, Volume 181, Issue 1, pp 25–37 | Cite as

Experimental soil warming and cooling alters the partitioning of recent assimilates: evidence from a 14C-labelling study at the alpine treeline

  • A. FerrariEmail author
  • F. Hagedorn
  • P. A. Niklaus
Highlighted Student Research


Despite concerns about climate change effects on ecosystems functioning, little is known on how plant assimilate partitioning changes with temperature. Particularly, large temperature effects might occur in cold ecosystems where critical processes are at their temperature limit. In this study, we tested temperature effects on carbon (C) assimilate partitioning in a field experiment at the alpine treeline. We warmed and cooled soils of microcosms planted with Pinus mugo or Leucanthemopsis alpina, achieving daily mean soil temperatures (3–10 cm depth) around 5.8, 12.7 and 19.2 °C in cooled, control and warmed soils. We pulse-labelled these systems with 14CO2 for one photoperiod and traced 14C over the successive 4 days. Plant net 14C uptake increased steadily with soil temperature. However, 14C amounts in fungal hyphae, soil microbial biomass, soil organic matter, and soil respiration showed a non-linear response to temperature. This non-linear pattern was particularly pronounced in P. mugo, with five times higher 14C activities in cooled compared to control soils, but no difference between warmed and control soil. Autoradiographic analysis of the spatial distribution of 14C in soils indicated that temperature effects on the vertical label distribution within soils depended on plant species. Our results show that plant growth, in particular root metabolism, is limited by low soil temperature. As a consequence, positive temperature effects on net C uptake may not be paralleled by similar changes in rhizodeposition. This has important implications for predictions of soil C storage, because rhizodeposits and plant biomass vary strongly in their residence times.


Carbon partitioning C isotopes Climate change Leucanthemopsis alpina Pinus mugo 



We acknowledge the financial support by the COST-SBF project C09.0130 in the framework of the COST Action FP0803.

Author contribution statement

PAN and FH formulated the idea and obtained the funding. AF carried out the field experiment and laboratory analysis. All authors contributed to study design, data analysis and interpretation. AF wrote the manuscript with input from PAN and FH


  1. Aerts R, Cornelissen JHC, Dorrepaal E (2006) Plant performance in a warmer world: general responses of plants from cold, northern biomes and the importance of winter and spring events. Plant Ecol 182:65–77. doi: 10.1007/s11258-005-9031-1 Google Scholar
  2. Alvarez-Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Funct Ecol 21:211–218. doi: 10.1111/j.1365-2435.2007.01231.x CrossRefGoogle Scholar
  3. Arft A, Walker M, Gurevitch J (1999) Responses of tundra plants to experimental warming: meta-analysis of the International tundra experiment. Ecol Monogr 69:491–511Google Scholar
  4. Bahn M, Janssens IA, Reichstein M et al (2010) Soil respiration across scales: towards an integration of patterns and processes. New Phytol 186:292–296. doi: 10.1111/j.1469-8137.2010.03237.x CrossRefPubMedGoogle Scholar
  5. Bradley R, Keimig F, Diaz H (2004) Projected temperature changes along the American cordillera and the planned GCOS network. Geophys Res Lett 31:L16210. doi: 10.1029/2004GL020229 CrossRefGoogle Scholar
  6. Chapin FI, McFarland J, McGuire A et al (2009) The changing global carbon cycle: linking plant-soil carbon dynamics to global consequences. J Ecol 97:840–850. doi: 10.1111/j.1365-2745.2009.01529.x CrossRefGoogle Scholar
  7. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. doi: 10.1038/nature04514 CrossRefPubMedGoogle Scholar
  8. Dawes MA, Hagedorn F, Zumbrunn T et al (2011) Growth and community responses of alpine dwarf shrubs to in situ CO2 enrichment and soil warming. New Phytol 191:806–818. doi: 10.1111/j.1469-8137.2011.03722.x CrossRefPubMedGoogle Scholar
  9. Dawes MA, Hagedorn F, Handa IT et al (2013) An alpine treeline in a carbon dioxide-rich world: synthesis of a 9 year free-air carbon dioxide enrichment study. Oecologia 171:623–637. doi: 10.1007/s00442-012-2576-5 CrossRefPubMedGoogle Scholar
  10. Delucia E, Day T, Oquist G (1991) The potential for photoinhibition of Pinus sylvestris L. seedlings exposed to high light and low soil temperature. J Exp Bot 42:611–617. doi: 10.1093/jxb/42.5.611 CrossRefGoogle Scholar
  11. Domisch T, Finer L, Lehto T (2001) Effects of soil temperature on biomass and carbohydrate allocation in Scots pine (Pinus sylvestris) seedlings at the beginning of the growing season. Tree Physiol 21:465–472. doi: 10.1093/treephys/21.7.465 CrossRefPubMedGoogle Scholar
  12. Dormann C, Woodin S (2002) Climate change in the Arctic: using plant functional types in a meta-analysis of field experiments. Funct Ecol 16:4–17. doi: 10.1046/j.0269-8463.2001.00596.x CrossRefGoogle Scholar
  13. Drotz SH, Sparrman T, Nilsson MB et al (2010) Both catabolic and anabolic heterotrophic microbial activity proceed in frozen soils. Proc Natl Acad Sci USA 107:21046–21051. doi: 10.1073/pnas.1008885107 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Epron D, Le Dantec V, Dufrene E, Granier A (2001) Seasonal dynamics of soil carbon dioxide efflux and simulated rhizosphere respiration in a beech forest. Tree Physiol 21:145–152. doi: 10.1093/treephys/21.2-3.145 CrossRefPubMedGoogle Scholar
  15. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90. doi: 10.1007/BF00386231 CrossRefPubMedGoogle Scholar
  16. Gavito ME, Olsson PA, Rouhier H et al (2005) Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi. New Phytol 168:179–188. doi: 10.1111/j.1469-8137.2005.01481.x CrossRefPubMedGoogle Scholar
  17. Giardina C, Ryan M, Binkley D, Fownes J (2003) Primary production and carbon allocation in relation to nutrient supply in a tropical experimental forest. Glob Change Biol 9:1438–1450. doi: 10.1046/j.1365-2486.2003.00558.x CrossRefGoogle Scholar
  18. Grace J (2002) Impacts of climate change on the tree line. Ann Bot 90:537–544. doi: 10.1093/aob/mcf222 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hagedorn F, Martin M, Rixen C et al (2010) Short-term responses of ecosystem carbon fluxes to experimental soil warming at the Swiss alpine treeline. Biogeochemistry 97:7–19. doi: 10.1007/s10533-009-9297-9 CrossRefGoogle Scholar
  20. Hagedorn F, Shiyatov SG, Mazepa VS et al (2014) Treeline advances along the urals mountain range––driven by improved winter conditions? Glob Change Biol 1–14:3530–3543. doi: 10.1111/gcb.12613 CrossRefGoogle Scholar
  21. Hartley IP, Heinemeyer A, Evans SP, Ineson P (2007) The effect of soil warming on bulk soil vs. rhizosphere respiration. Glob Change Biol 13:2654–2667. doi: 10.1111/j.1365-2486.2007.01454.x CrossRefGoogle Scholar
  22. Hawkes CV, Hartley IP, Ineson P, Fitter AH (2008) Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus. Glob Change Biol 14:1181–1190. doi: 10.1111/j.1365-2486.2007.01535.x CrossRefGoogle Scholar
  23. Heinemeyer A, Ineson P, Ostle N, Fitter AH (2006) Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. New Phytol 171:159–170. doi: 10.1111/j.1469-8137.2006.01730.x CrossRefPubMedGoogle Scholar
  24. Heinemeyer A, Hartley IP, Evans SP et al (2007) Forest soil CO 2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Glob Change Biol 13:1786–1797. doi: 10.1111/j.1365-2486.2007.01383.x CrossRefGoogle Scholar
  25. Hoch G, Körner C (2009) Growth and carbon relations of tree line forming conifers at constant vs. variable low temperatures. J Ecol 97:57–66. doi: 10.1111/j.1365-2745.2008.01447.x CrossRefGoogle Scholar
  26. Hollister RD, Flaherty KJ (2010) Above- and below-ground plant biomass response to experimental warming in Northern Alaska. Appl Veg Sci 13:378–387. doi: 10.1111/j.1654-109X.2010.01079.x Google Scholar
  27. Hudson JMG, Henry GHR, Cornwell WK (2011) Taller and larger: shifts in Arctic tundra leaf traits after 16 years of experimental warming. Glob Change Biol 17:1013–1021. doi: 10.1111/j.1365-2486.2010.02294.x CrossRefGoogle Scholar
  28. IPCC (2013) Summary for policymakers. In: Stocker TF, Qin D, Plattner G-K et al. (eds) Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  29. Janssens IA, Pilegaard K (2003) Large seasonal changes in Q10 of soil respiration in a beech forest. Glob Change Biol 9:911–918. doi: 10.1046/j.1365-2486.2003.00636.x CrossRefGoogle Scholar
  30. Jungqvist G, Oni SK, Teutschbein C, Futter MN (2014) Effect of climate change on soil temperature in Swedish boreal forests. PLoS ONE 9:e93957. doi: 10.1371/journal.pone.0093957 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kane E, Vogel J (2009) Patterns of total ecosystem carbon storage with changes in soil temperature in boreal black spruce forests. Ecosystems 12:322–335. doi: 10.1007/s10021-008-9225-1 CrossRefGoogle Scholar
  32. Kirschbaum MUF (1995) The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biol Biochem 27:753–760. doi: 10.1016/0038-0717(94)00242-S CrossRefGoogle Scholar
  33. Kolari P, Lappalainen HK, Hänninen H, Hari P (2007) Relationship between temperature and the seasonal course of photosynthesis in Scots pine at northern timberline and in southern boreal zone. Tellus 59:542–552. doi: 10.1111/j.1600-0889.2007.00262.x CrossRefGoogle Scholar
  34. Kontunen-Soppela S, Lankila J, Lähdesmäki P, Laine K (2002) Response of protein and carbohydrate metabolism of Scots pine seedlings to low temperature. J Plant Physiol 159:175–180. doi: 10.1078/0176-1617-00538 CrossRefGoogle Scholar
  35. Körner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115:445–459. doi: 10.1007/s004420050540 CrossRefGoogle Scholar
  36. Körner C, Paulsen J (2004) A world-wide study of high altitude treeline temperatures. J Biogeogr 31:713–732. doi: 10.1111/j.1365-2699.2003.01043.x CrossRefGoogle Scholar
  37. Kuzyakov Y, Gavrichkova O (2010) REVIEW: time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Glob Change Biol 16:3386–3406. doi: 10.1111/j.1365-2486.2010.02179.x CrossRefGoogle Scholar
  38. Leifeld J, Fuhrer J (2005) The temperature response of CO2 production from bulk soils and soil fractions is related to soil organic matter quality. Biogeochemistry 75:433–453. doi: 10.1007/s10533-005-2237-4 CrossRefGoogle Scholar
  39. Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Glob Change Biol 13:2089–2109. doi: 10.1111/j.1365-2486.2007.01420.x CrossRefGoogle Scholar
  40. Melillo JM, Butler S, Johnson J et al (2011) Soil warming, carbon–nitrogen interactions, and forest carbon budgets. Proc Natl Acad Sci USA 108:9508–9512. doi: 10.1073/pnas.1018189108 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Moser M (1958) Influence of low temperature on growth and functioning of the higher fungi, with special reference to mycorrhiza. Sydowia 12:386–399Google Scholar
  42. Moyano FE, Kutsch WL, Schulze E-D (2007) Response of mycorrhizal, rhizosphere and soil basal respiration to temperature and photosynthesis in a barley field. Soil Biol Biochem 39:843–853. doi: 10.1016/j.soilbio.2006.10.001 CrossRefGoogle Scholar
  43. Moyano FE, Kutsch WL, Rebmann C (2008) Soil respiration fluxes in relation to photosynthetic activity in broad-leaf and needle-leaf forest stands. Agric For Meteorol 148:135–143. doi: 10.1016/j.agrformet.2007.09.006 CrossRefGoogle Scholar
  44. Myers-Smith IH, Forbes BC, Wilmking M et al (2011) Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6:045509. doi: 10.1088/1748-9326/6/4/045509 CrossRefGoogle Scholar
  45. Pannatier-Graf E, Thimonier A, Schmitt M et al (2011) A decade of monitoring at swiss long-term forest ecosystem research (LWF) sites: can we observe trends in atmospheric acid deposition and in soil solution acidity? Environ Monit Assess 174:3–30. doi: 10.1007/s10661-010-1754-3 CrossRefGoogle Scholar
  46. Paradis M, Mercier C, Boudreau S (2014) Response of Betula glandulosa seedlings to simulated increases in nutrient availability, temperature and precipitation in a lichen woodland at the forest–tundra ecotone. Plant Ecol 215:305–314. doi: 10.1007/s11258-014-0299-x CrossRefGoogle Scholar
  47. Pietikäinen J, Pettersson M, Bååth E (2005) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58. doi: 10.1016/j.femsec.2004.10.002 CrossRefPubMedGoogle Scholar
  48. Pumpanen J, Heinonsalo J, Rasilo T et al (2012) The effects of soil and air temperature on CO2 exchange and net biomass accumulation in Norway spruce, Scots pine and silver birch seedlings. Tree Physiol 32:724–736. doi: 10.1093/treephys/tps007 CrossRefPubMedGoogle Scholar
  49. Rebetez M, Reinhard M (2007) Monthly air temperature trends in Switzerland 1901–2000 and 1975–2004. Theor Appl Climatol 91:27–34. doi: 10.1007/s00704-007-0296-2 CrossRefGoogle Scholar
  50. Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152:1–12. doi: 10.1007/s00442-006-0625-7 CrossRefPubMedGoogle Scholar
  51. Rustad L, Campbell J, Marion G et al (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562. doi: 10.1007/s004420000544 CrossRefGoogle Scholar
  52. Savage KE, Parton WJ, Davidson EA et al (2013) Long-term changes in forest carbon under temperature and nitrogen amendments in a temperate northern hardwood forest. Glob Change Biol 19:2389–2400. doi: 10.1111/gcb.12224 CrossRefGoogle Scholar
  53. Schindlbacher A, Zechmeister-Boltenstern S, Jandl R (2009) Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob Change Biol 15:901–913. doi: 10.1111/j.1365-2486.2008.01757.x CrossRefGoogle Scholar
  54. Sistla SA, Moore JC, Simpson RT et al (2013) Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497:615–618. doi: 10.1038/nature12129 CrossRefPubMedGoogle Scholar
  55. Stiehl-Braun PA, Powlson DS, Poulton PR, Niklaus PA (2011) Effects of N fertilizers and liming on the micro-scale distribution of soil methane assimilation in the long-term park grass experiment at Rothamsted. Soil Biol Biochem 43:1034–1041. doi: 10.1016/j.soilbio.2011.01.020 CrossRefGoogle Scholar
  56. Stitt M, Huber S, Kerr P (1987) Control of photosynthetic sucrose formation. In: Hatch M, Boardman N (eds) The Biochemistry of Plants, vol 10., Academic, San Diego, pp 327–409Google Scholar
  57. Stocker TF, Qin D, Plattner G-K (eds) (2013) IPCC 2013: Summary for policymakers. In: climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  58. Streit K, Rinne KT, Hagedorn F et al (2013) Tracing fresh assimilates through Larix decidua exposed to elevated CO2 and soil warming at the alpine treeline using compound-specific stable isotope analysis. New Phytol 197:838–849. doi: 10.1111/nph.12074 CrossRefPubMedGoogle Scholar
  59. Streit K, Hagedorn F, Hiltbrunner D et al (2014) Soil warming alters microbial substrate use in alpine soils. Glob Change Biol 20:1327–1338. doi: 10.1111/gcb.12396 CrossRefGoogle Scholar
  60. Subke J-A, Voke NR, Leronni V et al (2011) Dynamics and pathways of autotrophic and heterotrophic soil CO2 efflux revealed by forest girdling. J Ecol 99:186–193. doi: 10.1111/j.1365-2745.2010.01740.x CrossRefGoogle Scholar
  61. Turnbull M, Murthy R, Griffin K (2002) The relative impacts of daytime and night-time warming on photosynthetic capacity in populus deltoides. Plant Cell Environ 25:1729–1737. doi: 10.1046/j.1365-3040.2002.00947.x CrossRefGoogle Scholar
  62. Vance E, Brookes P, Jenkinson D (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707. doi: 10.1016/0038-0717(87)90052-6 CrossRefGoogle Scholar
  63. Virjamo V, Sutinen S, Julkunen-Tiitto R (2014) Combined effect of elevated UVB, elevated temperature and fertilization on growth, needle structure and phytochemistry of young Norway spruce (Picea abies) seedlings. Glob Change Biol 20:2252–2260. doi: 10.1111/gcb.12464 CrossRefGoogle Scholar
  64. Vogel JG, Bond-Lamberty BP, Schuur EAG et al (2008) Carbon allocation in boreal black spruce forests across regions varying in soil temperature and precipitation. Glob Change Biol 14:1503–1516. doi: 10.1111/j.1365-2486.2008.01600.x CrossRefGoogle Scholar
  65. Vogel JG, Bronson D, Gower ST, Schuur EAG (2014) The response of root and microbial respiration to the experimental warming of a boreal black spruce forest. Can J For Res 44:986–993. doi: 10.1139/cjfr-2014-0056 CrossRefGoogle Scholar
  66. Walker MD, Wahren CH, Hollister RD et al (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103:1342–1346. doi: 10.1073/pnas.0503198103 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wallander H, Nilsson LO, David H, Erland B (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–760. doi: 10.1046/j.0028-646x.2001.00199.x CrossRefGoogle Scholar
  68. Walthert L, Blaser P, Lüscher P et al (2003) Langfristige Waldökosystem-Forschung LWF in der Schweiz Kernprojekt Bodenmatrix Ergebnisse der ersten Erhebung 1994–1999. In: Eidgenössische Forschungsanstalt (WSL).
  69. Wang X, Liu L, Piao S et al (2014) Soil respiration under climate warming: differential response of heterotrophic and autotrophic respiration. Glob Change Biol 20:3229–3237. doi: 10.1111/gcb.12620 CrossRefGoogle Scholar
  70. Wu J, Joergensen RG, Pommerening B et al (1990) Measurement of soil microbial biomass C by fumigation–extraction. An automated procedure. Soil Biol Biochem 22:1167–1169. doi: 10.1016/0038-0717(90)90046-3 CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Institute of Evolutionary Biology and Environmental StudiesUniversity of ZurichZurichSwitzerland
  2. 2.Forest Soils and Biogeochemistry, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL)BirmensdorfSwitzerland

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