Photosynthesis in relation to leaf nitrogen, phosphorus and specific leaf area of seedlings and saplings in tropical montane rain forests of Hainan Island, south China

Abstract

In order to make clear the relationships between photosynthesis and leaf N, leaf P and SLA of tropical trees, and test the differences in the relationships among life-form groups (trees, shrub-like trees and shrubs), seedlings and saplings of 101 species from a tropical montane rain forest, located in the Diaoluo Mountain of Hainan Island, were selected. The net photosynthesis based on area and mass (A_area and A_mass), leaf nitrogen content based on area and mass (N_area and N_mass), leaf phosphorus content based on area and mass (P_area and P_mass) and specific leaf area (SLA) were measured and/or calculated. The results showed that A_area and A_mass tended to follow the order of shrubs>trees>shrub-like trees. One-way ANOVA showed that the difference in A_area between shrubs and shrub-like trees was significant (p<0.05), and for A_mass there were significant differences between shrubs and shrub-like trees and between shrubs and tree species (p<0.05). The relationships between A_area and N_mass were highly significant in all three life-form groups and for all species (p<0.0001). The correlation between A_area and P_mass was highly significant in shrubs (p=0.0038), shrub-like trees (p=0.0002) and for all species (p<0.0001), but not significant in trees (p>0.05). The relationship between A_area and SLA was highly significant in shrubs (p=0.0006), trees (p<0.0001) and for all species (p<0.0001), however this relation was not significant in shrub-like trees (p>0.05). The relationships between A_mass and leaf N and SLA were highly significant in all three life-form groups and for all species (p<0.0001). For A_mass and leaf P, there were significant correlations in tree groups (p=0.0377) and highly significant correlations in shrub groups (p=0.0004), shrub-like tree groups (p=0.0018) and for all species (p<0.0001). Stepwise regression showed that predicted A_mass values were closer to the observed values than those for predicted A_area values. Thus, it can be concluded that the relationships obtained from seedling and sapling measurements are close to those from mature individuals; correlations between photosynthesis and N_mass, P_mass and SLA traits are significant and the relationships are stronger and more stable for A_mass than for A_area.

Keywords

photosynthesis / tropical montane rain forest / sapling / leaf nitrogen and phosphorus / specific leaf area

Introduction

Photosynthesis is the basic source of material and energy in forest ecosystems and is also an important indication for appraising plant primary production. Studies of photosynthetic characteristics will play an important part in explaining and forecasting how endogenous and exogenous factors affect energy absorption, fixation, distribution and transformation during tree and forest growth, development and physical production processes (Chen et al., 2003a). The nitrogen content in leaves is much higher than in other organs (Trewavas, 1985). The nitrogen content in photosynthetic organs accounts for 50% of that of total leaves (He, 2001). Nitrogen deficiency will easily cause the depression of chlorophyll (Penuelas et al., 1993; Chen et al., 2003b) and soluble protein content (Evans, 1989; Schafer and Heim, 1992) as well as a change in stomatal conductance (Ciompi et al., 1996; Cechin, 1998), leading inevitably to a decline in the rate of photosynthesis. The amount of nitrogen in leaves determines their photosynthetic capacity (Mooney et al., 1981; Field and Mooney, 1986; Korner, 1989; Reich et al., 1991; Penuelas et al., 1993). Photosynthesis is correlated with phosphorus because bioenergetic molecules, such as ATP and NADPH, play an integral part in the processes of metabolism, such as photosynthesis and respiration (Wright et al., 2001). Many plants respond intensively to phosphorus during photosynthesis. If the amount of available phosphorus declines, even though light and CO₂ concentrations are suitable, the photosynthetic rate will also decline (Park et al., 1996). Phosphorus deficiency may cause the amount of chlorophyll and protein to drop and the photosynthetic rate to decline. But compared with nitrogen deficiency, the effect of phosphorus deficiency is small and can be negligible (Lima et al., 1999). Specific leaf area (SLA) is a measure of one kind of adaptation of plant leaves to a long-term light environment (Rosati et al., 1999). Plant photosynthesis, respiration and transpiration are all directly or indirectly related to SLA (Field and Mooney, 1986; Reich et al., 1991, 1992; Wright et al., 2001).

Physiological and ecological characteristics such as leaf photosynthetic rate, SLA, leaf nitrogen and phosphorus can show the biological characteristics of the species. These important factors determine the status of the species in the community. Functional leaf traits are a clear indication of the survival adaptation strategy of plants to gain the largest carbon harvest (Kikuzawa, 1995; Cordell et al., 2001) and are of ecological and biological evolutionary significance (Reich et al., 1992; Wright et al., 2004). Although the characteristics of the broadleaf will change greatly under different conditions, the mean changes of leaf traits under the same conditions are larger. Therefore, it is more important to study the relationships of functional leaf traits than their variation over some period (Wright et al., 2001).

So far, much data on photosynthesis from studies of tropical rain forest species has been obtained (Chen et al., 2003a; Reich et al., 2003), but the number of studies on seedlings and saplings on Hainan island, with its high biodiversity and complicated communities, are rare. Seedlings and saplings under the crown closure layer contain 90% of all tropical forest species (Wright and Westoby, 2000), which is important for community structural renewal and maintenance of biodiversity (Harms et al., 2000). Therefore, studies of the physiological and ecological characteristics of leaves of seedlings and saplings are important. In our study, we choose seedlings and saplings of 101 species as objects, which represent the main species and life forms in this area. Studies of the relationships between the photosynthetic rate and N, P and specific leaf area can provide a scientific basis for further exploration of the photosynthetic mechanism of tropical plants and their functional group division.

Study site

The Diaoluo Mountain lies in southeastern Hainan, at coordinates 18°52′N and 109°50′E. The type of climate is an east Asian tropical monsoon. The average annual temperature of the tropical rain forest at 600 m elevation is 20.8°C, the average maximum temperature is 23.9°C, the average minimum temperature is 16.3°C and the accumulated temperature above 10°C is up to 7989°C. Annual rainfall is about 2566 mm for the whole year, with clear dry and wet monsoon climate characteristics. The period from November to January is the dry season, February to March is a transition season, and the wet season is from April to October. The rainy season accounts for 96% of total precipitation. The soil originates from granite and diorite mother rocks. From the lowest point to the highest peak of the mountain, the soil changes from a latosol (<300 m elevation), to a mountain yellow soil (>300 m high) (Wang et al., 1999).

The Diaoluo mountain area has various forest vegetation types, with large areas of original evergreen trees and secondary forests. With changes in elevation, from the bottom towards the top, tropical valleys of rain forests occur at an elevation of<300 m, followed by tropical lowland monsoon rain forests (elevation between 300–700 m), tropical montane rain forests (700–1300 m), tropical-subtropical evergreen broad-leaved forests (1300–1500 m) and mountain evergreen coppice and shrubs (>1500 m) (Wang et al., 1999).

Methods

Species selection and grouping

According to the characteristics of the main type and distribution of the vegetation in the Diaoluo tropical montane rain forest, we selected seedlings and saplings of 101 species, belonging to 33 different families, as our study objects (Table 1); 3–5 individuals were chosen for each species. For study convenience, the species were classified into three groups by life form, i.e, shrubs, shrub-like trees and trees. There are 13 shrub species, 32 shrub-like tree species and 56 tree species.

Photosynthic measurements

Photosynthesis of the test plants was measured during March–April in 2004 and 2005. We selected three fully expanded and apparently healthy leaves from each individual for photosynthetic measurements. Maximum photosynthetic activity (P_max) was measured by a portable leaf chamber and open system infrared gas analyzer (IRGA) (LI-6400; Li-Cor Inc., Lincoln, NE, USA), with an air velocity of 0.5 L/min, air temperature of 26°C±2°C, relative humidity ranging from 50% to 70% and a CO₂ concentration of 380±10 μmol/mol. Measurements were conducted at 8:00–11:30 am for convenient testing and comparisons were done at 1500 μmol/(m²·s) photosynthetic photon flux density (PFD) provided by a red blue light source (6400-02B). Light conditions for seedlings and saplings in the understory were different, where photosynthesis was induced for 5–10 min, and the photosynthetic rate, measured at saturated light, was the maximum photosynthetic rate (P_mass) (Quilici and Medina, 1998; Thomas and Bazzaz, 1999; Nogueira et al., 2004). A_area was the maximum photosynthetic rate based on area and A_mass the maximum photosynthetic rate based on mass.

SLA measurement

We selected 10–15 fully expanded and apparently healthy leaves, and measured leaf areas with an electronic-optical area meter (WDY-500A). We then took these samples back to the laboratory and they were oven-dried (dessicated at 105°C for 30 min, then dried to constant weight at 80°C) and weighed. SLA is defined here as total leaf area / total leaf dry weight (Shipley et al., 2003; Chen et al., 2006).

Leaf nitrogen and phosphorus measurements

The fresh leaves were dessicated at 105°C for 30 min and oven-dried for at least 48 h at 80°C (Chen et al., 2006), then ground into powder of 2 mm size for element analyses. Dry leaf samples of 0.5 g were submitted to pre-digestion overnight, followed by double acid (H₂O₂+H₂SO₄) digestion. Total N content was determined in accordance with the Kjeldahl method and total P content was determined by spectrophotometry (Bao, 2000). N_area and P_area are defined as N, P content based on area, and N_mass and P_mass are defined as N, P content based on mass.

Data analyses

Data were analyzed by SPSS 12.0 software package. One-way ANOVA was used to analyze differences in photosynthetic rates in the three different life forms. Simple linear regressions were carried out to evaluate the effect of leaf N and P on photosynthetic rate, and we used stepwise regression to analyze relations between photosynthesis and each of N, P and SLA. We compared the absolute values of the regression coefficients to determine the contribution of leaf trait parameters to photosynthesis. Paired-samples t-test was used to test the relationships between predicted values accounted for by stepwise regression models and the observed values in different life forms and for all species.

Results

Comparison of photosynthesis in different life-form groups

In the understory of the tropical rain forest, A_area and A_mass of seedlings and saplings showed the following trend: shrub>tree>shrub-like tree. For mean A_area, ANOVA results showed that there were significant differences between shrubs and shrub-like trees, while no significant differences were found in A_area between shrubs and trees and between trees and shrub-like trees (Fig. 1a). For mean A_mass, there were significant differences between shrubs and shrub-like trees, and shrubs and trees, while no significant differences between shrub-like trees and trees were found (Fig. 1b).

Relationships among plant photosynthesis, leaf N, leaf P and SLA

Relationships between leaf N and P for all species and different life-form groups

Linear regression analysis showed that the correlations between A_area and N_mass were positive and highly significant for shrubs, trees, shrub-like trees and all species (Fig. 2(a), Table 2). The correlations between A_area and P_mass were positive and highly significant for shrubs, shrub-like trees and for all species, but not significant for tree groups (Fig. 2(b), Table 2). The relationships between A_mass and N_mass were positive and highly significant for all three life-forms and for all species (Fig. 2(c), Table 2). A_mass and P_mass are positively correlated and there were highly significant correlations for shrubs and shrub-like trees, and were also significant for tree groups (Fig. 2(d), Table 2).

With an increase in N_mass or P_mass, A_area and A_mass of the three life forms also showed a rising trend (Fig. 2), but the photosynthetic rate of shrubs was smaller than that of trees when N_mass or P_mass was lower; only when N_mass or P_mass attained a specific value did shrubs show a higher photosynthetic rate than trees. The analysis also suggests that the correlations between A_area/A_mass and N_area, A_area/A_mass and P_area were not significant.

Relationships between photosynthesis and SLA

The results of regression analysis showed that the relationships between A_area and SLA were positive and highly significant for shrubs, trees and for all species, but not significant for shrub-like trees (Fig. 3a, Table 3). The A_mass and SLA showed positive and highly significant correlations for all three life-forms and for all species (Fig. 3b, Table 3). With an increase in SLA, both the A_area and A_mass of each life-form group showed an upward trend. Interestingly, the photosynthetic rate of shrubs was the smallest when SLA was lower, while shrubs gradually attained their highest value as SLA increased.

Stepwise regression analysis for A_area and A_mass

Stepwise regression equation

According to the results and analysis above, both A_area and A_mass have close and stable relationships with functional leaf traits such as N_mass, P_mass and SLA. Using a stepwise regression analysis, the contribution of the functional leaf traits (N_mass, P_mass and SLA) to A_area and A_mass can be described in detail. The results suggest that, for shrubs, A_area was only correlated with N_mass, but the correlation was highly significant. However, A_mass of shrubs was closely connected with N_mass and SLA, with standardized regression coefficients of 0.497 and 0.483, respectively. When comparing the two absolute values of the standardized regression coefficients for the two variables, the N_mass made a greater contribution to the A_mass of shrubs than did SLA. For shrub-like trees, A_area was significantly related to N_mass and P_mass, and their standardized regression coefficients were 0.479 and 0.352, respectively, thus N_mass contributed more to A_area of the shrub-like trees.The A_mass of shrub-like trees was significantly correlated with SLA, N_mass and P_mass. Their standardized regression coefficients were 0.520, 0.346 and 0.284, respectively. The contribution of the three coefficients were SLA>N_mass> P_mass. For trees, A_area was only significantly correlated with N_mass, while A_mass was significantly correlated with SLA and N_mass, with standardized regression coefficients of 0.721 and 0.198, respectively, suggesting that for trees, the contribution of SLA to A_mass was far greater than that of N_mass. For all species, A_area was significantly correlated with N_mass and SLA, with standardized regression coefficients of 0.552 and 0.212, respectively, revealing that N_mass made the greater contribution to A_area; A_mass was significantly related to SLA, N_mass and P_mass, with standardized regression coefficients of 0.614, 0.272 and 0.150, respectively; their ordered contribution is SLA>N_mass> P_mass (Table 4).

Relationships between predicted and observed values

Given the results of the regression analyses above, relationships between predicted and observed values were tested by t-tests of paired-samples. The results showed that for each life-form group and for all species groups, there were no significant differences between the predicted A_area and observed A_area; however, the predicted A_area was higher than the observed A_area (Fig. 4a); the same result was also found between predicted A_mass and observed A_mass (Fig. 4b). When comparing the two patterns, we find that the relationship between predicted and observed values was stronger and more stable when expressed per leaf mass than per leaf area. The results also show that the observed predicted relationship was close to the 1∶1 line (Fig. 4a, b). Thus, leaf N, leaf P and SLA are highly associated with leaf A_max.

Conclusions and discussion

Compared with trees and shrub-like trees, shrubs had the highest average photosynthetic rate, which was significantly different from the average A_mass of trees and shrub-like trees. However, the mean A_area of shrubs was not significantly different from that of trees. According to the study by Delucia and Schlesinger (1991), shrubs have a higher photosynthetic capacity than trees, which was consistent with our results on the comparison of average photosynthetic rates for shrubs and trees. However, in our study, with N_mass, P_mass and SLA increasing, A_area and A_mass of each life form showed an upward trend. At a lower level of N_mass, P_mass and SLA, the shrub-like trees had a lower photosynthetic rate than trees. Shrubs had the maximum photosynthetic rate until N_mass, P_mass and SLA attained specific values.

Although there is a large diversity among plant species in life form, leaf size and leaf shape, leaf traits are generally correlated among and within species at a local scale, which provides evidence for convergent evolution (Wright et al., 2001). In our study, the correlation among A_mass, N_mass and SLA for trees, shrub-like trees, shrubs and all species were remarkable. Reich et al. (1999) suggested that A_mass, N_mass and SLA are usually positively correlated, and assumed the same relationship in broad-leaved species to extend on a global scale. Later research confirmed that the leaf trait relationships among species were largely the same in different biotic communities (Reich et al., 1991, 1992, 1999, 2003; He et al., 2006), powerfully supporting the idea of convergent evolution. The 101 species in our study had high diversity among plant species in life form and leaf type, which is at variance with former research results. The results of our study also supported the hypothesis that functional leaf traits in different communities have similar relationships and suggested that the relationships among N_mass, SLA, A_mass and their function, based on an appropriate scale, applied in general to different species. In general, leaf phosphorus changes less than leaf nitrogen in tropical montane rain forests (Wright et al., 2001), especially in nutrient barren areas; however, in our study P_mass, like N_mass, was similarly correlated with A_mass. Interestingly, in contrast to the relative constant slopes, the elevations of the regression lines often differed by site, with climate-related variation among sites in SLA often driving these differences (Reich et al., 1999). In tropical montane rain forests, multi-species vegetation is very complex; for example SLA shows a wide range of changes in broadleafed tree species. Among the 101 species in our study, Cinnamomum subavenium had the lowest SLA (38 cm²/g) and Saprosma hainanense, at 232 cm²/g, had the highest. This variation can lead to changes in the elevations of the regression lines in different species and life-form groups.

In our study, a correlation between A_area and N_area was absent, which agrees with the results of Reich et al. (1998) that A_area and N_area are not correlated in all plants at each site. The relationship between A_area and SLA was significant for shrubs, trees and for all species, but not significant for shrub-like trees, suggesting that there is no fundamental relationship between A_area and N_area among all species. This may be partially ascribed to offsetting relationships: A_mass is a positive function of N_mass and although N_mass decreases with decreasing SLA, the decreasing SLA increases N_area for any given N_mass. This results in the potential for leaves to have similar N_area but different N_mass. At a given N_area, leaves with higher N_mass realize a higher A_area than leaves with lower N_mass, due to the positive relationship between A_mass and N_mass, giving rise to considerable scatter among species in the relationship between A_area and N_area. Reich et al. (1998) also suggested that for the same functional groups, SLA and N_mass changes little. A_area and N_area may have significant correlation, however, this idea was not proved in our study.

In addition, we chose seedlings and saplings as research objects, although in the development of the ontogenetic stage of plants, the physiological and ecological characteristics of saplings will change considerably because of their changed environment and self regulation (Osunkoya, 1996). However, we aimed our study at the relationships between photosynthesis and leaf N, leaf P and SLA of tropical woody species. The results show that these relationships among seedlings and saplings are similar to those of adults. What is more, in all three different life-form groups, photosynthesis, N_mass, P_mass and SLA have stable relations. Accordingly, we can conclude that this kind of specific correlation is not only consistent with different habitats, different biological communities and different functional groups, but the same convergent evolution mode may also exist in seedlings and saplings. Therefore, although the physiological and ecological characteristics of saplings change during the ontogenetic stages, the relationships among photosynthetic rate, N_mass, P_mass and SLA of seedlings and saplings will reflect the connections between physiological and ecological characteristics in mature individuals. Validity of this inference should be tested in our next experiments, but this provides certain instruction for further research.

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