中国753种陆生植物叶片中N和P的化学计量学.doc

New Phytologist《新植物学家》
Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China
中国753种陆生植物叶片中N和P的化学计量学
Wenxuan Han, Jingyun Fang, Dali Guo and Yan Zhang
Department of Ecology, College of Environmental Sciences and Key Laboratory for Earth Surface Processes of the Ministry of Educ ation, Peking University,
100871, Beijing, China
韩文轩
Summary（摘要）
• Leaf nitrogen and phosphorus stoichiometry of Chinese terrestrial plants was studied based on a national data set including 753 species across the country.
中国陆生植物叶片中N和P化学计量学研究基于全国性的数据收集，包括全国753种植物种。
• Geometric means were calculated for functional groups based on life form, phylogeny and photosynthetic pathway, as well as for all 753 species. The relationships between leaf N and P stoichiometric traits and latitude (and temperature) were analysed.
本文计算了所有753个物种基于生活型功能组的几何平均数，发展史和光合途径，并且分析了叶片中N和P的化学计量特征与纬度（温度）之间的关系。
• The geometric means of leaf N, P, and N : P ratio for the 753 species were 18.6 and 1.21 mg g−1 and 14.4, respectively. With increasing latitude (decreasing mean annual temperature, MAT), leaf N and P increased, but the N : P ratio did not show significant changes.
这753个物种的叶片N,P以及N:P比率的几何平均数分别为18.6mg/g,12.2mg/g和14.4. 随着纬度的增加（意味着平均年均温的减少），叶片中N和P的量随之增加，但是N:P比率却没有显著地变化。
• Although patterns of leaf N, P and N : P ratios across the functional groups were generally consistent with those reported previously, the overall N : P ratio of China’s flora was considerably higher than the global averages, probably caused by a greater shortage of soil P in China than elsewhere. The relationships between leaf N, P and N: P ratio and latitude (and MAT) also suggested the existence of broad biogeographical patterns of these leaf traits in Chinese flora.
尽管这些跨功能组中叶片N,P和N:P比率的模式一般符合之前的文章，但是整个中国植物群落的N:P比率远远高于全球平均水平，由此可能导致相对于全球其他地方，中国土壤中严重缺乏P。叶片N,P, N:P比率与纬度（或年均温）之间的关系也表明：在中国植物的这些叶子中存在着广泛的生物地理学特征。
Key words: China, leaf nitrogen (N) and phosphorus (P) contents, N : P ratio, plant functional groups, soil P.
关键词：中国，叶片氮（N）和磷（P）含量，N:P比率，植物功能群，土壤磷
New Phytologist (2005) 168: 377–385
© New Phytologist (2005) doi: 10.1111/j.1469-8137.2005.01530.x

Introduction（引言）
Nitrogen and phosphorus play vital roles in plant functioning, and are among the most important limiting nutrients in terrestrial ecosystems (Chapin, 1980; Reich et al., 1997). Accordingly, patterns of N and P status in plant biomass, and especially in leaves, have been studied intensely (Foulds, 1993; Koerselman & Meuleman, 1996; Nielsen et al., 1996; Reich et al., 1997;Thompson et al., 1997; Cunningham et al., 1999; Reich et al., 1999, 2003; Reich & Oleksyn, 2004). A number of studies have revealed that plant N and P concentrations are associated with many biotic and abiotic factors, including habitat (Hou, 1982; Foulds, 1993; Koerselman & Meuleman, 1996; Thompson et al., 1997; Cunningham et al., 1999); growth stages (Nielsen et al., 1996; Thompson et al., 1997; Elser et al., 2000a; Sterner & Elser, 2002); and plant functional groups (Reich et al., 1999). Previous studies have also shown that the ratio of leaf N to leaf P content in plant biomass can be an indicator of vegetation composition, functioning and nutrient limitation at the community level (Koerselman & Meuleman, 1996; Güsewell, 2004). An N: P ratio <14 generally indicates N limitation, while a ratio >16 suggests P limitation (Koerselman & Meuleman, 1996). More recently, Reich & Oleksyn (2004) have uncovered some broad biogeographical patterns in N and P stoichiometry by analysing a global data set of leaf N and P, and found that leaf N and P increased and N : P ratios decreased with increasing latitude (or decreasing temperature), independent of taxonomic shifts.
氮和磷在植物功能中起到至关重要的作用,在陆地生态系统中是其中最重要的限制营养(Chapin, 1980; Reich et al., 1997)。因此，其是植物叶片中，N和P模式在生物量中的显示一直在集中研究中(Foulds, 1993; Koerselman & Meuleman, 1996; Nielsen et al., 1996; Reich et al., 1997;Thompson et al., 1997; Cunningham et al., 1999; Reich et al., 1999, 2003; Reich & Oleksyn, 2004)。大量的研究表明，植物中N和P浓度相关与许多生物和非生物因素,包括生境(Hou, 1982; Foulds, 1993; Koerselman & Meuleman, 1996; Thompson et al., 1997; Cunningham et al., 1999)；增长阶段(Nielsen et al., 1996; Thompson et al., 1997; Elser et al., 2000a; Sterner & Elser, 2002)；和植物功能群(Reich et al., 1999)。先前的研究还表明，植物生物量中的叶片N:P比率可以作为群落层次中被组成、功能和营养限制的一个指示器(Koerselman & Meuleman, 1996; Güsewell, 2004)。N:P比值< 14通常表明N的受限性,而比值> 16表明P限制(Koerselman & Meuleman,1996)。最近, Reich & Oleksyn(2004) 分析了全球收集的叶片氮和磷数据，通过N和P化学计量学模式，发现了一些广泛的生物地理学特征：随着纬度的增加(或温度的降低)，叶片N和P的含量增加以及N:P比率的下降，呈现独立的分类变化特征。
These previous studies have greatly advanced our understanding of the variations and patterns of leaf N and P in terrestrial plants. However, no studies have yet incorporated information on leaf N and P of plant species in China, home to >10% of the global plant species and a diverse array of ecosystems from tropical rainforests to alpine tundra. Here we compiled a national data set of leaf N and P for China’s terrestrial plants, based on literature previously unavailable to researchers outside China, to analyse the patterns of leaf N and P stoichiometry in Chinese plant species. Our objectives were to (1) document available information on leaf N and P for China’s terrestrial plants; (2) compare patterns of leaf N and P, and N : P ratios in China, with those of global data sets such as those reported by Elser et al. (2000b) and Reich & Oleksyn (2004); and (3) explore the possible causes of such patterns.
这些以前的研究极大地加深了我们对于陆生植物叶片氮、磷变化和模式的理解。然而,目前任然没有研究纳入中国植物物种叶片氮和磷的信息,中国植物物种从热带雨林到高山苔原，包括多于 10%的全球植物物种和多样的生态系统。我们建立了一个全国性的中国陆生植物叶片N和P数据库，基于之前的国外研究人员难以获得这些资料, 在中国植物物种中分析叶片氮和磷化学计量学的模式。我们的目标是(1)中国陆地植物叶片氮和磷有效信息的文献;(2)比较中国叶片叶氮和磷模式,与全球数据集如Elser等(2000 b)和Reich & Oleksyn (2004);(3)探索这样模式的可能性原因。
Materials and Methods（数据与方法）
Data set（数据收集）
We collected data from the published literature on leaf N and P concentrations in Chinese species, along with the geographical and climatic information associated with the leaf samples (Appendix S1, available online as supplementary material). Our database consists of 2094 observations from 127 sampling sites across China (Fig. 1), including 753 terrestrial plant species in 395 genera and 116 families. For each sampling site we recorded location (latitude and longitude), vegetation type and climate variables, and documented family/genus/species, life forms (tree/shrub/herb, evergreen/deciduous, conifer/broadleaf, gymnosperm/angiosperm) and leaf N and P content of plants, and the methods used for leaf N and P analysis (see Appendix S1 for details).
我们从已发表的文献中收集到的数据在叶N和P的浓度在中国物种,随着地理和气候信息关联叶样品(附录S1,可用在线作为补充材料)。我们的数据库包括2094个采样点的观测从127年在中国(图1),其中包括753名陆生植物物种在395属116个家庭。对于每个采样点我们记录的位置(经度和纬度),植被类型和气候变量和记录家庭/属/物种,生命形式(树/灌木/草,常绿阔叶落叶,针叶树/ /,裸子植物和被子植物)和叶N和P含量的植物,和方法用于叶N和P分析(见附录S1详情)。

Fig. 1 Sampling locations of leaf nitrogen and phosphorus for all species in this study. Provincial boundaries are shown.(这个研究中的对叶片的取样位置。省级边界显示。)
To examine biogeographical生物地理学 patterns of leaf N, P and N: P ratio along gradients （变化率）of latitude and temperature, as described by Reich & Oleksyn (2004), we documented（记录了）the information on latitude and temperature for each sampling site by the following procedure. For sampling sites where latitude and mean annual temperature (MAT) were recorded, data were obtained directly; for sampling sites lacking detailed geographical coordinates, we used the latitude of the geographical centre of the sample area (a county); and for sampling sites where MAT was not recorded, we obtained MAT estimates based on a 0.1°× 0.1°resolution climate database developed by Fang et al.(2001) and Piao et al.(2003),which was generated from 682 climatic stations in China during 1949–99.
The leaf samples for N and P analyses in this database were collected mostly during the growing season (July–September). Units from different studies were standardized (mg g−1 d. wt for leaf N and P), and N: P ratios were expressed on a mass basis.
Data analysis（数据分析）
Because frequency distributions of leaf N, P and N: P ratios were highly skewed (Fig. 2), we calculated their geometric means. We also present arithmetic means of leaf N, P and N: P mass ratios for all 753 species, for comparison with previous studies that showed only arithmetic means.

Fig. 2 Scatter plot (a); and histograms showing the distribution of leaf nitrogen (mg g−1) (b); phosphorus (mg g−1) (c); N: P mass ratio (d) for all 753 species. Dashed curves in (b–d) indicate fitted log-normal curves.
Geometric means of leaf N, P and N : P ratios were also calculated by life form (e.g. herbs, shrubs, trees; evergreen, deciduous, conifers, broadleaves); phylogeny (e.g. seed plants, ferns); and photosynthetic pathways (e.g. C3 and C4 herbs). Seed plants were divided into angiosperms and gymnosperms, and angiosperms were further grouped into dicotyledons and monocotyledons.
We compared the statistical differences in N and P stoichiometry between different functional groups by following three steps. First, for each species the geometric means of leaf N and P were calculated, and N: P mass ratios were obtained. Second, the species specific means of N, P and N: P ratio were log-transformed (base e) for all species combined and for each functional group. Finally, the log-transformed N, P and N: P ratios were compared between functional groups using one-way ANOVA. We also calculated Spearman’s rank correlation coefficients between mean leaf N and P for all 753 species and for each functional group. To characterize biogeographical patterns of leaf stoichiometry, we first computed geometric means of leaf N and P, and N: P ratios for each species for each sampling site, then log-transformed the means of leaf N, P and N : P ratios to perform linear regressions. All statistical analyses were conducted using SPSS software (2001, ver. 11.0; SPSS Inc., USA).
Results（结果
Patterns of leaf N, P and N: P ratio across all species
Leaf N, P and N: P mass ratio exhibited large variations, primarily ranging c. 8−50 mg g−1 for N; 0–5 mg g−1 for P, and 5 – 40 for N : P ratio (Fig. 2). Geometric means for all species were 18.6 and 1.21 mg g−1, and 14.4, respectively; the corresponding arithmetic means were 20.2 and 1.45 mg g−1, and 16.3, respectively (Table 1). Across all species, leaf N and P were highly positively correlated (Fig. 2a; Table 1).

Table 1 Geometric means of leaf nitrogen, phosphorus and N: P mass ratios of different plant functional groups
Patterns of leaf N, P and N: P ratio across functional groups
Leaf N and P varied markedly across the functional groups (Table 1; Fig. 3). For leaf N, geometric means ranged from 11.7 mg g−1 for conifers to 22.2 mg g−1 for deciduous trees. Those for P varied from 0.81 mg g−1 for ferns to 1.56 mg g−1 for C3 herbs. In contrast, mean N: P ratios showed a relatively narrow range, from 13.0 (conifers, gymnosperms, C4 herbs) to 17.6 (ferns), with 12 out of 15 groups taking a value between 13 and 15 (Table 1; Fig. 3). Statistical comparisons between functional groups further confirmed the relative constancy of N: P ratios across different functional groups (Table 2). Among nine comparison pairs, only one (monocotyledons vs dicotyledons) showed a significant difference (P < 0.05) in N: P ratio, in contrast with eight in leaf N, and four in leaf P (P < 0.05). Spearman’s rank correlation coefficients between leaf N and P concentrations also reflected the comparative stability of N: P ratios (Table 1). Eleven out of 15 functional groups showed a significant positive correlation (P < 0.001).
Relationships between leaf N, P, N : P and latitude (MAT)
Leaf N and P were significantly correlated with latitude and MAT across all species (Fig. 4a,b,d,e), while the leaf N : P ratio was weakly correlated with latitude and MAT (P = 0.257 and P =0.221) (Fig. 4c, f ). In general, leaf N and P increased and the N : P ratio decreased as latitude increased and MAT decreased.

Fig.3 Box-and-whisker plots showing geometric mean, geometric standard deviation and geometric standard error for leaf nitrogen (mg g−1), phosphorus (mg g−1), and N : P mass ratio.

Table 2 Results of ANOVA for comparisons between different functional groups
Discussion（讨论）
Overall patterns of N and P stoichoimetry in China’s flora
This work presents, to the best of our knowledge, the first analysis of leaf N and P stoichiometry of a large number of terrestrial plant species across China. Our analysis indicated that leaf N of all 753 species had a geometric mean of 18.6 mg g−1 (arithmetic mean 20.2 mg g−1), nearly identical to that reported by Elser et al. (2000b) for 397 terrestrial plant species (geometric mean 17.6 mg g−1; arithmetic mean 20.6 mg g−1); and by Reich & Oleksyn (2004) for 1251 world plant terrestrial species (excluding China’s plants) (geometric mean 18.3 mg g−1; arithmetic mean 20.1 mg g−1).

Fig. 4 Relationships between leaf nitrogen, phosphorus and N: P mass ratio of plants, latitude and mean annual temperature (MAT) in China. Each data point represents a log-transformed, species-specific average of all observations of N, P or N: P within each sampling site (see Appendix 2). Linear regressions are shown for (a) latitude and leaf N (r2 = 0.179, P < 0.001, n = 813); (b) latitude and leaf P ( r2 = 0.101, P < 0.001, n = 1177); (c) latitude and leaf N : P ( r2=0.002, P = 0.257, n = 780); (d) MAT and leaf N (r2= 0.141, P < 0.001, n = 813); (e) MAT and leaf P ( r2 = 0.100, P < 0.001, n = 1177); (f) MAT and leaf N : P ( r2 = 0.002, P = 0.221, n = 780).

Table 3 Statistics of leaf nitrogen, phosphorus and N: P mass ratio for all species analysed by this study; Elser et al. (2000b); and Reich & Oleksyn (2004)
Leaf P of China’s flora, however, was significantly lower than the global averages (Table 3). The geometric mean leaf P was 1.21 mg g−1 for China’s flora, 15% lower than the value reported by Reich & Oleksyn (2004) and 23% lower than that reported by Elser et al. (2000b) (Table 3).
A larger geometric mean N: P mass ratio (14.4) thus resulted for China’s flora–data from Elser et al . (2000b) and Reich & Oleksyn (2004) yielded a geometric mean N: P ratio of 11.0 and 11.8, respectively – primarily caused by lower leaf P in Chinese vegetation than in global vegetation (Table 3).Because leaf N : P mass ratio is an indicator of the relative limitation of N vs P (N : P ratios <14 often indicate N limitation and N : P ratios >16 frequently signify P limitation;
Koerselman & Meuleman, 1996; Aerts & Chapin, 2000), the higher N: P ratio in this study than in others (Elser et al .,2000b; Reich & Oleksyn, 2004) might imply that China’s flora are relatively more limited by P (geometric mean N : P ratio of Chinese flora = 14.4) than the world flora analysed by Reich & Oleksyn (2004).
Why, then, did lower leaf P (and higher N: P ratios) occur in China’s flora? A potential cause for such a low leaf P may be the low soil P content in China. Plant and soil P