Abstract
We evaluated the impacts of elevated CO2 in a treeline ecosystem in the Swiss Alps in a 9-year free-air CO2 enrichment (FACE) study. We present new data and synthesize plant and soil results from the entire experimental period. Light-saturated photosynthesis (A max) of ca. 35-year-old Larix decidua and Pinus uncinata was stimulated by elevated CO2 throughout the experiment. Slight down-regulation of photosynthesis in Pinus was consistent with starch accumulation in needle tissue. Above-ground growth responses differed between tree species, with a 33 % mean annual stimulation in Larix but no response in Pinus. Species-specific CO2 responses also occurred for abundant dwarf shrub species in the understorey, where Vaccinium myrtillus showed a sustained shoot growth enhancement (+11 %) that was not apparent for Vaccinium gaultherioides or Empetrum hermaphroditum. Below ground, CO2 enrichment did not stimulate fine root or mycorrhizal mycelium growth, but increased CO2 effluxes from the soil (+24 %) indicated that enhanced C assimilation was partially offset by greater respiratory losses. The dissolved organic C (DOC) concentration in soil solutions was consistently higher under elevated CO2 (+14 %), suggesting accelerated soil organic matter turnover. CO2 enrichment hardly affected the C–N balance in plants and soil, with unaltered soil total or mineral N concentrations and little impact on plant leaf N concentration or the stable N isotope ratio. Sustained differences in plant species growth responses suggest future shifts in species composition with atmospheric change. Consistently increased C fixation, soil respiration and DOC production over 9 years of CO2 enrichment provide clear evidence for accelerated C cycling with no apparent consequences on the N cycle in this treeline ecosystem.
Similar content being viewed by others
References
Andresen LC, Michelsen A, Jonasson S, Schmidt IK, Mikkelsen TN, Ambus P, Beier C (2010) Plant nutrient mobilization in temperate heathland responds to elevated CO2, temperature and drought. Plant Soil 328:381–396
Asshoff R, Hättenschwiler S (2005) Growth and reproduction of the alpine grasshopper Miramella alpina feeding on CO2-enriched dwarf shrubs at treeline. Oecologia 142:191–201
Bader MKF, Hiltbrunner E, Körner C (2009) Fine root responses of mature deciduous forest trees to free air carbon dioxide enrichment (FACE). Funct Ecol 23:913–921
Bader MKF, Siegwolf R, Körner C (2010) Sustained enhancement of photosynthesis in mature deciduous forest trees after 8 years of free air CO2 enrichment. Planta 232:1115–1125
Bednorz F, Reichstein M, Broll G, Holtmeier FK, Urfer W (2000) Humus forms in the forest-alpine tundra ecotone at Stillberg (Dischmatal, Switzerland): spatial heterogeneity and classification. Arct Antarct Alp Res 32:21–29
Brown A, Day F, Stover D (2009) Fine root biomass estimates from minirhizotron imagery in a shrub ecosystem exposed to elevated CO2. Plant Soil 317:145–153
Chapin FS, McFarland J, McGuire AD, Euskirchen ES, Ruess RW, Kielland K (2009) The changing global carbon cycle: linking plant–soil carbon dynamics to global consequences. J Ecol 97:840–850
Crous KY, Walters MB, Ellsworth DS (2008) Elevated CO2 concentration affects leaf photosynthesis and nitrogen relationships in Pinus taeda over nine years in FACE. Tree Physiol 28:607–614
Dawes MA, Hagedorn F, Zumbrunn T, Handa IT, Hättenschwiler S, Wipf S, Rixen C (2011a) Growth and community responses of alpine dwarf shrubs to in situ CO2 enrichment and soil warming. New Phytol 191:806–818
Dawes MA, Hättenschwiler S, Bebi P, Hagedorn F, Handa IT, Körner C, Rixen C (2011b) Species-specific tree growth responses to nine years of CO2 enrichment at the alpine treeline. J Ecol 99:383–394
Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Phillips RP, Pippen JS, Pritchard SG, Treseder KK, Schlesinger WH, DeLucia EH, Finzi AC (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357
Finzi AC, Norby RJ, Calfapietra C, Gallet-Budynek A, Gielen B, Holmes WE, Hoosbeek MR, Iversen CM, Jackson RB, Kubiske ME, Ledford J, Liberloo M, Oren R, Polle A, Pritchard SG, Zak DR, Schlesinger WH, Ceulemans R (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Natl Acad Sci USA 104:14014–14019
Godbold D, Hoosbeek M, Lukac M, Cotrufo M, Janssens I, Ceulemans R, Polle A, Velthorst E, Scarascia-Mugnozza G, De Angelis P, Miglietta F, Peressotti A (2006) Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281:15–24
Gwynn-Jones D, Lee JA, Callaghan TV (1997) Effects of enhanced UV-B radiation and elevated carbon dioxide concentrations on a sub-arctic forest heath ecosystem. Plant Ecol 128:242–249
Hagedorn F, van Hees PAW, Handa IT, Hättenschwiler S (2008) Elevated atmospheric CO2 fuels leaching of old dissolved organic matter at the alpine treeline. Global Biogeochem Cycles 22:GB2004
Hagedorn F, Martin MA, Rixen C, Rusch S, Zürcher A, Siegwolf RTW, Wipf S, Escape C, Roy J, Hättenschwiler S (2010) Short-term responses of ecosystem carbon fluxes to experimental soil warming at the Swiss alpine treeline. Biogeochemistry 97:7–19
Handa IT, Körner C, Hättenschwiler S (2005) A test of the tree-line carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology 86:1288–1300
Handa IT, Körner C, Hättenschwiler S (2006) Conifer stem growth at the altitudinal treeline in response to four years of CO2 enrichment. Glob Change Biol 12:2417–2430
Handa IT, Hagedorn F, Hättenschwiler S (2008) No stimulation in root production in response to four years of in situ CO2 enrichment at the Swiss treeline. Funct Ecol 22:348–358
Hättenschwiler S, Zumbrunn T (2006) Hemiparasite abundance in an alpine treeline ecotone increases in response to atmospheric CO2 enrichment. Oecologia 147:47–52
Hättenschwiler S, Handa IT, Egli L, Asshoff R, Ammann W, Körner C (2002) Atmospheric CO2 enrichment of alpine treeline conifers. New Phytol 156:363–375
Hoch G, Körner C (2003) The carbon charging of pines at the climatic treeline: a global comparison. Oecologia 135:10–21
Högberg P, Nordgren A, Buchmann N, Taylor AF, Ekblad A, Högberg MN, Nyberg G, Ottosson-Lofvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792
Holmgren M, Stapp P, Dickman CR, Gracia C, Graham S, Gutierrez JR, Hice C, Jaksic F, Kelt DA, Letnic M, Lima M, Lopez BC, Meserve PL, Milstead WB, Polis GA, Previtali MA, Michael R, Sabate S, Squeo FA (2006) Extreme climatic events shape arid and semiarid ecosystems. Front Ecol Environ 4:87–95
Inauen N, Körner C, Hiltbrunner E (2012) No growth stimulation by CO2 enrichment in alpine glacier forefield plants. Glob Change Biol 18:985–999
Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202
Jackson RB, Cook CW, Pippen JS, Palmer SM (2009) Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest. Ecology 90:3352–3366
Jentsch A, Kreyling J, Beierkuhnlein C (2007) A new generation of climate-change experiments: events, not trends. Front Ecol Environ 5:365–374
Kasurinen A, Keinänen MM, Kaipainen S, Nilsson L-O, Vapaavuori E, Kontro MH, Holopainen T (2005) Below-ground responses of silver birch trees exposed to elevated CO2 and O3 levels during three growing seasons. Glob Change Biol 11:1167–1179
King JS, Hanson PJ, Bernhardt E, DeAngelis P, Norby RJ, Pregitzer KS (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Glob Change Biol 10:1027–1042
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin
Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411
Körner C (2012) Alpine treelines. Springer, Berlin
Körner C, Diemer M, Schappi B, Niklaus PA, Arnone JA (1997) The responses of alpine grassland to four seasons of CO2 enrichment: a synthesis. Acta Oecol Int J Ecol 18:165–175
Kostiainen K, Kaakinen S, Saranpaa P, Sigurdsson BD, Linder S, Vapaavuori E (2004) Effect of elevated [CO2] on stem wood properties of mature Norway spruce grown at different soil nutrient availability. Glob Change Biol 10:1526–1538
Langley JA, Megonigal JP (2011) Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift. Nature 466:96–99
Langley JA, McKinley DC, Wolf AA, Hungate BA, Drake BG, Megonigal JP (2009) Priming depletes soil carbon and releases nitrogen in a scrub-oak ecosystem exposed to elevated CO2. Soil Biol Biochem 41:54–60
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876
Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628
Luo YQ, Su B, Currie WS, Dukes JS, Finzi AC, Hartwig U, Hungate BA, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739
Martin MA, Gavazov K, Körner C, Hättenschwiler S, Rixen C (2010) Reduced early growing season freezing resistance in alpine treeline plants under elevated atmospheric CO2. Glob Change Biol 16:1057–1070
Norby RJ, Zak DR (2011) Ecological lessons from free air CO2 enrichment (FACE) experiments. Annu Rev Ecol Evol Syst 42:181–203
Norby RJ, Ledford J, Reilly C, Miller N, O’Neill E (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. Proc Natl Acad Sci USA 101:9689–9693
Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci USA 107:19368–19373
Oechel WC, Cowles S, Grulke N, Hastings SJ, Lawrence B, Prudhomme T, Riechers G, Strain B, Tissue D, Vourlitis G (1994) Transient nature of CO2 fertilization in arctic tundra. Nature 371:500–503
Parrent JL, Vilgalys R (2007) Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO2 and nitrogen fertilization. New Phytol 176:164–174
Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194
Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Core Team (2008) nlme: linear and nonlinear mixed effects models. R package version 3.1-89
Pollierer MM, Langel R, Körner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736
Pritchard SG, Strand AE, McCormack ML, Davis MA, Finzi AC, Jackson RB, Matamala R, Rogers HH, Oren R (2008) Fine root dynamics in a loblolly pine forest are influenced by free air CO2 enrichment: a six-year-minirhizotron study. Glob Change Biol 14:588–602
Rixen C, Dawes MA, Wipf S, Hagedorn F (2012) Evidence of enhanced freezing damage in treeline plants during six years of CO2 enrichment and soil warming. Oikos 121:1532–1543
Rossi S, Anfodillo T, Menardi R (2006) Trephor: A new tool for sampling microcores from tree stems. IAWA J 27:89–97
Schäppi B, Körner C (1996) Growth responses of an alpine grassland to elevated CO2. Oecologia 105:43–52
Schleppi P, Bucher-Wallin I, Hagedorn F, Körner C (2012) Increased nitrate availability in the soil of a mixed mature temperate forest subjected to elevated CO2 concentration (canopy FACE). Glob Change Biol 18:757–768
Schmitt M, Thöni M, Waldner P, Thimonier A (2005) Total deposition of nitrogen on Swiss long-term forest ecosystem research (LWF) plots: comparison of the throughfall and the interferential method. Atmos Environ 39:1079–1091
Seiler TJ, Rasse DP, Li J, Dijkstra P, Anderson HP, Johnson DP, Powell TL, Hungate BA, Hinkle CR, Drake BG (2009) Disturbance, rainfall and contrasting species responses mediated aboveground biomass response to 11 years of CO2 enrichment in a Florida scrub-oak ecosystem. Glob Change Biol 15:356–367
R Development Core Team (2008–2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Tinner W, Kaltenrieder P (2005) Rapid responses of high-mountain vegetation to early Holocene environmental changes in the Swiss Alps. J Ecol 93:936–947
Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355
Wallander H, Nilsson LO, Hagerberg D, Bååth E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–760
Zak DR, Pregitzer KS, Kubiske ME, Burton AJ (2011) Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol Lett 14:1220–1226
Zavaleta ES, Shaw MR, Chiariello NR, Mooney HA, Field CB (2003) Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proc Natl Acad Sci USA 100:7650–7654
Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a meta-analysis. Glob Change Biol 12:27–41
Acknowledgments
We thank many colleagues at the SLF, WSL, Paul-Scherrer Institute and University of Basel for their assistance with field and lab measurements and technical support. We are especially grateful to E. Amstutz, L. Egli, G. Grun, A. Studer, S. Wipf and P. Bebi for helping to ensure successful operation of the FACE system. Major funding sources included: the Swiss National Science Foundation 2001–2005 (grant 31-061428.00 to S. H.) and 2007–2009 (grant 315200-116861 to C. R.); an ANR-biodiversité grant to S. H. 2006–2008; and the Velux foundation 2007–2009 (grant 371 to F. H.). Additional financial support was provided by the CCES-ETH project MOUNTLAND, Swiss State Secretariat for Education and Research (COST Action 639, projects C07.0032 and C07.0033), WSL, University of Basel Botanical Institute, Swiss Federal Office for the Environment and the Fonds québecois de recherche sur la nature et les technologies (scholarship to I. T. H.).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Russell Monson.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Dawes, M.A., Hagedorn, F., Handa, I.T. et al. An alpine treeline in a carbon dioxide-rich world: synthesis of a nine-year free-air carbon dioxide enrichment study. Oecologia 171, 623–637 (2013). https://doi.org/10.1007/s00442-012-2576-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-012-2576-5