植物生态化学计量特征及其主要假说

doi:10.17521/cjpe.2020.0331

植物生态学报 ›› 2021, Vol. 45 ›› Issue (7): 682-713.DOI: 10.17521/cjpe.2020.0331

所属专题：生态化学计量

植物生态化学计量特征及其主要假说

田地¹(), 严正兵², 方精云³^,^**()

¹森林培育与保护教育部重点实验室, 北京林业大学林学院, 北京 100083
²香港大学生物科学学院, 香港
³北京大学生态研究中心, 地表过程分析与模拟教育部重点实验室, 城市与环境学院, 北京 100871

收稿日期:2020-10-10 接受日期:2021-01-07 出版日期:2021-07-20 发布日期:2021-10-22
通讯作者: ** 方精云 jyfang@urban.pku.edu.cn
作者简介:* 田地, 北京林业大学青年研究员, 硕士研究生导师, 主要从事植物生态化学计量学和全球变化生态学等方面的研究, 研究兴趣在于探索陆生植物不同器官间的化学计量关系、植物功能属性的生物地理格局及成因、陆地生态系统结构与功能对环境变化的响应及预测。在National Science Review、Ecology、Environmental Pollution等刊物发表论文35篇, 获专利2项, 出版译著1部。主持国家级和省部级科研项目共6项。 E-mail: tiandi@bjfu.edu.cn。ORCID:0000-0002-0389-8683
严正兵, 香港大学博士后, 主要从事植物生态化学计量学、植物功能性状、植物光谱学等方面的研究。在Ecology Letters、New Phytologist、Functional Ecology等刊物发表论文40余篇, 被引用950余次。主持国家级和香港地区科研项目共4项。现任《草业科学》期刊青年编委, 并任Diversity专刊编辑。ORCID:0000-0003-4908-042X
方精云, 北京大学教授、云南大学校长、中国科学院院士。主要从事全球变化生态学、植被生态与生物多样性、生态遥感、生态草牧业等方面的研究。发表论文350余篇, 被引用4万余次。曾获国家自然科学奖二等奖、长江学者成就奖、教育部及北京市自然科学一等奖以及惠泰克杰出生态学家奖等奖项。
基金资助:
国家自然科学基金(31800397);国家自然科学基金(31901086);国家自然科学基金(31988102)

Review on characteristics and main hypotheses of plant ecological stoichiometry

TIAN Di¹(), YAN Zheng-Bing², FANG Jing-Yun³^,^**()

¹The Key Laboratory for Silviculture and Conservation of Ministry of Education, College of Forestry, Beijing Forestry University, Beijing 100083, China
²School of Biological Sciences, The University of Hong Kong, Hong Kong, China
³Institute of Ecology, Key Laboratory for Earth Surface Processes of the Ministry of Education, and College of Urban and Environmental Science, Peking University, Beijing 100871, China

Received:2020-10-10 Accepted:2021-01-07 Online:2021-07-20 Published:2021-10-22
Contact: ** FANG Jing-Yun jyfang@urban.pku.edu.cn
Supported by:
National Natural Science Foundation of China(31800397);National Natural Science Foundation of China(31901086);National Natural Science Foundation of China(31988102)

摘要/Abstract

摘要：

植物生态化学计量学是生态化学计量学的重要分支, 主要研究植物器官元素含量的计量特征, 以及它们与环境因子、生态系统功能之间的关系。19世纪, 化学家们通过室内实验, 分析了植物器官的元素含量, 开始了对植物化学元素之间关系的探索。如今, 生态学家通过野外采样和控制实验, 探索植物化学元素计量特征的变化规律、对全球变化的响应以及与植物功能属性之间的关系, 促进了植物生态化学计量学的快速发展。该文在概述植物生态化学计量学发展简史的基础上, 综述了19世纪以来该领域的研究进展。首先, 该文将植物生态化学计量学的发展历程概括为思想萌芽期、假说奠基期和理论构建期3个时期, 对各个时期的主要研究进行了简要回顾和梳理。第二, 概述了植物主要器官的化学计量特征, 尤其是陆生植物叶片氮(N)和磷(P)的计量特征。总体上, 全球陆生植物叶片N、P含量和N:P (质量比)的几何平均值分别为18.74 mg∙g^-1、1.21 mg∙g^-1和15.55 (与16:1的Redfield比一致); 在物种或群落水平上, 叶片N和P含量一般呈现随温度升高、降水增加而降低的趋势。不同生活型植物叶片N和P计量特征差异明显, 尤其是草本植物叶片N和P含量高于木本植物, 落叶阔叶木本植物叶片N和P含量高于常绿木本植物。与叶片相比, 细根和其他器官化学计量特征研究较少。第三, 总结了养分添加实验对植物化学元素计量特征的影响。总体上, N添加一般会提高土壤N的可利用性, 使植物器官中N含量和N:P升高, 在一定程度上提高植物生产力; P添加可能会缓解过量N输入导致的N-P失衡问题, 提高植物器官P含量。但是, 长期过量施肥会打破植物器官原有的元素间计量关系, 导致元素计量关系失衡和生产力下降。第四, 梳理总结了植物生态化学计量学的重要理论、观点和假说, 主要包括刻画化学计量特征与植物生长功能关系的功能关联假说、刻画化学计量特征与环境因子关系的环境关联假说或理论以及刻画化学计量特征与植物进化历史关系的进化关联假说。最后, 指出了植物生态化学计量学研究中存在的问题, 展望了10个未来需要重点关注的研究方向。

关键词: 化学计量, 氮, 磷, 生态, 植物, 假说, 简史

Abstract:

Plant ecological stoichiometry, as a branch of ecological stoichiometry, focuses on the study of elemental content, ratios and relationships within and across plant organs, and the underlying biotic and abiotic drivers. In the 19th century, chemists detected the elemental contents in plant organs via laboratory experiments, sprouting the exploration of plant stoichiometric characteristics. Nowadays, ecologists have explored plant ecological stoichiometric characteristics and their responses to global changes and relationships with plant functional traits, using both field investigation and manipulative experiments. These sustained efforts have largely enriched the knowledge and understanding of plant ecological stoichiometry. In this paper, we briefly introduced the history and reviewed the research progresses of plant stoichiometry since the 19th century. Firstly, we proposed the developmental history of plant ecological stoichiometry as three main periods: sprouting, hypothesis foundation, and theoretical construction periods, and introduced some representative works for each period. Secondly, we overviewed plant ecological stoichiometric characteristics across organs, life forms and environmental gradients. The geometric mean values of leaf nitrogen (N) and phosphorus (P) contents and N:P mass ratios in global terrestrial plants are 18.74 mg∙g^-1, 1.21 mg∙g^-1 and 15.55 (i.e. similar to the Redfield ratio of 16:1), respectively. Leaf N and P contents at either species or community level generally show a decreasing trend with increasing temperature and precipitation, and have large variations among life forms, with higher values in herbaceous than woody plants, and deciduous broad-leaved than evergreen broad-leaved and coniferous woody plants. Compared with leaves, the stoichiometric characteristics of fine roots and other organs in plants remain poorly documented. Thirdly, we reviewed the effects of nutrient addition on plant ecological stoichiometric characteristics. In general, N addition increases soil N availability, then the N content and N:P in plants, thus leading to an increase in plant productivity to some extents. P addition might alleviate the N and P imbalance induced by excessive N inputs, and then increase plant P content. However, long-term nutrient fertilization could perturb the intrinsic stoichiometric characteristics in plants, resulting in the deteriorated nutrient imbalance in tissues and then the subsequent decline in plant productivity. Fourthly, we introduced the main hypotheses of plant ecological stoichiometry. These hypotheses include function-associated hypotheses, environment-associated hypotheses and evolution-associated hypotheses, which delineate the relationships of stoichiometric characteristics with plant growth functions, environmental factors and plant evolutionary history, respectively. Finally, we made an outlook on future research in the area of plant ecological stoichiometry, and highlighted ten potential and important research themes.

Key words: stoichiometry, nitrogen, phosphorus, ecology, plant, hypothesis, brief history

田地, 严正兵, 方精云. 植物生态化学计量特征及其主要假说. 植物生态学报, 2021, 45(7): 682-713. DOI: 10.17521/cjpe.2020.0331

TIAN Di, YAN Zheng-Bing, FANG Jing-Yun. Review on characteristics and main hypotheses of plant ecological stoichiometry. Chinese Journal of Plant Ecology, 2021, 45(7): 682-713. DOI: 10.17521/cjpe.2020.0331

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2020.0331

https://www.plant-ecology.com/CN/Y2021/V45/I7/682

图/表 14

表1 全球陆生植物叶片氮(N)和磷(P)含量和N:P在不同生活型间的差异

Table 1 Leaf nitrogen (N), phosphorus (P) content and N:P mass ratio across different lifeforms of global terrestrial plants

功能群 Functional group	N (mg∙g^-1)	P (mg∙g^-1)	N:P (g∙g^-1)	n
所有生活型 All functional groups	18.74 (±8.33)	1.21 (±0.94)	15.55 (±9.95)	12 721
所有木本 All woody species	18.22 (±7.77)	1.10 (±0.81)	16.53 (±9.30)	9 098
常绿针叶 Evergreen conifers	12.79 (±4.25)	1.06 (±0.81)	12.07 (±8.39)	480
常绿阔叶 Evegreen broadleaved	15.29 (±6.66)	0.79 (±0.56)	19.29 (±10.60)	3 476
落叶阔叶 Deciduous broadleaved	21.29 (±7.53)	1.40 (±0.86)	15.24 (±7.66)	4 981
其他木本 Other woody species	18.63 (±8.32)	1.23 (±0.64)	16.58 (±8.77)	101
草本 Herbaceous species	20.56 (±9.33)	1.56 (±1.12)	13.17 (±11.03)	3 489
蕨 Ferns	11.46 (±4.75)	0.65 (±0.62)	17.75 (±13.06)	134

图1 中国陆生植物群落水平的叶、茎和根碳氮磷计量特征随年平均气温的变化趋势(引自Tang等(2018))。

Fig. 1 Changes of carbon (C), nitrogen (N), and phosphorus (P) content in leaves, stems, and roots of terrestrial plants in China with mean annual air temperature (cited from Tang et al. (2018)).

表2 关于根系氮磷计量特征研究的文献及主要结果*

Table 2 Root nitrogen (N), phosphorus (P) concentration and N:P ratios from previous published researches*

图2 植物叶片碳(C)、氮(N)、磷(P)计量特征对N和P添加的响应(改自Yuan和Chen (2015))。圆圈表示自然环境中的样本, 灰色和绿色分别表示ln (响应比)与0差异不显著(p > 0.05)和差异显著(p? ≤ 0.05); 三角形表示控制环境中的样本, 灰色和红色分别表示ln (响应比)与0差异不显著(p > 0.05)和差异显著(p? ≤ 0.05)。误差线显示的是平均值的95%置信区间。括号外和括号内的数字分别代表自然环境和控制环境中的样本量。

Fig. 2 Natural log response ratios of plant carbon (C), nitrogen (N), phosphorus (P) and their stoichiometric ratios to N and P additions, respectively (replotted based on Yuan & Chen (2015)). Circles are for results in natural environments with grey and green representing insignificant (p > 0.05) and significant (p ≤ 0.05) difference between the log response ratio and zero, respectively. Triangles are for results in controlled environments with grey and red representing insignificant (p > 0.05) and significant (p ≤ 0.05) difference between the log response ratio and zero, respectively. Error bars are the 95% confidence intervals for the mean. The numbers out- and inside parentheses represent the numbers of observations for experiments in natural and controlled environments, respectively.

图3 植物生态化学计量学的主要理论和假说。这些理论和假说主要包含3类: (1)功能关联假说(蓝色标注), (2)环境关联理论和假说(棕色标注), (3)进化关联假说(绿色标注)。图中卡通图和谱系树图于2020年12月10日引自Google图片网站。

Fig. 3 Main theories and hypotheses in plant stoichiometry. Three categaries are included: (1) function-associated hypotheses (annotated in blue), (2) environment-associated hypotheses (annotated in brown), and (3) evolution-associated hypotheses (annotated in green). The cartoon graphs and phylogenetic tree graph are cited from the google image website (https://www.google.com/imghp?hl=en) in December 10, 2020.

图4 菟葵和拟南芥的叶片磷含量和氮磷质量比与生长速率的关系。A, B, 改自Niklas和Cobb (2005)。C, D, 数据来自严正兵(2017)拟南芥控制实验数据。

Fig. 4 Bivariate plots of lg-transformed data for growth rates vs leaf phosphorus (P) content and N:P, respectively, of Eranthis hyemalis and Arabidopsis thaliana. A and B are replotted based on Niklas & Cobb (2005). C and D are plotted based on data from Yan’s nutrient enrichment manipulation experiment on A. thaliana (Yan, 2017).

图5 植物N:P阈值假说的提出和再评估。A, Koerselman和Meuleman (1996)提出N:P的14和16阈值可以作为养分限制类型的判断标准, 改自Koerselman和Meuleman (1996)。B, Yan等(2017)参照Koerselman和Meuleman (1996)的数据分析方法, 并扩充样本量来评估N:P阈值适用性的情形, 改自Yan等(2017)。A和B中养分限制类型是基于野外施肥实验结果判断的, 每个点为单个野外控制实验站点数据。

Fig. 5 Original proposition and re-evaluation of the N:P Threshold Hypothesis. A, The N:P threshold values of 14 and 16 as the judgement standard for N and P limitations proposed by Koerselman & Meuleman (1996), redrawn from Koerselman & Meuleman (1996). B, Re-evaluation of the N:P Threshold Hypothesis by Yan et al. (2017) with a larger dataset following the same statistic method as Koerselman & Meuleman (1996), redrawn from Yan et al. (2017). Nutrient limitation here is judged by results of field nutrient fertilization experiments. Each point indicates a field experiment site.

图6 叶片N-P幂函数关系在全球尺度、站点尺度和施肥控制实验的规律。A, 改自Tian等(2018b), 说明叶片N-P幂函数关系在站点尺度存在很大变异。B, C, 改自Yan等(2018), 说明拟南芥叶片N-P幂函数关系受到N或P添加的影响。

Fig. 6 Leaf N-P scaling relationship at global level, site level and nutrient fertilization experimental level. A, Replotted based on Tian et al. (2018b), showing the significant variation of leaf N-P scaling relationship at site levels. B, C, Replotted based on Yan et al. (2018), indicating the effects of N and P fertilizations on leaf N-P scaling relationship of Arabidopsis thaliana.

图7 生态系统总初级生产力(GPP)与叶片氮和磷含量的关系。数据来自Tang等(2018)。

Fig. 7 Relationship between ecosystem gross primary productivity (GPP) and leaf nitrogen (N) and phosphorus (P) content, respectively. This figure is replotted using data from Tang et al. (2018).

图8 化学计量内稳性理论的示意图。A, 生物体中的元素比率随环境中元素比率的变化呈现协同变化, 无内稳性。B, 生物体中的元素比率随环境中元素比率的变化而不变, 呈现出严格的内稳性。图引自Sterner和Elser (2002)。

Fig. 8 Schematic diagram of Stoichiometric Homeostasis Theory. A shows the coordinated variation of organism vs environment nutrient ratios (i.e. no stoichiometric homeostasis). B shows that organism nutrient ratios keep stable with the changing environment nutrient ratios (i.e. strict stoichiometric homeostasis). This figure is replotted from Sterner & Elser (2002).

图9 限制性元素假说提出的数据分析图。改自Han等(2011)。

Fig. 9 Re-analysis of the original data of the Stability of Limiting Elements Hypothesis. This figure is replotted based on Han et al. (2011).

图10 中国不同生物群区植物器官间氮(N)磷(P)含量的关系图。叶片氮磷含量相比茎和根氮磷含量的斜率均小于1, 说明叶片养分含量相比根、茎养分含量更稳定, 对外界环境条件的响应程度更低。该结果支持“叶片养分含量稳定假说”。改自Tang等(2018)。

Fig. 10 Scaling relationships of nitrogen (N) and phosphorus (P) content among different organs from different biomes in China. The scaling exponents from leaf vs stem and leaf nutrient vs root nutrient relationships are all below 1, suggesting that nutrient content in leaves relative to stems and roots is more stable and less sensitive to environmental changes. These results support the Stable Leaf Nutrient Content Hypothesis. This figure is replotted based on Tang et al. (2018).

图11 相对重吸收假说提出的数据分析图, 改自Han等(2013)。纵坐标为氮重吸收效率(NRE)与磷重吸收效率(PRE)的差值。①沙漠; ②热带雨林; ③亚热带森林; ④湿地; ⑤中国温带森林; ⑥温带森林; ⑦中国北方森林; ⑧草甸; ⑨北方森林; ⑩欧石南灌丛; ?高草草原。

Fig. 11 Diagram of Relative Resorption Hypothesis, replotted based on Han et al. (2013). The y-axis shows the relative resorption efficiency of nitrogen (N) and phosphorus (P) (NRE - PRE). ① desert; ② tropical forest; ③ subtropical forest; ④ wetland; ⑤ China temperate forest; ⑥ temperate forest; ⑦ China boreal forest; ⑧ meadow; ⑨ boreal forest; ⑩ heathland; ? tallgrass prairie.

图12 生物地球化学生态位假说示意图, 改自Peñuelas等(2019)。A, 共生植物在多种元素化学计量特征的双主成分上所呈现的生物地球化学生态位。B, 干旱实验处理下共生植物的生物地球化学生态位的偏移。图中不同颜色组成的单个椭圆形表示某个特定的生物地球化学生态位。

Fig. 12 Diagram of Biogeochemical Niche Hypothesis, modified from Peñuelas et al. (2019). A shows biogeochemical niche segregation of multi-nutrients among coexisting plant species based on the principal component analysis. B shows the shift in biogeochemical niche among coexisting plant species in a drought experiment. Ellipses in different colours show specific biogeochemical niches.

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植物生态化学计量特征及其主要假说

Review on characteristics and main hypotheses of plant ecological stoichiometry

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