayor JR, Prevey J, Pantazatou K, Rousk J, Sponseller RA, Sundqvist MK, Tang J, Uddling J, Wallin G, Zhang WX, Ahlstrom A, Tenenbaum DE, Abdi AM (2018) Patchy field sampling biases understanding of climate change impacts across the Arctic. Nat Ecol Evol 2:1443–1448
Moore TR, Lafleur PM, Poon DMI, Heumann BW, Seaquist JW, Roulet NT (2006) Spring photosynthesis in a cool temperate bog. Glob Chang Biol 12:2323–2335
Myers-Smith IH, Forbes BC, Wilmking M, Hallinger M, Lantz T, Blok D, Tape KD, Macias-Fauria M, Sass-Klaassen U, Lévesque 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, Ménard 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
Natali SM, Schuur EAG, Trucco C, Hicks-Pries CE, Crummer KG, Lopez AFB (2011) Effects of experimental warming of air, soil and permafrost on carbon balance in Alaskan tundra. Glob Chang Biol 17:1394–1407
Natali SM, Schuur EG, Webb EE, Hicks-Pries CE, Crummer KG (2014) Permafrost degradation stimulates carbon loss from experimentally warmed tundra. Ecology 95:602–608
Natali SM, Schuur EAG, Mauritz M, Schade JD, Celis G, Crummer KG, Johnston C, Krapek J, Pegoraro E, Salmon VG, Webb EE (2015) Permafrost thaw and soil moisture driving CO2 and CH4 release from upland tundra. J Geophys Res Biogeosci 120:525–537
Oberbauer SF, Tweedie CE, Welker JM, Fahnestock JT, Henry GHR, Webber PJ, Hollister RD, Walker MD, Kuchy A, Elmore E, Starr G (2007) Tundra CO2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecol Monogr 77:221–238
Pedersen EP, Elberling B, Michelsen A (2017) Seasonal variations in methane fluxes in response to summer warming and leaf litter addition in a subarctic heath ecosystem. J Geophys Res Biogeosci 122:2137–2153
Phillips CA, Elberling B, Michelsen A (2019) Soil carbon and nitrogen stocks and turnover following 16 years of warming and litter addition. Ecosystems 22:110–124
Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Hoye TT, Ims RA, Jeppesen E, Klein DR, Madsen J, McGuire AD, Rysgaard S, Schindler DE, Stirling I, Tamstorf MP, Tyler NJC, van der Wal R, Welker J, Wookey PA, Schmidt NM, Aastrup P (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358
PP Systems (2018) EGM-5 portable CO2 gas analyzer operation manual, version 1.03, Amesbury, MA 01913 U.S.A.; www.ppsystems.com
Ravn NR, Ambus P, Michelsen A (2017) Impact of decade-long warming, nutrient addition and shading on emission and carbon isotopic composition of CO2 from two subarctic dwarf shrub heaths. Soil Biol Biochem 111:15–24
Rinnan R, Michelsen A, Jonasson S (2008) Effects of litter addition and warming on soil carbon, nutrient pools and microbial communities in a subarctic heath ecosystem. Appl Soil Ecol 39:271–281
Schuur EAG, McGuire AD, Schadel C, Grosse G, Harden JW, Hayes DJ, Hugelius G, Koven CD, Kuhry P, Lawrence DM, Natali SM, Olefeldt D, Romanovsky VE, Schaefer K, Turetsky MR, Treat CC, Vonk JE (2015) Climate change and the permafrost carbon feedback. Nature 520:171–179
Seneviratne SI, Rogelj J, Seferian R, Wartenburger R, Allen MR, Cain M, Millar RJ, Ebi KL, Ellis N, Hoegh-Guldberg O, Payne AJ, Schleussner CF, Tschakert P, Warren RF (2018) The many possible climates from the Paris Agreement's aim of 1.5 degrees C warming. Nature 558:41–49
Serreze MC, Walsh JE, Chapin FS, Osterkamp T, Dyurgerov M, Romanovsky V, Oechel WC, Morison J, Zhang T, Barry RG (2000) Observational evidence of recent change in the northern high-latitude environment. Clim Chang 46:159–207
Shaver GR, Chapin FS III (1980) Response to fertilization by various plant growth forms in an Alaskan tundra. Ecology 61:662–675
Sistla SA, Moore JC, Simpson RT, Gough L, Shaver GR, Schimel JP (2013) Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497:615–618
Sorensen PL, Michelsen A (2011) Long-term warming and litter addition affects nitrogen fixation in a subarctic heath. Glob Chang Biol 17:528–537
Starr G, Oberbauer SF (2003) Photosynthesis of arctic evergreens under snow: implications for tundra ecosystem carbon balance. Ecology 84:1415–1420
Street LE, Shaver GR, Willliams M, van Wijk MT (2007) What is the relationship between changes in canopy leaf area and changes in photosynthetic CO2 flux in arctic ecosystems? J Ecol 95:139–150
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
Tiiva P, Faubert P, Michelsen A, Holopainen T, Holopainen JK, Rinnan R (2008) Climatic warming increases isoprene emission from a subarctic heath. New Phytol 180:853–863
Virkkala AM, Virtanen T, Lehtonen A, Rinne J, Luoto M (2018) The current state of CO2 flux chamber studies in the Arctic tundra: a review. Progress in Physical Geography-Earth and Environment 42:162–184
Voigt C, Lamprecht RE, Marushchak ME, Lind SE, Novakovskiy A, Aurela M, Martikainen PJ, Biasi C (2016) Warming of subarctic tundra increases emissions of all three important greenhouse gases - carbon dioxide, methane and nitrous oxide. Glob Chang Biol 43:4566–4575
Webb EE, Schuur EAG, Natali SM, Oken KL, Bracho R, Krapek JP, Risk D, Nickerson NR (2016) Increased wintertime CO2 loss as a result of sustained tundra warming. J Geophys Res Biogeosci 121:249–265
Welker JM, Brown KB, Fahnestock JT (1999) CO2 flux in Arctic and alpine dry tundra: comparative field responses under ambient and experimentally warmed conditions. Arct Antarct Alp Res 31:272–277
Welker JM, Fahnestock JT, Henry GHR, O'dea KW, Chimner RA (2004) CO2 exchange in three Canadian high Arctic ecosystems: response to long-term experimental warming. Glob Chang Biol 10:1981–1995
We acknowledge The Danish Council for Independent Research and The Danish National Research Foundation (CENPERM DNRF100) for financial support. The research has additionally received funding from INTERACT (grant agreement No 262693) under the European Community’s Seventh Framework Programme. We thank Marie Glahn for field assistance, Abisko Scientific Research Station for logistic support and access to climatic data and Casper T. Christiansen for internal revision of the manuscript.
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Finderup Nielsen, T., Ravn, N.R. & Michelsen, A. Increased CO2 efflux due to long-term experimental summer warming and litter input in subarctic tundra – CO2 fluxes at snowmelt, in growing season, fall and winter. Plant Soil 444, 365–382 (2019). https://doi.org/10.1007/s11104-019-04282-9
- Carbon dioxide fluxes
- Climate change
- Net ecosystem production