Oecologia

, Volume 175, Issue 3, pp 747–762 | Cite as

Long-term 13C labeling provides evidence for temporal and spatial carbon allocation patterns in mature Picea abies

  • Manuel Mildner
  • Martin K.-F. Bader
  • Sebastian Leuzinger
  • Rolf T. W. Siegwolf
  • Christian Körner
Physiological ecology - Original research

Abstract

There is evidence of continued stimulation of foliage photosynthesis in trees exposed to elevated atmospheric CO2 concentrations; however, this is mostly without a proportional growth response. Consequently, we lack information on the fate of this extra carbon (C) acquired. By a steady application of a 13CO2 label in a free air CO2 enrichment (FACE) experiment, we traced the fate of C in 37-m-tall, ca. 110-year-old Picea abies trees in a natural forest in Switzerland. Hence, we are not reporting tree responses to elevated CO2 (which would require equally 13C labeled controls), but are providing insights into assimilate processing in such trees. Sunlit needles and branchlets grow almost exclusively from current assimilates, whereas shaded parts of the crowns also rely on stored C. Only 2.5 years after FACE initiation, tree rings contained 100 % new C. Stem-respiratory CO2 averaged 50 % of new C over the entire FACE period. Fine roots and mycorrhizal fungi contained 49–56 and 26–43 % new C, respectively, after 2.5 years. The isotopic signals in soil CO2 arrived 12 days after the onset of FACE, yet it contained only ca. 15 % new C thereafter. We conclude that new C first feeds into fast turnover C pools in the canopy and becomes increasingly mixed with older C sources as one moves away (downward) from the crown. We speculate that enhanced C turnover (its metabolic cost) along the phloem path, as evidenced by basipetal isotope signal depletion, explains part of the ‘missing carbon’ in trees that assimilated more C under elevated CO2.

Keywords

Carbon isotopes Elevated CO2 FACE Forest Respiration 

Notes

Acknowledgments

We greatly appreciate help from M. Saurer and K. Lötscher at the Paul Scherrer Institute for C isotope analyses, E. Amstutz for crane operation and FACE maintenance, Georges Grun for FACE supervision, Olivier Bignucolo and several student helpers for their support in data collection and sample processing (notably Martin Trischler as part of his Master thesis), and Rigobert Keller and members of the Mycological Association Basel for fungal taxonomic classification. This project was funded by the Swiss National Science Foundation (Grants 31003AB-126028 and 31003A_140753, 31-67775.02, 3100-059769.99, 3100-067775.02, and 3100AO-111914/1). The crane was sponsored by the Swiss Federal Office of the Environment (FOEN).

References

  1. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedCrossRefGoogle Scholar
  2. Andersen CP, Ritter W, Gregg J, Matyssek R, Grams TEE (2010) Below-ground carbon allocation in mature beech and spruce trees following long-term, experimentally enhanced O3 exposure in Southern Germany. Environ Pollut 158:2604–2609PubMedCrossRefGoogle Scholar
  3. Andrews JA, Harrison KG, Matamala R, Schlesinger WH (1999) Separation of root respiration from total soil respiration using 13C labeling during free-air carbon dioxide enrichment (FACE). Soil Sci Soc Am J 63:1429–1435CrossRefGoogle Scholar
  4. Badeck FW, Tcherkez G, Nogués S, Piel C, Ghashghaie J (2005) Post-photosynthetic fractionation of stable carbon isotopes between plant organs: a widespread phenomenon. Rapid Commun Mass Spectrom 19:1381–1391PubMedCrossRefGoogle Scholar
  5. Bader MKF, Hiltbrunner E, Körner C (2009) Fine root responses of mature deciduous forest trees to free air carbon dioxide enrichment (FACE). Funct Ecol 23:913–921CrossRefGoogle Scholar
  6. Bader MKF, Siegwolf RTW, Körner C (2010) Sustained enhancement of photosynthesis in mature deciduous forest trees after 8 years of free air CO2 enrichment. Planta 232:1115–1125PubMedCrossRefGoogle Scholar
  7. Bader MKF, Leuzinger S, Keel SG, Siegwolf RTW, Hagedorn F, Schleppi P, Körner C (2013) Central European hardwood trees in a high-CO2 future: synthesis of an 8-year forest canopy CO2 enrichment project. J Ecol. doi:10.1111/1365-2745.12149 Google Scholar
  8. Boström B, Comstedt D, Ekblad A (2007) Isotope fractionation and c-13 enrichment in soil profiles during the decomposition of soil organic matter. Oecologia 153:89–98PubMedCrossRefGoogle Scholar
  9. Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40PubMedCrossRefGoogle Scholar
  10. Brownlee C, Duddridge JA, Malibari A, Read DJ (1983) The structure and function of mycelial systems of ectomycorrhizal roots with special reference to their role in forming inter-plant connections and providing pathways for assimilate and water transport. Plant Soil 71:433–443CrossRefGoogle Scholar
  11. Brüggemann N, Gessler A, Kayler Z, Keel SG, Badeck F, Barthel M, Boeckx P, Buchmann N, Brugnoli E, Esperschütz J, Gavrichkova O, Ghashghaie J, Gomez-Casanovas N, Keitel C, Knohl A, Kuptz D, Palacio S, Salmon Y, Uchida Y, Bahn M (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences 8:3457–3489CrossRefGoogle Scholar
  12. Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, Dawson TE, Griffiths HG, Farquhar GD, Wright IJ (2009) Viewpoint: why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Funct Plant Biol 36:199–213CrossRefGoogle Scholar
  13. Ceulemans R, Mousseau M (1994) Tansley review no-71: effects of elevated atmospheric CO2 on woody-plants. New Phytol 127:425–446CrossRefGoogle Scholar
  14. Comstedt D, Boström B, Marshall JD, Holm A, Slaney M, Linder S, Ekblad A (2006) Effects of elevated atmospheric carbon dioxide and temperature on soil respiration in a boreal forest using δ13C as a labeling tool. Ecosystems 9:1266–1277CrossRefGoogle Scholar
  15. Dannoura M, Maillard P, Fresneau C, Plain C, Berveiller D, Gerant D, Chipeaux C, Bosc A, Ngao J, Damesin C, Loustau D, Epron D (2011) In situ assessment of the velocity of carbon transfer by tracing 13C in trunk CO2 efflux after pulse labelling: variations among tree species and seasons. New Phytol 190:181–192PubMedCrossRefGoogle Scholar
  16. Ekblad A, Boström B, Holm A, Comstedt D (2005) Forest soil respiration rate and δ13C is regulated by recent above ground weather conditions. Oecologia 143:136–142PubMedCrossRefGoogle Scholar
  17. Endrulat T, Saurer M, Buchmann N, Brunner I (2010) Incorporation and remobilization of 13C within the fine-root systems of individual Abies alba trees in a temperate coniferous stand. Tree Physiol 30:1515–1527PubMedCrossRefGoogle Scholar
  18. Epron D, Ngao J, Dannoura M, Bakker MR, Zeller B, Bazot S, Bosc A, Plain C, Lata JC, Priault P, Barthes L, Loustau D (2011) Seasonal variations of belowground carbon transfer assessed by in situ 13CO2 pulse labeling of trees. Biogeosciences 8:1153–1168CrossRefGoogle Scholar
  19. Epron D, Bahn M, Derrien D, Lattanzi FA, Pumpanen J, Gessler A, Högberg P, Maillard P, Dannoura M, Gerant D, Buchmann N (2012) Pulse-labelling trees to study carbon allocation dynamics: a review of methods, current knowledge and future prospects. Tree Physiol 32:776–798PubMedCrossRefGoogle Scholar
  20. Etzold S, Zweifel R, Ruehr NK, Eugster W, Buchmann N (2013) Long-term stem CO2 concentration measurements in Norway spruce in relation to biotic and abiotic factors. New Phytol 197:1173–1184PubMedCrossRefGoogle Scholar
  21. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the inter-cellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137CrossRefGoogle Scholar
  22. Fatichi S, Leuzinger S (2013) Reconciling observations with modeling: the fate of water and carbon allocation in a mature deciduous forest exposed to elevated CO2. Agric For Meteorol 174:144–157CrossRefGoogle Scholar
  23. Flower-Ellis JGK (1993) Dry-matter allocation in Norway spruce branches: a demographic approach. Stud For Suec 191:51–73Google Scholar
  24. Freeland RO (1952) Effect of age of leaves upon the rate of photosynthesis in some conifers. Plant Physiol 27:685–690PubMedCentralPubMedCrossRefGoogle Scholar
  25. Friedlingstein P, Houghton RA, Marland G, Hackler J, Boden TA, Conway TJ, Canadell JG, Raupach MR, Ciais P, Le Quéré C (2010) Update on CO2 emissions. Nat Geosci 3:811–812CrossRefGoogle Scholar
  26. Gessler A, Brandes E, Buchmann N, Helle G, Rennenberg H, Barnard RL (2009) Tracing carbon and oxygen isotope signals from newly assimilated sugars in the leaves to the tree-ring archive. Plant Cell Environ 32:780–795PubMedCrossRefGoogle Scholar
  27. Gleixner G, Danier HJ, Werner RA, Schmidt HL (1993) Correlations between the 13C content of primary and secondary plant-products in different cell compartments and that in decomposing basidiomycetes. Plant Physiol 102:1287–1290PubMedCentralPubMedGoogle Scholar
  28. Gordon JC, Larson PR (1968) Seasonal course of photosynthesis respiration and distribution of 14C in young Pinus resinosa trees as related to wood formation. Plant Physiol 43:1617–1624PubMedCentralPubMedCrossRefGoogle Scholar
  29. Hansen J, Beck E (1994) Seasonal-changes in the utilization and turnover of assimilation products in 8-year-old Scots pine (Pinus-sylvestris L.) trees. Trees Struct Funct 8:172–182CrossRefGoogle Scholar
  30. Hansen J, Vogg G, Beck E (1996) Assimilation, allocation and utilization of carbon by 3-year-old Scots pine (Pinus sylvestris L.) trees during winter and early spring. Trees Struct Funct 11:83–90Google Scholar
  31. Hättenschwiler S, Handa IT, Egli L, Asshoff R, Ammann W, Körner C (2002) Atmospheric CO2 enrichment of alpine treeline conifers. New Phytol 156:363–375CrossRefGoogle Scholar
  32. Hobbie EA, Werner RA (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytol 161:371–385CrossRefGoogle Scholar
  33. Hobbie EA, Tingey DT, Rygiewicz PT, Johnson MG, Olszyk DM (2002) Contributions of current year photosynthate to fine roots estimated using a 13C-depleted CO2 source. Plant Soil 247:233–242CrossRefGoogle Scholar
  34. Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659CrossRefGoogle Scholar
  35. Hoch G, Keel SG (2006) 13C labelling reveals different contributions of photoassimilates from infructescences for fruiting in two temperate forest tree species. Plant Biol 8:606–614PubMedCrossRefGoogle Scholar
  36. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081CrossRefGoogle Scholar
  37. Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792PubMedCrossRefGoogle Scholar
  38. Högberg P, Högberg MN, Göttlicher SG, Betson NR, Keel SG, Metcalfe DB, Campbell C, Schindlbacher A, Hurry V, Lundmark T, Linder S, Näsholm T (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177:220–228PubMedGoogle Scholar
  39. Högberg MN, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, Thornton B, Hurry V, Linder S, Näsholm T, Högberg P (2010) Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytol 187:485–493PubMedCrossRefGoogle Scholar
  40. Holt CC (1957) Forecasting trends and seasonals by exponentially weighted moving averages. ONR Research Memorandum. Carnegie Institute of Technology 52Google Scholar
  41. Idso SB (1999) The long-term response of trees to atmospheric CO2 enrichment. Glob Change Biol 5:493–495CrossRefGoogle Scholar
  42. Jäggi M, Saurer M, Fuhrer J, Siegwolf RTW (2002) The relationship between the stable carbon isotope composition of needle bulk material, starch, and tree rings in Picea abies. Oecologia 131:325–332CrossRefGoogle Scholar
  43. Jensen KH, Liesche J, Bohr T, Schulz A (2012) Universality of phloem transport in seed plants. Plant Cell Environ 35:1065–1076PubMedCrossRefGoogle Scholar
  44. Kagawa A, Sugimoto A, Maximov TC (2006) Seasonal course of translocation, storage and remobilization of 13C pulse-labeled photoassimilate in naturally growing Larix gmelinii saplings. New Phytol 171:1571–1584CrossRefGoogle Scholar
  45. Kaufmann MR (1982) Leaf conductance as a function of photosynthetic photon flux-density and absolute-humidity difference from leaf to air. Plant Physiol 69:1018–1022PubMedCentralPubMedCrossRefGoogle Scholar
  46. Keel SG, Siegwolf RTW, Körner C (2006) Canopy CO2 enrichment permits tracing the fate of recently assimilated carbon in a mature deciduous forest. New Phytol 172:319–329PubMedCrossRefGoogle Scholar
  47. Keel SG, Siegwolf RTW, Jäggi M, Körner C (2007) Rapid mixing between old and new C pools in the canopy of mature forest trees. Plant Cell Environ 30:963–972PubMedCrossRefGoogle Scholar
  48. Keeling CD (1958) The concentration and isotopic abundances of atmospheric carbon dioxide in rural areas. Geochim Cosmochim Acta 13:322–334CrossRefGoogle Scholar
  49. Klumpp K, Schäufele R, Lötscher M, Lattanzi FA, Feneis W, Schnyder H (2005) C-isotope composition of CO2 respired by shoots and roots: fractionation during dark respiration? Plant Cell Environ 28:241–250CrossRefGoogle Scholar
  50. Körner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl 10:1590–1619Google Scholar
  51. Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411PubMedCrossRefGoogle Scholar
  52. Körner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG, Pelaez-Riedl S, Pepin S, Siegwolf RTW, Zotz G (2005) Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309:1360–1362PubMedCrossRefGoogle Scholar
  53. Kuptz D, Fleischmann F, Matyssek R, Grams TEE (2011a) Seasonal patterns of carbon allocation to respiratory pools in 60-year-old deciduous (Fagus sylvatica) and evergreen (Picea abies) trees assessed via whole-tree stable carbon isotope labeling. New Phytol 191:160–172PubMedCrossRefGoogle Scholar
  54. Kuptz D, Matyssek R, Grams TEE (2011b) Seasonal dynamics in the stable carbon isotope composition (δ13C) from non-leafy branch, trunk and coarse root CO2 efflux of adult deciduous (Fagus sylvatica) and evergreen (Picea abies) trees. Plant Cell Environ 34:363–373PubMedCrossRefGoogle Scholar
  55. Le Quéré C, Raupach MR, Canadell JG, Marland G, Bopp L, Ciais P, Conway TJ, Doney SC, Feely RA, Foster P, Friedlingstein P, Gurney K, Houghton RA, House JI, Huntingford C, Levy PE, Lomas MR, Majkut J, Metzl N, Ometto JP, Peters GP, Prentice IC, Randerson JT, Running SW, Sarmiento JL, Schuster U, Sitch S, Takahashi T, Viovy N, van der Werf GR, Woodward FI (2009) Trends in the sources and sinks of carbon dioxide. Nat Geosci 2:831–836CrossRefGoogle Scholar
  56. Leuzinger S, Bader MKF (2012) Experimental vs. modeled water use in mature Norway spruce (Picea abies) exposed to elevated CO2. Front Plant Sci 3:229PubMedCentralPubMedCrossRefGoogle Scholar
  57. Leuzinger S, Luo Y, Beier C, Dieleman W, Vicca S, Körner C (2011) Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol Evol 26:236–241PubMedCrossRefGoogle Scholar
  58. Lippu J (1994) Patterns of dry matter partitioning and 14C-photosynthate allocation in 1.5-year-old Scots pine seedlings. Silva Fenn 28:145–153CrossRefGoogle Scholar
  59. Livingston NJ, Whitehead D, Kelliher FM, Wang YP, Grace JC, Walcroft AS, Byers JN, McSeveny TM, Millard P (1998) Nitrogen allocation and carbon isotope fractionation in relation to intercepted radiation and position in a young Pinus radiata D. Don tree. Plant Cell Environ 21:795–803CrossRefGoogle Scholar
  60. Marshall JD, Linder S (2013) Mineral nutrition and elevated CO2 interact to modify δ13C, an index of gas exchange, in Norway spruce. Tree Physiol 33:1132–1144PubMedCrossRefGoogle Scholar
  61. Maunoury F, Berveiller D, Lelarge C, Pontailler J-Y, Vanbostal L, Damesin C (2007) Seasonal, daily and diurnal variations in the stable carbon isotope composition of carbon dioxide respired by tree trunks in a deciduous oak forest. Oecologia 151:268–279PubMedCrossRefGoogle Scholar
  62. McCarthy HR, Oren R, Johnsen KH, Gallet-Budynek A, Pritchard SG, Cook CW, LaDeau SL, Jackson RB, Finzi AC (2010) Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric CO2 with nitrogen and water availability over stand development. New Phytol 185:514–528PubMedCrossRefGoogle Scholar
  63. Medhurst J, Parsby J, Linder S, Wallin G, Ceschia E, Slaney M (2006) A whole-tree chamber system for examining tree-level physiological responses of field-grown trees to environmental variation and climate change. Plant Cell Environ 9:1853–1869CrossRefGoogle Scholar
  64. Medlyn BE, Barton CVM, Broadmeadow MSJ, Ceulemans R, De Angelis P, Forstreuter M, Freeman M, Jackson SB, Kellomäki S, Laitat E, Rey A, Roberntz P, Sigurdsson BD, Strassemeyer J, Wang K, Curtis PS, Jarvis PG (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytol 149:247–264CrossRefGoogle Scholar
  65. Mencuccini M, Hölttä T (2010) The significance of phloem transport for the speed with which canopy photosynthesis and belowground respiration are linked. New Phytol 185:189–203PubMedCrossRefGoogle Scholar
  66. Norby RJ, Zak DR (2011) Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annu Rev Ecol Evol Syst 42:181–203CrossRefGoogle Scholar
  67. Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci USA 107:19368–19373PubMedCentralPubMedCrossRefGoogle Scholar
  68. Oren R, Ellsworth DS, Johnsen KH, Phillips N, Ewers BE, Maier C, Schäfer KVR, McCarthy H, Hendrey G, McNulty SG, Katul GG (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411:469–472PubMedCrossRefGoogle Scholar
  69. Pepin S, Körner C (2002) Web-FACE: a new canopy free-air CO2 enrichment system for tall trees in mature forests. Oecologia 133:1–9PubMedCrossRefGoogle Scholar
  70. Popp M, Lied W, Meyer AJ, Richter A, Schiller P, Schwitte H (1996) Sample preservation for determination of organic compounds: microwave versus freeze-drying. J Exp Bot 47:1469–1473CrossRefGoogle Scholar
  71. R Development Core Team (2008–2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  72. Richter A, Wanek W, Werner RA, Ghashghaie J, Jäggi M, Gessler A, Brugnoli E, Hettmann E, Göttlicher SG, Salmon Y, Bathellier C, Kodama N, Nogués S, Søe A, Volders F, Sörgel K, Blöchl A, Siegwolf RTW, Buchmann N, Gleixner G (2009) Preparation of starch and soluble sugars of plant material for the analysis of carbon isotope composition: a comparison of methods. Rapid Commun Mass Spectrom 23:2476–2488PubMedCrossRefGoogle Scholar
  73. Ritter W, Andersen CP, Matyssek R, Grams TEE (2011) Carbon flux to woody tissues in a beech/spruce forest during summer and in response to chronic O3 exposure. Biogeosciences 8:3127–3138CrossRefGoogle Scholar
  74. Roberntz P, Stockfors J (1998) Effects of elevated CO2 concentration and nutrition on net photosynthesis, stomatal conductance and needle respiration of field-grown Norway spruce trees. Tree Physiol 18:233–241PubMedCrossRefGoogle Scholar
  75. Schädel C, Blöchl A, Richter A, Hoch G (2009) Short-term dynamics of nonstructural carbohydrates and hemicelluloses in young branches of temperate forest trees during bud break. Tree Physiol 29:901–911PubMedCrossRefGoogle Scholar
  76. Schädel C, Richter A, Blöchl A, Hoch G (2010) Hemicellulose concentration and composition in plant cell walls under extreme carbon source-sink imbalances. Physiol Plant 139:241–255PubMedGoogle Scholar
  77. Schäfer KVR, Oren R, Ellsworth DS, Lai CT, Herrick JD, Finzi AC, Richter DD, Katul GG (2003) Exposure to an enriched CO2 atmosphere alters carbon assimilation and allocation in a pine forest ecosystem. Glob Change Biol 9:1378–1400CrossRefGoogle Scholar
  78. 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 18:757–768CrossRefGoogle Scholar
  79. Schlesinger WH, Bernhardt ES, DeLucia EH, Ellsworth DS, Finzi AC, Hendrey GR, Hofmockel KS, Lichter J, Matamala R, Moore D, Oren R, Pippen JS, Thomas RB (2006) The Duke forest FACE experiment: CO2 enrichment of a loblolly pine forest. In: Nösberger J, Long SP, Norby RJ, Stitt M, Hendrey GR, Blum H (eds) Ecological studies 187. Springer, Berlin, pp 197–212Google Scholar
  80. Sigurdsson BD, Medhurst JL, Wallin G, Eggertsson O, Linder S (2013) Growth of mature boreal Norway spruce was not affected by elevated CO2 and/or air temperature unless nutrient availability was improved. Tree Physiol 33:1192–1205PubMedCrossRefGoogle Scholar
  81. Spinnler D, Egli P, Körner C (2002) Four-year growth dynamics of beech-spruce model ecosystems under CO2 enrichment on two different forest soils. Trees Struct Funct 16:423–436CrossRefGoogle Scholar
  82. Sprugel DG (2002) When branch autonomy fails: Milton’s law of resource availability and allocation. Tree Physiol 22:1119–1124PubMedCrossRefGoogle Scholar
  83. Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334CrossRefGoogle Scholar
  84. Steinmann KTW, Siegwolf RTW, Saurer M, Körner C (2004) Carbon fluxes to the soil in a mature temperate forest assessed by C-13 isotope tracing. Oecologia 141:489–501PubMedCrossRefGoogle Scholar
  85. Ubierna N, Marshall JD, Cernusak LA (2009a) A new method to measure carbon isotope composition of CO2 respired by trees: stem CO2 equilibration. Funct Ecol 23:1050–1058CrossRefGoogle Scholar
  86. Ubierna N, Kumar AS, Cernusak LA, Pangle RE, Gag PJ, Marshall JD (2009b) Storage and transpiration have negligible effects on 13C of stem CO2 efflux in large conifer trees. Tree Physiol 29:1563–1574PubMedCrossRefGoogle Scholar
  87. von Felten S, Hättenschwiler S, Saurer M, Siegwolf RTW (2007) Carbon allocation in shoots of alpine treeline conifers in a CO2 enriched environment. Trees Struct Funct 21:283–294CrossRefGoogle Scholar
  88. Warren CR (2006) Why does photosynthesis decrease with needle age in Pinus pinaster? Trees Struct Funct 20:157–164CrossRefGoogle Scholar
  89. Warren JM, Iversen CM, Garten CT Jr, Norby RJ, Childs J, Brice D, Evans RM, Gu L, Thornton P, Weston DJ (2012) Timing and magnitude of C partitioning through a young Loblolly pine (Pinus taeda L.) stand using 13C labeling and shade treatments. Tree Physiol 32:799–813PubMedCrossRefGoogle Scholar
  90. Watson MA, Casper BB (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Annu Rev Ecol Syst 15:233–258CrossRefGoogle Scholar
  91. Werth M, Kuzyakov Y (2010) 13C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42:1372–1384CrossRefGoogle Scholar
  92. Würth MKR, Winter K, Körner C (1998) Leaf carbohydrate responses to CO2 enrichment at the top of a tropical forest. Oecologia 116:18–25Google Scholar
  93. Zhu B, Cheng W (2011) 13C isotope fractionation during rhizosphere respiration of C3 and C4 plants. Plant Soil 342:277–287CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Manuel Mildner
    • 1
  • Martin K.-F. Bader
    • 1
    • 2
  • Sebastian Leuzinger
    • 1
    • 3
  • Rolf T. W. Siegwolf
    • 4
  • Christian Körner
    • 1
  1. 1.Institute of BotanyUniversity of BaselBaselSwitzerland
  2. 2.New Zealand Forest Research Institute (SCION)RotoruaNew Zealand
  3. 3.Institute for Applied Ecology New Zealand, School of Applied SciencesAuckland University of TechnologyAucklandNew Zealand
  4. 4.Laboratory of Atmospheric ChemistryPaul Scherrer Institute, PSIVilligenSwitzerland

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