Skip to main content
SpringerLink
Log in

Sustained enhancement of photosynthesis in mature deciduous forest trees after 8 years of free air CO2 enrichment

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Carbon uptake by forests constitutes half of the planet’s terrestrial net primary production; therefore, photosynthetic responses of trees to rising atmospheric CO2 are critical to understanding the future global carbon cycle. At the Swiss Canopy Crane, we investigated gas exchange characteristics and leaf traits in five deciduous tree species during their eighth growing season under free air carbon dioxide enrichment in a 35-m tall, ca. 100-year-old mixed forest. Net photosynthesis of upper-canopy foliage was 48% (July) and 42% (September) higher in CO2-enriched trees and showed no sign of down-regulation. Elevated CO2 had no effect on carboxylation efficiency (V cmax) or maximal electron transport (J max) driving ribulose-1,5-bisphosphate (RuBP) regeneration. CO2 enrichment improved nitrogen use efficiency, but did not affect leaf nitrogen (N) concentration, leaf thickness or specific leaf area except for one species. Non-structural carbohydrates accumulated more strongly in leaves grown under elevated CO2 (largely driven by Quercus). Because leaf area index did not change, the CO2-driven stimulation of photosynthesis in these trees may persist in the upper canopy under future atmospheric CO2 concentrations without reductions in photosynthetic capacity. However, given the lack of growth stimulation, the fate of the additionally assimilated carbon remains uncertain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

A growth :

Light-saturated net photosynthesis measured at growth CO2 concentration (ambient CO2: A agrowth ; elevated CO2: A egrowth )

A 550 :

Light-saturated net photosynthesis measured at 550 ppm leaf chamber CO2 concentration

A 380 :

Light-saturated net photosynthesis measured at 380 ppm leaf chamber CO2 concentration

C:

Carbon

E :

A egrowth /A agrowth

E′:

A 550 /A 380

FACE:

Free air carbon dioxide enrichment

J max :

Maximal photosynthetic electron transport rate (a proxy for ribulose-1,5-bisphosphate regeneration)

LAI:

Leaf area index

N:

Nitrogen

PPFD:

Photosynthetic photon flux density

SLA:

Specific leaf area

NSC:

Non-structural carbohydrates

SCC:

Swiss canopy crane

SE:

Standard error of the mean

V cmax :

Maximal carboxylation rate of Rubisco

ALVPD:

Air-to-leaf vapour pressure deficit

References

  • Adam NR, Wall GW, Kimball BA, Idso SB, Webber AN (2004) Photosynthetic down-regulation over long-term CO2 enrichment in leaves of sour orange (Citrus aurantium) trees. New Phytol 163:341–347

    Article  Google Scholar 

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–371

    Article  PubMed  Google Scholar 

  • Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising CO2: mechanisms and environmental interactions. Plant Cell Environ 30:258–270

    Article  CAS  PubMed  Google Scholar 

  • Asshoff R, Zotz G, Körner C (2006) Growth and phenology of mature temperate forest trees in elevated CO2. Glob Change Biol 12:848–861

    Article  Google Scholar 

  • Bader M, Körner C (2010) No overall stimulation of soil respiration under mature deciduous forest trees after 7 years of CO2 enrichment. Glob Change Biol. doi:10.1111/j.1365-2486.2010.02159.x (in press)

  • Bader M, 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

    Article  Google Scholar 

  • Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449

    Article  CAS  PubMed  Google Scholar 

  • Cech PG, Pepin S, Körner C (2003) Elevated CO2 reduces sap flux in mature deciduous forest trees. Oecologia 137:258–268

    Article  PubMed  Google Scholar 

  • Crous KY, Walters MB, Ellsworth DS (2008) Elevated CO2 concentration affects leaf photosynthesis–nitrogen relationships in Pinus taeda over nine years in FACE. Tree Physiol 28:607–614

    CAS  PubMed  Google Scholar 

  • Curtis PS, Wang XZ (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313

    Article  Google Scholar 

  • Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639

    Article  CAS  PubMed  Google Scholar 

  • Egli P, Maurer S, Spinnler D, Landolt W, Gunthardt-Georg MS, Körner C (2001) Downward adjustment of carbon fluxes at the biochemical, leaf, and ecosystem scale in beech-spruce model communities exposed to long-term atmospheric CO2 enrichment. Oikos 92:279–290

    Article  CAS  Google Scholar 

  • Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Glob Change Biol 10:2121–2138

    Article  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  Google Scholar 

  • Gielen B, Liberloo M, Bogaert J, Calfapietra C, De Angelis P, Miglietta F, Scarascia-Mugnozza G, Ceulemans R (2003) Three years of free-air CO2 enrichment (POPFACE) only slightly affect profiles of light and leaf characteristics in closed canopies of Populus. Glob Change Biol 9:1022–1037

    Article  Google Scholar 

  • Gunderson CA, Wullschleger SD (1994) Photosynthetic acclimation in trees to rising atmospheric CO2—a broader perspective. Photosynth Res 39:369–388

    Google Scholar 

  • Gunderson CA, Sholtis JD, Wullschleger SD, Tissue DT, Hanson PJ, Norby RJ (2002) Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during 3 years of CO2 enrichment. Plant Cell Environ 25:379–393

    Article  Google Scholar 

  • Hättenschwiler S, Miglietta F, Raschi A, Körner C (1997) Thirty years of in situ tree growth under elevated CO2: a model for future forest responses? Glob Change Biol 3:463–471

    Article  Google Scholar 

  • Herrick JD, Thomas RB (2001) No photosynthetic down-regulation in sweetgum trees (Liquidambar styraciflua L.) after three years of CO2 enrichment at the Duke forest FACE experiment. Plant Cell Environ 24:53–64

    Article  CAS  Google Scholar 

  • 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 172:319–329

    Article  CAS  PubMed  Google Scholar 

  • Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411

    Article  PubMed  Google Scholar 

  • Körner C, Miglietta F (1994) Long-term effects of naturally elevated CO2 on mediterranean grassland and forest trees. Oecologia 99:343–351

    Article  Google Scholar 

  • 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 309:1360–1362

    Article  PubMed  Google Scholar 

  • 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 2:421–436

    Article  Google Scholar 

  • Leuzinger S, Körner C (2007) Water savings in mature deciduous forest trees under elevated CO2. Glob Change Biol 13:2498–2508

    Article  Google Scholar 

  • Liberloo M, Tulva I, Raim O, Kull O, Ceulemans R (2007) Photosynthetic stimulation under long-term CO2 enrichment and fertilization is sustained across a closed Populus canopy profile (EUROFACE). New Phytol 173:537–549

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628

    Article  CAS  PubMed  Google Scholar 

  • Medlyn BE, Badeck FW, De Pury DGG, Barton CVM, Broadmeadow M, Ceulemans R, De Angelis P, Forstreuter M, Jach ME, Kellomaki S, Laitat E, Marek M, Philippot S, Rey A, Strassemeyer J, Laitinen K, Liozon R, Portier B, Roberntz P, Wang K, Jarvis PG (1999) Effects of elevated CO2 on photosynthesis in European forest species: a meta-analysis of model parameters. Plant Cell Environ 22:1475–1495

    Article  CAS  Google Scholar 

  • Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582

    Article  CAS  Google Scholar 

  • Noormets A, McDonald EP, Dickson RE, Kruger EL, Sober A, Isebrands JG, Karnosky DF (2001) The effect of elevated carbon dioxide and ozone on leaf- and branch-level photosynthesis and potential plant-level carbon gain in aspen. Trees Struct Funct 15:262–270

    CAS  Google Scholar 

  • 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 22:683–714

    Article  CAS  Google Scholar 

  • Norby RJ, Sholtis JD, Gunderson CA, Jawdy SS (2003) Leaf dynamics of a deciduous forest canopy: no response to elevated CO2. Oecologia 136:574–584

    Article  PubMed  Google Scholar 

  • Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280

    Article  Google Scholar 

  • 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 411:469–472

    Article  CAS  PubMed  Google Scholar 

  • Pepin S, Körner C (2002) Web-FACE: a new canopy free-air CO2 enrichment system for tall trees in mature forests. Oecologia 133:1–9

    Article  Google Scholar 

  • Rogers A, Ellsworth DS (2002) Photosynthetic acclimation of Pinus taeda (loblolly pine) to long-term growth in elevated pCO2 (FACE). Plant Cell Environ 25:851–858

    Article  CAS  Google Scholar 

  • Roy J, Saugier B, Mooney HA (2001) Terrestrial global productivity. Academic Press, San Diego

    Google Scholar 

  • Sabine CL, Heimann M, Artaxo P, Bakker DCE, Chen C-TA, Field CB, Gruber N, Le Quéré C, Prinn RG, Richey JE, Lankao PR, Sathaye JA, Valentini R (2004) Current status and past trends of the global carbon cycle. In: Field CB, Raupach MR (eds) Global carbon cycle—integrating humans climate and the natural world. Island Press, Washington, DC, pp 17–44

    Google Scholar 

  • Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139:395–436

    Google Scholar 

  • Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Glob Change Biol 1:77–91

    Article  Google Scholar 

  • Sholtis JD, Gunderson CA, Norby RJ, Tissue DT (2004) Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand. New Phytol 162:343–354

    Article  Google Scholar 

  • Stitt M (1991) Rising CO2 level and their potential significance for cabon flow in photosynthetic cells. Plant Cell Environ 14:741–762

    Article  CAS  Google Scholar 

  • Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621

    Article  CAS  Google Scholar 

  • Tans P (2008) Trends in atmospheric carbon dioxide. Web page NOAA/ESRL http://www.esrl.noaa.gov/gmd/ccgg/trends/. Accessed 27 July 2009

  • Uddling J, Teclaw RM, Kubiske ME, Pregitzer KS, Ellsworth DS (2008) Sap flux in pure aspen and mixed aspen—birch forests exposed to elevated concentrations of carbon dioxide and ozone. Tree Physiol 28:1231–1243

    CAS  PubMed  Google Scholar 

  • Uddling J, Teclaw RM, Pregitzer KS, Ellsworth DS (2009) Leaf and canopy conductance in aspen and aspen—birch forests under free-air enrichment of carbon dioxide and ozone. Tree Physiol 29:1367–1380

    Article  CAS  PubMed  Google Scholar 

  • Zotz G, Pepin S, Körner C (2005) No down-regulation of leaf photosynthesis in mature forest trees after three years of exposure to elevated CO2. Plant Biol 7:369–374

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Erwin Amstutz for crane operations and for his efforts in data collection. We are grateful to the Paul Scherrer Institute (Switzerland) for the provision of equipment. Further, we thank Olivier Bignucolo for various laboratory analyses of leaf parameters. The SCC FACE study was supported by the Swiss National Science Foundation (grant 3100AO-111914/1).

Author information

Authors and Affiliations

  1. Institute of Botany, University of Basel, Schönbeinstrasse 6, 4056, Basel, Switzerland

    Martin Karl-Friedrich Bader & Christian Körner

  2. Paul Scherrer Institute, 5323, Villigen PSI, Switzerland

    Rolf Siegwolf

Authors
  1. Martin Karl-Friedrich Bader
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rolf Siegwolf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Körner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Karl-Friedrich Bader.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bader, M.KF., Siegwolf, R. & Körner, C. Sustained enhancement of photosynthesis in mature deciduous forest trees after 8 years of free air CO2 enrichment. Planta 232, 1115–1125 (2010). https://doi.org/10.1007/s00425-010-1240-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1240-8

Keywords

Search

Navigation