Changes in leaf nitrogen and phosphorus stoichiometry of woody plants along an altitudinal gradient in Changbai Mountain, China

doi:10.17521/cjpe.2017.0115

Abstract

Abstract:

Aims Leaf is the organ of plant photosynthesis, and it is important to understand the drivers for the variations of leaf nitrogen (N) and phosphorus (P) stoichiometry along geographical and climatic gradients. Here we aimed to explore: 1) the changes in leaf nitrogen (N) and phosphorus (P) stoichiometry of woody plants along an altitudinal gradient in Changbai Mountain, and 2) the relative contribution of climate, plant characteristics, and phylogeny to the changes in leaf N, P concentration and N:P.

Methods We measured leaf N and P concentration, and N:P of 48 woody species in 14 plots along an altitudinal gradient in Changbai Mountain. General linear models (GLMs) and variation partitioning analyses were used to explain leaf N and P stoichiometry with parameters related to plant functional groups, climate and phylogenetic groups.

Important findings Leaf N concentration and N:P decreased with altitude, and were positively correlated with mean annual temperature (MAT) but negatively correlated with mean annual precipitation (MAP). Leaf P concentration had no significant relationship with altitude. Leaf N, P concentration and N:P were significantly different among different plant functional groups. Leaf N concentration of shrubs was higher than that of trees, but leaf P concentration and N:P did not differ significantly between shrubs and trees. Leaf N, P concentration and N:P of broad-leaved plants were significantly higher than those of coniferous plants. Similarly, leaf N, P concentration and N:P of deciduous plants were significantly higher than those of evergreen plants. The effects of climate on leaf N, P concentration and N:P were significant but very weak, with MAT and MAP together explaining 1.50%-2.98% of the variations. Phylogenetic groups explained 30.36%-54.38% of the variations, suggesting the critical effect of phylogeny. Our study also showed that the synergistic effect of climate and species composition (phylogeny) on leaf N and P stoichiometry was neglectable, at least along the altitude gradient of Changbai Mountain. More comparative studies between altitudinal and latitudinal gradients are needed to better understand the drivers of the changes in leaf stoichiometry along an environmental gradient.

Key words: leaf stoichiometry, altitude gradient, climate, plant functional groups, phylogeny, woody plants

YANG Lei, SUN Han, FAN Yan-Wen, HAN Wei, ZENG Ling-Bing, LIU Chao, WANG Xiang-Ping. Changes in leaf nitrogen and phosphorus stoichiometry of woody plants along an altitudinal gradient in Changbai Mountain, China[J]. Chin J Plan Ecolo, 2017, 41(12): 1228-1238.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2017.0115

https://www.plant-ecology.com/EN/Y2017/V41/I12/1228

Figures/Tables 9

References 40

1	Aerts R, Champion FS (1999). The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns.Advances in Ecological Research, 30, 1-67. DOI URL
2	Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B (2006). Quantifying the evidence for biodiversity effects on ecosystem functioning and services.Ecology Letters, 9, 1146-1156. DOI URL
3	Chapin FS, Schulze ED, Mooney HA (1990). The ecology and economics of plants.Annual Review of Ecology & Systematics, 21, 423-447. DOI URL
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. DOI URL
5	Cordell S, Goldstein G, Meinzer FC, Vitousek PM (2001). Morphological and physiological adjustment to N and P fertilization in nutrient-limited Metrosideros polymorpha canopy trees in Hawaii.Tree Physiology, 21, 43-50. DOI URL PMID
6	Crawley MJ (2007). The R Book. Wiley Publishing. London.
7	Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003). Growth rate-stoichiometry couplings in diverse biota.Ecology Letters, 6, 936-943. DOI URL
8	Fan JW, Zhang LX, Zhang WY, Zhong HP (2014). The spatial pattern of plant nitrogen and phosphorus in relation to climate factors in Chinese grassland transect. Acta Agrestia Sinica, 22, 1-6.(in Chinese with English abstract) [樊江文, 张良侠, 张文彦, 钟华平 (2014). 中国草地样带植物氮磷元素空间格局及其与气候因子的关系. 草地学报, 22, 1-6.]
9	Fang JY (1992). Study on the geographic elements affecting temperature distribution in China.Acta Ecologica Sinica, 12, 97-104.(in Chinese with English abstract) [方精云 (1992). 地理要素对我国气温分布影响的数量评价. 生态学报, 12, 97-104.]
10	Fang JY, Wang XP, Shen ZH, Tang ZY, He JS, Yu D, Jiang Y, Wang ZH, Zheng CY, Zhu JL, Guo ZD (2009). Methods and protocols for plant community inventory.Biodiversity Science, 17, 533-548.(in Chinese with English abstract) [方精云, 王襄平, 沈泽昊, 唐志尧, 贺金生, 于丹, 江源, 王志恒, 郑成洋, 朱江玲, 郭兆迪 (2009). 植物群落清查的主要内容、方法和技术规范. 生物多样性, 17, 533-548.] DOI URL
11	Fisher JB, Malhi Y, Torres IC, Metcalfe DB, van de Weg MJ, Meir P, Silva-Espejo JE, Huasco WH (2013). Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes.Oecologia, 172, 889-902. DOI URL
12	Güsewell S (2004). N:P ratios in terrestrial plants: Variation and functional significance.New Phytologist, 164, 243-266. DOI URL
13	Han WX, Fang JY, Guo DL, Zhang Y (2005). Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China.New Phytologist, 168, 377-385. DOI URL
14	Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH (2011). Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China.Ecology Letters, 14, 788-796. DOI URL
15	He JS, Fang JY, Wang ZH, Guo DL, 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. DOI URL PMID
16	He JS, Han XG (2010). Ecological stoichiometry: Searching for unifying principles from individuals to ecosystem.Chinese Journal of Plant Ecology, 34, 2-6.(in Chinese with English abstract) [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.]
17	He JS, Wang L, Flynn DFB, Wang XP, Ma WH, Fang JY (2008). Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes.Oecologia, 155, 301-310. DOI URL PMID
18	He JS, Wang XP, Schmid B, Flynn DFB, Li XF, Reich PB, Fang JY (2010). Taxonomic identity, phylogeny, climate and soil fertility as drivers of leaf traits across Chinese grassland biomes.Journal of Plant Research, 123, 551-561. DOI URL
19	He JS, Wang XP, Flynn DFB, Wang L, Schmid B, Fang JY (2009). Taxonomic, phylogenetic, and environmental trade-offs between leaf productivity and persistence.Ecology, 90, 2779-2791. DOI URL PMID
20	Hedin LO (2004). Global organization of terrestrial plant- nutrient interactions.Proceedings of the National Academy of Sciences of the United States of America, 101, 10849-10850. DOI URL PMID
21	Kay AD, Ashton IW, Gorokhova E, Kerkhoff AJ, Liess A, Litchman E (2005). Toward a stoichiometric framework for evolutionary biology.Oikos, 109, 6-17. DOI URL
22	Koerselman W, Meuleman AFM (1996). The vegetation N:P: A new tool to detect the nature of nutrient limitation.Journal of Applied Ecology, 33, 1441-1450. DOI URL
23	K?rner C (1989). The nutritional status of plants from high altitudes.Oecologia, 81, 379-391. DOI URL
24	Liu C, Wang XP, Wu X, Dai S, He JS, Yin WL (2013). Relative effects of phylogeny, biological characters and environments on leaf traits in shrub biomes across central Inner Mongolia, China.Journal of Plant Ecology, 5, 220-231. DOI URL
25	Lovelock CE, Feller IC, Ball MC, Ellis J, Sorrell B (2007). Testing the growth rate vs. geochemical hypothesis for latitudinal variation in plant nutrients.Ecology Letters, 10, 1154-1163. DOI URL
26	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. DOI URL PMID
27	Ren SJ, Yu GR, Tao B, Wang SQ (2007). Leaf nitrogen and phosphorus stoichiometry across 654 terrestrial plant species in NSTEC.Chinese Journal of Environmental Science, 28, 2665-2673.(in Chinese with English abstract) [任书杰, 于贵瑞, 陶波, 王绍强 (2007). 中国东部南北样带654种植物叶片氮和磷的化学计量学特征研究. 环境科学, 28, 2665-2673.] DOI URL
28	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. DOI URL PMID
29	Smeck NE (1985). Phosphorus dynamics in soils and landscapes.Geoderma, 36, 185-199. DOI URL
30	Sun H, Wang XP, Fan YW, Liu C, Wu P, Li QY, Yin WL (2017). Effects of biophysical constraints, climate and phylogeny on forest shrub allometries along an altitudinal gradient in Northeast China.Scientific Reports, 7, 43769. doi: 10.1038/srep43769. DOI URL PMID
31	van de Weg MJ, Meir P, Grace J, Atkin OK (2009). Altitudinal variation in leaf mass per unit area, leaf tissue density and foliar nitrogen and phosphorus content along an Amazon-Andes gradient in Peru.Plant Ecology & Diversity, 2, 243-254.
32	Wang XP, Fang JY, Zhu B (2008). Forest biomass and root-shoot allocation in northeast China.Forest Ecology and Management, 255, 4007-4020. DOI URL
33	Wang Z, Xu ZB, Li X, Peng DS, Tan ZX (1980). The main forest types and their features of community structure in northern slope of Changbai Mountain.Research of Forest Ecosystem, 1, 1-8.(in Chinese with English abstract) [王战, 徐振邦, 李昕, 彭定山, 谭征详 (1980). 长白山北坡主要森林类型及其群落结构特点. 森林生态系统研究,1, 1-8.]
34	Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005). Modulation of leaf economic traits and trait relationships by climate.Global Ecology & Biogeography, 14, 411-421. DOI
35	Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004). The worldwide leaf economics spectrum.Nature, 428, 821-827. DOI URL
36	Wu TG, Chen BF, Xiao YH, Pan YJ, Chen Y, Xiao JH (2010). Leaf stoichiometry of trees in three forest types in Pearl River Delta, South China. Chinese Journal of Plant Ecology, 34, 58-63.(in Chinese with English abstract) [吴统贵, 陈步峰, 肖以华, 潘勇军, 陈勇, 萧江华 (2010). 珠江三角洲3种典型森林类型乔木叶片生态化学计量学. 植物生态学报, 34, 58-63.]
37	Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, Aarssen L, Bertin RI, Calaminus A, Govaerts R, Hemmings F, Leishman MR, Oleksyn J, Soltis PS, Swenson NG, Warman L, Beaulieu JM (2014). Three keys to the radiation of angiosperms into freezing environments.Nature, 506, 89-92. DOI URL
38	Zhao N, He NP, Wang QF, Zhang XY, Wang RL, Xu ZW, Yu GR (2014). The altitudinal patterns of leaf C:N:P stoichiometry are regulated by plant growth form, climate and soil on Changbai Mountain, China.PLOS ONE, 9, e95196. doi: 10.1371/journal.pone.0095196. DOI URL
39	Zhao SQ, Fang JY, Zong ZJ, Zhu B, Shen HH (2004). Composition, structure and species diversity of plant communities along an altitudinal gradient on the northern slope of Mt. Changbai, Northeast China.Biodiversity Science, 12, 164-173.(in Chinese with English abstract) [赵淑清, 方精云, 宗占江, 朱彪, 沈海花 (2004). 长白山北坡植物群落组成、结构及物种多样性的垂直分布. 生物多样性, 12, 164-173.] DOI URL
40	Zhu B, Wang XP, Fang JY, Piao SL, Shen HH, Zhao SQ, Peng CH (2010). Altitudinal changes in carbon storage of temperate forests on Mt. Changbai, Northeast China.Journal of Plant Research, 123, 439-452. DOI URL PMID

叶性状 Leaf trait	功能群 Functional group		样本量 n	平均值 Mean	最大值 Max	最小值 Min	标准偏差 SD	标准误差 SE	变异系数 CV
氮含量 N concentration (g·kg^-1)	全部样品 All samples		431	21.46	37.90	5.10	6.75	0.33	0.31
	生活型 Life form	乔木 Tree	240	20.74^b	37.90	5.10	6.80	0.44	0.33
	生活型 Life form	灌木 Shrub	191	22.37^a	37.40	6.80	6.59	0.48	0.29
	叶型 Leaf shape	针叶 Coniferous	89	15.50^b	36.80	8.50	4.91	0.52	0.32
	叶型 Leaf shape	阔叶 Broad-leaved	342	23.02^a	37.90	5.10	6.29	0.34	0.27
	叶片习性 Leaf habit	常绿 Evergreen	87	14.49^b	35.00	8.44	4.42	0.47	0.31
	叶片习性 Leaf habit	落叶 Deciduous	344	23.23^a	37.90	5.10	6.06	0.33	0.26
磷含量 P concentration (g·kg^-1)	全部样品 All samples		431	2.23	6.75	0.66	0.87	0.04	0.39
	生活型 Life form	乔木 Tree	240	2.22	6.75	0.66	0.93	0.06	0.42
	生活型 Life form	灌木 Shrub	191	2.25	5.29	0.77	0.80	0.06	0.35
	叶型 Leaf shape	针叶 Coniferous	89	1.91^b	4.13	0.66	0.77	0.08	0.40
	叶型 Leaf shape	阔叶 Broad-leaved	342	2.32^a	6.75	0.77	0.88	0.05	0.38
	叶片习性 Leaf habit	常绿 Evergreen	87	1.74^b	3.30	0.66	0.66	0.07	0.38
	叶片习性 Leaf habit	落叶 Deciduous	344	2.36^a	6.75	0.99	0.87	0.05	0.37
N:P	全部样品 All samples		431	10.81	33.70	2.47	4.77	0.23	0.44
	生活型 Life form	乔木 Tree	240	10.60	33.70	2.47	4.89	0.32	0.46
	生活型 Life form	灌木 Shrub	191	11.07	26.34	3.12	4.62	0.33	0.42
	叶型 Leaf shape	针叶 Coniferous	89	9.35^b	25.92	3.90	4.68	0.50	0.50
	叶型 Leaf shape	阔叶 Broad-leaved	342	11.19^a	33.70	2.47	4.72	0.26	0.42
	叶片习性 Leaf habit	常绿 Evergreen	87	9.75^b	25.92	3.28	4.93	0.53	0.51
	叶片习性 Leaf habit	落叶 Deciduous	344	11.08^a	33.70	2.47	4.70	0.25	0.42

叶性状 Leaf trait	功能群 Functional group		样本量 n	平均值 Mean	最大值 Max	最小值 Min	标准偏差 SD	标准误差 SE	变异系数 CV
氮含量 N concentration (g·kg^-1)	全部样品 All samples		431	21.46	37.90	5.10	6.75	0.33	0.31
	生活型 Life form	乔木 Tree	240	20.74^b	37.90	5.10	6.80	0.44	0.33
	生活型 Life form	灌木 Shrub	191	22.37^a	37.40	6.80	6.59	0.48	0.29
	叶型 Leaf shape	针叶 Coniferous	89	15.50^b	36.80	8.50	4.91	0.52	0.32
	叶型 Leaf shape	阔叶 Broad-leaved	342	23.02^a	37.90	5.10	6.29	0.34	0.27
	叶片习性 Leaf habit	常绿 Evergreen	87	14.49^b	35.00	8.44	4.42	0.47	0.31
	叶片习性 Leaf habit	落叶 Deciduous	344	23.23^a	37.90	5.10	6.06	0.33	0.26
磷含量 P concentration (g·kg^-1)	全部样品 All samples		431	2.23	6.75	0.66	0.87	0.04	0.39
	生活型 Life form	乔木 Tree	240	2.22	6.75	0.66	0.93	0.06	0.42
	生活型 Life form	灌木 Shrub	191	2.25	5.29	0.77	0.80	0.06	0.35
	叶型 Leaf shape	针叶 Coniferous	89	1.91^b	4.13	0.66	0.77	0.08	0.40
	叶型 Leaf shape	阔叶 Broad-leaved	342	2.32^a	6.75	0.77	0.88	0.05	0.38
	叶片习性 Leaf habit	常绿 Evergreen	87	1.74^b	3.30	0.66	0.66	0.07	0.38
	叶片习性 Leaf habit	落叶 Deciduous	344	2.36^a	6.75	0.99	0.87	0.05	0.37
N:P	全部样品 All samples		431	10.81	33.70	2.47	4.77	0.23	0.44
	生活型 Life form	乔木 Tree	240	10.60	33.70	2.47	4.89	0.32	0.46
	生活型 Life form	灌木 Shrub	191	11.07	26.34	3.12	4.62	0.33	0.42
	叶型 Leaf shape	针叶 Coniferous	89	9.35^b	25.92	3.90	4.68	0.50	0.50
	叶型 Leaf shape	阔叶 Broad-leaved	342	11.19^a	33.70	2.47	4.72	0.26	0.42
	叶片习性 Leaf habit	常绿 Evergreen	87	9.75^b	25.92	3.28	4.93	0.53	0.51
	叶片习性 Leaf habit	落叶 Deciduous	344	11.08^a	33.70	2.47	4.70	0.25	0.42

叶性状 Leaf traits		年平均气温 Mean annual temperature	年降水量 Mean annual precipitation	生活型 Life form	叶型 Leaf shape	叶片习性 Leaf habit	90 Mya谱系组 90 Mya division	60 Mya谱系组 60 Mya division	物种 Species
氮含量 N concentration	R²	0.012	0.012	0.016	0.229	0.324	0.415	0.459	0.536
氮含量 N concentration	p	0.023^*	0.025^*	0.008^**	0.000^***	0.000^***	0.000^***	0.000^***	0.000^***
磷含量 P concentration	R²	0.003	0.003	0.002	0.049	0.115	0.216	0.306	0.391
磷含量 P concentration	p	0.233	0.247	0.342	0.000^***	0.000^***	0.000^***	0.000^***	0.000^***
N:P	R²	0.016	0.016	0.003	0.028	0.018	0.152	0.215	0.303
N:P	p	0.008^**	0.009^**	0.257	0.000^***	0.005^**	0.000^***	0.000^***	0.000^***

叶性状 Leaf traits		年平均气温 Mean annual temperature	年降水量 Mean annual precipitation	生活型 Life form	叶型 Leaf shape	叶片习性 Leaf habit	90 Mya谱系组 90 Mya division	60 Mya谱系组 60 Mya division	物种 Species
氮含量 N concentration	R²	0.012	0.012	0.016	0.229	0.324	0.415	0.459	0.536
氮含量 N concentration	p	0.023^*	0.025^*	0.008^**	0.000^***	0.000^***	0.000^***	0.000^***	0.000^***
磷含量 P concentration	R²	0.003	0.003	0.002	0.049	0.115	0.216	0.306	0.391
磷含量 P concentration	p	0.233	0.247	0.342	0.000^***	0.000^***	0.000^***	0.000^***	0.000^***
N:P	R²	0.016	0.016	0.003	0.028	0.018	0.152	0.215	0.303
N:P	p	0.008^**	0.009^**	0.257	0.000^***	0.005^**	0.000^***	0.000^***	0.000^***

	N			P			N:P
	df	%SS	p	df	%SS	p	df	%SS	p
气候 Climate
年平均气温 Mean annual temperature	1	1.21	0.001^**	1	0.33	0.146	1	1.65	0.002^**
年降水量 Mean annual precipitation	1	0.61	0.022^*	1	0.45	0.089	1	1.28	0.007^**
植物功能型 Plant functional groups
生活型 Life form	1	1.54	0.000^***	1	0.22	0.237	1	0.27	0.214
叶型 Leaf shape	1	22.60	0.000^***	1	5.70	0.000^***	1	2.24	0.000^***
叶片习性 Leaf habit	1	9.34	0.000^***	1	6.46	0.000^***	1	0.02	0.767
谱系 Phylogeny
90 Mya谱系组 90 Mya division	18	12.06	0.000^***	18	13.03	0.000^***	18	13.18	0.000^***
60 Mya谱系组 60 Mya division	10	3.82	0.000^***	10	8.10	0.000^***	10	7.34	0.000^***
物种 Species	17	5.01	0.000^***	17	6.33	0.002^**	17	7.32	0.001^**
残差 Residuals	380	43.81		380	59.36		380	66.72