Abstract
We combined dendrochronological methods and interannual δ13C measurements to investigate radial growth and physiological responses of Schrenk spruce (Picea schrenkiana) in response to rising atmospheric CO2 concentration (C a) and changing climate in high-elevation forests in China’s western Tianshan Mountains. The mean maximum temperature in May to August, reconstructed from δ13C, revealed an overall warming trend, with persistent warm periods from 1910 to 1920, and from 1970 to 1980. Intrinsic water use efficiency (iWUE) increased by 28 % over the last 160 years; temporal trends in iWUE were calculated under three theoretical scenarios as a baseline for interpreting the observed gas-exchange at increasing C a. Basal area increment (BAI) increased by 51.4 % since 1850 with two apparent increases and decreases. Trees exhibited sharp declines in BAI along with enhanced iWUE during the warmer periods; this was possibly due to a reduced stomatal conductance which prevented excessive water loss from trees. Conversely, BAI increased at reduced iWUE (−3.6 %, −7.4 %) during two cold-wet periods (e.g., 1880 to 1992, and 1945 to 1960), suggesting that a diminished water stress caused the observed growth pattern. However, BAI increased significantly (49.4 %) from 1965 to 1983 with constant intercellular atmospheric CO2 concentrations (C i) response scenario under acute water limitations, indicating the CO2 stimulation of tree growth. These results showed that even at high elevations, increased iWUE may not lead to long-term enhancement of tree growth, and other factors may counteract CO2-fertilization effects, especially those related to a warming-induced drought. The results of this study suggest that the current models may overestimate the sink capacity of temperate forests, and indicate that multi-proxy records are needed to disentangle the role of a limiting factor in modulating the response of the Schrenk spruce forest to current climate change scenarios.
Similar content being viewed by others
References
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg E (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol Manag 259:660–684. doi:10.1016/j.foreco.2009.09.001
Andreu-Hayles L, Planells O, Gutierrez E, Muntan E, Helle G, Anchukaitis KJ, Schleser GH (2011) Long tree-ring chronologies reveal 20th century increases in water-use efficiency but no enhancement of tree growth at five Iberian pine forests. Global Change Biol 17:2095–2112. doi:10.1111/j.1365-2486.2010.02373.x
Betson NR, Johannisson C, Löfvenius MO, Grip H, Granström A, Högberg P (2007) Variation in the δ13C of foliage of Pinus sylvestris L. in relation to climate and additions of nitrogen: analysis of a 32 year chronology. Global Change Biol 13:2317–2328. doi:10.1111/j.1365-2486.2007.01431.x
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449. doi:10.1126/science.1155121
Chen J, Wang L, Zhu H, Wu P (2009) Reconstructing mean maximum temperature of growing season from the maximum density of the Schrenk Spruce in Yili, Xinjiang, China. Chin Sci Bull 54:2300–2308. doi:10.1007/s11434-009-0051-4
Chen F, Yuan Y, Wei W, Wang L, Yu S, Zhang R, Fan Z, Shang H, Zhang T, Li Y (2012) Tree ring density-based summer temperature reconstruction for Zajsan Lake area, East Kazakhstan. Int J Climatol 32:1089–1097. doi:10.1002/joc.2327
Cole CT, Anderson JE, Lindroth RL, Waller DM (2010) Rising concentrations of atmospheric CO2 have increased growth in natural stands of quaking aspen (Populus tremuloides). Global Change Biol 16:2186–2197. doi:10.1111/j.1365-2486.2009.02103.x
Cook ER (1985) A time series analysis approach to tree ring standardization (Dendrochronology, Forestry, Dendroclimatology, Autoregressive process). The University of Arizona, Arizona
Coplen TB (1995) Discontinuance of SMOW and PDB. Nature 375:285. doi:10.1038/375285a0
Farquhar GD, O’Leary M, Berry J (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Funct Plant Biol 9:121–137. doi:10.1071/PP9820121
Feng X, Epstein S (1995) Carbon isotopes of trees from arid environments and implications for reconstructing atmospheric CO2 concentration. Geochim Cosmochim Acta 59:2599–2608. doi:10.1016/0016-7037(95)00152-2
Fisher JB, Badgley G, Blyth E (2012) Global nutrient limitation in terrestrial vegetation. Global Biogeochem Cycles 26(GB3007):1–9. doi:10.1029/2011GB004252
Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:28–31. doi:10.1038/297028a0
Friedlingstein P, Cox P, Betts R et al (2006) Climate-carbon cycle feedback analysis: results from the C4MIP model intercomparison. J Climate 19:3337–3353. doi:10.1175/JCLI3800.1
Gagen M, McCarroll D, Loader NJ, Robertson I, Jalkanen R, Anchukaitis KJ (2007) Exorcising the segment length curse’: summer temperature reconstruction since AD 1640 using non-detrended stable carbon isotope ratios from pine trees in northern Finland. Holocene 17:435–446. doi:10.1177/0959683607077012
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. Global Change Biol 19:1748–1758. doi:10.1111/gcb.12170
Gradowski T, Thomas S (2006) Phosphorus limitation of sugar maple growth in central Ontario. Forest Ecol Manag 226:104–109. doi:10.1016/j.foreco.2005.12.062
Granda E, Rossatto D, Camarero JJ, Voltas J, Valladares F (2014) Growth and carbon isotopes of Mediterranean trees reveal contrasting responses to increased carbon dioxide and drought. Oecologia 174:307–317. doi:10.1007/s00442-013-2742-4
Green JW (1963) Wood cellulose. In: Methods in carbohydrate chemistry, vol. 3: cellulose. Academic Press, New York, pp 9–20
Holmes RL (1983) Computer-assisted quality control in tree-ring dating and measurement. Tree-ring Bull 43:69–78
Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15:56–61. doi:10.1016/s0169-5347(99)01764-4
Körner C (2000) Biosphere responses to CO2 enrichment. Ecol Appl 10:1590–1619. doi:10.2307/2641226
Kürschner WM (1996) Leaf stomata as biosensors of palaeoatmospheric CO2 levels = Bladstomata als biosensoren van palaeoatmosferische CO2 consentraties = Blatt stomata als Biosensoren palaeoatmosphaerischer CO2 Gehalte, vol 5. LPP Foundation, Utrecht
Laumer W, Andreu L, Helle G, Schleser G, Wieloch T, Wissel H (2009) A novel approach for the homogenization of cellulose to use micro-amounts for stable isotope analyses. Rapid Commun Mass Spectrom 23:1934–1940. doi:10.1002/rcm.4105
Leavitt SW (2008) Tree-ring isotopic pooling without regard to mass: no difference from averaging δ13C values of each tree. Chem Geol 252:52–55. doi:10.1016/j.chemgeo.2008.01.014
Leuzinger S, Körner C (2007) Water savings in mature deciduous forest trees under elevated CO2. Global Change Biol 13:2498–2508. doi:10.1111/j.1365-2486.2007.01467.x
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 203:94–109. doi:10.1111/nph.12772
Liñán IC, Gutiérrez E, Helle G, Heinrich I, Andreu-Hayles L, Planells O, Leuenberger M, Bürger C, Schleser G (2011) Pooled versus separate measurements of tree-ring stable isotopes. Sci Total Environ 409:2244–2251. doi:10.1016/j.scitotenv.2011.02.010
Linares JC, Camarero JJ (2012) From pattern to process: linking intrinsic water-use efficiency to drought-induced forest decline. Global Change Biol 18:1000–1015. doi:10.1111/j.1365-2486.2011.02566.x
Linares JC, Delgado-Huertas A, Camarero JJ, Merino J, Carreira JA (2009) Competition and drought limit the response of water-use efficiency to rising atmospheric carbon dioxide in the Mediterranean fir Abies pinsapo. Oecologia 161:611–624. doi:10.1007/s00442-009-1409-7
Liu Y, Wang R, Leavitt SW, Song H, Linderholm HW, Li Q, An Z (2012) Individual and pooled tree-ring stable-carbon isotope series in Chinese pine from the Nan Wutai region, China: common signal and climate relationships. Chem Geol 330–331:17–26. doi:10.1016/j.chemgeo.2012.08.008
Liu X, Wang W, Xu G, Zeng X, Wu G, Zhang X, Qin D (2014) Tree growth and intrinsic water-use efficiency of inland riparian forests in northwestern China: evaluation via δ13C and δ18O analysis of tree rings. Tree Physiol 34:966–980. doi:10.1093/treephys/tpu067
Loader N, Robertson I, Barker A, Switsur V, Waterhouse J (1997) An improved technique for the batch processing of small wholewood samples to α-cellulose. Chem Geol 136:313–317. doi:10.1016/S0009-2541(96)00133-7
Loader NJ, McCarroll D, Gagen M, Robertson I, Jalkanen R (2007) Extracting climatic information from stable isotopes in tree rings. Terr Ecol 1:27–48. doi:10.1016/S1936-7961(07)01003-2
Loader N, Santillo P, Woodman-Ralph J, Rolfe J, Hall M, Gagen M, Robertson I, Wilson R, Froyd C, McCarroll D (2008) Multiple stable isotopes from oak trees in southwestern Scotland and the potential for stable isotope dendroclimatology in maritime climatic regions. Chem Geol 252:62–71. doi:10.1016/j.chemgeo.2008.01.006
Marshall J, Brooks J, Lajtha K (2007) Sources of variation in the stable isotopic composition of plants. In: Mitchener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Scientific, Oxford, pp 22–60
McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801. doi:10.1016/j.quascirev.2003.06.017
McCarroll D, Gagen MH, Loader NJ, Robertson I, Anchukaitis KJ, Los S, Young GH, Jalkanen R, Kirchhefer A, Waterhouse JS (2009) Correction of tree ring stable carbon isotope chronologies for changes in the carbon dioxide content of the atmosphere. Geochim Cosmochim Acta 73:1539–1547. doi:10.1016/j.gca.2008.11.041
McMahon SM, Parker GG, Miller DR (2010) Evidence for a recent increase in forest growth. Proc Natl Acad Sci USA 107:3611–3615. doi:10.1073/pnas.0912376107
Morgan J, Pataki D, Körner C, Clark H, Del Grosso S, Grünzweig J, Knapp A, Mosier A, Newton P, Niklaus P (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140:11–25. doi:10.1007/s00442-004-1550-2
Morison J (1993) Response of plants to CO2 under water limited conditions. Vegetatio 104–105:193–209. doi:10.1007/BF00048153
Nock CA, Baker PJ, Wanek W, Leis A, Grabner M, Bunyavejchewin S, Hietz P (2011) Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand. Global Change Biol 17:1049–1063. doi:10.1111/j.1365-2486.2010.02222.x
Overdieck D, Forstreuter M (1994) Evapotranspiration of beech stands and transpiration of beech leaves subject to atmospheric CO2 enrichment. Tree Physiol 14:997–1003. doi:10.1093/treephys/14.7-8-9.997
Peñuelas J, Hunt JM, Ogaya R, Jump AS (2008) Twentieth century changes of tree-ring δ13C at the southern range-edge of Fagus sylvatica: increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes. Global Change Biol 14:1076–1088. doi:10.1111/j.1365-2486.2008.01563.x
Peñuelas J, Canadell JG, Ogaya R (2011) Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Global Ecol Biogeogr 20:597–608. doi:10.1111/j.1466-8238.2010.00608.x
Phipps RL, Whiton JC (1988) Decline in long-term growth trends of white oak. Can J Forest Res 18:24–32. doi:10.1139/x88-005
Saurer M, Siegwolf RT, Schweingruber FH (2004) Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Global Change Biol 10:2109–2120. doi:10.1111/j.1365-2486.2004.00869.x
Silva LC, Anand M (2013) Probing for the influence of atmospheric CO2 and climate change on forest ecosystems across biomes. Global Ecol Biogeogr 22:83–92. doi:10.1111/j.1466-8238.2012.00783.x
Silva LC, Horwath WR (2013) Explaining global increases in water use efficiency: why have we overestimated responses to rising atmospheric CO2 in natural forest ecosystems? PLoS ONE 8:e53089. doi:10.1371/journal.pone.0053089
Sitch S, Huntingford C, Gedney N, Levy PE, Lomas M, Piao SL, Betts R, Ciais P, Cox P, Friedlingstein P, Jones CD, Prentice IC, Woodward FI (2008) Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using five dynamic global vegetation models (DGVMs). Global Change Biol 14:2015–2039. doi:10.1111/j.1365-2486.2008.01626.x
Szymczak S, Joachimski MM, Bräuning A, Hetzer T, Kuhlemann J (2012) Are pooled tree ring δ13C and δ18O series reliable climate archives? A case study of Pinus nigra ssp. laricio (Corsica/France). Chem Geol 308–309:40–49. doi:10.1016/j.chemgeo.2012.03.013
Treydte K, Schleser GH, Schweingruber FH, Winiger M (2001) The climatic significance of δ13C in subalpine spruces (Lötschental, Swiss Alps): a case study with respect to altitude, exposure and soil moisture. Tellus B 53:593–611. doi:10.1034/j.1600-0889.2001.530505.x
Treydte KS, Frank DC, Saurer M, Helle G, Schleser GH, Esper J (2009) Impact of climate and CO2 on a millennium-long tree-ring carbon isotope record. Geochim Cosmochim Ac 73:4635–4647. doi:10.1016/j.gca.2009.05.057
Van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524. doi:10.1126/science.1165000
Wang W, Liu X, Shao X, Leavitt S, Xu G, An W, Qin D (2011) A 200 year temperature record from tree ring δ13C at the Qaidam Basin of the Tibetan Plateau after identifying the optimum method to correct for changing atmospheric CO2 and δ13C. J Geophys Res Biogeosci (2005–2012) 116(G4). doi:10.1029/2011JG001665
Wang W, Liu X, An W, Xu G, Zeng X (2012) Increased intrinsic water-use efficiency during a period with persistent decreased tree radial growth in northwestern China: causes and implications. Forest Ecol Manag 275:14–22. doi:10.1016/j.foreco.2012.02.027
Waterhouse JS, Switsur V, Barker A, Carter A, Hemming D, Loader NJ, Robertson I (2004) Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations. Quat Sci Rev 23:803–810. doi:10.1016/j.quascirev.2003.06.011
Williams AP, Allen CD, Millar CI, Swetnam TW, Michaelsen J, Still CJ, Leavitt SW (2010) Forest responses to increasing aridity and warmth in the southwestern United States. Proc Natl Acad Sci USA 107:21289–21294. doi:10.1073/pnas.0914211107
Woodley EJ, Loader NJ, McCarroll D, Young GHF, Robertson I, Heaton THE, Gagen MH (2012) Estimating uncertainty in pooled stable isotope time-series from tree-rings. Chem Geol 294–295:243–248. doi:10.1016/j.chemgeo.2011.12.008
Wu X, Liu H, Wang Y, Deng M (2013) Prolonged limitation of tree growth due to warmer spring in semi-arid mountain forests of Tianshan, northwest China. Environ Res Lett 8:024016. doi:10.1088/1748-9326/8/2/024016
Wu CY, Hember RA, Chen JM, Kurz WA, Price DT, Boisvenue C, Gonsamo A, Ju W (2014) Accelerating forest growth enhancement due to climate and atmospheric changes in British Colombia, Canada over 1956–2001. Sci Rep 4:4461. doi:10.1038/srep-05561
Xu G (2014) Climatic significance of stable oxygen (δ18O) in tree-ring in north part of Xinjiang Uygur Autonomous Region. Dissertation, Chinese Academy of Sciences, State Key Lab of Cryospheric Sciences, Cold and Arid Regions Environmental and Engineering Research Institute, pp 99–100 (in Chinese)
Xu G, Liu X, Qin D, Chen T, An W, Wang W, Wu G, Zeng X, Ren J (2013) Climate warming and increasing atmospheric CO2 have contributed to increased intrinsic water-use efficiency on the northeastern Tibetan Plateau since 1850. Trees 27:465–475. doi:10.1007/s00468-013-0855-3
Xu G, Liu X, Qin D, Chen T, Sun W, An W, Wang W, Wu G, Zeng X, Ren J (2014) Drought history inferred from tree ring δ13C and δ18O in the central Tianshan Mountains of China and linkage with the North Atlantic Oscillation. Theor Appl Climatol 116:385–401. doi:10.1007/s00704-013-0958-1
Yin ZY, Shao X, Qin N, Liang E (2008) Reconstruction of a 1436-year soil moisture and vegetation water use history based on tree-ring widths from Qilian junipers in northeastern Qaidam Basin, northwestern China. Int J Climatol 28:37–53. doi:10.1002/joc.1515
Yu S, Yuan Y, Wei W, Chen F, Zhang T, Shang H, Zhang R, Qing L (2013) A 352-year record of summer temperature reconstruction in the western Tianshan Mountains, China, as deduced from tree-ring density. Quaternary Res 80:158–166. doi:10.1016/j.yqres.2013.05.005
Zhu KZ (1985) Chinese physical geography pandect. Science Press, Beijing, pp 385–389 (in Chinese)
Acknowledgments
This research was supported by the Major State Basic Research Development Program of China (973 Program) (2013CBA01808), the Self-Determination Project of the State Key Laboratory of Cryospheric Sciences (SKLCS-ZZ-2015-01-12), and by the National Natural Science Foundation of China (41171167, 41121001).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by K. Apostol.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wu, G., Liu, X., Chen, T. et al. Long-term variation of tree growth and intrinsic water-use efficiency in Schrenk spruce with increasing CO2 concentration and climate warming in the western Tianshan Mountains, China. Acta Physiol Plant 37, 150 (2015). https://doi.org/10.1007/s11738-015-1903-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-015-1903-y