Stoichiometric characteristics of leaf, branch and root in Larix gmelinii in response to climate warming based on latitudinal transplantation

doi:10.17521/cjpe.2023.0013

Abstract

Abstract:

Aims Exploring the impact of climate warming on stoichiometric characteristics of trees is of significance for better understanding the response mechanism of trees to climate change.
Methods In 2004, we conducted a common garden experiment by transplanting Larix gmelinii trees from four provenances to a common garden near the warm edge of this species’ range in the Mao’ershan Ecological Station of China, in order to measure the concentrations of carbon (C), nitrogen (N) and phosphorus (P) in leaves of short branch, leaves of long branch, short branches, long branches, and fine roots at three diameter classes in response to warming.
Important findings The C, N, and P concentrations in leaves of short branch and roots of all diameter classes, and the N and P concentrations in leaves of old branch significantly differed among provenances. The provenances at high latitude sites were characterized by lower C and N concentrations and higher P concentration compared to those at low latitude sites. Warming treatment significantly increased the C concentration in all organs (except root at 1-2 mm diameter), and also significantly increased the N concentration in leaves, long branches and roots <1 mm diameter, and the P concentration in all organs (except short and long branches). The effect of warming on C and P concentrations decreased with the increasing warming, but increased for N concentration. The C:N, C:P and N:P in all organs (except short and long branches) significantly varied with provenances. The provenances at high latitude sites had higher C:N and lower C:P and N:P compared to those at low latitude sites. Warming treatment significantly decreased the C:N, C:P and N:P in all organs except short and long branches. In summary, the stoichiometric characteristics had evident geographical variations in resource acquisition organs of leaves and roots of L. gmelinii. Warming treatment mainly alleviated the constraints on the demand for N and P in leaves and roots, and simultaneously reduced the C sequestration efficiency of N and P. The impact of climate warming on the stoichiometric characteristics of C and P elements decreased as the increasing warming, except N element.

Key words: climate change, Larix gmelinii, transplanting experiment, stoichiometric characteristic

ZANG Miao-Han, WANG Chuan-Kuan, LIANG Yi-Xian, LIU Yi-Xiao, SHANGGUAN Hong-Yu, QUAN Xian-Kui. Stoichiometric characteristics of leaf, branch and root in Larix gmelinii in response to climate warming based on latitudinal transplantation[J]. Chin J Plant Ecol, 2024, 48(4): 469-482.

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Figures/Tables 7

Table 1 Geographical and climatic conditions of Larix gmelinii at the four transplanting sites and common garden in Mao’ershan

地点 Site	纬度 Latitude (° N)	经度 Longitude (° E)	年平均气温 Mean annual air temperature (℃)	平均年降水量 Mean annual precipitation (mm)	无霜期 Frost-free duration (d)	N_soil-c (g·kg^-1)	N_soil-t (g·kg^-1)
帽儿山 Mao’ershan	45.40	127.50	3.10	629.00	140.0	(8.10 ± 0.45)^a	无 None
带岭 Dailing	47.08	128.90	1.34	621.27	139.0	(6.75 ± 0.31)^b	(6.83 ± 0.33)^a
黑河 Heihe	49.22	127.20	0.62	554.08	90.0	(3.11 ± 0.26)^c	(3.13 ± 0.23)^b
松岭 Songling	50.72	124.42	−0.54	525.36	93.8	(3.07 ± 0.21)^c	(3.03 ± 0.19)^b
塔河 Tahe	52.52	124.65	−2.30	463.44	89.7	(2.47 ± 0.11)^d	(2.31 ± 0.15)^c

Fig. 1 Comparisons of carbon (C), nitrogen (N) and phosphorus (P) concentration in different organs of Larix gmelinii by treatments and sites (mean ± SE). DL, Dailing; HH, Heihe; SL, Songling; TH, Tahe. n = 4 for each site, n = 32 for all sites. Different uppercase letters indicate significant differences between trees at transplanting sites (p < 0.05), different lowercase letters indicate significant differences between trees in the common garden (p < 0.05), * indicates significant effects of warming treatment on C, N and P concentrations (p < 0.05).

Fig. 2 Relationships between carbon (C), nitrogen (N), phosphorus (P) concentration in different organs of Larix gmelinii and latitude of four sites (n = 4).

Fig. 3 Comparisons of C:N, C:P and N:P in different organs of Larix gmelinii by treatments and sites (mean ± SE). C, carbon; N, nitrogen; P, phosphorus. DL, Dailing; HH, Heihe; SL, Songling; TH, Tahe. n = 4 for each site, n = 32 for all sites. Different uppercase letters indicate significant differences between trees at transplanting sites (p < 0.05), different lowercase letters indicate significant differences between trees in the common garden (p < 0.05), * indicates significant effects of climate warming on C:N, C:P and N:P (p < 0.05).

Table 2 Variance analysis of carbon (C), nitrogen (N) and phosphorus (P) stoichiometric characteristics in different organs of Larix gmelinii (n = 224)

主效应 Main effect	C		N		P		C:N		C:P		N:P
主效应 Main effect	F	p	F	p	F	p	F	p	F	p	F	p
处理 Treatment	32.35	<0.01	47.04	<0.01	68.37	<0.01	10.80	<0.01	77.68	<0.01	73.26	<0.01
地点 Site	9.86	<0.01	113.64	<0.01	131.61	<0.01	65.65	<0.01	114.42	<0.01	511.26	<0.01
器官 Organ	14.65	<0.01	1 801.69	<0.01	244.38	<0.01	888.05	<0.01	205.56	<0.01	267.42	<0.01
处理×地点 Treatment × site	1.58	0.21	276.32	<0.05	8.17	<0.01	198.62	<0.01	9.43	<0.01	325.99	<0.01
处理×器官 Treatment × organ	3.35	<0.01	26.48	<0.01	5.73	<0.01	14.08	<0.01	10.98	<0.01	10.24	<0.01
地点×器官 Site × organ	1.05	0.40	22.13	<0.01	10.86	<0.01	18.90	<0.01	4.43	<0.01	43.34	<0.01
处理×地点×器官 Treatment × site × organ	2.00	0.05	27.44	<0.01	4.22	<0.01	14.91	<0.01	2.00	0.05	25.71	<0.01

Fig. 4 Relationships between relative increasing rate of carbon (C) concentration, nitrogen (N) concentration, phosphorus (P) concentration in different organs of Larix gmelinii and warming amount (ΔT) (n = 4). ΔT is the difference in annual mean air temperature between the common garden and the transplanting sites. Relative increasing rate (%) = (C2 - C1)/C1 × 100%, C1 is the C (or N, P) concentration of trees at transplanting sites, C2 is the C (or N, P) concentration of trees in common garden.

Fig. 5 Climate warming effects of carbon (C), nitrogen(N), phosphorus (P) concentration in different organs of Larix gmelinii (n = 4). Climate warming effect = (C2 - C1)/ΔT (C1 is the C (or N, P) concentration of trees at transplanting sites, C2 is the C (or N, P) concentration of trees in common garden, ΔT is the difference in annual mean air temperature between the common garden and the latitudinal sites).

References 67

[1]	Albert CH, Thuiller W, Yoccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010). Intraspecific functional variability: extent, structure and sources of variation. Journal of Ecology, 98, 604-613.
[2]	Augusto L, Achat DL, Jonard M, Vidal D, Ringeval B (2017). Soil parent material—A major driver of plant nutrient limitations in terrestrial ecosystems. Global Change Biology, 23, 3808-3824.
[3]	Cai Q, Ding JX, Zhang ZL, Hu J, Wang QT, Yin MZ, Liu Q, Yin HJ (2019). Distribution patterns and driving factors of leaf C, N and P stoichiometry of coniferous species on the eastern Qinghai-Xizang Plateau, China. Chinese Journal of Plant Ecology, 43, 1048-1060. DOI
	[蔡琴, 丁俊祥, 张子良, 胡君, 汪其同, 尹明珍, 刘庆, 尹华军 (2019). 青藏高原东缘主要针叶树种叶片碳氮磷化学计量分布格局及其驱动因素. 植物生态学报, 43, 1048-1060.] DOI
[4]	Chen YH, Han WX, Tang LY, Tang ZY, Fang JY (2013). Leaf nitrogen and phosphorus concentrations of woody plants differ in responses to climate, soil and plant growth form. Ecography, 36, 178-184.
[5]	Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC (2005). Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology, 86, 12-19.
[6]	Crous KY, O’Sullivan OS, Zaragoza-Castells J, Bloomfield KJ, Negrini ACA, Meir P, Turnbull MH, Griffin KL, Atkin OK (2017). Nitrogen and phosphorus availabilities interact to modulate leaf trait scaling relationships across six plant functional types in a controlled-environment study. New Phytologist, 215, 992-1008. DOI PMID
[7]	Crous KY, Quentin AG, Lin YS, Medlyn BE, Williams DG, Barton CVM, Ellsworth DS (2013). Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO₂ and climate warming. Global Change Biology, 19, 3790-3807.
[8]	Crous KY, Wujeska-Klause A, Jiang MK, Medlyn BE, Ellsworth DS (2019). Nitrogen and phosphorus retranslocation of leaves and stemwood in a mature Eucalyptus forest exposed to 5 years of elevated CO₂. Frontiers in Plant Science, 10, 664. DOI: 10.3389/fpls.2019.00664.
[9]	Ding D, Arif M, Liu M, Li J, Hu X, Geng Q, Yin F, Li C (2022). Plant-soil interactions and C:N:P stoichiometric homeostasis of plant organs in riparian plantation. Frontiers in Plant Science, 13, 979023. DOI: 10.3389/fpls.2022.979023.
[10]	Dong N, Prentice I, Wright I, Evans B, Togashi HF, Caddy- Retalic S, McInerney FA, Sparrow B, Leitch E, Lowe A (2020). Components of leaf-trait variation along environmental gradients. New Phytologist, 228, 82-94.
[11]	Drenovsky RE, Richards JH (2004). Critical N:P values: predicting nutrient deficiencies in desert shrublands. Plant and Soil, 259, 59-69.
[12]	Dusenge ME, Sasha M, Way DA (2020). Contrasting acclimation responses to elevated CO₂ and warming between an evergreen and a deciduous boreal conifer. Global Change Biology, 26, 3639-3657.
[13]	Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007). Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters, 10, 1135-1142. DOI PMID
[14]	Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010). Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytologist, 186, 593-608. DOI PMID
[15]	Fang Z, Li DD, Jiao F, Yao J, Du HT (2019). The latitudinal patterns of leaf and soil C:N:P stoichiometry in the Loess Plateau of China. Frontiers in Plant Science, 10, 85. DOI: 10.3389/fpls.2019.00085.
[16]	Frenne P, Graae BJ, Rodríguez-Sánchez F, Kolb A, Chabrerie O, Decocq G, Kort H, Schrijver A, Diekmann M, Eriksson O, Gruwez R, Hermy M, Lenoir J, Plue J, Coomes DA, Verheyen K (2013). Latitudinal gradients as natural laboratories to infer species’ responses to temperature. Journal of Ecology, 101, 784-795.
[17]	Güsewell S (2004). N:P ratios in terrestrial plants: variation and functional significance. New Phytologist, 164, 243-266. DOI PMID
[18]	Güsewell S, Koerselman W, Verhoeven JTA (2003). Biomass N:P ratios as indicators of nutrient limitation limitation for plant populations in wetlands. Ecological Applications, 13, 372-384.
[19]	He J, Fang J, Wang Z, Guo D, Flynn DFB, Geng Z (2006). Stoichiometry and large-scale patterns of leaf carbon and nitrogen in the grassland biomes of China. Oecologia, 149, 115-122.
[20]	He JS, Han XG (2010). Ecological stoichiometry: searching for unifying principles from individuals to ecosystems. Chinese Journal of Plant Ecology, 34, 2-6.
	[贺金生, 韩兴国 (2010). 生态化学计量学: 探索从个体到生态系统的统一化理论. 植物生态学报, 34, 2-6.] DOI
[21]	He MZ, Song X, Tian FP, Zhang K, Zhang ZS, Chen N, Li XR (2016). Divergent variations in concentrations of chemical elements among shrub organs in a temperate desert. Scientific Reports, 6, 20124. DOI: 10.1038/srep20124.
[22]	Hong JT, Wu JB, Wang XD (2013). Effects of global climate change on the C, N, and P stoichiometry of terrestrial plants. Chinese Journal of Applied Ecology, 24, 2658-2665.
	[洪江涛, 吴建波, 王小丹 (2013). 全球气候变化对陆地植物碳氮磷生态化学计量学特征的影响. 应用生态学报, 24, 2658-2665.]
[23]	Jiang PP, Han XJ, Liu ZY, Fan SJ, Zhang XJ (2023). C:N:P stoichiometric variations of herbs and its relationships with soil properties and species relative abundance along the Xiaokai River irrigation in the Yellow River Delta, China. Frontiers in Plant Science, 14, 1130477. DOI: 10.3389/fpls.2023.1130477
[24]	Jiang Q, Chen GS, Guo RQ, Song TT, Chen TT, Chen YH, Jia LQ, Xiong DC (2020). Effects of warming and nitrogen addition on fine root stoichiometry of Chinese fir seedlings. Chinese Journal of Ecology, 39, 723-732.
	[姜琦, 陈光水, 郭润泉, 宋涛涛, 陈廷廷, 陈宇辉, 贾林巧, 熊德成 (2020). 增温与氮添加对杉木幼苗细根化学计量学的影响. 生态学杂志, 39, 723-732.]
[25]	Ju YL, Wang CK, Wang N, Quan XK (2022). Transplanting larch trees into warmer areas increases the photosynthesis and its temperature sensitivity. Tree Physiology, 42, 2521-2533. DOI PMID
[26]	Kramer-Walter KR, Laughlin DC (2017). Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation. Plant and Soil, 416, 539-550.
[27]	Li A, Guo DL, Wang ZQ, Liu HY (2010). Nitrogen and phosphorus allocation in leaves, twigs, and fine roots across 49 temperate, subtropical and tropical tree species: a hierarchical pattern. Functional Ecology, 24, 224-232.
[28]	Li H, Crabbe MJC, Xu F, Wang W, Ma L, Niu R, Gao X, Li X, Zhang P, Ma X, Chen H (2017). Seasonal variations in carbon, nitrogen and phosphorus concentrations and C:N:P stoichiometry in different organs of a Larix principis-rupprechtii Mayr. plantation in the Qinling Mountains, China. PLoS ONE, 12, e0185163. DOI: 10.1371/journal.pone.0185163.
[29]	Li M, Huang C, Yang T, Drosos M, Wang J, Kang X, Liu F, Xi B, Hu Z (2019). Role of plant species and soil phosphorus concentrations in determining phosphorus: nutrient stoichiometry in leaves and fine roots. Plant and Soil, 445, 231-242.
[30]	Li TA, Zhang ZH, Sun JK, Fu ZY, Zhao YH, Xu WJ (2022). Seasonal variation characteristics of C, N, and P stoichiometry and water use efficiency of Messerschmidia sibirica and its relationship with soil nutrients. Frontiers in Ecology and Evolution, 10, 948682. DOI: 10.1371/journal.pone.0185163.
[31]	Li X, Tan ND, Wu T, Cheng Y, Liu SZ, Fu SL, Li YY, Liu JX (2021). Plant growth and C:N:P stoichiometry characteristics in response to experimental warming in four co-occurring subtropical forest tree seedlings. Acta Ecologica Sinica, 41, 6146-6158.
	[李旭, 谭钠丹, 吴婷, 程严, 刘世忠, 傅松玲, 李义勇, 刘菊秀 (2021). 增温对南亚热带常绿阔叶林4种幼树生长和碳氮磷化学计量特征的影响. 生态学报, 41, 6146-6158.]
[32]	Li XX, Du TY, Wei YW, Zhou YB (2018). Characteristics of ecological stoichiometry in broad-leaved and Korean pine mixed forest and its response to latitude gradient in Northeast China. Acta Ecologica Sinica, 38, 3952-3960.
	[李喜霞, 杜天雨, 魏亚伟, 周永斌 (2018). 阔叶红松林生态化学计量学特征及其对纬度梯度的响应. 生态学报, 38, 3952-3960.]
[33]	Lin Y, Medlyn BE, Ellsworth DS (2012). Temperature responses of leaf net photosynthesis: the role of component processes. Tree Physiology, 32, 219-231.
[34]	Liu JX, Fang X, Tang XL, Wang WT, Zhou GY, Xu S, Huang WJ, Wang GX, Yan JH, Ma KP, Du S, Li SG, Han SJ, Ma YX (2019). Patterns and controlling factors of plant nitrogen and phosphorus stoichiometry across China’s forests. Biogeochemistry, 143, 191-205.
[35]	Liu MS, Wang CK, Quan XK (2022). Transcriptome analysis on responses of leaf photosynthesis and nitrogen metabolism of Larix gmelinii to environmental change. Chinese Journal of Applied Ecology, 33, 957-962.
	[刘梅朔, 王传宽, 全先奎 (2022). 兴安落叶松叶光合与氮代谢对环境变化响应的转录组分析. 应用生态学报, 33, 957-962.] DOI
[36]	Luo Y, Peng QW, Li KH, Gong YM, Liu YY, Han WX (2021). Patterns of nitrogen and phosphorus stoichiometry among leaf, stem and root of desert plants and responses to climate and soil factors in Xinjiang, China. Catena, 199, 105100. DOI: 10.1016/j.catena.2020.105100.
[37]	Ma YZ, Zhong QL, Jin BJ, Lu HD, Guo BQ, Zheng Y, Li M, Cheng DL (2015). Spatial changes and influencing factors of fine root carbon, nitrogen and phosphorus stoichiometry of plants in China. Chinese Journal of Plant Ecology, 39, 159-166.
	[马玉珠, 钟全林, 靳冰洁, 卢宏典, 郭炳桥, 郑媛, 李曼, 程栋梁 (2015). 中国植物细根碳、氮、磷化学计量学的空间变化及其影响因子. 植物生态学报, 39, 159-166.] DOI
[38]	McGroddy ME, Daufresne T, Hedin LO (2004). Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology, 85, 2390-2401.
[39]	Minden V, Kleyer M (2014). Internal and external regulation of plant organ stoichiometry. Plant Biology, 16, 897-907. DOI PMID
[40]	Pearse IS, McIntyre P, Cacho NI, Strauss SY (2022). Fitness homeostasis across an experimental water gradient predicts species’ geographic range and climatic breadth. Ecology, 103, e3827. DOI: 10.1002/ecy.3827
[41]	Quan XK, Wang CK (2018). Acclimation and adaptation of leaf photosynthesis, respiration and phenology to climate change: a 30-year Larix gmelinii common-garden experiment. Forest Ecology and Management, 411, 166-175.
[42]	Quan XK, Wang NN, Wang CK (2020). Thermal acclimation of leaf dark respiration of Larix gmelinii: a latitudinal transplant experiment. Science of the Total Environment, 743, 140634. DOI: 10.1016/j.scitotenv.2020.140634.
[43]	Rastetter EB, Kwiatkowski BL, Kicklighter DW, Barker Plotkin A, Genet H, Nippert JB, O’Keefe K, Perakis SS, Porder S, Roley SS, Ruess RW, Thompson JR, Wieder WR, Wilcox K, Yanai RD (2022). N and P constrain C in ecosystems under climate change: role of nutrient redistribution, accumulation, and stoichiometry. Ecological Applications, 32, e2684. DOI: 10.1002/eap.2684.
[44]	Reich PB, Oleksyn J (2004). Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences of the United States of America, 101, 11001-11006.
[45]	Ren SJ, Yu GR, Tao B, Guan LL, Fang HJ, Jiang CM (2009). Spatial patterns for variations in leaf nutrient contents of Dahurian larch (Larix gmelinii Rupr.). Acta Ecologica Sinica, 29, 1989-1996.
	[任书杰, 于贵瑞, 陶波, 官丽莉, 方华军, 姜春明 (2009). 兴安落叶松(Larix gmelinii Rupr.)叶片养分的空间分布格局. 生态学报, 29, 1989-1996.]
[46]	Rivas-Ubach A, Sardans J, Pérez-Trujillo M, Estiarte M, Peñuelas J (2012). Strong relationship between elemental stoichiometry and metabolome in plants. Proceedings of the National Academy of Sciences of the United States of America, 109, 4181-4186.
[47]	Sardans J, Rivas-Ubach A, Peñuelas J (2012). The C:N:P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspectives in Plant Ecology, Evolution and Systematics, 14, 33-47.
[48]	Shi WQ, Wang GA, Han WX (2012). Altitudinal variation in leaf nitrogen concentration on the eastern slope of Mount Gongga on the Tibetan Plateau, China. PLoS ONE, 7, e44628. DOI: 10.1371/journal.pone.0044628.
[49]	Sun Y, Wang C, Chen HYH, Luo X, Qiu N, Ruan H (2021). Asymmetric responses of terrestrial C:N:P stoichiometry to precipitation change. Global Ecology and Biogeography, 30, 1724-1735.
[50]	Tang Z, Xu W, Zhou G, Bai Y, Li J, Tang X, Chen D, Liu Q, Ma W, Xiong G, He H, He N, Guo Y, Guo Q, Zhu J, et al. (2018). Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China’s terrestrial ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 115, 4033-4038.
[51]	Tian D, Kattge J, Chen Y, Han W, Luo Y, He J, Hu H, Tang Z, Ma S, Yan Z, Lin Q, Schmid B, Fang J (2019). A global database of paired leaf nitrogen and phosphorus concentrations of terrestrial plants. Ecology, 100, e02812. DOI: 10.5167/uzh-180655.
[52]	Tian D, Yan ZB, Fang JY (2021). Review on characteristics and main hypotheses of plant ecological stoichiometry. Chinese Journal of Plant Ecology, 45, 682-713. DOI
	[田地, 严正兵, 方精云 (2021). 植物生态化学计量特征及其主要假说. 植物生态学报, 45, 682-713.] DOI
[53]	Tian D, Yan ZB, Niklas KJ, Han WX, Kattge J, Reich PB, Luo YK, Chen YH, Tang ZY, Hu HF, Wright IJ, Schmid B, Fang JY (2018). Global leaf nitrogen and phosphorus stoichiometry and their scaling exponent. National Science Review, 5, 728-739.
[54]	Tomlinson KW, Poorter L, Bongers F, Borghetti F, Jacobs L, van Langevelde F (2014). Relative growth rate variation of evergreen and deciduous savanna tree species is driven by different traits. Annals of Botany, 114, 315-324. DOI PMID
[55]	Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007). Controls over foliar N:P ratios in tropical rain forests. Ecology, 88, 107-118. DOI PMID
[56]	Wan LN (2019). The Response of Dark Respiration for Larix gmelinii Needles to Climate Warming. Master degree dissertation, Northeast Forestry University, Harbin. 13-14.
	[万丽娜 (2019). 纬度梯度移栽对兴安落叶松叶片暗呼吸的影响. 硕士学位论文, 东北林业大学, 哈尔滨. 13-14.]
[57]	Wang M, Murphy MT, Moore TR (2014). Nutrient resorption of two evergreen shrubs in response to long-term fertilization in a bog. Oecologia, 174, 365-377.
[58]	Wang RL, Wang QF, Zhao N, Yu GR, He NP (2017). Complex trait relationships between leaves and absorptive roots: coordination in tissue N concentration but divergence in morphology. Ecology and Evolution, 7, 2697-2705. DOI PMID
[59]	Xing W, Wu HP, Shi Q, Liu H, Liu GH (2015). Ecological stoichiometry theory: a review about applications and improvements. Ecological Science, 34, 190-197.
	[邢伟, 吴昊平, 史俏, 刘寒, 刘贵华 (2015). 生态化学计量学理论的应用、完善与扩展. 生态科学, 34, 190-197.]
[60]	Yan ZB, Li P, Chen YH, Han WX, Fang JY (2016). Nutrient allocation strategies of woody plants: an approach from the scaling of nitrogen and phosphorus between twig stems and leaves. Scientific Reports, 6, 20099. DOI: 10.1038/srep20099.
[61]	Yu Q, Wilcox K, La Pierre K, Knapp AK, Han X, Smith MD (2015). Stoichiometric homeostasis predicts plant species dominance, temporal stability, and responses to global change. Ecology, 96, 2328-2335. PMID
[62]	Yue K, Fornara DA, Yang W, Peng Y, Li Z, Wu F, Peng C (2017). Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis. Global Change Biology, 23, 2450-2463. DOI PMID
[63]	Zeng DH, Chen GS (2005). Ecological stoichiometry: a science to explore the complexity of living systems. Acta Phytoecologica Sinica, 29, 1007-1019.
	[曾德慧, 陈广生 (2005). 生态化学计量学: 复杂生命系统奥秘的探索. 植物生态学报, 29, 1007-1019.] DOI
[64]	Zhang L, Liu H, Zhang L, Chen Y, Baskin CC (2022). Effects of increased precipitation on C, N and P stoichiometry at different growth stages of a cold desert annual. Global Ecology and Conservation, 37, e02158. DOI: 10.1016/j.gecco.2022.e02158.
[65]	Zhang QF, Zhou JC, Li XJ, Yang ZJ, Zheng Y, Wang J, Lin WS, Xie JS, Chen Y, Yang YS (2019). Are the combined effects of warming and drought on foliar C:N:P:K stoichiometry in a subtropical forest greater than their individual effects? Forest Ecology and Management, 448, 256-266.
[66]	Zhao N, Yu GR, He NP, Xia FC, Wang QF, Wang RL, Xu ZW, Jia YL (2016). Invariant allometric scaling of nitrogen and phosphorus in leaves, stems, and fine roots of woody plants along an altitudinal gradient. Journal of Plant Research, 129, 647-657. DOI PMID
[67]	Zhou Y, Tang J, Melillo JM, Butler S, Mohan JE (2011). Root standing crop and chemistry after six years of soil warming in a temperate forest. Tree Physiology, 31, 707-717. DOI PMID