Radial growth and its low-temperature threshold of Abies georgei var. smithii at different altitudes in Jiaozi Mountain, Yunnan, China

doi:10.17521/cjpe.2021.0399

Abstract

Abstract:

Aims In view of the overarching significance for tree function and survival, it is essential to explore the environmental influences on tree development. Our objective was to clarify the altitudinal differences in the onset and offset of each stage of tree radial growth, to analyze the response of cambium activity and xylem differentiation to temperature at different altitudes, and to identify low temperature threshold for radial growth of trees.

Methods Weekly microcores and hourly in situ climate data were collected at 3 600, 3 800 and 4 000 m along the altitude gradient of Abies georgei var. smithii forest in Jiaozi Mountain, Yunnan.

Important findings The results showed that: (1) There were differences in the phenology of radial growth at three altitudes. The onset of radial growth was delayed by 4.7 d per 100 m, the end of radial growth was advanced by 7.2 d per 100 m, and the growing season was shortened by 12.8 d per 100 m with increasing altitude; (2) The radial growth of Abies georgei var. smithii at different altitudes had similar low temperature thresholds (about 5 °C), and temperature controlled the onset of cambium activity and the end of xylem differentiation; (3) The degree of cell division activity at different altitude decreased at higher temperatures (around the summer solstice), and photoperiod was involved in the regulation of the end of cambium activity to ensure the completion of cell mature before the freezing. The relationship between the cambium activity and altitude-induced temperature change is weak. The photoperiod may be involved in regulating the end of cambium activity to ensure the completion of cell mature before the freezing. This study contributes to understand the response mechanisms of tree growth dynamics to climate change and provides a scientific basis for better adaptation and response to climate change.

Key words: radial growth, temperature threshold, cambium activity, xylem differentiation, micro-core

ZHU Ming-Yang, LIN Lin, SHE Yu-Long, XIAO Cheng-Cai, ZHAO Tong-Xing, HU Chun-Xiang, ZHAO Chang-You, WANG Wen-Li. Radial growth and its low-temperature threshold of Abies georgei var. smithii at different altitudes in Jiaozi Mountain, Yunnan, China[J]. Chin J Plant Ecol, 2022, 46(9): 1038-1049.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0399

https://www.plant-ecology.com/EN/Y2022/V46/I9/1038

Figures/Tables 15

References 50

[1]	Alvarez-Uria P, Körner C (2007). Low temperature limits of root growth in deciduous and evergreen temperate tree species. Functional Ecology, 21, 211-218. DOI URL
[2]	Antonucci S, Rossi S, Deslauriers A, Lombardi F, Marchetti M, Tognetti R (2015). Synchronisms and correlations of spring phenology between apical and lateral meristems in two boreal conifers. Tree Physiology, 35, 1086-1094. DOI PMID
[3]	Bai XP, Zhang XL, Li JX, Duan XY, Jin YT, Chen ZJ (2019). Altitudinal disparity in growth of Dahurian larch (Larix gmelinii Rupr.) in response to recent climate change in northeast China. Science of the Total Environment, 670, 466-477. DOI URL
[4]	Creber GT, Chaloner WG (1984). Influence of environmental factors on the wood structure of living and fossil trees. The Botanical Review, 50, 357-448. DOI URL
[5]	Cullen LE, Palmer JG, Duncan RP, Stewart GH (2001). Climate change and tree-ring relationships of Nothofagus menziesii tree-line forests. Canadian Journal of Forest Research, 31, 1981-1991. DOI URL
[6]	Deslauriers A, Morin H, Begin Y (2003). Cellular phenology of annual ring formation of Abies balsamea in the Quebec boreal forest (Canada). Canadian Journal of Forest Research, 33, 190-200. DOI URL
[7]	Deslauriers A, Rossi S, Anfodillo T, Saracino A (2008). Cambial phenology, wood formation and temperature thresholds in two contrasting years at high altitude in southern Italy. Tree Physiology, 28, 863-871. PMID
[8]	Du XL, Du F, Zeng H, Chen Y, Yao Y, Zhang H, Li ZY (2010). A study on the community of Abies georgei var. smithii in Jiaozi Mountain Nature Reserve. Journal of Yunnan University (Natural Sciences Edition), 32, 358-364.
	[杜小浪, 杜凡, 曾辉, 陈勇, 姚莹, 张辉, 李朝阳 (2010). 轿子山自然保护区急尖长苞冷杉林群落特征研究. 云南大学学报(自然科学版), 32, 358-364.]
[9]	Elliott GP, Bailey SN, Cardinal SJ (2021). Hotter drought as a disturbance at upper treeline in the southern rocky mountains. Annals of the American Association of Geographers, 111, 756-770. DOI URL
[10]	Gao LL, Gou XH, Deng Y, Yang MX, Zhang F (2017). Assessing the influences of tree species, elevation and climate on tree-ring growth in the Qilian Mountains of northwest China. Trees, 31, 393-404. DOI URL
[11]	Gruber A, Baumgartner D, Zimmermann J, Oberhuber W (2008). Temporal dynamic of wood formation in Pinus cembra along the alpine treeline ecotone and the effect of climate variables. Trees, 23, 623-635. DOI URL
[12]	Häsler R, Streule A, Turner H (1999). Shoot and root growth of young Larix decidua in contrasting microenvironments near the alpine timberline. Phyton-Annales Rei Botanicae, 39, 47-52.
[13]	Huang JG, Ma QQ, Rossi S, Biondi F, Deslauriers A, Fonti P, Liang EY, Mäkinen H, Oberhuber W, Rathgeber CBK, Tognetti R, Treml V, Yang B, Zhang JL, Antonucci S, et al. (2020). Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers. Proceedings of the National Academy of Sciences of the United States of America, 117, 20645-20652.
[14]	James JC, Grace J, Hoad SP (1994). Growth and photosynthesis of Pinus sylvestris at its altitudinal limit in Scotland. Journal of Ecology, 82, 297-306. DOI URL
[15]	Jiménez-Noriega MS, López-Mata L, Terrazas T (2021). Cambial activity and phenology in three understory species along an altitude gradient in Mexico. Forests, 12, 506. DOI: 10.3390/f12040506. DOI
[16]	Jochner M, Bugmann H, Nötzli M, Bigler C (2018). Tree growth responses to changing temperatures across space and time: a fine-scale analysis at the treeline in the Swiss Alps. Trees, 32, 645-660. DOI URL
[17]	Körner C (2012). Alpine Treelines: Functional Ecology of the Global High Elevation Tree Limits. Springer-Verlag, Heidelberg.
[18]	Körner C, Paulsen J (2004). A world-wide study of high altitude treeline temperatures. Journal of Biogeography, 31, 713-732. DOI URL
[19]	Lenz A, Hoch G, Körner C (2013). Early season temperature controls cambial activity and total tree ring width at the alpine treeline. Plant Ecology & Diversity, 6, 365-375.
[20]	Li XX, Liang EY, Gričar J, Rossi S, Čufar K, Ellison AM (2017). Critical minimum temperature limits xylogenesis and maintains treelines on the southeastern Tibetan Plateau. Science Bulletin, 62, 804-812. DOI URL
[21]	Li ZY, Liu K, Chen Y, Yao Y, Du XL, Zhang H (2010). Studies on the vegetation form and distribution characteristics in Jiaozishan Nature Reserve. Journal of Shandong Forestry Science and Technology, 40(2), 32-35.
	[李朝阳, 刘恺, 陈勇, 姚莹, 杜小浪, 张辉 (2010). 轿子山自然保护区植被类型及其分布特点研究. 山东林业科技, 40(2), 32-35.]
[22]	Lin YT, Whitman WB, Coleman DC, Jien SH, Wang HC, Chiu CY (2021). Soil bacterial communities at the treeline in subtropical alpine areas. CATENA, 201, 105205. DOI: 10.1016/j.catena.2021.105205. DOI
[23]	Liu B, Li Y, Eckstein D, Zhu LP, Dawadi B, Liang EY (2013). Has an extending growing season any effect on the radial growth of Smith fir at the timberline on the southeastern Tibetan Plateau? Trees, 27, 441-446. DOI URL
[24]	Luo TX, Liu XS, Zhang L, Li X, Pan YD, Wright IJ (2018). Summer solstice marks a seasonal shift in temperature sensitivity of stem growth and nitrogen-use efficiency in cold-limited forests. Agricultural and Forest Meteorology, 248, 469-478. DOI URL
[25]	Malik R, Rossi S, Sukumar R (2020). Cambial phenology in Abies pindrow (Pinaceae) along an altitudinal gradient in northwestern Himalaya. IAWA Journal, 41, 186-201. DOI URL
[26]	McIntyre S, Lavorel S, Landsberg J, Forbes TDA (1999). Disturbance response in vegetation—Towards a global perspective on functional traits. Journal of Vegetation Science, 10, 621-630. DOI URL
[27]	Moser L, Fonti P, Büntgen U, Esper J, Luterbacher J, Franzen J, Frank D (2009). Timing and duration of European larch growing season along altitudinal gradients in the Swiss Alps. Tree Physiology, 30, 225-233. DOI URL
[28]	Oberhuber W (2004). Influence of climate on radial growth of Pinus cembra within the alpine timberline ecotone. Tree Physiology, 24, 291-301. PMID
[29]	Quinn GP, Keough MJ (2002). Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.
[30]	Rahman MH, Kudo K, Yamagishi Y, Nakamura Y, Nakaba S, Begum S, Nugroho WD, Arakawa I, Kitin P, Funada R (2020). Winter-spring temperature pattern is closely related to the onset of cambial reactivation in stems of the evergreen conifer Chamaecyparis pisifera. Scientific Reports, 10, 14341. DOI: 10.1038/S41598-020-70356-9. DOI
[31]	Rathgeber CBK, Rossi S, Bontemps JD (2011). Cambial activity related to tree size in a mature silver-fir plantation. Annals of Botany, 108, 429-438. DOI PMID
[32]	Rossi S, Anfodillo T, Čufar K, Cuny HE, Deslauriers A, Fonti P, Frank D, Gričar J, Gruber A, Huang JG, Jyske T, Kašpar J, King G, Krause C, Liang E et al. (2016). Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere. Global Change Biology, 22, 3804-3813. DOI PMID
[33]	Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007). Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia, 152, 1-12. DOI PMID
[34]	Rossi S, Deslauriers A, Anfodillo T, Morin H, Saracino A, Motta R, Borghetti M (2006). Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytologist, 170, 301-310. PMID
[35]	Rossi S, Deslauriers A, Griçar J, Seo JW, Rathgeber CB, Anfodillo T, Morin H, Levanic T, Oven P, Jalkanen R (2008). Critical temperatures for xylogenesis in conifers of cold climates. Global Ecology and Biogeography, 17, 696-707. DOI URL
[36]	Sakio H, Masuzawa T (1985). Ecological studies on the timberline of Mt. Fuji. The Botanical Magazine, 98, 15-28. DOI URL
[37]	Splechtna BE, Dobrys J, Klinka K (2000). Tree-ring characteristics of subalpine fir (Abies lasiocarpa (Hook.) Nutt.) in relation to elevation and climatic fluctuations. Annals of Forest Science, 57, 89-100. DOI URL
[38]	Stangler DF, Kahle HP, Raden M, Larysch E, Seifert T, Spiecker H (2021). Effects of intra-seasonal drought on kinetics of tracheid differentiation and seasonal growth dynamics of Norway spruce along an elevational gradient. Forests, 12, 274. DOI: 10.3390/f12030274. DOI
[39]	Treml V, Kašpar J, Kuželová H, Gryc V (2015). Differences in intra-annual wood formation in Picea abies across the treeline ecotone, Giant Mountains, Czech Republic. Trees, 29, 515-526. DOI URL
[40]	Usmani A, Silvestro R, Zhang SK, Huang JG, Saracino A, Rossi S (2020). Ecotypic differentiation of black spruce populations: temperature triggers bud burst but not bud set. Trees, 34, 1313-1321. DOI URL
[41]	Vaganov EA, Hughes MK, Kirdyanov AV, Schweingruber FH, Silkin PP (1999). Influence of snowfall and melt timing on tree growth in subarctic Eurasia. Nature, 400, 149-151. DOI URL
[42]	Verrall B, Pickering CM (2020). Alpine vegetation in the context of climate change: a global review of past research and future directions. Science of the Total Environment, 748, 141344. DOI: 10.1016/j.scitotenv.2020.141344. DOI
[43]	Wei CY, Karger DN, Wilson AM (2020). Spatial detection of alpine treeline ecotones in the Western United States. Remote Sensing of Environment, 240, 111672. DOI: 10.1016/j.rse.2020.111672. DOI
[44]	Wilson BF, Wodzicki TJ, Zahner R (1966). Differentiation of cambial derivatives: proposed terminology. Forest Science, 12, 438-440.
[45]	Yang JW, Cooper DJ, Zhang X, Song WQ, Li ZS, Zhang YD, Zhao HY, Han SJ, Wang XC (2021). Climatic controls of Pinus pumila radial growth along an altitude gradient. New Forests, 2, 319-335.
[46]	Zhai LH, Bergeron Y, Huang JG, Berninger F (2012). Variation in intra-annual wood formation, and foliage and shoot development of three major Canadian boreal tree species. American Journal of Botany, 99, 827-837. DOI PMID
[47]	Zhang JZ, Alexander MR, Gou XH, Deslauriers A, Fonti P, Zhang F, Pederson N (2020). Extended xylogenesis and stem biomass production in Juniperus przewalskii Kom. during extreme late-season climatic events. Annals of Forest Science, 77, 1-11. DOI URL
[48]	Zhang JZ, Gou XH, Pederson N, Zhang F, Niu HG, Zhao SD, Wang F (2018). Cambial phenology in Juniperus przewalskii along different altitudinal gradients in a cold and arid region. Tree Physiology, 38, 840-852. DOI URL
[49]	Zhang YP, Jiang Y, Wen Y, Ding XY, Wang B, Xu JL (2019). Comparing primary and secondary growth of co-occurring deciduous and evergreen conifers in an alpine habitat. Forests, 10, 574. DOI: 10.3390/f10070574. DOI
[50]	Zhou P, Huang JG, Liang HX, Rossi S, Bergeron Y, Shishov VV, Jiang SW, Kang J, Zhu HX, Dong ZC (2021). Radial growth of Larix sibirica was more sensitive to climate at low than high altitudes in the Altai Mountains, China. Agricultural and Forest Meteorology, 304, 108392. DOI: 10.1016/j.agrformet.2021.108392. DOI

	空气温度 Air temperature (℃)				土壤温度 Soil temperature (℃)
海拔 Altitude (m)	平均 Mean	最高 Maximum	最低 Minimum	直减率 Direct reduction rate (℃·m^-1)	平均 Mean	最高 Maximum	最低 Minimum	直减率 Direct reduction rate (℃·m^-1)
3 600	5.56	14.25	-4.66	0.005 9 ± 0.000 7	5.82	11.26	-0.39	0.005 7 ± 0.000 6
3 800	4.25	10.06	-7.49		4.57	11.30	-3.73
4 000	3.20	10.41	-9.04		3.54	9.33	-1.10

	空气温度 Air temperature (℃)				土壤温度 Soil temperature (℃)
海拔 Altitude (m)	平均 Mean	最高 Maximum	最低 Minimum	直减率 Direct reduction rate (℃·m^-1)	平均 Mean	最高 Maximum	最低 Minimum	直减率 Direct reduction rate (℃·m^-1)
3 600	5.56	14.25	-4.66	0.005 9 ± 0.000 7	5.82	11.26	-0.39	0.005 7 ± 0.000 6
3 800	4.25	10.06	-7.49		4.57	11.30	-3.73
4 000	3.20	10.41	-9.04		3.54	9.33	-1.10

	形成层细胞 Cambial cell	细胞膨大 Cell enlarging	细胞壁加厚 Cell wall-thickening	细胞成熟 Mature cells
开始 Onset	0.001^**	0.001^**	0.016^*	0.826
结束 Ending	0.534	0.024^*	0.311	0.011^*
持续 Duration	0.096	0.001^**	0.02^*	0.015^*

	形成层细胞 Cambial cell	细胞膨大 Cell enlarging	细胞壁加厚 Cell wall-thickening	细胞成熟 Mature cells
开始 Onset	0.001^**	0.001^**	0.016^*	0.826
结束 Ending	0.534	0.024^*	0.311	0.011^*
持续 Duration	0.096	0.001^**	0.02^*	0.015^*

					空气温度 Air temperature (℃)					土壤温度 Soil temperature (℃)
海拔 Altitude (m)	最低 Minimum	最高 Maximum	平均 Mean	>0 ℃积温 >0 ℃ accumulation	>5 ℃积温 >5 ℃ accumulation	最低 Minimum	最高 Maximum	平均 Mean	>0 ℃积温 >0 ℃ accumulation	>5 ℃积温 >5 ℃ accumulation	生长季长度 (平均值±标准差) Growing season length (mean ± SD) (d)
3 600	0.06	14.25	8.87	1 775.83	1 730.18	2.80	11.26	8.78	1 718.75	1 654.99	195 ± 4
3 800	1.52	10.06	7.63	1 419.37	1 389.24	2.79	11.30	7.90	1 457.26	1 420.16	177 ± 1
4 000	2.40	10.41	7.19	1 000.10	959.21	2.70	9.33	7.33	983.20	927.57	144 ± 16