Radial growth in Qinghai spruce is most sensitive to severe drought in the Qilian Mountains of Northwest China

Abstract

Global warming and frequent extreme drought events lead to tree death and extensive forest decline, but the underlying mechanism is not clear. In drought years, cambial development is more sensitive to climate change, but in different phenological stages, the response relationship is nonlinear. Therefore, the dynamic relationship between tree radial growth and climatic/environmental factors needs to be studied. We thus continuously monitored radial growth of Qinghai spruce (Picea crassifolia Kom.) and environmental factors from January 2021 to November 2022 using point dendrometers and portable meteorological weather stations in the central area of the Qilian Mountains. The relationship and stability between the radial growth of Qinghai spruce and environmental factors were compared for different levels of drought in 2021 and 2022. The year 2022 had higher temperatures and less precipitation and was drier than 2021. Compared with 2021, the growing period in 2022 for Qinghai spruce was 10 days shorter, maximum growth rate (Grmax) was 4.5 μm·d⁻¹ slower, and the initiation of growth was 6 days later. Growth of Qinghai spruce was always restricted by drought, and the stem radial increment (SRI) was more sensitive to precipitation and air relative humidity. Seasonal changes in cumulative radial growth were divided into four phenological stages according to the time of growth onset, cessation, and maximum growth rate (Grmax) of Qinghai spruce. Stability responses of SRI to climate change were stronger in Stage 3 and Stage 4 of 2021 and stronger in Stage 1 (initiation growth stage) and Stage 3 of 2022. The results provide important information on the growth of the trees in response to drought and for specific managing forests as the climate warms.

Keywords

Picea crassifolia / Radial growth dynamics / Severe drought / Response stability / Point dendrometer

References

[1]	Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259(4):660–684. https://doi.org/10.1016/j.foreco.2009.09.001
[2]	Anderegg WRL, Anderegg LDL, Kerr KL, Trugman AT (2019) Widespread drought-induced tree mortality at dry range edges indicates that climate stress exceeds species’ compensating mechanisms. Glob Chang Biol 25(11):3793–3802. https://doi.org/10.1111/gcb.14771
[3]	Andreu L, Gutierrez E, Macias M, Ribas M, Bosch O, Camarero JJ (2007) Climate increases regional tree-growth variability in Iberian pine forests. Glob Chang Biol 13(4):804–815. https://doi.org/10.1111/j.1365-2486.2007.01322.x
[4]	Bonaldo D, Bellafiore D, Ferrarin C, Ferretti R, Ricchi A, Sangelantoni L, Vitelletti ML (2023) The summer 2022 drought: a taste of future climate for the Po valley (Italy)? Reg Environ Change 23:1. https://doi.org/10.1007/s10113-022-02004-z
[5]	Borken W, Davidson EA, Savage K, Sundquist ET, Steudler P (2006) Effect of summer throughfall exclusion, summer drought, and winter snow cover on methane fluxes in a temperate forest soil. Soil Biol Biochem 38(6):1388–1395. https://doi.org/10.1016/j.soilbio.2005.10.011
[6]	Camarero JJ, Guerrero-Campo G (1998) Tree-ring growth and structure of Pinus uncinata and Pinus sylvestris in the Central Spanish Pyrenees. Arct Antarct Alp Res 30(1):1–10. https://doi.org/10.2307/1551739
[7]	Chang XX, Zhao WZ, He ZB (2014) Radial pattern of sap flow and response to microclimate and soil moisture in Qinghai spruce (Picea crassifolia) in the upper Heihe River Basin of arid northwestern China. Agric for Meteorol 187:14–21. https://doi.org/10.1016/j.agrformet.2013.11.004
[8]	Claeys H, Inzé D (2013) The agony of choice: how plants balance growth and survival under water-limiting conditions. J Plant Physiol Pathol 162(4):1768–1779. https://doi.org/10.1104/pp.113.220921
[9]	Dai AG (2013) Increasing drought under global warming in observations and models. Nat Clim Chang 3(2):52–58. https://doi.org/10.1038/nclimate1633
[10]	Deslauriers A, Morin H (2005) Intra-annual tracheid production in balsam fir stems and the effect of meteorological variables. Trees 19(4):402–408. https://doi.org/10.1007/s00468-004-0398-8
[11]	Deslauriers A, Morin H, Urbinati C, Carrer M (2003) Daily weather response of balsam fir (Abies balsamea L. Mill.) stem radius increment from dendrometer analysis in the boreal forests of Qubec (Canada). Trees-Struct Funct 17(6):477–484. https://doi.org/10.1007/s00468-003-0260-4
[12]	Deslauriers A, Rossi S, Anfodillo T (2007) Dendrometer and intra-annual tree growth: What kind of information can be inferred? Dendrochronologia 25(2):113–124. https://doi.org/10.1016/j.dendro.2007.05.003
[13]	De Schepper V, Steppe K (2010) Development and verification of a water and sugar transport model using measured stem diameter variations. J Exp Bot 61(8):2083–2099. https://doi.org/10.1093/jxb/erq018
[14]	Duchesne L, Houle D, D’Orangeville L (2012) Influence of climate on seasonal patterns of stem increment of balsam fir in a boreal forest of Québec, Canada. Agric for Meteorol 162–163:108–114. https://doi.org/10.1016/j.agrformet.2012.04.016
[15]	Gao JN, Yang B, He MH, Shishov V (2019) Intra-annual stem radial increment patterns of Chinese pine, Helan Mountains. Northern Central China Trees 33(3):751–763. https://doi.org/10.1007/s00468-019-01813-w
[16]	Gou XH, Deng Y, Gao LL, Chen FH, Cook E, Yang MX, Zhang F (2014) Millennium tree-ring reconstruction of drought variability in the eastern Qilian Mountains, northwest China. Clim Dyn 45(7–8):1761–1770. https://doi.org/10.1007/s00382-014-2431-y
[17]	Gou XX, Zhang TW, Yu SL, Liu KX, Zhang RB, Shang HM, Qin L, Fan YT, Jiang SX, Zhang HL, Guo D (2023) Climate response of Picea schrenkiana based on tree-ring width and maximum density. Dendrochronologia. https://doi.org/10.1016/j.dendro.2023.126067
[18]	Hartmann H (2015) Carbon starvation during drought-induced tree mortality—Are we chasing a myth? J Plant Hydraul 2:e005. https://doi.org/10.20870/jph.2015.e005
[19]	IPCC (2018) Summary for Policymakers. In: Global Warming of 1.5 °C. An IPCC Special Report on the impacts of global warming of 1.5 °C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty [Masson-Delmotte, V., P. Zhai, H.-O. P?rtner, D. Roberts, J. Skea, P.R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J.B.R. Matthews, Y. Chen, X. Zhou, M.I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, T. Waterfield (eds.)]. World Meteorological Organization, Geneva, Switzerland, 32 pp
[20]	Jacoby GC, D’Arrigo RD (1995) Tree ring width and density evidence of climatic and potential forest change in Alaska. Global Biogeochem Cycles 9(2):227–234. https://doi.org/10.1029/95GB00321
[21]	Jiang Y, Wang BQ, Dong MY, Huang YM, Wang MC, Wang B (2015) Response of daily stem radial growth of Platycladus orientalis to environmental factors in a semi-arid area of North China. Trees 29(1):87–96. https://doi.org/10.1007/s00468-014-1089-8
[22]	Jiao L, Jiang Y, Wang MC, Kang XY, Zhang WT, Zhang LN, Zhao SD (2016) Responses to climate change in radial growth of Picea schrenkiana along elevations of the eastern Tianshan Mountains, northwest China. Dendrochronologia 40:117–127. https://doi.org/10.1016/j.dendro.2016.09.002
[23]	King GM, Gugerli F, Fonti P, Frank DC (2013) Tree growth response along an elevational gradient: Climate or genetics? Oecologia 173(4):1587–1600. https://doi.org/10.1007/s00442-013-2696-6
[24]	K?cher P, Horna V, Leuschner C (2012) Environmental control of daily stem growth patterns in five temperate broad-leaved tree species. Tree Physiol 32(8):1021–1032. https://doi.org/10.1093/treephys/tps049
[25]	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(1):94–109. https://doi.org/10.1111/nph.12772
[26]	Liang E, Dawadi B, Pederson N, Eckstein D (2016) Is the growth of birch at the upper timberline in the Himalayas limited by moisture or by temperature? Ecology 95(9):2453–2465. https://doi.org/10.1890/13-1904.1
[27]	Liu LS, Shao XM, Liang EY (2006) Climate signals from tree ring chronologies of the upper and lower treelines in the Dulan region of the Northeastern Qinghai-Tibetan Plateau. J Integr Plant Biol 48(3):278–285. https://doi.org/10.1111/j.1744-7909.2006.00158.x
[28]	Liu XH, AN WL, Liang EY, Wang WZ, Shao XM, Huang L, Qin DH (2010) Spatio-temporal variability and climatic significance of tree ring's δ~(13)C of Picea crassifolia on the Qilian Mountains. J Glaciol Geocryol. Corpus ID: 131665239
[29]	Liu ZB, Wang YH, Tian A, Yu PT, Xiong W, Xu LH, Wang YR (2017) Intra-annual variation of stem radius of Larix principis-rupprechtii and its response to environmental factors in Liupan Mountains of Northwest China. Forests. https://doi.org/10.3390/f8100382
[30]	Lv AF, Fan L, Zhang WX (2022) Impact of ENSO events on droughts in China. Atmosphere 13(11):1764. https://doi.org/10.3390/atmos13111764
[31]	Ma J, Guo JB, Wang YH, Liu ZB, Gao D, Hong L, Zhang ZY (2021) Variations in stem radii of Larix principis-rupprechtiito environmental factors at two slope locations in the Liupan Mountains, northwest China. J for Res 32:513–527. https://doi.org/10.1007/s11676-020-01114-w
[32]	M?kinen H, N?jd P, Kahle HP, Neumann U, Tveite B, Mielik?inen K, R?hle H, Spiecker H (2002) Radial growth of Norway spruce (Picea abies (L.) Karst) across latitudinal and altitudinal gradients in central and northern Europe. For Ecol Manag 171(3):243–259. https://doi.org/10.1016/S0378-1127(01)00786-1
[33]	M?kinen H, N?jd P, Saranp?? P (2003) Seasonal changes in stem radius and production of new tracheids in Norway spruce. Tree Physiol 23(14):959–968. https://doi.org/10.1093/treephys/23.14.959
[34]	Misson L, Rocheteau A, Rambal S, Ourcival JM, Limousin JM, Rodriguez R (2009) Functional changes in the control of carbon fluxes after 3 years of increased drought in a Mediterranean evergreen forest? Glob Chang Biol 16(9):2461–2475. https://doi.org/10.1111/j.1365-2486.2009.02121.x
[35]	Piao SL, Ciais P, Huang Y, Shen ZH, Peng SS, Li JS, Zhou LP, Liu HY, Ma YC, Ding YH, Friedlingstein P, Liu CZ, Tan K, Yu YQ, Zhang TY, Fang JY (2010) The impacts of climate change on water resources and agriculture in China. Nature 467:43–51. https://doi.org/10.1038/nature09364
[36]	Qian NP, Gao HX, Xu ZZ, Song CJ, Dong CC, Zeng W, Sun Z, Bilige S, Liu QJ (2023) Cambial phenology and wood formation of Korean pine in response to climate change in Changbai Mountain, Northeast China. Dendrochronologia. https://doi.org/10.1016/j.dendro.2022.126045
[37]	Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152:1–12. https://doi.org/10.1007/s00442-006-0625-7
[38]	Rossi S, Morin H, Deslauriers A, Plourdep PY (2011) Predicting xylem phenology in black spruce under climate warming. Glob Chang Biol 17(1):614–625. https://doi.org/10.1111/j.1365-2486.2010.02191.x
[39]	Shi JF, Liu Y, Vaganov EA, Li JB, Cai QF (2008) Statistical and process-based modeling analyses of tree growth response to climate in semi-arid area of north central China: a case study of Pinus tabulaeformis. J Geophys Res Biogeosci. https://doi.org/10.1029/2007JG000547
[40]	Sun CF, Liu Y (2016) Climate response of tree radial growth at different timescales in the Qinling Mountains. PLoS ONE. https://doi.org/10.1371/journal.pone.0160938
[41]	Suseela V, Conant RT, Wallenstein MD, Dukes JS (2012) Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob Chang Biol 18(1):336–348. https://doi.org/10.1111/j.1365-2486.2011.02516.x
[42]	Takahashi K, Tokumitsu Y, Yasue K (2005) Climatic factors affecting the tree-ring width of Betula ermanii at the timberline on Mount Norikura, central Japan. Ecol Res 20(4):445–451. https://doi.org/10.1007/s11284-005-0060-y
[43]	Teets A, Fraver S, Weiskittel AR, Hollinger DY (2018) Quantifying climate–growth relationships at the stand level in a mature mixed-species conifer forest. Glob Chang Biol 24(8):3587–3602. https://doi.org/10.1111/gcb.14120
[44]	Tian QY, He ZB, Xiao SC, Du J, Peng XM, Chen LF, Lin PF, Zhu X, Ding AJ (2018) Growing season stem water status assessment of Qinghai spruce through the sap flow and stem radial variations in the Qilian Mountains of China. Forests. https://doi.org/10.3390/f9010002
[45]	Tian QY, He ZB, Xiao SC, Du J, Peng XM, Lin PF, Ding AJ (2019) Effects of artificial warming on stem radial changes in Qinghai spruce saplings in the Qilian Mountains of China. Dendrochronologia 55:110–118. https://doi.org/10.1016/j.dendro.2019.04.009
[46]	Tian QY, He ZB, Xiao SC, Peng XM, Ding AJ, Lin PF (2017) Response of stem radial growth of Qinghai spruce (Picea crassifolia) to environmental factors in the Qilian Mountains of China. Dendrochronologia 44:76–83. https://doi.org/10.1016/j.dendro.2017.04.001
[47]	Touchan R, Shishov VV, Tychkov II, Sivrikaya F, Attieh J, Jihad A, Ketmen M, Stephan J, Mitsopoulos I, Christou A, Meko DM (2016) Elevation-layered dendroclimatic signal in eastern Mediterranean tree rings. Environ Res Lett. https://doi.org/10.1088/1748-9326/11/4/044020
[48]	Vieira J, Rossi S, Campelo F, Freitas H, Nabais C (2013) Seasonal and daily cycles of stem radial variation of Pinus pinaster in a drought-prone environment. Agric for Meteorol 180(8):173–181. https://doi.org/10.1016/j.agrformet.2013.06.009
[49]	Wan YF, Yu PT, Li XQ, Wang YH, Wang B, Yu YP, Zhang L, Liu XD, Wang SL (2022) Divergent seasonal patterns of Qinghai spruce growth with elevation in Northwestern China. Forests 13(3):388. https://doi.org/10.3390/f13030388
[50]	Wang B, Yu PT, Yu YP, Wang YH, Zhang L, Wan YF, Wang SL, Liu XD (2021) Trees at a moderately arid site were more sensitive to long-term drought. Forests 12(5):579. https://doi.org/10.3390/f12050579
[51]	Wang B, Yu PT, Zhang L, Wang YH, Yu YP, Wang SL (2019) Differential trends of Qinghai spruce growth with elevation in northwestern China during the recent warming hiatus. Forests 10(9):712. https://doi.org/10.3390/f10090712
[52]	Wang WB, Zhang F, Yuan LM, Wang QT, Zheng K, Zhao CY (2016) Environmental factors effect on stem radial variations of Picea crassifolia in Qilian Mountains, Northwestern China. Forests 7(10):210. https://doi.org/10.3390/f7100210
[53]	Wang ZY, Yang B, Deslauriers A, Br?uning A (2015) Intra-annual stem radial increment response of Qilian juniper to temperature and precipitation along an altitudinal gradient in northwestern China. Trees 29(1):25–34. https://doi.org/10.1007/s00468-014-1037-7
[54]	Wang ZY, Yang B, Deslauriers A, Br?uning A (2014) Intra-annual stem radial increment response of Qilian juniper to temperature and precipitation along an altitudinal gradient in northwestern China. Trees 29(1):25–34. https://doi.org/10.1007/s00468-014-1037-7
[55]	Westermann J, Zerbe S, Eckstein D (2008) Age structure and growth of degraded Populus euphratica floodplain forests in north-west China and perspectives for their recovery. J Integr Plant Biol 50(5):536–546. https://doi.org/10.1111/j.1744-7909.2007.00626.x
[56]	Williams AP, Allen CD, Macalady AK, Griffin D, Woodhouse CA, Meko DM, Swetnam TW, Rauscher SA, Seager R, Grission-Mayer HD, Dean JS, Cook ER, Gangodagamage C, Cai M, McDowell NG (2013) Temperature as a potent driver of regional forest drought stress and tree mortality. Nat Clim Chang 3(3):292–297. https://doi.org/10.1038/NCLIMATE1693
[57]	Wu CY, Chen DS, Sun XM, Zhang SG (2023) Influence of altitude and tree class on climate-growth relationships in a larch plantation in subtropical China. J for Res 34(6):1869–1880. https://doi.org/10.1007/s11676-023-01630-5
[58]	Yang RQ, Fu PL, Fan ZX, Panthi S, Gao J, Niu Y, Li ZS, Br?uning A (2022) Growth-climate sensitivity of two pine species shows species-specific changes along temperature and moisture gradients in southwest China. Agric for Meteorol. https://doi.org/10.1016/j.agrformet.2022.108907
[59]	Zeng XM, Wei CF, Liu XH, Zhang LN (2019) Qinghai spruce (Picea crassifolia) and Chinese pine (Pinus tabuliformis) show high vulnerability and similar resilience to early growing-season drought in the Helan Mountains, China. Ecol Indic. https://doi.org/10.1016/j.ecolind.2019.105871
[60]	Zhang JZ, Gou XH, Zhang YX, Lu M, Xu XY, Zhang F, Liu WH, Gao LL (2016a) Forward modeling analyses of Qilian Juniper (Sabina przewalskii) growth in response to climate factors in different regions of the Qilian Mountains, northwestern China. Trees 30(1):175–188. https://doi.org/10.1007/s00468-015-1286-0
[61]	Zhang LN, Jiang Y, Zhao SD, Dong MY, Chen HYH, Kang XY (2016b) Different responses of the radial growth of conifer species to increasing temperature along altitude gradient: Pinus tabulaeformis in the Helan Mountains (Northwestern China). Pol J Ecol 64(4):509–525. https://doi.org/10.3161/15052249PJE2016.64.4.006
[62]	Zhang QB, Cheng GD, Yao TD, Kang XC, Huang JG (2003) A 2,326-year tree-ring record of climate variability on the northeastern Qinghai-Tibetan Plateau. Geophys Res Lett. https://doi.org/10.1029/2003gl017425
[63]	Zhang RB, Yuan YJ, Gou XH, Zhang TW, Zou C, Ji CR, Fan Z, Qin L, Shang HM, Li XJ (2016c) Intra-annual radial growth of Schrenk spruce (Picea schrenkiana Fisch. et Mey) and its response to climate on the northern slopes of the Tianshan Mountains. Dendrochronologia 40:36–42. https://doi.org/10.1016/j.dendro.2016.06.002
[64]	Zhu LJ, Cooper DJ, Yang JW, Zhang X, Wang XC (2018) Rapid warming induces the contrasting growth of Yezo spruce (Picea jezoensis var. microsperma) at two elevation gradient sites of northeast China. Dendrochronologia 50:52–63. https://doi.org/10.1016/j.dendro.2018.05.002
[65]	Zhu LJ, Liu SG, Zhu HF, Cooper DJ, Yuan DY, Zhu Y, Li ZS, Zhang YD, Liang HX, Zhang X, Song WQ, Wang XC (2022) Multi-species approach strengthens the reliability of dendroclimatic reconstructions in monsoonal Northeast China. Clim Change 171(1):7. https://doi.org/10.1007/s10584-022-03328-9
[66]	Zuidema PA, Heinrich I, Rahman M, Vlam M, Zwartsenberg SA, van der Sleen P (2020) Recent CO2 rise has modified the sensitivity of tropical tree growth to rainfall and temperature. Glob Chang Biol 26(7):4028–4041. https://doi.org/10.1111/gcb.15092
[67]	Zweifel R, Zimmermann L, Zeugin F, Newbery DM (2006) Intra-annual radial growth and water relations of trees: implications towards a growth mechanism. J Exp Bot 57(6):1445–1459. https://doi.org/10.1093/jxb/erj125