Photosynthetica 2025, 63(1):51-63 | DOI: 10.32615/ps.2025.006

Response of leaf internal CO2 concentration and intrinsic water-use efficiency in Norway spruce to century-long gradual CO2 elevation

J. ŠANTRŮČEK1, J. KUBÁSEK1, J. JANOVÁ1, H. ŠANTRŮČKOVÁ1, J. ALTMAN2, 3, J. TUMAJER4, 5, M. HRÁDKOVÁ1, 2, E. CIENCIALA4
1 Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
2 Institute of Botany, AS CR, Zámek 1, 252 43 Průhonice, Czech Republic
3 Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Prague 6 - Suchdol, Czech Republic
4 IFER - Institute of Forest Ecosystem Research, Čs. armády 655, 254 01 Jílové u Prahy, Czech Republic
5 Department of Physical Geography and Geoecology, Faculty of Science, Charles University, Albertov 6, 12843 Prague, Czech Republic

The strategies of Norway spruce [Picea abies (L.) Karst.] to increasing atmospheric CO2 concentration (Ca) are not entirely clear. Here, we reconstructed centennial trajectories of leaf internal CO2 concentration (Ci) and intrinsic water-use efficiency (WUEi) from the amount of 13C in tree-ring cellulose. We collected 57 cores across elevations, soil, and atmospheric conditions in central Europe. Generally, WUEi and Ci increased over the last 100 years and the Ci/Ca ratio remained almost constant. However, two groups were distinguished. The first group showed a quasi-linear response to Ca and the sensitivity of Ci to Ca (s = dCi/dCa) ranged from 0 to 1. Trees in the second group showed nonmonotonic responses with extremes during the peak of industrial air pollution in the 1980s and s increase from -1 to +1.6. Our study shows a marked attenuation of the rise in WUEi during the 20th century leading to invariant WUEi in recent decades.

Additional key words: carbon dioxide enrichment; photosynthesis; Picea abies; stable carbon isotopes; tree rings; water-use efficiency.

Received: October 1, 2024; Revised: January 29, 2025; Accepted: February 10, 2025; Prepublished online: March 13, 2025; Published: March 27, 2025  Show citation

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ŠANTRŮČEK, J., KUBÁSEK, J., JANOVÁ, J., ŠANTRŮČKOVÁ, H., ALTMAN, J., TUMAJER, J., HRÁDKOVÁ, M., & CIENCIALA, E. (2025). Response of leaf internal CO2 concentration and intrinsic water-use efficiency in Norway spruce to century-long gradual CO2 elevation. Photosynthetica63(1), 51-63. doi: 10.32615/ps.2025.006
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References

  1. Adams M.A., Buckley T.N., Turnbull T.L.: Diminishing CO2-driven gains in water-use efficiency of global forests. - Nat. Clim. Change 10: 466-471, 2020. Go to original source...
  2. Ainsworth E.A., Long S.P.: 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, 2005. Go to original source...
  3. Ainsworth E.A., Rogers A.: The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. - Plant Cell Environ. 30: 258-270, 2007. Go to original source...
  4. Altman J., Fibich P., Santruckova H. et al.: Environmental factors exert strong control over the climate-growth relationships of Picea abies in Central Europe. - Sci. Total Environ. 609: 506-516, 2017. Go to original source...
  5. Andreu-Hayles L., Planells O., Gutiérrez E. et al.: Long tree-ring chronologies reveal 20th century increases in water-use efficiency but no enhancement of tree growth at five Iberian pine forests. - Glob. Change Biol. 17: 2095-2112, 2011. Go to original source...
  6. Arco Molina J.G., Saurer M., Altmanova N. et al.: Recent warming and increasing CO2 stimulate growth of dominant trees under no water limitation in South Korea. - Tree Physiol. 44: tpae 103, 2024. Go to original source...
  7. Baillie M.G.L., Pilcher J.R.: A simple crossdating program for tree-ring research. - Tree-Ring Bull. 33: 7-14, 1973. Go to original source...
  8. Betts R.A., Boucher O., Collins M. et al.: Projected increase in continental runoff due to plant responses to increasing carbon dioxide. - Nature 448: 1037-1041, 2007. Go to original source...
  9. Boettger T., Haupt M., Friedrich M., Waterhouse J.S.: Reduced climate sensitivity of carbon, oxygen and hydrogen stable isotope ratios in tree-ring cellulose of silver fir (Abies alba Mill.) influenced by background SO2 in Franconia (Germany, Central Europe). - Environ. Pollut. 185: 281-294, 2014. Go to original source...
  10. Brienen R.J.W., Gloor E., Clerici S. et al.: Tree height strongly affects estimates of water-use efficiency responses to climate and CO2 using isotopes. - Nat. Commun. 8: 288, 2017. Go to original source...
  11. Brümmer C., Black T.A., Jassal R.S. et al.: How climate and vegetation type influence evapotranspiration and water use efficiency in Canadian forest, peatland and grassland ecosystems. - Agr. Forest Meteorol. 153: 14-30, 2012. Go to original source...
  12. Buras A., van der Maaten-Theunissen M., van der Maaten E. et al.: Tuning the voices of a choir: detecting ecological gradients in time-series populations. - PLoS ONE 11: e0158346, 2016. Go to original source...
  13. Čada V., Šantrůčková H., Šantrůček J. et al.: Complex physiological response of norway spruce to atmospheric pollution - decreased carbon isotope discrimination and unchanged tree biomass increment. - Front. Plant Sci. 7: 805, 2016. Go to original source...
  14. Cavender-Bares J., Bazzaz F.A.: Changes in drought response strategies with ontogeny in Quercus rubra: implications for scaling from seedlings to mature trees. - Oecologia 124: 8-18, 2000. Go to original source...
  15. Cernusak L.A.: Gas exchange and water-use efficiency in plant canopies. - Plant Biol. 22: 52-67, 2020. Go to original source...
  16. Cienciala E., Russ R., Šantrůčková H. et al.: Discerning environmental factors affecting current tree growth in Central Europe. - Sci. Total Environ. 573: 541-554, 2016. Go to original source...
  17. Coumou D., Lehmann J., Beckmann J.: The weakening summer circulation in the Northern Hemisphere mid-latitudes. - Science 348: 324-327, 2015. Go to original source...
  18. Cowan I.R., Farquhar G.D.: Stomatal function in relation to leaf metabolism and environment. - In: Jennings D.H. (ed.): Integration of Activity in the Higher Plant. Pp. 471-505. The University Press, Cambridge 1977.
  19. Drake B.G., Gonzalez-Meler M.A., Long S.P.: More efficient plants: A consequence of rising atmospheric CO2? - Annu. Rev. Plant Phys. 48: 609-639, 1997. Go to original source...
  20. Duffy J.E., McCarroll D., Barnes A. et al.: Short-lived juvenile effects observed in stable carbon and oxygen isotopes of UK oak trees and historic building timbers. - Chem. Geol. 472: 1-7, 2017. Go to original source...
  21. Eckstein D., Bauch J.: Beitrag zur Rationalisierung eines dendrochronologischen Verfahrens und zur Analyse seiner Aussagesicherheit. - Forstwiss. Centralbl. 88: 230-250, 1969. Go to original source...
  22. Farquhar G.D., Dubbe D.R., Raschke K.: Gain of feedback loop involving carbon dioxide and stomata: theory and measurement. - Plant Physiol. 62: 406-412, 1978. Go to original source...
  23. Farquhar G.D., Ehleringer J.R., Hubick K.T.: Carbon isotope discrimination and photosynthesis. - Annu. Rev. Plant Phys. 40: 503-537, 1989. Go to original source...
  24. Farquhar G.D., OꞌLeary M.H., Berry J.A.: On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. - Aust. J. Plant Physiol. 9: 121-137, 1982. Go to original source...
  25. Farquhar G.D., Sharkey T.D.: Stomatal conductance and photosynthesis. - Annu. Rev. Plant Biol. 33: 317-345, 1982. Go to original source...
  26. Feng X.H.: Long-term ci/ca response of trees in western North America to atmospheric CO2 concentration derived from carbon isotope chronologies. - Oecologia 117: 19-25, 1998. Go to original source...
  27. Francey R.J., Allison C.E., Etheridge D.M. et al.: A 1000-year high precision record of δ13C in atmospheric CO2. - Tellus B 51: 170-193, 1999. Go to original source...
  28. Francey R.J., Farquhar G.D.: An explanation of 13C/12C variations in tree rings. - Nature 297: 28-31, 1982. Go to original source...
  29. Frank D.C., Poulter B., Saurer M. et al.: Water-use efficiency and transpiration across European forests during the Anthropocene. - Nat. Clim. Change 5: 579-583, 2015. Go to original source...
  30. Franks P.J., Adams M.A., Amthor J.S. et al.: Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. - New Phytol. 197: 1077-1094, 2013. Go to original source...
  31. Fritts H.C.: Tree Rings and Climate. Pp. 567. Academic Press, New York 1976.
  32. Gagen M., Finsinger W., Wagner-Cremer F. et al.: Evidence of changing intrinsic water-use efficiency under rising atmospheric CO2 concentrations in Boreal Fennoscandia from subfossil leaves and tree ring delta 13C ratios. - Glob. Change Biol. 17: 1064-1072, 2011. Go to original source...
  33. Gagen M., McCarroll D., Robertson I. et al.: Do tree ring δ13C series from Pinus sylvestris in northern Fennoscandia contain long-term non-climatic trends? - Chem. Geol. 252: 42-51, 2008. Go to original source...
  34. Gärtner H., Nievergelt D.: The core-microtome: A new tool for surface preparation on cores and time series analysis of varying cell parameters. - Dendrochronologia 28: 85-92, 2010. Go to original source...
  35. Gebauer G., Schulze E.-D.: Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, NE Bavaria. - Oecologia 87: 198-207, 1991. Go to original source...
  36. Gessler A., Ferrio J.P., Hommel R. et al.: Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the leaves to the wood. - Tree Physiol. 34: 796-818, 2014. Go to original source...
  37. Guerrieri R., Mencuccini M., Sheppard L.J. et al.: The legacy of enhanced N and S deposition as revealed by the combined analysis of δ13C, δ18O and δ15N in tree rings. - Glob. Change Biol. 17: 1946-1962, 2011. Go to original source...
  38. Hetherington A.M., Woodward F.I.: The role of stomata in sensing and driving environmental change. - Nature 424: 901-908, 2003. Go to original source...
  39. Hoshika Y., Omasa K., Paoletti E.: Whole-tree water use efficiency is decreased by ambient ozone and not affected by O3-induced stomatal sluggishness. - PLoS ONE 7: e39270, 2012. Go to original source...
  40. Jasechko S., Sharp Z.D., Gibson J.J. et al.: Terrestrial water fluxes dominated by transpiration. - Nature 496: 347-350, 2013. Go to original source...
  41. Keeling C.D., Whorf T.P.: Atmospheric CO2 Records from Sites in the Scripps Institution of Oceanography (SIO) Air Sampling Network (1985-2007). CDIAC, ESS-DIVE repository 2004. Available at: https://data.ess-dive.lbl.gov/datasets/doi:10.3334/CDIAC/ATG.NDP001. Go to original source...
  42. Keenan T.F., Hollinger D.Y., Bohrer G. et al.: Increase in forest water-use efficiency as atmospheric carbon dioxide concentrations rise. - Nature 499: 324-327, 2013. Go to original source...
  43. Keller K.M., Lienert S., Bozbiyik A. et al.: 20th century changes in carbon isotopes and water-use efficiency: tree-ring-based evaluation of the CLM4.5 and LPX-Bern models. - Biogeosciences 14: 2641-2673, 2017. Go to original source...
  44. Köhler I.H., Macdonald A.J., Schnyder H.: Last-century increases in intrinsic water-use efficiency of grassland communities have occurred over a wide range of vegetation composition, nutrient inputs, and soil pH. - Plant Physiol. 170: 881-890, 2016. Go to original source...
  45. Körner C.: Ecological impacts of atmospheric CO2 enrichment on terrestrial ecosystems. - Philos. T. Roy. Soc. A 361: 2023-2041, 2003. Go to original source...
  46. Körner C.: Plant CO2 responses: an issue of definition, time and resource supply. - New Phytol. 172: 393-411, 2006. Go to original source...
  47. Lake J.A., Quick W.P., Beerling D.J., Woodward F.I.: Signals from mature to new leaves. - Nature 411: 154, 2001. Go to original source...
  48. Lake J.A., Woodward F.I.: Response of stomatal numbers to CO2 and humidity: control by transpiration rate and abscisic acid. - New Phytol. 179: 397-404, 2008. Go to original source...
  49. Laumer W., Andreu L., Helle G. et al.: A novel approach for the homogenization of cellulose to use micro-amounts for stable isotope analyses. - Rapid Commun. Mass Sp. 23: 1934-1940, 2009. Go to original source...
  50. Leuzinger S., Körner C.: Water savings in mature deciduous forest trees under elevated CO2. - Glob. Change Biol. 13: 2498-2508, 2007. Go to original source...
  51. Loader N.J., McCarroll D., Gagen M. et al.: Extracting climatic information from stable isotopes in tree rings. - In: Dawson T.E., Siegwolf R.T.W. (ed.): Stable Isotopes as Indicators of Ecological Change. Pp. 27-48. Elsevier, Amsterdam-Boston-Tokyo 2007. Go to original source...
  52. Loader N.J., Robertson I., Barker A.C. et al.: An improved technique for the batch processing of small wholewood samples to α-cellulose. - Chem. Geol. 136: 313-317, 1997. Go to original source...
  53. Maseyk K., Hemming D., Angert A. et al.: Increase in water-use efficiency and underlying processes in pine forests across a precipitation gradient in the dry Mediterranean region over the past 30 years. - Oecologia 167: 573-585, 2011. Go to original source...
  54. McCarroll D., Gagen M.H., Loader N.J. et al.: Correction of tree ring stable carbon isotope chronologies for changes in the carbon dioxide content of the atmosphere. - Geochim. Cosmochim. Ac. 73: 1539-1547, 2009. Go to original source...
  55. McCarroll D., Loader N.J.: Stable isotopes in tree rings. - Quaternary Sci. Rev. 23: 771-801, 2004. Go to original source...
  56. Medlyn B.E., Barton C.V.M., Broadmeadow M.S.J. et al.: Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. - New Phytol. 149: 247-264, 2001. Go to original source...
  57. Menezes-Silva P.E., Loram-Lourenço L., Alves R.D.F.B. et al.: Different ways to die in a changing world: Consequences of climate change for tree species performance and survival through an ecophysiological perspective. - Ecol. Evol. 9: 11979-11999, 2019. Go to original source...
  58. Millard P., Grelet G.A.: Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. - Tree Physiol. 30: 1083-1095, 2010. Go to original source...
  59. Miller-Rushing A.J., Primack R.B., Templer P.H. et al.: Long-term relationships among atmospheric CO2, stomata, and intrinsic water use efficiency in individual trees. - Am. J. Bot. 96: 1779-1786, 2009. Go to original source...
  60. Novick K.A., Ficklin D.L., Grossiord C. et al.: The impacts of rising vapour pressure deficit in natural and managed ecosystems. - Plant Cell Environ. 47: 3561-3589, 2024. Go to original source...
  61. Oulehle F., Urban O., Tahovská K. et al.: Calcium availability affects the intrinsic water-use efficiency of temperate forest trees. - Commun. Earth Environ. 4: 199, 2023. Go to original source...
  62. Peñuelas J., Canadell J.G., Ogaya R.: Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. - Global Ecol. Biogeogr. 20: 597-608, 2011. Go to original source...
  63. Ponton S., Flanagan L.B., Alstad K.P. et al.: Comparison of ecosystem water-use efficiency among Douglas-fir forest, aspen forest and grassland using eddy covariance and carbon isotope techniques. - Glob. Change Biol. 12: 294-310, 2006. Go to original source...
  64. Rennenberg H., Dannenmann M., Gessler A. et al.: Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. - Plant Biol. 11: 4-23, 2009. Go to original source...
  65. Sage R.F.: Acclimation of photosynthesis to increasing atmospheric CO2: The gas-exchange perspective. - Photosynth. Res. 39: 351-368, 1994. Go to original source...
  66. Sala A., Piper F., Hoch G.: Physiological mechanisms of drought-induced tree mortality are far from being resolved. - New Phytol. 186: 274-281, 2010. Go to original source...
  67. Santrucek J., Sage R.F.: Acclimation of stomatal conductance to a CO2-enriched atmosphere and elevated temperature in Chenopodium album. - Aust. J. Plant Physiol. 23: 467-478, 1996. Go to original source...
  68. Šantrůčková H., Cienciala E., Kaňa J., Kopáček J.: The chemical composition of forest soils and their degree of acidity in Central Europe. - Sci. Total Environ. 687: 96-103, 2019. Go to original source...
  69. Šantrůčková H., Šantrůček J., Šetlík J. et al.: Carbon isotopes in tree rings of Norway spruce exposed to atmospheric pollution. - Environ. Sci. Technol. 41: 5778-5782, 2007. Go to original source...
  70. Saurer M., Siegwolf R.T.W., Schweingruber F.H.: Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. - Glob. Change Biol. 10: 2109-2120, 2004. Go to original source...
  71. Saurer M., Spahni R., Frank D.C. et al.: Spatial variability and temporal trends in water-use efficiency of European forests. - Glob. Change Biol. 20: 3700-3712, 2014. Go to original source...
  72. Schweingruber F.H.: Tree Rings and Environment: Dendroecology. Pp. 609. Paul Haupt, Bern 1996.
  73. Schymanski S.J., Or D.: Wind increases leaf water use efficiency. -Plant Cell Environ. 39: 1448-1459, 2016. Go to original source...
  74. Seibt U., Rajabi A., Griffiths H., Berry J.A.: Carbon isotopes and water use efficiency: sense and sensitivity. - Oecologia 155: 441-454, 2008. Go to original source...
  75. Tumajer J., Altman J., Štěpánek P. et al.: Increasing moisture limitation of Norway spruce in Central Europe revealed by forward modelling of tree growth in tree-ring network. - Agr. Forest Meteorol. 247: 56-64, 2017. Go to original source...
  76. Venäläinen A., Lehtonen I., Laapas M. et al.: Climate change induces multiple risks to boreal forests and forestry in Finland: A literature review. - Glob. Change Biol. 26: 4178-4196, 2020. Go to original source...
  77. Vicente-Serrano S.M., Beguería S., López-Moreno J.I.: A multiscalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index. - J. Climate 23: 1696-1718, 2010. Go to original source...
  78. Vico G., Manzoni S., Palmroth S. et al.: A perspective on optimal leaf stomatal conductance under CO2 and light co-limitations. -Agr. Forest Meteorol. 182-183: 191-199, 2013. Go to original source...
  79. Voelker S.L., Brooks J.R., Meinzer F.C. et al.: A dynamic leaf gas-exchange strategy is conserved in woody plants under changing ambient CO2: evidence from carbon isotope discrimination in paleo and CO2 enrichment studies. - Glob. Change Biol. 22: 889-902, 2016. Go to original source...
  80. Voelker S.L., Roden J.S., Dawson T.E.: Millennial-scale tree-ring isotope chronologies from coast redwoods provide insights on controls over California hydroclimate variability. - Oecologia 187: 897-909, 2018. Go to original source...
  81. Waterhouse J.S., Switsur V.R., Barker A.C. et al.: Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations. - Quaternary Sci. Rev. 23: 803-810, 2004. Go to original source...
  82. Wong S.-C., Cowan I.R., Farquhar G.D.: Leaf conductance in relation to rate of CO2 assimilation. I. Influence of nitrogen nutrition, phosphorus nutrition, photon flux density, and ambient partial pressure of CO2 during ontogeny. - Plant Physiol. 78: 821-825, 1985. Go to original source...
  83. Yamaguchi D.K.: A simple method for cross-dating increment cores from living trees. - Can. J. Forest Res. 21: 414-416, 1991. Go to original source...
  84. Yu G., Song X., Wang Q. et al.: Water-use efficiency of forest ecosystems in eastern China and its relations to climatic variables. - New Phytol. 177: 927-937, 2008. Go to original source...