阔叶红松林3种典型蕨类叶功能性状的垂直变异

doi:10.17521/cjpe.2022.0423

摘要/Abstract

摘要：

研究蕨类在不同垂直高度下叶功能性状及其相关关系的差异, 可为揭示大型蕨类叶片的资源利用策略提供科学依据。以阔叶红松(Pinus koraiensis)林内的粗茎鳞毛蕨(Dryopteris crassirhizoma)、东北蹄盖蕨(Athyrium brevifrons)和荚果蕨(Matteuccia struthiopteris) 3种蕨类为研究对象, 将个体按叶片垂直高度分为上、中、下3层, 分别测定其比叶面积、叶干物质含量、净光合速率、瞬时水分利用效率、叶氮含量和叶磷含量, 并测定每株个体的光环境和土壤因子, 重点揭示叶功能性状的垂直变异规律及相关关系。结果表明: (1) 3种蕨类叶干物质含量随叶片垂直高度增加均呈递增趋势, 比叶面积无显著差异; 东北蹄盖蕨和荚果蕨净光合速率随叶片垂直高度增加呈递增趋势; 荚果蕨瞬时水分利用效率随叶片垂直高度增加先增后减, 叶氮含量逐渐减少; 粗茎鳞毛蕨叶磷含量随叶片垂直高度增加表现为先增后减。(2)叶氮含量与比叶面积, 瞬时水分利用效率与净光合速率显著正相关; 叶氮含量与叶干物质含量, 叶干物质含量与比叶面积则显著负相关; 上述叶功能性状间的相关关系在不同垂直高度间均无显著差异。(3)土壤有效磷含量和土壤pH是不同垂直高度叶功能性状变异的主要影响因子, 土壤有效磷含量对叶功能性状变异的解释度最高。该研究表明, 阔叶红松林内大型蕨类的叶功能性状存在一定的垂直差异, 然而个体内部性状间的变化速率基本恒定, 光环境和土壤因子对不同垂直高度叶功能性状变异的影响程度不同。

关键词: 叶功能性状, 蕨类, 垂直高度, 相关关系, 环境因子

Abstract:

Aims Understanding the differences in leaf functional traits and their correlations in ferns at different vertical heights can provide a scientific basis for revealing the resource utilization strategies of large fern fronds.

Methods Individuals of three fern species in a mixed broadleaved-Korean pine (Pinus koraiensis) forest, i.e., Dryopteris crassirhizoma, Athyrium brevifrons and Matteuccia struthiopteris were divided into upper, middle, and lower layers according to the vertical height of leaves. We measured specific leaf area, leaf dry matter content, net photosynthetic rate, instantaneous water use efficiency, leaf nitrogen content and leaf phosphorus content, as well as the light environment and soil factors of each individual plant to reveal the vertical variation patterns and correlations of leaf functional traits.

Important findings (1) Leaf dry matter content of the three fern species increased with the vertical height of the fronds, but specific leaf area showed no variation. The net photosynthetic rate of A. brevifrons and M. struthiopteris showed an increasing trend with the increases of vertical height of fronds, the instantaneous water use efficiency of M. struthiopteris increased and then decreased with the vertical height of the fronds, and leaf nitrogen content gradually decreased; leaf phosphorus content of D. crassirhizoma showed an increase and then decreased trend. (2) There were positive correlations between leaf nitrogen content and specific leaf area, and also between instantaneous water use efficiency and net photosynthetic rate. There were negative correlations between leaf nitrogen content and leaf dry matter content, and between leaf dry matter content and specific leaf area. The correlations among those leaf functional traits did not differ significantly among different vertical heights. (3) Soil available phosphorus content and soil pH were the main factors affecting the variation of leaf functional traits at different vertical heights, with soil available phosphorus content having the highest explanatory degree to the variation of leaf functional traits. Our results indicated that there were vertical differences in leaf functional traits of large ferns in the mixed broadleaved-Korean pine forest, but the rate of change among individual characters was basically constant, the effects of light environment and soil factors on the variation of leaf functional traits differed among vertical heights. This study provided reference for further research on the mechanism of leaf functional traits variation in different vertical heights of ferns in understory.

Key words: leaf functional trait, fern, vertical height, correlation, environmental factor

赵孟娟, 金光泽, 刘志理. 阔叶红松林3种典型蕨类叶功能性状的垂直变异. 植物生态学报, 2023, 47(8): 1131-1143. DOI: 10.17521/cjpe.2022.0423

ZHAO Meng-Juan, JIN Guang-Ze, LIU Zhi-Li. Vertical variations in leaf functional traits of three typical ferns in mixed broadleaved- Korean pine forest. Chinese Journal of Plant Ecology, 2023, 47(8): 1131-1143. DOI: 10.17521/cjpe.2022.0423

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0423

https://www.plant-ecology.com/CN/Y2023/V47/I8/1131

图/表 6

图1 阔叶红松林3种典型蕨类。L,下层; M, 中层; U, 上层。

Fig. 1 Three typical ferns in mixed broadleaved-Korean pine forest. L, lower layer; M, middle layer; U, upper layer. AN, available nitrogen; AP, available phosphorus; SWC, soil water content; TN, total nitrogen; TP, total phosphorus.

表1 3种蕨类所处生境的环境因子概况(平均值±标准误)

Table 1 Profile of environmental factors in the habitats of the three ferns (mean ± SE)

环境因子 Environmental factor	粗茎鳞毛蕨 Dryopteris crassirhizoma	东北蹄盖蕨 Athyrium brevifrons	荚果蕨 Matteuccia struthiopteris
冠层开放度 Canopy openness (%)	24.29 ± 1.04^a	24.90 ± 0.66^a	23.68 ± 2.45^a
土壤水分含量 Soil water content	0.90 ± 0.09^a	0.87 ± 0.17^a	0.99 ± 0.12^a
土壤全氮含量 Soil total nitrogen content (mg·g^-1)	9.32 ± 0.74^a	6.57 ± 0.91^b	9.06 ± 0.64^ab
土壤全磷含量 Soil total phosphorus content (mg·g^-1)	0.82 ± 0.08^a	0.89 ± 0.16^a	0.88 ± 0.10^a
土壤pH Soil pH	5.67 ± 0.11^ab	5.31 ± 0.10^b	5.76 ± 0.11^a
土壤有效氮含量 Soil available nitrogen content (mg·g^-1)	0.59 ± 0.05^a	0.50 ± 0.06^a	0.59 ± 0.03^a
土壤有效磷含量 Soil available phosphorus content (mg·g^-1)	0.02 ± 0.00^a	0.01 ± 0.00^a	0.02 ± 0.00^a

图2 阔叶红松林3种典型蕨类叶功能性状的垂直变异。A.bre, 东北蹄盖蕨; D.cra, 粗茎鳞毛蕨; M.str, 荚果蕨。LDMC, 叶干物质含量; LNC, 叶氮含量; LPC, 叶磷含量; Pn, 净光合速率; SLA, 比叶面积; WUEi, 瞬时水分利用效率。不同大写字母表示种间差异显著(p < 0.05), 不同小写字母表示种内差异显著(p < 0.05)。黑色虚线为平均值。

Fig. 2 Differences in leaf functional traits of three typical ferns in mixed broadleaved-Korean pine forest. A.bre, Athyrium brevifrons; D.cra, Dryopteris crassirhizoma; M.str, Matteuccia struthiopteris. LDMC, leaf dry matter content; LNC, leaf nitrogen content; LPC, leaf phosphorus content; Pn, leaf net photosynthetic rate; SLA, specific leaf area; WUEi, instantaneous water use efficiency. Different uppercase letters indicate significant differences between species (p < 0.05), and different lowercase letters indicate significant intraspecific differences (p < 0.05). The black dashed line represents the average value.

图3 阔叶红松林3种典型蕨类不同垂直高度叶功能性状的相关性。Corr, 相关系数; L, 下层; M, 中层; U, 上层。A, 净光合速率; LDMC, 叶干物质含量; LNC, 叶氮含量; LPC, 叶磷含量; SLA, 比叶面积; WUEi, 瞬时水分利用效率。*, p < 0.05; **, p < 0.01; ***, p < 0.001。

Fig. 3 Correlation of leaf functional traits at different vertical heights in three typical ferns in mixed broadleaved-Korean pine forest. Corr, correlation coefficient; L, lower layer; M, middle layer; U, upper layer. A, leaf net photosynthetic rate; LDMC, leaf dry matter content; LNC, leaf nitrogen content; LPC, leaf phosphorus content; SLA, specific leaf area; WUEi, instantaneous water use efficiency. *, p < 0.05; **, p < 0.01; ***, p < 0.001.

图4 阔叶红松林3种典型蕨类的叶功能性状相关关系在不同高度间的差异。A, 净光合速率; LDMC, 叶干物质含量; LNC, 叶氮含量; LPC, 叶磷含量; SLA, 比叶面积; WUEi, 瞬时水分利用效率。Common slope, 共同斜率; Slope, 斜率。图中彩色实线表示性状间相关关系显著, 黑色实线表示3条实线重合。

Fig. 4 Differences in leaf trait correlations among different heights for three typical ferns in mixed broadleaved-Korean pine forest. A, leaf net photosynthetic rate; LDMC, leaf dry matter content; LNC, leaf nitrogen content; LPC, leaf phosphorus content; SLA, specific leaf area; WUEi, instantaneous water use efficiency. The colored solid lines in the figure indicate that the correlations between traits were significant, the black solid line indicates that the three solid lines overlap.

图5 阔叶红松林3种典型蕨类不同垂直高度下叶功能性状与环境因子的冗余分析(RDA)排序。A, 上层。B, 中层。C, 下层。A, 净光合速率; AN, 土壤有效氮含量; AP, 土壤有效磷含量; CO, 冠层开放度; LDMC, 叶干物质含量; LNC, 叶氮含量; LPC, 叶磷含量; pH, 土壤pH; SLA, 比叶面积; SWC, 土壤水分含量; TN, 土壤全氮含量; TP, 土壤全磷含量; WUEi, 瞬时水分利用效率。

Fig. 5 Redundancy analysis (RDA) ranking of leaf functional traits and environmental factors in three typical ferns in mixed broadleaved-Korean pine forest. A, Lower layer; B, Middle layer; C, Upper layer. A, leaf net photosynthetic rate; AN, soil available nitrogen content; AP, soil available phosphorus content; CO, canopy openness; LDMC, leaf dry matter content; LNC, leaf nitrogen content; LPC, leaf phosphorus content; pH, soil pH; SLA, specific leaf area; SWC, soil water content; TN, soil total nitrogen content; TP, soil total phosphorus content; WUEi, instantaneous water use efficiency.

参考文献 73

[1]	Allison VJ (2002). Nutrients, arbuscular mycorrhizas and competition interact to influence seed production and germination success in Achillea millefolium. Functional Ecology, 16, 742-749. DOI URL
[2]	Asner GP, Martin RE, Anderson CB, Kryston K, Vaughn N, Knapp DE, Bentley LP, Shenkin A, Salinas N, Sinca F, Tupayachi R, Quispe Huaypar K, Montoya Pillco M, Delis Ccori Álvarez F, Díaz S, et al. (2017). Scale dependence of canopy trait distributions along a tropical forest elevation gradient. New Phytologist, 214, 973-988. DOI PMID
[3]	Brock JMR, Perry GLW, Burkhardt T, Burns BR (2018). Forest seedling community response to understorey filtering by tree ferns. Journal of Vegetation Science, 29, 887-897. DOI URL
[4]	Bucher SF, Auerswald K, Grün-Wenzel C, Higgins SI, Römermann C (2021). Abiotic site conditions affect photosynthesis rates by changing leaf functional traits. Basic and Applied Ecology, 57, 54-64. DOI URL
[5]	Burton JI, Perakis SS, McKenzie SC, Lawrence CE, Puettmann KJ (2017). Intraspecific variability and reaction norms of forest understorey plant species traits. Functional Ecology, 31, 1881-1893. DOI URL
[6]	Cheng X, Ping T, Li Z, Wang T, Han H, Epstein HE (2022). Effects of environmental factors on plant functional traits across different plant life forms in a temperate forest ecosystem. New Forests, 53, 125-142. DOI
[7]	Cicuzza D, Mammides C (2022). Soil, topography and forest structure shape the abundance, richness and composition of fern species in the fragmented tropical landscape of Xishuangbanna, Yunnan, China. Forests, 13, 1453. DOI: 10.3390/f13091453.
[8]	Coble AP, Cavaleri MA (2017). Vertical leaf mass per area gradient of mature sugar maple reflects both height-driven increases in vascular tissue and light-driven increases in palisade layer thickness. Tree Physiology, 37, 1337-1351. DOI PMID
[9]	Coble AP, Fogel ML, Parker GG (2017). Canopy gradients in leaf functional traits for species that differ in growth strategies and shade tolerance. Tree Physiology, 37, 1415-1425. DOI PMID
[10]	Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003). A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany, 51, 335-380. DOI URL
[11]	Cornwell WK, Wright IJ, Turner J, Maire V, Barbour MM, Cernusak LA, Dawson T, Ellsworth D, Farquhar GD, Griffiths H, Keitel C, Knohl A, Reich PB, Williams DG, Bhaskar R, et al. (2018). Climate and soils together regulate photosynthetic carbon isotope discrimination within C₃ plants worldwide. Global Ecology and Biogeography, 27, 1056-1067. DOI URL
[12]	de la Riva EG, Tosto A, Pérez-Ramos IM, Navarro-Fernández CM, Olmo M, Anten NPR, Marañón T, Villar R (2016). A plant economics spectrum in Mediterranean forests along environmental gradients: Is there coordination among leaf, stem and root traits? Journal of Vegetation Science, 27, 187-199. DOI URL
[13]	Delpiano CA, Prieto I, Loayza AP, Carvajal DE, Squeo FA (2020). Different responses of leaf and root traits to changes in soil nutrient availability do not converge into a community-level plant economics spectrum. Plant and Soil, 450, 463-478. DOI
[14]	Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Colin Prentice I, Garnier E, Bönisch G, Westoby M, Poorter H,Reich PB, et al. (2016). The global spectrum of plant form and function. Nature, 529, 167-171. DOI
[15]	Digrado A, Mitchell NG, Montes CM, Dirvanskyte P, Ainsworth EA (2020). Assessing diversity in canopy architecture, photosynthesis, and water-use efficiency in a cowpea magic population. Food and Energy Security, 9, e236. DOI: 10.1002/fes3.236. PMID
[16]	Ewers RM, Banks-Leite C (2013). Fragmentation impairs the microclimate buffering effect of tropical forests. PLoS ONE, 8, e58093. DOI: 10.1371/journal.pone.0058093.
[17]	Funk JL, Larson JE, Vose G (2021). Leaf traits and performance vary with plant age and water availability in Artemisia californica. Annals of Botany, 127, 495-503. DOI URL
[18]	Guo Y, Yan Z, Gheyret G, Zhou G, Xie Z, Tang Z (2020). The community-level scaling relationship between leaf nitrogen and phosphorus changes with plant growth, climate and nutrient limitation. Journal of Ecology, 108, 1276-1286. DOI URL
[19]	Han LD, Wo XT, Liu YK (2022). Analysis of photosynthetic characteristics of Pinus koraiensis with different slope orientations. Forestry Science & Technology, 47(5), 41-43.
	[韩丽冬, 沃晓棠, 刘延坤 (2022). 不同坡向红松光合特性分析. 林业科技, 47(5), 41-43.]
[20]	Jenny H (1941). Factors of Soil Formation. McGrawHill Book Company, New York.
[21]	Jiang F, Xun YH, Cai HY, Jin GZ (2017). Coordination and determinants of leaf community economics spectrum for canopy trees and shrubs in a temperate forest in northeastern China. Forests, 8, 202. DOI: 10.3390/f8060202.
[22]	Jin DM, Zhou XL, Schneider H, Wei HJ, Wei HY, Yan YH (2021). Functional traits: adaption of ferns in forest. Journal of Systematics and Evolution, 59, 1040-1050. DOI
[23]	Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrison SP, van Bodegom PM, Reichstein M, et al. (2011). TRY—A global database of plant traits. Global Change Biology, 17, 2905-2935.
[24]	Khan A, Yan L, Mahadi Hasan M, Wang W, Xu K, Zou G, Liu XD, Fang XW (2022). Leaf traits and leaf nitrogen shift photosynthesis adaptive strategies among functional groups and diverse biomes. Ecological Indicators, 141, 109098. DOI: 10.1016/j.ecolind.2022.109098.
[25]	Le Roux X, Walcroft AS, Daudet FA, Sinoquet H, Chaves MM, Rodrigues A, Osorio L (2001). Photosynthetic light acclimation in peach leaves: importance of changes in mass:area ratio, nitrogen concentration, and leaf nitrogen partitioning. Tree Physiology, 21, 377-386. DOI PMID
[26]	Leal DB, Thomas SC (2003). Vertical gradients and tree-to-tree variation in shoot morphology and foliar nitrogen in an old-growth Pinus strobus stand. Canadian Journal of Forest Research, 33, 1304-1314. DOI URL
[27]	Lehtonen S, Silvestro D, Karger DN, Scotese C, Tuomisto H, Kessler M, Peña C, Wahlberg N, Antonelli A (2017). Environmentally driven extinction and opportunistic origination explain fern diversification patterns. Scientific Reports, 7, 4831. DOI: 10.1038/s41598-017-05263-7. PMID
[28]	Li H, Yang H, Xie R (2021). Canopy characteristics in gaps and its relationship with seedlings and saplings in a spruce-fir forest in the Changbai Mountain area of northeastern China. Journal of Beijing Forestry University, 43(7), 54-62.
	[李晖, 杨华, 谢榕 (2021). 长白山云冷杉林林隙冠层特征及与幼苗幼树的关系. 北京林业大学学报, 43(7), 54-62.]
[29]	Li J, Chen X, Wu P, Niklas KJ, Lu Y, Zhong Q, Hu D, Cheng L, Cheng D (2022). The fern economics spectrum is unaffected by the environment. Plant, Cell & Environment, 45, 3205-3218.
[30]	Li YP, Ni YL, Xu H, Lian JY, Ye WH (2021). Relationship between variation of plant functional traits and individual growth at different vertical layers in a subtropical evergreen broad-leaved forest of Dinghushan. Biodiversity Science, 29, 1186-1197. DOI URL
	[李艳朋, 倪云龙, 许涵, 练琚愉, 叶万辉 (2021). 鼎湖山南亚热带常绿阔叶林植物功能性状变异与不同垂直层次个体生长的关联. 生物多样性, 29, 1186-1197.] DOI
[31]	Lin D, Yang S, Dou P, Wang H, Wang F, Qian S, Yang G, Zhao L, Yang Y, Fanin N (2020). A plant economics spectrum of litter decomposition among coexisting fern species in a sub-tropical forest. Annals of Botany, 125, 145-155. DOI PMID
[32]	Liu GF, Liu YP, Baiyila DF, Cheng WY, Gao XL, Jiang LL (2017). Leaf traits of dominant plants of main forest communities in Daqinggou Nature Reserve. Acta Ecologica Sinica, 37, 4646-4655.
	[刘贵峰, 刘玉平, 达福白乙拉, 程伟燕, 高学磊, 姜丽丽 (2017). 大青沟自然保护区主要森林群落优势种的叶性状. 生态学报, 37, 4646-4655.]
[33]	Liu MX, Liang GL (2016). Research progress on leaf mass per area. Chinese Journal of Plant Ecology, 40, 847-860. DOI URL
	[刘明秀, 梁国鲁 (2016). 植物比叶质量研究进展. 植物生态学报, 40, 847-860.] DOI
[34]	Liu XJ, Ma KP (2015). Plant functional traits—Concepts, applications and future directions. Scientia Sinica (Vitae), 45, 325-339.
	[刘晓娟, 马克平 (2015). 植物功能性状研究进展. 中国科学: 生命科学, 45, 325-339.]
[35]	Lovelock CE, Feller IC, McKee KL, Engelbrecht BMJ, Ball MC (2004). The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panamá. Functional Ecology, 18, 25-33. DOI URL
[36]	Lu YM (2021). Study on Functional Traits of Ferns from Different Habitats in Wuyi Mountain. Master degree dissertation, Fujian Normal University, Fuzhou. 1-101.
	[卢艺苗 (2021). 武夷山不同生境蕨类植物功能性状研究. 硕士学位论文, 福建师范大学, 福州. 1-101.]
[37]	Luo D, Shi YJ, Song FH, Li JC (2021). Variation and correlation of leaf functional traits and photosynthetic characteristics of 38 hazelnut germplasm resources. Chinese Journal of Ecology, 40, 11-22.
	[罗达, 史彦江, 宋锋惠, 李嘉诚 (2021). 38个榛种质资源叶功能性状与光合特征变异及其相关性. 生态学杂志, 40, 11-22.]
[38]	Luo T, Yu FY, Lian JY, Wang JJ, Shen J, Wu ZF, Ye WH (2022). Impact of canopy vertical height on leaf functional traits in a lower subtropical evergreen broad-leaved forest of Dinghushan. Biodiversity Science, 30, 21414. DOI: 10.17520/biods.2021414.
	[罗恬, 俞方圆, 练琚愉, 王俊杰, 申健, 吴志峰, 叶万辉 (2022). 冠层垂直高度对植物叶片功能性状的影响: 以鼎湖山南亚热带常绿阔叶林为例. 生物多样性, 30, 21414. DOI: 10.17520/biods.2021414.]
[39]	Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, van Bodegom PM, Cornwell WK, Ellsworth D, Niinemets Ü, Ordonez A, Reich PB, Santiago LS (2015). Global effects of soil and climate on leaf photosynthetic traits and rates. Global Ecology and Biogeography, 24, 706-717. DOI URL
[40]	Martin AR, Isaac ME (2021). The leaf economics spectrum’s morning coffee: plant size-dependent changes in leaf traits and reproductive onset in a perennial tree crop. Annals of Botany, 127, 483-493. DOI PMID
[41]	Meng TT, Ni J, Wang GH (2007). Plant functional traits, environments and ecosystem functioning. Journal of Plant Ecology (Chinese Version), 31, 150-165.
	[孟婷婷, 倪健, 王国宏 (2007). 植物功能性状与环境和生态系统功能. 植物生态学报, 31, 150-165.] DOI
[42]	Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang Z, Schneider H, Donoghue PCJ (2018). The timescale of early land plant evolution. Proceedings of The National Academy of Sciences of the United States of America, 115, E2274-E2283.
[43]	Ordoñez JC, van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R (2009). A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Global Ecology and Biogeography, 18, 137-149. DOI URL
[44]	Osada N, Hiura T (2017). How is light interception efficiency related to shoot structure in tall canopy species? Oecologia, 185, 29-41. DOI PMID
[45]	Pierangelini M, Stojkovic S, Orr PT, Beardall J (2014). Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. Journal of Phycology, 50, 292-302. DOI PMID
[46]	Poorter H, Pepin S, Rijkers T, de Jong Y, Evans JR, Körner C (2006). Construction costs, chemical composition and payback time of high- and low-irradiance leaves. Journal of Experimental Botany, 57, 355-371. PMID
[47]	Prior LD, Eamus D, Bowman DMJS (2003). Leaf attributes in the seasonally dry tropics a comparison of four habitats in northern Australia. Functional Ecology, 17, 504-515. DOI URL
[48]	Reich PB, Walters MB, Ellsworth DS (1997). From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences of the United States of America, 94, 13730-13734. PMID
[49]	Roche P, Díaz-Burlinson N, Gachet S (2004). Congruency analysis of species ranking based on leaf traits: Which traits are the more reliable? Plant Ecology, 174, 37-48. DOI URL
[50]	Royer DL, Miller IM, Peppe DJ, Hickey LJ (2010). Leaf economic traits from fossils support a weedy habit for early angiosperms. American Journal of Botany, 97, 438-445. DOI PMID
[51]	Santiago LS, Schuur EAG, Silvera K (2005). Nutrient cycling and plant-soil feedbacks along a precipitation gradient in lowland Panama. Journal of Tropical Ecology, 21, 461-470. DOI URL
[52]	Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011). Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiology, 156, 832-843. DOI PMID
[53]	Smith DL, Johnson L (2004). Vegetation-mediated changes in microclimate reduce soil respiration as woodlands expand into grasslands. Ecology, 85, 3348-3361. DOI URL
[54]	Song J, Li RH, Zhu SD, Ye Q (2013). Leaf functional traits of ferns from different habitats in monsoon evergreen broad-leaved forest in Dinghushan Mountain. Journal of Tropical and Subtropical Botany, 21, 489-495.
	[宋娟, 李荣华, 朱师丹, 叶清 (2013). 鼎湖山季风常绿阔叶林不同生境蕨类植物的叶片功能性状研究. 热带亚热带植物学报, 21, 489-495.]
[55]	Tian JX, Wei LP, He NP, Xu L, Chen Z, Hou JH (2018). Vertical variation of leaf functional traits in temperate forest canopies in China. Acta Ecologica Sinica, 38, 8383-8391.
	[田俊霞, 魏丽萍, 何念鹏, 徐丽, 陈智, 侯继华 (2018). 温带针阔混交林叶片性状随树冠垂直高度的变化规律. 生态学报, 38, 8383-8391.]
[56]	Tosens T, Nishida K, Gago J, Coopman RE, Cabrera HM, Carriquí M, Laanisto L, Morales L, Nadal M, Rojas R, Talts E, Tomas M, Hanba Y, Niinemets Ü, Flexas J (2016). The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO₂ diffusion as a key trait. New Phytologist, 209, 1576-1590. DOI PMID
[57]	Viana JL, Dalling JW (2022). Soil fertility and water availability effects on trait dispersion and phylogenetic relatedness of tropical terrestrial ferns. Oecologia, 198, 733-748. DOI PMID
[58]	Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007). Let the concept of trait be functional! Oikos, 116, 882-892. DOI URL
[59]	Vivek P, Parthasarathy N (2018). Contrasting leaf-trait strategies in dominant liana and tree species of Indian tropical dry evergreen forest. Flora, 249, 143-149. DOI URL
[60]	Waite M, Sack L (2010). How does moss photosynthesis relate to leaf and canopy structure? Trait relationships for 10 Hawaiian species of contrasting light habitats. New Phytologist, 185, 156-172. DOI PMID
[61]	Walcroft A, Le Roux X, Diaz-Espejo A, Dones N, Sinoquet H (2002). Effects of crown development on leaf irradiance, leaf morphology and photosynthetic capacity in a peach tree. Tree Physiology, 22, 929-938. PMID
[62]	Wang H, Prentice IC, Keenan TF, Davis TW, Wright IJ, Cornwell WK, Evans BJ, Peng C (2017). Towards a universal model for carbon dioxide uptake by plants. Nature Plants, 3, 734-741. DOI PMID
[63]	Wang L, Han X, Yin Q, Wang G, Xu J, Chai Y, Yue M (2021). Differences in leaf phenological traits between trees and shrubs are closely related to functional traits in a temperate forest. Acta Oecologica, 112, 103070. DOI: 10.1016/j.actao.2021.103760.
[64]	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. DOI URL
[65]	Westerband AC, Funk JL, Barton KE (2021). Intraspecific trait variation in plants: a renewed focus on its role in ecological processes. Annals of Botany, 127, 397-410. DOI PMID
[66]	Westoby M, Reich PB, Wright IJ (2013). Understanding ecological variation across species area-based vs mass- based expression of leaf traits. New Phytologist, 199, 322-323. DOI PMID
[67]	Wilson PJ, Thompson K, Hodgson JG (1999). Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytologist, 143, 155-162. DOI URL
[68]	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, et al. (2004). The worldwide leaf economics spectrum. Nature, 428, 821-827. DOI
[69]	Xun YH, Di XY, Jin GZ (2020). Vertical variation and economic strategy of leaf trait of major tree species in a typical mixed broadleaved-Korean pine forest. Chinese Journal of Plant Ecology, 44, 730-741. DOI URL
	[荀彦涵, 邸雪颖, 金光泽 (2020). 典型阔叶红松林主要树种叶性状的垂直变异及经济策略. 植物生态学报, 44, 730-741.]
[70]	Yang Y, Wang H, Harrison SP, Prentice IC, Wright IJ, Peng C, Lin G (2018). Quantifying leaf-trait covariation and its controls across climates and biomes. New Phytologist, 221, 155-168. DOI URL
[71]	Yu M, Sun OJ (2013). Effects of forest patch type and site on herb-layer vegetation in a temperate forest ecosystem. Forest Ecology and Management, 300, 14-20. DOI URL
[72]	Zhao ZG, Zhao FJ, Xia JB, Wang YH (2019). Effects of groundwater salinities on photosynthesis and water consumption characteristics of Tamarix chinensis in the Yellow River Delta. Journal of Natural Resources, 34, 2588-2600. DOI URL
	[赵自国, 赵凤娟, 夏江宝, 王月海 (2019). 地下水矿化度对黄河三角洲柽柳光合及耗水特征的影响. 自然资源学报, 34, 2588-2600.] DOI
[73]	Zhu JT, Li XY, Zhang XM, Zeng FJ, Yang SG (2010). Leaf functional traits of Ceratoides latens in northern slope of Kunlun Mountain and its regional difference with the altitude. Journal of Desert Research, 30, 1325-1330.
	[朱军涛, 李向义, 张希明, 曾凡江, 杨尚功 (2010). 昆仑山北坡驼绒藜叶片功能性状及其海拔差异性. 中国沙漠, 30, 1325-1330.]