The increase of atmospheric CO2 affects growth potential and intrinsic water-use efficiency of Norway spruce forests: insights from a multi-stable isotope analysis in tree rings of two Alpine chronosequences

Published Date
April 2017, Volume 31, Issue 2, pp 503–515

Author

• Francesco GiammarchiEmail author
• Paolo Cherubini 
• Hans Pretzsch 
• Giustino Tonon

1. 1.
2. 2.
3. 3.
4. 4.

Original Article

First Online: 

11 October 2016

DOI: 10.1007/s00468-016-1478-2

Cite this article as:

Giammarchi, F., Cherubini, P., Pretzsch, H. et al. Trees (2017) 31: 503. doi:10.1007/s00468-016-1478-2

Abstract

Key message

Relevant CO2increase affects iWUE and growth potential of Alpine Norway spruce forests due to triggering of photosynthetic capacity. Minor effect on iWUE of tree size/age ontogenetic factors.

Abstract

An increase in European forest productivity has been widely reported, but evidences on its causal relationship with climate change are still scarce, though they are crucial to understand the mitigation potential of forests and their future dynamics. In the present study, we first assessed the changes in forest productivity of two even-aged Norway spruce forests. Consequently, we investigated the role of several environmental drivers, such as atmospheric CO2 levels, temperature, and precipitation regimes on the intrinsic water-use efficiency (iWUE) temporal patterns of the above-mentioned forests. We applied a chronosequence approach, combining it with a multi-stable isotope analysis, including δ13C and δ18O, to infer tree responses to climate change over time in terms of iWUE changes. By this innovative methodology, we were able to separate environmental and age/size-related factors on iWUE changes. Results showed an increase in forest productivity in both sites, paralleled by a significant increase of iWUE, mainly triggered by a CO2-driven increase in photosynthetic capacity, rather than by a reduction of stomatal conductance. The paramount role of the increase in photosynthetic capacity was confirmed by a strong correlation between atmospheric CO2 concentration and iWUE temporal patterns. The effect of size/age of trees on iWUE temporal changes resulted to be less defining than that of climate change.

Keywords

Water-use efficiency CO2 increase Stable isotopes Forest productivity Tree size Chronosequence 

Communicated by A. Gessler.

References

1. Allen CD, Macalady AK, Chenchouni H et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684CrossRefGoogle Scholar
2. Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6(8):129CrossRefGoogle Scholar
3. Andreu-Hayles L, Planells O, Gutiérrez E et al (2011) 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 17:2095–2112CrossRefGoogle Scholar
4. Barbour MM, Farquhar GD (2000) Relative humidity- and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant Cell Environ 23:473–485CrossRefGoogle Scholar
5. Barbour MM, Walcroft AS, Farquhar GD (2002) Seasonal variation in delta C-13 and delta O-18 of cellulose from growth rings of Pinus radiata. Plant Cell Environ 25:1483–1499CrossRefGoogle Scholar
6. Barnard HR, Brooks JR, Bond BJ (2012) Applying the dual-isotope conceptual model to interpret physiological trends under uncontrolled conditions. Tree Physiol 32:1183–1198CrossRefPubMedGoogle Scholar
7. Battipaglia G, Saurer M, Cherubini P, Calfapietra C, McCarthy HR, Norby RJ, Francesca Cotrufo M (2013) Elevated CO2 increases tree-level intrinsic water use efficiency: insights from carbon and oxygen isotope analyses in tree rings across three forest FACE sites. New Phytol 197:544–554CrossRefPubMedGoogle Scholar
8. Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5:349–353CrossRefPubMedGoogle Scholar
9. Bontemps JD, Herve JC, Dhote JF (2009) Long-term changes in forest productivity: a consistent assessment in even-aged stands. For Sci 55:549–564Google Scholar
10. Bottinga Y, Craig H (1969) Oxygen isotope fractionation between CO2 and water, and the isotopic composition of marine atmospheric CO2. Earth Planet Sci Lett 5:285–295CrossRefGoogle Scholar
11. Cook ER (1985) A time series approach to tree-ring standardization. Dissertation, University of Arizona, Tucson
12. Craig H, Gordon L (1965) Deuterium and oxygen-18 variations in the ocean and the marine atmosphere. In: Tongiorgi T (ed) Proceedings of conference on stable isotopes on oceanographic studies and paleotemperatures. Lischi and Figli, Pisa, pp 9–130Google Scholar
13. Day ME, Greenwood MS, Diaz-Sala C (2002) Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiol 22:507–513CrossRefPubMedGoogle Scholar
14. Deleuze C, Houllier F (1995) Prediction of stem profile of Picea abies using a process-based tree growth model. Tree Physiol 15:113–120CrossRefPubMedGoogle Scholar
15. Dongmann G, Nürnberg HW, Förstel H, Wagener K (1974) On the enrichment of H2 18O in the leaves of transpiring plants. Radiat Environ Biophys 11:41–52CrossRefPubMedGoogle Scholar
16. Duquesnay A, Breda N, Stievenard M, Dupouey JL (1998) Changes of tree-ring delta13C and water-use efficiency of beech (Fagus sylvatica L.) in north-eastern France during the past century. Plant Cell Environ 21:565–572CrossRefGoogle Scholar
17. Farquhar G (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 40:503–537CrossRefGoogle Scholar
18. Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon-water relations. Academic Press, San Diego, pp 47–70CrossRefGoogle Scholar
19. Farquhar GD, Cernusak LA, Barnes B (2006) Heavy water fractionation during transpiration. Plant Physiol 143:11–18CrossRefGoogle Scholar
20. Francey RJ, Allison CE, Etheridge DM et al (1999) A 1000-year high precision record of delta13C in atmospheric CO2. Tellus B 51:170–193CrossRefGoogle Scholar
21. Frank DC, Poulter B, Saurer M et al (2015) Water use efficiency and transpiration across European forests during the Anthropocene. Nat Clim Change 5:579–583CrossRefGoogle Scholar
22. Gagen M, Finsinger W, Wagner-Cremer F et al (2010) Evidence of changing intrinsic water-use efficiency under rising atmospheric CO2 concentrations in Boreal Fennoscandia from subfossil leaves and tree ring δ13C ratios. Glob Change Biol 2:1064–1072Google Scholar
23. Gessler A, Löw M, Heerdt C et al (2009) Within-canopy and ozone fumigation effects on δ13C and δ18O in adult beech (Fagus sylvatica) trees: relation to meteorological and gas exchange parameters. Tree Physiol 29:1349–1365CrossRefPubMedGoogle Scholar
24. Gessler A, Ferrio JP, Hommel R, Treydte K, Werner RA, Monson RK (2014) Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the leaves to the wood. Tree Physiol 34:796–818CrossRefPubMedGoogle Scholar
25. Gómez-Guerrero A, Silva LCR, Barrera-Reyes M, Kishchuk B, Velázquez-Martínez A, Martínez-Trinidad T, Plascencia-Escalante FO, Horwath WR (2013) Growth decline and divergent tree ring isotopic composition (δ13C and δ18O) contradict predictions of CO2 stimulation in high altitudinal forests. Glob Change Biol 19:1748–1758CrossRefGoogle Scholar
26. Gottfried M, Pauli H, Futschik A et al (2012) Continent-wide response of mountain vegetation to climate change. Nat Clim Change 2:111–115CrossRefGoogle Scholar
27. Gower ST, McMurtrie RE, Murty D (1996) Aboveground net primary production decline with stand age: potential causes. Trends Ecol Evol 11:378–382CrossRefPubMedGoogle Scholar
28. Grams TEE, Kozovits AR, Häberle K-H, Matyssek R, Dawson TE (2007) Combining delta 13 C and delta 18 O analyses to unravel competition, CO2 and O3 effects on the physiological performance of different-aged trees. Plant Cell Environ 30:1023–1034CrossRefPubMedGoogle Scholar
29. Guerrieri R, Siegwolf R, Saurer M, Ripullone F, Mencuccini M, Borghetti M (2010) Anthropogenic NOx emissions alter the intrinsic water-use efficiency (WUEi) for Quercus cerris stands under Mediterranean climate conditions. Environ Pollut 158:2841–2847CrossRefPubMedGoogle Scholar
30. Guerrieri R, Vanguelova E, Michalski G, Heaton T, Mencuccini M (2015) Isotopic evidence for the occurrence of biological nitrification and nitrogen deposition processing in forest canopies. Glob Change Biol 21(12):4613–4626CrossRefGoogle Scholar
31. Hyvönen R, Agren GI, Linder S et al (2007) The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytol 173:463–480CrossRefPubMedGoogle Scholar
32. Jandl R, Neumann M, Eckmüllner O (2007) Productivity increase in Northern Austria Norway spruce forests due to changes in nitrogen cycling and climate. J Plant Nutr Soil Sci 170:157–165CrossRefGoogle Scholar
33. Kahle HP, Karjalainen T, Schuck A, Ågren GI, Kellomäki S, Mellert KH, Pritzel J, Rehfuess KE, Spiecker H (eds) (2008) Causes and consequences of forest growth trends in Europe—results of the recognition project. Brill, Leiden, p 272Google Scholar
34. Karlsson K (2000) Height growth patterns of Scots pine and Norway spruce in the coastal areas of western Finland. For Ecol Manage 135:205–216CrossRefGoogle Scholar
35. Keenan TF, Hollinger DY, Bohrer G, Dragoni G, Munger JW, Schmid HP, Richardson AD (2013) Increase in forest water-use efficiency as atmospheric carbon dioxide concentration rise. Nature 499:324–327CrossRefPubMedGoogle Scholar
36. Körner C (2015) Paradigm shift in plant growth control. Curr Opin Plant Biol 25:107–114CrossRefPubMedGoogle Scholar
37. Leonardi S, Gentilesca T, Guerrieri R et al (2012) Assessing the effects of nitrogen deposition and climate on carbon isotope discrimination and intrinsic water-use efficiency of angiosperm and conifer trees under rising CO2 conditions. Glob Change Biol 18:2925–2944CrossRefGoogle Scholar
38. Lévesque M, Siegwolf R, Saurer M, Eilmann B, Rigling A (2014) Increased water-use efficiency does not lead to enhanced tree growth under xeric and mesic conditions. New Phytol 203:94–109CrossRefPubMedGoogle Scholar
39. Linares JC, Camarero JJ (2011) Growth patterns and sensitivity to climate predict silver fir decline in the Spanish Pyrenees. Eur J For Res 131:1001–1012CrossRefGoogle Scholar
40. Loader NJ, Robertson I, Barker AC, Switsur VR, Waterhouse JS (1997) An improved technique for the batch processing of small wholewood samples to a-cellulose. Geology 136:313–317Google Scholar
41. Lopatin E (2007) Long-term dynamics in growth of Scots pine and Siberian spruce in Komi Republic (European part of Russia). Diss For 53:35Google Scholar
42. Marshall JD, Monserud RA (1996) Homeostatic gas-exchange parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105:13–21CrossRefPubMedGoogle Scholar
43. Martínez-Vilalta J, Vanderklein D, Mencuccini M (2007) Tree height and age-related decline in growth in Scots pine (Pinus sylvestris L.). Oecologia 150:529–544CrossRefPubMedGoogle Scholar
44. McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801CrossRefGoogle Scholar
45. Mencuccini M, Martínez-Vilalta J, Vanderklein D et al (2005) Size-mediated ageing reduces vigour in trees. Ecol Lett 8:1183–1190CrossRefPubMedGoogle Scholar
46. Mitchell TD, Jones PD (2005) An improved method of constructing a database of monthly climate observations and associated high-resolution grids. Int J Climatol 25:693–712CrossRefGoogle Scholar
47. Nehrbass-Ahles C, Babst F, Klesse S, Nötzli M, Bouriaud O, Neukom R, Dobbertin M, Frank D (2014) The influence of sampling design on tree-ring based quantification of forest growth. Glob Change Biol 20:2867–2885CrossRefGoogle Scholar
48. Niinemets Ü (1997) Distribution patterns of foliar carbon and nitrogen as affected by tree dimensions and relative light conditions in the canopy of Picea abies. Trees 11:144–154Google Scholar
49. Niinemets Ü (2002) Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiol 22:515–535CrossRefPubMedGoogle Scholar
50. Nock CA, Baker PJ, Wanek W, Leis A, Grabner M, Bunyavejchewin S, Hietz P (2010) Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand. Glob Change Biol 17:1049–1063CrossRefGoogle Scholar
51. 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 162:253–280CrossRefGoogle Scholar
52. Peñuelas J, Canadell JG, Ogaya R (2011) Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Glob Ecol Biogeogr 20:597–608CrossRefGoogle Scholar
53. Pretzsch H et al (2014a) Changes of forest stand dynamics in Europe. Facts from long-term observational plots and their relevance for forest ecology and management. For Ecol Manage 316:65–77CrossRefGoogle Scholar
54. Pretzsch H, Biber P, Schütze G, Uhl E, Rötzer T (2014b) Forest stand growth dynamics in Central Europe have accelerated since 1870. Nature Commun 5:4967CrossRefGoogle Scholar
55. Richards FJ (1959) A flexible growth function for empirical use. J Exp Bot 10:290–301CrossRefGoogle Scholar
56. Roden J, Siegwolf R (2012) Is the dual-isotope conceptual model fully operational? Tree Physiol 32:1179–1182CrossRefPubMedGoogle Scholar
57. Roden JS, Lin G, Ehleringer JR (2000) A mechanistic model for interpretation of hydrogen and oxygen isotope ratios in tree-ring cellulose. Geochim Cosmochim Acta 64:21–35CrossRefGoogle Scholar
58. Rossi S, Tremblay M-J et al (2009) Growth and productivity of black spruce in even- and uneven-aged stands at the limit of the closed boreal forest. For Ecol Manage 258:2153–2161CrossRefGoogle Scholar
59. Rubino D, McCarthy BC (2004) Comparative analysis of dendroecological methods used to assess disturbance events. Dendrochronologia 21:97–115CrossRefGoogle Scholar
60. Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. Bioscience 47:235–242CrossRefGoogle Scholar
61. Saurer M, Siegwolf RTW, Schweingruber FH (2004) Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Glob Change Biol 10:2109–2120CrossRefGoogle Scholar
62. Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125:350–357CrossRefGoogle Scholar
63. Skovsgaard JP, Vanclay JK (2008) Forest site productivity: a review of the evolution of dendrometric concepts for even-aged stands. Forestry 81:13–31CrossRefGoogle Scholar
64. Spiecker H, Mielikäinen K, Köhl M, Skovsgaard JP (1996) Growth trends in European forests. Studies from 12 countries. Springer, BerlinCrossRefGoogle Scholar
65. Sternberg L, Deniro MJD (1983) Biogeochemical implications of the isotopic equilibrium fractionation factor between the oxygen-atoms of acetone and water. Geochim Cosmochim Acta 47:2271–2274CrossRefGoogle Scholar
66. Strömgren M, Linder S (2002) Effects of nutrition and soil warming on stemwood production in a boreal Norway spruce stand. Glob Change Biol 12:1195–1204Google Scholar
67. Voelker SL, Brooks JR, Meinzer FC et al (2015) 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 22:889–902CrossRefGoogle Scholar
68. Walker LR, Wardle DA, Bardgett RD, Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98:725–736CrossRefGoogle Scholar
69. Waterhouse JS, Switsur VR, Barker AC et al (2004) Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations. Quat Sci Rev 23:803–810CrossRefGoogle Scholar

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