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Trees

, Volume 25, Issue 2, pp 187–198 | Cite as

A free-air system for long-term stable carbon isotope labeling of adult forest trees

  • Thorsten E. E. GramsEmail author
  • Herbert Werner
  • Daniel Kuptz
  • Wilma Ritter
  • Frank Fleischmann
  • Christian P. Andersen
  • Rainer Matyssek
Original Paper

Abstract

Stable carbon (C) isotopes, in particular employed in labeling experiments, are an ideal tool to broaden our understanding of C dynamics in trees and forest ecosystems. Here, we present a free-air exposure system, named isoFACE, designed for long-term stable C isotope labeling in the canopy of 25 m tall forest trees. Labeling of canopy air was achieved by continuous release of CO2 with a δ13C of −46.9‰. To this end, micro-porous tubes were suspended at c. 1 m distance vertically through the canopy, minimizing CO2 gradients from the exterior to the interior and allowing for C labeling exposure during periods of low wind speed. Target for CO2 concentration ([CO2]) increase was ambient +100 μmol mol−1. Canopy [CO2] stayed within 10% of the target during more than 57% of the time and resulted in a drop of δ13C in canopy air by 7.8‰. After 19 labeling days about 50% of C in phloem sugars and stem CO2 efflux were turned over and 20–30% in coarse root CO2 efflux and soil CO2. The isoFACE system successfully altered δ13C of canopy air for studying turn-over of C pools in forest trees and soils, highlighting their slow turn-over rates.

Keywords

Canopy CO2 concentrations European beech (Fagus sylvatica L.) Free-air carbon isotope labeling infrastructure (isoFACE) Soil respired CO2 Stable carbon isotope (δ13C) Stem CO2 efflux (respiration) 

Notes

Acknowledgments

The authors gratefully acknowledge the help of T. Feuerbach, M. Goisser and Dr. C. Heerdt during experimentation and sample analyses. J. Heckmair, P. Kuba, H. Lohner and I. Süß are thanked for their skilful assistance. The investigation was funded through SFB 607 “Growth and Parasite Defense—Competition for Resources in Economic Plants from Agronomy and Forestry, Projects A6, B2 and B5” by the “Deutsche Forschungsgemeinschaft” (DFG). The information in this document has been subjected to EPA peer and administrative review, and it has been approved for publication as an EPA document. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

References

  1. Acosta M, Pavelka M, Pokorny R, Janous D, Marek MV (2008) Seasonal variation in CO2 efflux of stems and branches of Norway spruce trees. Ann Bot 101:469–477PubMedCrossRefGoogle Scholar
  2. Andersen CP, Nikolov I, Nikolova P, Matyssek R, Häberle KH (2005) Estimating “autotrophic” belowground respiration in spruce and beech forests: decreases following girdling. Eur J Forest Res 124:155–163CrossRefGoogle Scholar
  3. 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
  4. Bathellier C, Tcherkez G, Bligny R, Gout E, Cornic G, Ghashghaie J (2009) Metabolic origin of the δ13C of respired CO2 in roots of Phaseolus vulgaris. New Phytol 181:387–399PubMedCrossRefGoogle Scholar
  5. Berry SC, Varney GT, Flanagan LB (1997) Leaf δ13C in Pinus resinosa trees and understory plants: variation associated with light and CO2 gradients. Oecologia 109:499–506CrossRefGoogle Scholar
  6. Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40PubMedCrossRefGoogle Scholar
  7. Carbone MS, Czimczik CI, McDuffee KE, Trumbore SE (2007) Allocation and residence time of photosynthetic products in a boreal forest using a low-level 14C pulse-chase labeling technique. Glob Change Biol 13:466–477CrossRefGoogle Scholar
  8. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559CrossRefGoogle Scholar
  9. deVisser R, Vianden H, Schnyder H (1997) Kinetics and relative significance of remobilized and current C and N incorporation in leaf and root growth zones of Lolium perenne after defoliation: assessment by 13C and 15N steady-state labelling. Plant Cell Environ 20:37–46CrossRefGoogle Scholar
  10. Dieuaidenoubhani M, Raffard G, Canioni P, Pradet A, Raymond P (1995) Quantification of compartmented metabolic fluxes in maize root-tips using isotope distribution from C13-labelled or C14-labelled glucose. J Biol Chem 270:13147–13159CrossRefGoogle Scholar
  11. Dyckmans J, Flessa H (2001) Influence of tree internal N status on uptake and translocation of C and N in beech: a dual 13C and 15N labeling approach. Tree Physiol 21:395–401PubMedGoogle Scholar
  12. Ehleringer JR (1991) 13C/12C fractionation and its utility in terrestrial plant studies. In: Coleman DC, Fry B (eds) Carbon isotope techniques. Academic, Harcourt Brace Jovanovich Publishers, San Diego, USA, pp 187–200Google Scholar
  13. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
  14. Geßler A, Rennenberg H, Keitel C (2004) Stable isotope composition of organic compounds transported in the phloem of European beech—evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf-to-stem transport. Plant Biol 6:721–729PubMedCrossRefGoogle Scholar
  15. Geßler A, Tcherkez G, Peuke AD, Ghashghaie J, Farquhar GD (2008) Experimental evidence for diel variations of the carbon isotope composition in leaf, stem and phloem sap organic matter in Ricinus communis. Plant Cell Environ 31:941–953PubMedCrossRefGoogle Scholar
  16. Grams TEE, Anegg S, Häberle KH, Langebartels C, Matyssek R (1999) Interactions of chronic exposure to elevated CO2 and O3 levels in the photosynthetic light and dark reactions of European beech (Fagus sylvatica). New Phytol 144:95–107CrossRefGoogle Scholar
  17. Grams TEE, Kozovits AR, Häberle K-H, Matyssek R, Dawson TE (2007) Combining δ13C and δ18O analyses to unravel competition, CO2 and O3 effects on the physiological performance of different-aged trees. Plant Cell Environ 30:1023–1034PubMedCrossRefGoogle Scholar
  18. Granier A (1985) A new method of sap flow measurement in tree stems. Ann Sci Forest 42:193–200CrossRefGoogle Scholar
  19. Gunderson CA, Norby RJ, Wullschleger SD (1993) Foliar gas exchange response of two deciduous hardwoods during 3 years of growth in elevated CO2: no loss of photosynthetic enhancement. Plant Cell Environ 16:797–807CrossRefGoogle Scholar
  20. Heerdt C (2007) Methodenentwicklung zum kleinräumigen Pzonmonitoring in einem 60-jährigen Buchen/Fichten Mischbestand unter doppelt ambienter Free-Air-Ozonexposition. Ph.D. Technische Universität München, Department of Ecology and Ecosystem Management, Freising, p 9999Google Scholar
  21. Hendrey GR, Miglietta F (2006) FACE technology: past, present, and future. In: Nösberger J, Long SP, Norby RJ, Stitt M, Hendrey GR, Blum H (eds) Managed ecosystems and CO2: case studies processes and perspectives, vol 187. Springer, Berlin, pp 15–43Google Scholar
  22. Hendrey GR, Lewin KF, Nagy J (1993) Free air carbon-dioxide enrichment—development, progress, results. Vegetatio 104:17–31CrossRefGoogle Scholar
  23. Hendrey GR, Ellsworth DS, Lewin KF, Nagy J (1999) A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Glob Change Biol 5:293–309CrossRefGoogle Scholar
  24. 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
  25. Högberg P, Högberg MN, Gottlicher SG, Betson NR, Keel SG, Metcalfe DB, Campbell C, Schindlbacher A, Hurry V, Lundmark T, Linder S, Nasholm T (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177:220–228PubMedGoogle Scholar
  26. IPCC (2007) Climate change 2007: synthesis report. Contribution of the working groups I, II and II to the forth assessment report of the intergovernmental panel on climate change. In: Pachauri RK, Reisinger A, Core Writing Team (eds) IPCC, Geneva, Switzerland, p 104Google Scholar
  27. Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a 14C-labeled hardwood forest. New Phytol 172:523–535PubMedCrossRefGoogle Scholar
  28. Karnosky DF, Werner H, Holopainen T, Percy K, Oksanen T, Oksanen E, Heerdt C, Fabian P, Nagy J, Heilman W, Cox R, Nelson N, Matyssek R (2007) Free-air exposure systems to scale up ozone research to mature trees. Plant Biol 9:181–190PubMedCrossRefGoogle Scholar
  29. 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
  30. Keel SG, Pepin S, Leuzinger S, Körner C (2007) Stomatal conductance in mature deciduous forest trees exposed to elevated CO2. Trees-Struct Funct 21:151–159Google Scholar
  31. Kitao M, Löw M, Heerdt C, Grams TEE, Häberle K-H, Matyssek R (2009) Effects of chronic ozone exposure on gas exchange responses of adult beech trees (Fagus sylvatica) as related to the within-canopy light gradient. Environ Pollut 157:537–544PubMedCrossRefGoogle Scholar
  32. Kodama N, Barnard RL, Salmon Y, Weston C, Ferrio JP, Holst J, Werner RA, Saurer M, Rennenberg H, Buchmann N, Geßler A (2008) Temporal dynamics of the carbon isotope composition in a Pinus sylvestris stand: from newly assimilated organic carbon to respired carbon dioxide. Oecologia 156:737–750PubMedCrossRefGoogle Scholar
  33. Kuptz D, Matyssek R, Grams TEE (2010) Seasonal dynamics in stable carbon isotope composition (δ13C) from non-leafy branch, trunk and coarse root CO2 efflux of adult deciduous (Fagus sylvatica) and evergreen trees (Picea abies). Plant Cell Environ (accepted)Google Scholar
  34. Kuzyakov Y, Garvrichkova O (2010) Time lag between photosynthesis and carbon dioxide efflux from soil: a review. Glob Change Biol. doi: 10.1111/j.1365-2486.2010.02179.x
  35. Lattanzi FA, Schnyder H, Thornton B (2005) The sources of carbon and nitrogen supplying leaf growth. Assessment of the role of stores with compartmental models. Plant Physiol 137:383–395PubMedCrossRefGoogle Scholar
  36. Leake JR, Donnelly DP, Saunders EM, Boddy L, Read DJ (2001) Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood-decomposer fungus. Tree Physiol 21:71–82PubMedGoogle Scholar
  37. Lehmeier CA, Lattanzi FA, Schäufele R, Wild M, Schnyder H (2008) Root and shoot respiration of perennial ryegrass are supplied by the same substrate pools: assessment by dynamic 13C labeling and compartmental analysis of tracer kinetics. Plant Physiol 148:1148–1158PubMedCrossRefGoogle Scholar
  38. Lewin KF, Hendrey GR, Kolber Z (1992) Brookhaven National Laboratory free-air carbon-dioxide enrichment facility. Crit Rev Plant Sci 11:135–141Google Scholar
  39. Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Glob Change Biol 13:2089–2109CrossRefGoogle Scholar
  40. Luyssaert S, Ciais P, Piao SL, Schulze E-D, Jung M, Zaehle S, Schelhaas MJ, Reichstein M, Churkina G, Papale D, Abril G, Beer C, Grace J, Loustau D, Matteucci G, Magnani F, Nabuurs GJ, Verbeeck H, Sulkava M, GRvd Werf, Janssens IA (2010) The European carbon balance. Part 3: forests. Glob Change Biol 16:1429–1450CrossRefGoogle Scholar
  41. Matyssek R, Bahnweg G, Ceulemans R, Fabian P, Grill D, Hanke DE, Kraigher H, Oßwald W, Rennenberg H, Sandermann H, Tausz M, Wieser G (2007) Synopsis of the CASIROZ case study: Carbon sink strength of Fagus sylvatica L. in a changing environment - Experimental risk assessment of mitigation by chronic ozone impact. Plant Biol 9:163–180PubMedCrossRefGoogle Scholar
  42. Miglietta F, Peressotti A, Vaccari FP, Zaldei A, deAngelis P, Scarascia-Mugnozza G (2001) Free-air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system. New Phytol 150:465–476CrossRefGoogle Scholar
  43. Moore DJP, Gonzalez-Meler MA, Taneva L, Pippen JS, Kim HS, DeLucia EH (2008) The effect of carbon dioxide enrichment on apparent stem respiration from Pinus taeda L. is confounded by high levels of soil carbon dioxide. Oecologia 158:1–10PubMedCrossRefGoogle Scholar
  44. Mortazavi B, Chanton JP (2002) Carbon isotopic discrimination and control of nighttime canopy δ18O-CO2 in a pine forest in the southeastern United States. Glob Biogeochem Cycles 16Google Scholar
  45. Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell Environ 22:683–714CrossRefGoogle Scholar
  46. Nunn AJ, Kozovits AR, Reiter IM, Heerdt C, Leuchner M, Lütz C, Liu X, Löw M, Winkler JB, Grams TEE, Häberle KH, Werner H, Fabian P, Rennenberg H, Matyssek R (2005) Comparison of ozone uptake and sensitivity between a phytotron study with young beech and a field experiment with adult beech (Fagus sylvatica). Environ Pollut 137:406–494CrossRefGoogle Scholar
  47. Okada M, Lieffering M, Nakamura H, Yoshimoto M, Kim HY, Kobayashi K (2001) Free-air CO2 enrichment (FACE) using pure CO2 injection: system description. New Phytol 150:251–260CrossRefGoogle Scholar
  48. Ostle N, Briones MJI, Ineson P, Cole L, Staddon P, Sleep D (2007) Isotopic detection of recent photosynthate carbon flow into grassland rhizosphere fauna. Soil Biol Biochem 39:768–777CrossRefGoogle Scholar
  49. Paembonan SA, Hagihara A, Hozumi K (1992) Long-term respiration in relation to growth and maintenance processes of the aboveground parts of a Hinoki forest tree. Tree Physiol 10:101–110PubMedGoogle Scholar
  50. Pepin S, Körner C (2002) Web-FACE: A new canopy free-air CO2 enrichment system for tall trees in mature forests. Oecologia 133:1–9CrossRefGoogle Scholar
  51. Plain C, Gerant D, Maillard P, Dannoura M, Dong Y, Zeller B, Priault P, Parent F, Epron D (2009) Tracing of recently assimilated carbon in respiration at high temporal resolution in the field with a tuneable diode laser absorption spectrometer after in situ 13CO2 pulse labelling of 20-year-old beech trees. Tree Physiol 29:1433–1445PubMedCrossRefGoogle Scholar
  52. Prater JL, Mortazavi B, Chanton JP (2006) Diurnal variation of the δ13C of pine needle respired CO2 evolved in darkness. Plant Cell Environ 29:202–211PubMedCrossRefGoogle Scholar
  53. Pretzsch H, Kahn M, Grote R (1998) The mixed spruce-beech forest stands of the ‘‘Sonderforschungsbereich 607—growth or parasite defence?’’ in the forest district Kranzberger Forst. Forstwissenschaftliches Centralblatt 117:241–257CrossRefGoogle Scholar
  54. Reiter IM, Häberle KH, Nunn AJ, Heerdt C, Reitmayer H, Grote R, Matyssek R (2005) Competitive strategies in adult beech and spruce: space-related foliar carbon investment versus carbon gain. Oecologia 146:337–349PubMedCrossRefGoogle Scholar
  55. Ryan MG (1991) Effects of climate change on plant respiration. Ecol Appl 1:157–167CrossRefGoogle Scholar
  56. Sauer D, Kuzyakov Y, Stahr K (2006) Spatial distribution of root exudates of five plant species as assessed by 14C labeling. J Plant Nutri 169:360–362CrossRefGoogle Scholar
  57. Schnyder H, Schäufele R, Lötscher M, Gebbing T (2003) Disentangling CO2 fluxes: direct measurements of mesocosm-scale natural abundance 13CO2/12CO2 gas exchange, 13C discrimination, and labelling of CO2 exchange flux components in controlled environments. Plant, Cell Environ 26:1863–1874CrossRefGoogle Scholar
  58. Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R (1997) Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–582CrossRefGoogle Scholar
  59. Steinmann KTW, Siegwolf R, Saurer M, Körner C (2004) Carbon fluxes to the soil in a mature temperate forest assessed by 13C isotope tracing. Oecologia 141:489–501PubMedCrossRefGoogle Scholar
  60. Subke JA, Vallack HW, Magnusson T, Keel SG, Metcalfe DB, Hogberg P, Ineson P (2009) Short-term dynamics of abiotic and biotic soil 13CO2 effluxes after in situ 13CO2 pulse labelling of a boreal pine forest. New Phytol 183:349–357PubMedCrossRefGoogle Scholar
  61. Talhelm AF, Qadir SA, Powers MD, Bradley KL, Friend AL, Pregitzer KS (2007) 13C labeling of plant assimilates using a simple canopy-scale open air system. Plant Soil 296:227–234CrossRefGoogle Scholar
  62. Tang JW, Bolstad PV, Desai AR, Martin JG, Cook BD, Davis KJ, Carey EV (2008) Ecosystem respiration and its components in an old-growth forest in the Great Lakes region of the United States. Agric For Meteorol 148:171–185CrossRefGoogle Scholar
  63. Tcherkez G, Nogues S, Bleton J, Cornic G, Badeck F, Ghashghaie J (2003) Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in French bean. Plant Physiol 131:237–244PubMedCrossRefGoogle Scholar
  64. Teskey RO, Saveyn A, Steppe K, McGuire MA (2008) Origin, fate and significance of CO2 in tree stems. New Phytol 177:17–32PubMedGoogle Scholar
  65. Thornton B, Paterson E, Midwood AJ, Sim A, Pratt SM (2004) Contribution of current carbon assimilation in supplying root exudates of Lolium perenne measured using steady-state 13C labelling. Physiol Plant 120:434–441PubMedCrossRefGoogle Scholar
  66. Ubierna N, Kumar AS, Cernusak LA, Pangle RE, Gag PJ, Marshall JD (2009) Storage and transpiration have negligible effects on 13C of stem CO2 efflux in large conifer trees. Tree Physiol 29:1563–1574PubMedCrossRefGoogle Scholar
  67. Werner H, Fabian P (2002) Free-air fumigation of mature trees—a novel system for controlled ozone enrichment in grown-up beech and spruce canopies. Environ Sci Pollut Res 9:117–121CrossRefGoogle Scholar
  68. Wieser G, Gruber A, Bahn M, Catala E, Carrillo E, Jimenez MS, Morales D (2009) Respiratory fluxes in a Canary Islands pine forest. Tree Physiol 29:457–466PubMedCrossRefGoogle Scholar
  69. Wingate L (2008) Weighty issues in respiratory metabolism: intriguing carbon isotope signals from roots and leaves. New Phytol 177:285–287PubMedCrossRefGoogle Scholar
  70. Wingate L, Ogee J, Burlett R, Bosc A, Devaux M, Grace J, Loustau D, Geßler A (2010) Photosynthetic carbon isotope discrimination and its relationship to the carbon isotope signals of stem, soil and ecosystem respiration. New Phytol 188:576–589Google Scholar
  71. Winterhalter M (1998) Die Bestimmung turbulenter Flüsse am Messturm Schachtenau im Nationalpark Bayerischer Wald—Ein Vergleich mikrometeorologischer Methoden. Ph.D. Ludwig-Maximilians-Universität München, Forstwissenschaftliche Fakültät, Freising, p 113Google Scholar
  72. Zobitz JM, Keener JP, Schnyder H, Bowling DR (2006) Sensitivity analysis and quantification of uncertainty for isotopic mixing relationships in carbon cycle research. Agric For Meteorol 136:56–75CrossRefGoogle Scholar

Copyright information

© Springer-Verlag (outside the USA) 2010

Authors and Affiliations

  • Thorsten E. E. Grams
    • 1
    Email author
  • Herbert Werner
    • 2
  • Daniel Kuptz
    • 1
  • Wilma Ritter
    • 1
  • Frank Fleischmann
    • 3
  • Christian P. Andersen
    • 4
  • Rainer Matyssek
    • 1
  1. 1.Ecophysiology of Plants, Department of Ecology and Ecosystem ManagementTechnische Universität MünchenFreisingGermany
  2. 2.Ecoclimatology, Department of Ecology and Ecosystem ManagementTechnische Universität MünchenFreisingGermany
  3. 3.Pathology of Woody Plants, Department of Ecology and Ecosystem ManagementTechnische Universität MünchenFreisingGermany
  4. 4.Western Ecology DivisionUS Environmental Protection AgencyCorvallisUSA

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