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AOBPreview originally published online on August 5, 2008
Annals of Botany 2008 102(4):623-629; doi:10.1093/aob/mcn135
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© The Author 2008. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

The Generality of Leaf Size versus Number Trade-off in Temperate Woody Species

Dongmei Yang1, Guoyong Li1 and Shucun Sun1,2,*

1 Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China
2 Department of Biology, Nanjing University, Nanjing 210093, China

* For correspondence. E-mail shcs{at}nju.edu.cn

Received: 6 May 2008    Returned for revision: 29 May 2008    Accepted: 20 June 2008    Published electronically: 5 August 2008


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 SUPPLEMENTARY INFORMATION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

Background and Aims: Trade-offs are fundamental to life-history theory, and the leaf size vs. number trade-off has recently been suggested to be of importance to our understanding leaf size evolution. The purpose of the present study was to test whether the isometric, negative relationship between leaf size and number found by Kleiman and Aarssen is conserved between plant functional types and between habitats.

Methods: Leaf mass, area and number, and stem mass and volume of current-year shoots were measured for 107 temperate broadleaved woody species at two altitudes on Gongga Mountain, south-west China. The scaling relationships of leaf size (leaf area and mass) vs. (mass- and volume-based) leafing intensity were analysed in relation to leaf habit, leaf form and habitat type. Trait relationships were determined with both a standardized major axis method and a phylogenetically independent comparative method.

Key Results: Significant negative, isometric scaling relationships between leaf size and leafing intensity were found to be consistently conserved across species independent of leaf habit, leaf form and habitat type. In particular, about 99 % of the variation in leaf mass across species could be accounted for by proportional variation in mass-based leafing intensity. The negative correlations between leaf size and leafing intensity were also observed across correlated evolutionary divergences. However, evergreen species had a lower y-intercept in the scaling relationships of leaf area vs. leafing intensity than deciduous species. This indicated that leaf area was smaller in the evergreen species at a given leafing intensity than in the deciduous species. The compound-leaved deciduous species were observed usually to have significant upper shifts along the common slopes relative to the simple-leaved species, which suggested that the compound-leaved species were larger in leaf size but smaller in leafing intensity than their simple counterparts. No significant difference was found in the scaling relationships between altitudes.

Conclusions: The negative, isometric scaling relationship between leaf size and number is largely conserved in plants, while the leaf size vs. number trade-off can be mediated by leaf properties. The isometry of the leaf size vs. number relationship may simply result from a biomass allocation trade-off, although a twig size constraint may provide an alternative mechanism.

Key words: Allometry, trade-off, leafing intensity, leaf size, leaf habit, leaf form


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 SUPPLEMENTARY INFORMATION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Trade-offs represent a fitness cost in one trait when organisms gain a benefit in another trait (Stearns, 1989); trade-offs provide keys to understanding the evolution of life-history strategies. They often damp the magnitude of organisms' phenotypic plasticity with physiological and allocation constraints and hence limit possible trait combinations. However, a number of trade-offs, as recognized in both plants and animals (e.g. Stearns, 1989; Aarssen and Jordan, 2001; Shipley et al., 2006; Kleiman and Aarssen, 2007), allow for different trait combinations in co-occurring species of an ecological community. Therefore, trade-offs are also of great significance to understanding species coexistence and the maintenance of local species diversity (Bonsall et al., 2004).

One particularly important trade-off in plants is between leaf size and leaf number. At a given leaf biomass allocation or total leaf area, plants may have few large or many small leaves, depending on environmental conditions. For example, few large leaves are advantageous in light interception and photosynthetic carbon gain in shaded environments due to a thick boundary layer for heat exchange (Horn, 1971), but they have to invest disproportionally more in supporting and transporting structures such as petioles and mid-ribs compared with small leaves (Niinemets et al., 2006, 2007; Li et al., 2008). Many small leaves tend to be advantageous in dry, cold, windy, high-altitude and low-nutrient habitats (e.g. Givnish, 1984; Fonseca et al., 2000; McDonald et al., 2003), but their photosynthetic capacity is usually limited by the stressful environments. Theoretically, this environment-mediated leaf size/number trade-off may substantially account for large variation in leaf size between and within habitats, which has been highlighted by a recent study (Kleiman and Aarssen, 2007). Kleiman and Aarssen (2007) found a negative, isometric relationship between leaf number per unit shoot volume and leaf size in plant twigs, and they suggested that small leaves can be interpreted in terms of selection favouring large leaf number. This obviously improves the understanding of leaf size evolution and the frequency distribution of leaf size variation in nature (Kleiman and Aarssen, 2007). Furthermore, a more recent study has applied the isometric trade-off to estimate the parameters of plant crown and stand levels (Ogawa, 2008). However, the isometric trade-off was obtained with only 24 deciduous broadleaved tree species (Kleiman and Aarssen, 2007). As they pointed out, it remains unclear whether the isometry of the leaf size/number relationship is conserved between plant functional groups and between habitats.

Leaf habit, leaf form and habitat type may greatly affect leaf size/number trade-off. At a given leaf number and a given twig size, leaf size should increase with increasing leaf mass fraction but decrease with increasing leaf mass per area (LMA). First, compared with deciduous species, evergreens are higher in LMA (Wright et al., 2004, 2007) and they also have to allocate a larger fractional investment in ecophysiologically transporting structures at a given plant twig size (White, 1983; Brouat et al., 1998; Sun et al., 2006) given that they are usually smaller in vessel size and in stem conductive capacity than temperate deciduous species (Cavender-Bares and Holbrook, 2001; Cavender-Bares et al., 2005). Secondly, compared with simple-leaved species, compound-leaved species are usually higher in within-leaf support costs because of the additional structure of rachises (Givnish, 1978; Niinemets, 1998; Li et al., 2008), which possibly results in a large LMA. Thirdly, between habitats, plants usually allocate more biomass to stems of plant twigs and have higher LMA in stressful sites of low temperature, low rainfall, low soil fertility and high elevation than in favourable environments (Fonseca et al., 2000; Westoby et al., 2002; Wright et al., 2002, 2005; Sun et al., 2006). Thus, it can be expected that species with evergreen leaves or compound leaves and that species at stressful sites would be smaller in leaf size at a given leaf number per unit twig size than their counterparts.

The present study investigated the leaf size/number relationship of woody species at two altitudes of a subtropical mountain, south-west China. Leaf size could be expressed as individual leaf area or dry mass (with a conversion factor of LMA) and twig size could be expressed as twig mass or twig volume. The forms of the scaling relationships between leaf size and number were determined and compared in terms of leaf area or mass and twig mass or volume, for species with different leaf habit, leaf form and habitat type. The primary objectives of the study were to test the generality of the isometry of the leaf size/number relationship and to test whether the size/number relationship is affected by plant functional type and habitat type.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 SUPPLEMENTARY INFORMATION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Study site
This study, as part of a large survey of twig ecology, was conducted along the eastern slope of Gongga Mountain in the Hailuogou National Nature Reserve in Sichuan Province, south-west China (29°32' –29°37'N, 101°58' –102°04'E). Altitude varies from 1400 m (base) to 7556 m asl (top), with a relative elevation difference of over 6000 m. Climatic and edaphic conditions are as described in Li et al. (2008).

Three distinct forest zones can be identified along the eastern slope of Gongga Mountain, i.e. the evergreen broadleaved forest zone (1800–2400 m), the mixed coniferous and deciduous forest zone (2400–2800 m) and the coniferous forest zone (2800–3800 m) (Liu, 1985; Shen et al., 2004). Lithocarpus cleistocarpus, Quercus engleriana and Phoebe glaucifolia dominate the evergreen broadleaved forest and Picea brachytyla, Abies fabris, Acer spp., Sorbus astateria and Rhododendron calostrotum dominate the mixed forest (Cheng and Luo, 2002).

Twig sampling
The sampled woody species covered the range of local leaf size variation. The twig was defined as the terminal branches of the current year's shoots. Therefore, the twigs in our study were always unbranched, each consisting of a terminal set of internodes and the leaves borne by them. Meanwhile, leaf mass was regarded as the mass sum of laminas and petioles, and petioles included within-leaf rachises in compound-leaved species. Twig mass was the sum of leaf mass and stem mass. We sampled 61 simple- and broadleaved species (34 deciduous and 27 evergreen species) and 24 compound-leaved deciduous species in the evergreen broad-leaved forest at low altitude, and 28 simple-leaved deciduous species in the mixed forest at high altitude. The total number of sampled species was 107, belonging to 64 genera of 35 families (see Supplementary Information, available online), with the simple-leaved deciduous species groups at low and high altitudes sharing six species in common.

For each of the study species, three to five individual adults were randomly selected away from track edges, and three to five random branches with tips at the outer surface of a plant's crown were chosen in July and August 2006, when leaf expansion and shoot growth were completed. Only twigs without apparent leaf area loss were selected. The following parameters were recorded (see Supplementary Information) for each twig: the number of leaves borne on the twig, stem length and stem diameter (diameters were measured in the middle of the internodes with a vernier caliper). Total projected leaf area was calculated by scanning all leaves of every twig and the pictures were then digitized by using MapInfo software. Total leaf mass and total lamina mass were measured for each twig without any appendages, which was dried to constant mass at 70 °C for 48 h and then weighted. Leaf area (referred to individual leaf area unless specified) and leaf or lamina mass (referred to individual leaf or lamina mass unless specified) were calculated from total leaf area, total leaf or lamina mass, and the leaf number on the twigs.

Leafing intensity was estimated by two different methods. One is mass-based leafing intensity, calculated as the number of leaves borne on a twig divided by the twig mass. The other is volume-based leafing intensity, calculated as the number of leaves borne on a twig divided by the twig stem volume. Twig stem volume was calculated from the length and diameter of the stem by assuming the stem has the dimensions of a cylinder. In addition, leaf mass fraction was calculated as the ratio of leaf mass to total twig mass, and wood density was calculated as the stem mass divided by stem volume.

Data analysis
All data on plant functional traits were log10 transformed to fit a normal distribution before analysis. Traits were averaged arithmetically in individuals and then within species, and species averages were log10 transformed to provide interspecific comparisons. A hierarchical ANOVA was conducted for the measured variables. Variance between species was found to be consistently the largest component, and variance between individual plants was always greater than that between twigs on the same individual (Table 1).


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  		TABLE 1. Hierarchical variance components for the functional traits of the species at low altitude on Gongga Mountain (ANOVA type I sums of squares, converted to percentages at each level)

 
The relationships between leaf size and number were analysed by using a Model Type II regression method because allometric slopes were of particular interest. The slopes were calculated as standardized major axes (SMA) (Warton et al., 2006). Confidence intervals for individual regression slopes were calculated following Pitman (1939). The methods of Warton and Weber (2002) were followed to test the heterogeneity of regression slopes and to calculate the common slopes when homogeneity of the slopes was demonstrated. Differences in the elevation of regression slopes (y-intercept) and in shifting along the common slope were tested by ANOVA (and post-hoc Tukey tests where appropriate). Calculation of allometric equation parameters was conducted using (S)MATR version 2·0 (Falster et al., 2006; http://www.bio.mq.edu.au/ecology/SMATR/).

Phylogenetically independent contrasts (PIC) were conducted using Phylogenetic Comparative Methods of COMPARE, version 4·6b (http://compare.bio.indiana.edu/). The calculation method of PIC followed Martins (2004). The phylogenetic tree was constructed following ECCAS (1974–1999). The tree was constructed and PIC conducted only for the simple-leaved deciduous species at low altitude as a representative, as species number was the largest among plant functional types. Regression of evolutionary divergence data was conducted with standard model I techniques. In this way, it was possible to determine whether the correlation between different functional traits varied with evolutionary divergence.

In addition, differences in the means of the functional traits between plant functional types and altitudes were determined using one-way ANOVA (and post-hoc Tukey's HSD tests). Pearson correlation coefficients were estimated to characterize the relationships between the functional traits. These calculations, as well as the regressive coefficients for PIC, were completed with STATISTICA for Windows (StatSoft Inc., 2000).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 SUPPLEMENTARY INFORMATION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Relationship between leaf mass and leafing intensity
Leaf mass (the sum of lamina and petiole) was negatively correlated with both mass-based and volume-based leafing intensities within each species group (Fig. 1A, B, Table 2). The best-fit common regression slope was –1·019 [95 % confidence intervals (CI) = (–1·033, –1·004), P = 0·836] for mass-based leafing intensity, and was –0·917 [95 % CI = (–1·020, –0·825), P = 0·764] for volume-based leafing intensity, both indicating negative, isometric relationships. In particular, more than 99 % (r2 > 0·99, P < 0·001) of the variation in leaf mass across species could be accounted for by the variation in the mass-based leafing intensity. For both the scaling relationships, no evident difference was found between any two species groups in the y-intercept. However, the compound-leaved deciduous species had a significant upper shift along the common slopes of the scaling relationships than the other species (Fig. 1A, B), indicating that they had a larger leaf mass and a lower mass-based or volume-based leafing intensity relative to the other species groups (see Table 4).


Figure 1
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  		FIG. 1. The scaling relationships (A) between leaf mass and mass-based leafing intensity and (B) between leaf mass and volume-based leafing intensity for the four species groups at two altitudes of Gongga Mountain, south-west China. For both (A) and (B), individual slopes were non-heterogeneous. As no significant difference in the y-intercepts was found between any two groups, only the common slopes (solid line) were shown. The compound-leaved species were found to have significant upper shifts along the common slopes of both the relationships, but the difference could not be shown graphically. LD, simple-leaved deciduous species at low altitude; LE, evergreen species; HD, simple-leaved deciduous species at high altitude; LC, compound-leaved deciduous species.

 


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  		TABLE 2. Standardized major axis regression slopes and 95 % confidence intervals (CIs) of the slopes of log–log linear relationships between the study functional traits for different species groups

 
The correlations between the mass-based leafing intensity, volume-based leafing intensity and leaf mass were also significant when expressed as correlated evolutionary divergences (Table 3).


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  		TABLE 3. The regression coefficients (a, the regression coefficient; b, the y-intercept) between the functional traits (log–log transformed data) of correlated evolutionary divergences for the simple-leaved deciduous species (n = 34) at low altitude on Gongga Mountain, south-west China

 
Relationship between leaf area and leafing intensity
A significant negative correlation was found between leaf area and mass-based leafing intensity in the four species groups (Fig. 2A, Table 2), with a common scaling slope of –0·951 [95 % CI = (–1·010, –0·895), P = 0·673], which did not deviate significantly from –1·0. The y-intercept of the relationship was significantly lower in the evergreen species, but no evident difference was found between any two other species groups (Fig. 2A), indicating that evergreens had a smaller leaf area at a given mass-based leafing intensity. The compound-leaved deciduous species showed a significant upper shift along the common slope, indicating that they had a lower mass-based leafing intensity but a larger leaf area than the other species groups (Table 4). The result of PIC analysis also showed a negative correlation between correlated evolutionary divergences (Table 3).


Figure 2
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  		FIG. 2. The scaling relationships (A) between leaf area and mass-based leafing intensity and (B) between leaf area and volume-based leafing intensity for the four species groups at two altitudes of Gongga Mountain, south-west China. For both (A) and (B), individual standardized major axes were non-heterogeneous, and the compound-leaved species shifted significantly along the common slopes. In (A), the y-intercept was lower in the evergreen species than in the other species groups, so the regression line of the evergreen species group (dashed line) and the common regression line of the other groups (the solid line) were shown. In (B), the y-intercept was lowest in the evergreen species (dashed line), then the deciduous group (dotted line), and then the compound-leaved group (solid line). However, no evident difference was found for the simple-leaved deciduous group between the two altitudes. Therefore, three regression lines are shown in (B). Symbols are as in Fig. 1.

 


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  		TABLE 4. Means (± s.e.) of the functional traits of the study species groups at two altitudes on Gongga Mountain, south-west China

 
Leaf area was negatively correlated with volume-based leafing intensity in all the species groups (Fig. 2B, Table 2), each with an isometric scaling slope. The common slope was –0·855 [95 % CI = (–0·953, –0·768), P = 0·931]. This was consistent with the negative relationship between correlated evolutionary divergences (Table 3). Significant differences in the y-intercept were found between any two groups. The evergreen species had the lowest y-intercept, followed by the simple-leaved deciduous and then compound-leaved deciduous species (Fig. 2B). The compound-leaved species had the highest leaf area at a given volume-based leafing intensity. However, no evident difference was found for the deciduous species between the two altitudes. The compound-leaved species also showed a significant upper shift along the common slope (Fig. 2B), indicating that they had a lower volume-based leafing intensity but a larger leaf area (Table 4).

Leaf mass fraction, leaf mass per area and wood density
The fraction of leaf mass within twigs (LMR) was higher in the compound-leaved species than in the simple-leaved deciduous species at low altitude. However, there was no significant difference between the evergreen species and the deciduous species, or between low altitude and high altitude (Table 4).

LMA was significantly higher in the evergreen species than the simple-leaved deciduous species at low altitude. However, there was no significant difference between the simple-leaved and compound-leaved species, or between low altitude and high altitude (Table 4).

Wood density was significantly larger in the deciduous, simple-leaved species at high altitude than the evergreen species and the deciduous, compound-leaved species at low altitude (Table 4). However, the differences in wood density were not significant between different functional groups or different habitats (Table 4).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
SUPPLEMENTARY INFORMATION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
The leaf size/number trade-off
Consistent with prediction, leaf size negatively and isometrically scaled with leafing intensity across plant functional types and habitat types, regardless of whether leaf/twig size was expressed as area or volume/mass. Moreover, leaf size variation could be largely attributed to the variation in leafing intensity, especially when leaf mass and mass-based leafing intensity were used. These results suggest that the leaf size/number trade-off found in the twigs of deciduous broadleaved woody species (Kleiman and Aarssen, 2007) is largely conserved. In addition, these negative correlations were observed in both cross-specific analysis and among evolutionary divergences, indicating that these trait combinations are possibly ecologically important.

The leaf size/number trade-off is predictable in plant twigs (Westoby et al., 2002) simply due to the biomass allocation constraint. The twigs, as defined here, have the property of permitting the leaf size/number trade-off to be detected, because they include only the annual growth of the plant species with very low levels of secondary growth. Within-twig materials are more likely to be transported and translocated, relative to whole plants in which trade-offs based on biomass allocation are often questioned (Watson and Casper, 1984; Bonser and Aarssen, 1996). Moreover, there exists a proximate mechanism for the isometric trade-off. Within twigs, total leaf mass isometrically scaled with stem mass [slope = 0·951, CI = (0·876, 1·033), P < 0·001] for the pooled data, consistent with the results of previous studies (Niklas and Enquist, 2002; Sun et al., 2006). It can be deduced that total leaf mass increased proportionally with increasing twig mass (the sum of leaf mass and stem mass). Thus, leaf mass should proportionally decrease with the increase of leaf number per unit twig mass, consistent with the tightly isometric relationship between leaf mass and mass-based leafing intensity (Fig. 1A).

A twig size constraint could also be a potential explanation for the leaf size/number trade-off. On the one hand, leaf size and twig size has long been recognized to be positively correlated (Corner, 1949) and the so-called Corner's rule has been widely demonstrated both intraspecifically and interspecifically (Brouat et al., 1998; Preston and Ackerly, 2003; Westoby and Wright, 2003; Sun et al., 2006). Twig mass was positively correlated with both leaf area (r2 ranged from 0·424 to 0·672, P < 0·001 for each group) and leaf mass (r2 ranged from 0·558 to 0·733, P < 0·001 for each group). On the other hand, twig size may affect leafing intensity with an endogenous mechanism. Twig mass was negatively correlated with mass-based leafing intensity (r2 ranged from 0·608 to 0·774, P < 0·001 for each group) and volume-based leafing intensity (r2 ranged from 0·796 to 0·889, P < 0·001 for each group), which indicated that large twigs tended to have relatively fewer leaves than small twigs. This is consistent with the result of Yagi (2004) who found that the ratio of leaf number per stem length was intraspecifically smaller in long current-year shoots than in short ones. A strong negative relationship was also found between stem length and leaf number per stem length not only in each functional group (r2 ranged from 0·616 to 0·786; P < 0·001) but also in the pooled database (r2 = 0·674; P < 0·001). This suggests that lateral axillary buds are more likely to be suppressed in large twigs than in small ones, which leads to a lower leafing intensity in large twigs. Collectively, the leaf size/number trade-off may be a by-product of the twig size effect on leaf size and leafing intensity.

The conserved isometric trade-off may have important implications for understanding leaf size evolution. The trade-off suggests that both leaf size and leafing intensity may be direct products of natural selection. For example, small leaves may have evolved because the fitness benefit gained by high leafing intensity is larger than by small leaves. Kleiman and Aarssen (2007) even proposed a leafing intensity premium hypothesis for deciduous angiosperm tree species, with supporting evidence of the right-skewed distribution of leaf size frequency. Furthermore, the role of the twig size constraint in the leaf size/number trade-off indicates other possible explanations for leaf size variation. For example, because leaf size, leafing intensity and twig size all are highly correlated, small leaves may result from natural selection favouring either small leaves, high leafing intensity or small twigs. It is difficult to distinguish the mechanism controlling leaf size variation and/or how these mechanisms interactively influence leaf size evolution. In addition, the success of detecting the leaf size/number trade-off suggests that plant twigs may be a good subject for plant functional ecology studies. Because fruits, leaves and other appendages mostly grow on plant twigs especially of deciduous woody species, they may interact and correlate with each other, as indicated by some previous studies (e.g. Westoby et al., 2002; Westoby and Wright, 2003). Dimensions such as LMA–leaf life span, seed size/number and leaf size–twig size could be concurrently studied in plant twigs and can be integrated to determine plant functional traits in relation to environmental changes, as noted by Wright et al. (2007).

Leaf habit, leaf form and habitat effects
Theoretically, differences between the scaling relationships of leaf mass vs. mass-based leafing intensity (Fig. 1A) and of leaf area vs. volume-based leafing intensity (Fig. 2B) may be ascribed to the three functional parameters, i.e. LMA, stem wood density and leaf mass fraction. At a given twig mass, large leaf mass fraction, small LMA and high wood density should lead to a higher y-intercept in the scaling relationship between leaf area and volume-base leafing intensity. Hence, the leaf habit, leaf form and habitat effects on the leaf size/number trade-off may be explained via these three functional traits.

Consistent with prediction, the evergreen species were found to have a significantly smaller leaf area at a given leafing intensity (both mass-based and volume-based) than the deciduous species at low altitude, although the leaf habit effect was not significant in the scaling relationships in which leaf size was expressed as leaf mass. The leaf habit effect can be attributed to the large difference in LMA between the evergreen and deciduous species studied (Table 4). The slight difference in stem wood density between the evergreen and deciduous species might have also contributed to the leaf habit effect. Low wood density tends to decrease the y-intercept of the scaling relationship of leaf mass vs. mass-based leafing intensity provided that the other variables remain constant. However, the present study did not detect a significant difference in leaf mass fraction between the deciduous and evergreen species.

In contrast to prediction, the compound-leaved deciduous species did not have a significantly lower leaf mass at a given leafing intensity (Fig. 1A, B), and they even had a significantly larger leaf area at a given volume-based leafing intensity than the simple-leaved deciduous species (Fig. 2B). These unexpected results could be due to two major factors. One is that LMA was not significantly different between the compound and simple leaves (Table 4) primarily because the compound leaves had a lower lamina mass per area than the simple leaves (Table 4). The other factor is that the compound-leaved species had a higher fractional leaf mass within twigs than the simple-leaved deciduous species (Table 4). In addition, stem wood density was slightly lower, although not significantly, in the compound-leaved species than their counterparts (Table 4), which might have contributed to the difference in the observed scaling relationships of leaf size and volume-based leafing intensity.

There was no significant habitat effect on the leaf size/number relationship as long as the parameters involved were considered, inconsistent with the prediction. This may be because the altitudinal difference was not large enough to result in significant differences in the functional traits, or that the leaf size/number scaling relationship was too conserved to be distinguished for the same plant functional type. A further examination of the habitat effect is under investigation.

In conclusion, the negative, isometric relationship of leaf size/number trade-off was conserved across the study species, regardless of leaf habit, leaf form and habitat type. However, when the y-intercepts of the scaling relationships between leaf area and leafing intensity were examined, the effect of leaf properties emerged and became significant. The conserved isometric trade-off could be attributed to the biomass allocation constraint; the twig size constraint could also be a potential mechanism underlying this trade-off. The differences in the y-intercepts of the scaling relationships could be accounted for by differences in LMA, leaf mass fraction and stem wood density between plant functional types. In addition, the correlation was much tighter between leaf mass and mass-based leafing intensity than between leaf mass and volume-based leafing intensity (Table 2). Mass-based leafing intensity appears to be a reasonable means to study the leaf size/number trade-off possibly because ‘mass’ may be a more appropriate substitute for energy than ‘volume’.


   SUPPLEMENTARY INFORMATION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 SUPPLEMENTARY INFORMATION
ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Supplementary information is available online at www.aob.oxfordjournals.org/ and lists the trait means for the 107 temperate broadleaved species examined.


   ACKNOWLEDGEMENTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 SUPPLEMENTARY INFORMATION
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
We thank Dr David Ackerly for insightful suggestions regarding the manuscript, and Xiang Shuang, Guo Ruqing, Yanan Li, Yin Zhou, Wang Shuo and Shi Qin for assistance in the field. Thanks are also due to the staff of the biological station at Gongga Mountain for permitting this study to be conducted. This study was funded by National Science Foundation of China (30670333), the Chinese Academy of Sciences (KZCX2-XB2-02) and NCET to S.S.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 SUPPLEMENTARY INFORMATION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

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