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In tropical rain forests, light is probably the most important environmental factor affecting plant establishment, growth and survival. Plant performance is enhanced through morphological and physiological acclimation to the light environment. Growth analyses of tree seedlings under controlled conditions indicate how such plants adjust to the light environment (e.g. Popma & Bongers 1988; Osunkoya et al. 1994; Veenendaal et al. 1996; Poorter 1999). At low irradiance, shade plants enhance interception of light by a large biomass fraction in leaves (leaf mass fraction, LMF). In combination with a large leaf area per unit leaf biomass (specific leaf area, SLA), this leads to a large interceptive leaf area per unit plant mass (leaf area ratio, LAR). Shade leaves have slow respiration and light-saturated photosynthetic rates (Langenheim et al. 1984; Oberbauer & Strain 1985). Little physiological activity means smaller maintenance costs, and in this way, carbon losses in the understorey are reduced and potential relative growth rates (RGR) enhanced (Lehto & Grace 1994; Sims, Gebauer & Pearcy 1994). At high irradiance, nutrient and water availability may limit plant growth. Accordingly, sun plants invest relatively more biomass in roots (i.e. they have a large root mass fraction, RMF). Carbon fixation is increased by the formation of thick leaves with fast light-saturated photosynthetic rates, increasing biomass growth per unit leaf area (net assimilation rate, NAR) and potential RGR.
Plant growth in the understorey is limited by the amount of light intercepted for photosynthesis. Growth in the understorey may depend on the amount of incident radiation and the leaf area (Oberbauer et al. 1988). Incident radiation is composed of direct light and diffuse light. Because 50–80% of the total daily radiation in the forest understorey may be as sunflecks (Pearcy 1987; Chazdon 1988), direct light is probably a more important determinant of plant growth than diffuse light. However, this is not always supported by field observations (Clark, Clark & Rich 1993).
A plant’s carbon balance is affected by the partitioning of fixed carbon to photosynthesizing tissue (leaf partitioning ratio, LPR) and its longevity (i.e. the leaf lifespan). At low irradiance, a greater biomass partitioning to leaves increases the leaf area. As carbon gain in the understorey is slow, leaf longevity should be increased to return the construction costs of the leaves (Chabot & Hicks 1982; Williams, Field & Mooney 1989). Pioneer species have short-lived leaves (Bongers & Popma 1990; Reich, Ellsworth & Uhl 1995). They must therefore replace lost leaf area quickly to sustain growth (King 1994), a prerequisite that is difficult to meet in the forest understorey.
Plant growth analysis is useful to evaluate how plants differ in growth rate, either inherently or dependent on the environment (Lambers 1998). Few studies have analysed growth of saplings in this way (but see King 1991, 1994). To evaluate whether (i) species differ in their response to the light environment, and (ii) similar patterns are found for large saplings in the field compared to small seedlings grown under controlled conditions, a field study was carried out on growth and biomass partitioning of six rain forest tree species differing in shade tolerance. Naturally established saplings occurring along a light gradient were selected, and the growth and turnover of shoots and their components were analysed. The following questions were addressed:
How is height growth related to light environment, and what factors cause this relationship? It is hypothesized that sapling growth depends on the amount of incident radiation and leaf area, and that direct light is a more important determinant for plant growth than diffuse light.
How does RGR and its components (NAR, LAR, LMF and SLA) vary with irradiance? Do species differ in light-dependent changes in biomass allocation, and what is their effect on growth? It is expected that NAR increases with irradiance, due to faster photosynthetic rates, and that LMF, SLA and LAR increase with shade to enhance light interception.
How do LPR and leaf lifespan vary with light environment? LPR and leaf longevity are postulated to increase with shading. Because leaf turnover of pioneer species exceed those of shade-tolerant species, it is also expected that they will have a larger leaf partitioning ratio.
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Seven of the 91 saplings died during the study period. Cecropia had the poorest survival (69%), whereas 92–100% of the saplings of the other species survived. Initial plant height or DSF had no effect on survival probability when all species were pooled (logistic regression, P > 0·05).
Height growth was positively related to light environment, leaf area, or a combination of the two (Table 2), whereas initial plant height had no effect. The regression models explained 76% of the variation, on average (range 27–98%). Leaf area affected the growth of all species but Theobroma. The light environment affected growth of all species but Cariniana. For the other four species, the combined effects of light and leaf area explained more than either alone. There was no single measure of the light environment that best explained height growth for all species; for some species, height growth was more closely related to DSF, whereas for other species it was more closely related to ISF.
Table 2. Effect of direct site factor (DSF) indirect site factor (ISF), initial height and initial leaf area on height growth of six rain forest tree species. A backward multiple regression was carried out, and standardized partial regression coefficients are shown for those variables which contributed significantly to the model
|Species||DSF (%)||ISF (%)||Height (cm)||Leaf area (m2)||r2|
An increased height growth at higher irradiance was due to the combined effect of a greater internode production rate and longer internodes (Table 3). For some species, the enhanced height growth was largely due to an increase in internode production rate (e.g. Cariniana). For other species (e.g. Theobroma), it was mainly due to increased internode length.
Table 3. Effect of initial plant height and light environment (DSF) on internode production rate (IPR) and internode length (IL) of six rain forest tree species. Regression coefficients (b) indicate the effect of 1 cm change in height or 1% change in direct light on the dependent variables. Light has an effect on height growth (expressed as cm change in height per year per percent change in DSF) via the IPR and via the IL
| ||Internode production rate (year−1)||Internode length (cm)||Effect DSF on height growth|
| ||Height (cm)||DSF (%)|| ||Height (cm)||DSF (%)|| ||Via IPR||Via IL|
|Cecropia|| 0·06||*|| 0·37||***||0·91|| 0·01||ns||0·06||*||0·52|| 2·1||0·9|
|Bellucia|| 0·00||ns|| 0·15||***||0·90||−0·02||ns||0·46||***||0·95|| 1·4||3·7|
|Tachigali|| 0·04||*|| 0·40||*||0·61|| 0·00||ns||0·65||***||0·67|| 3·5||3·3|
|Cariniana||−0·03||ns|| 2·04||**||0·84|| 0·00||ns||0·18||ns||0·46|| 5·3||1·0|
|Capirona|| 0·01||ns|| 0·19||***||0·72|| 0·02||ns||0·29||*||0·36|| 1·7||0·9|
|Theobroma|| 0·01||ns||−0·03||ns||0·21|| 0·01||ns||0·87||ns||0·29||−0·1||0·9|
Fourteen of the 84 surviving individuals (17%) had a net negative RGR, as a result of leaf shedding, branch loss or stem breakage. Saplings which showed negative growth rates were not confined to severely shaded microsites; theywere also growing in relatively brighter conditions (mean DSF = 5·0%, range 2·9–9·5). In general, net RGR (RGRn) and NAR were positively correlated with DSF (Table 4, Fig. 1). Responses of RGRn and NAR did not show a saturating response to light over the light range evaluated here. There was a striking lack of significant correlations between LAR and light environment as LMF and SLA showed opposite responses to irradiance. For three species, the LMF increased with irradiance whereas for five species, the SLA decreased.
Table 4. Relation between sapling light environment (direct site factor, %) and net RGR (RGRn), NAR, LAR, LMF, SLA and leaf lifespan. LAR and LMF are given for the initial measurement, SLA for the final measurement. Pearson’s correlation coefficients are shown and significance levels are indicated by *
|Species||RGRn (mg g−1 d−1)||NAR (g m−2 d−1)||LAR (m2 kg−1)||LMF (g g−1)||SLA (m2 kg−1)||Lifespan (yr)|
Figure 1. Relationship between above-ground RGRn, NAR, LAR, LMF, SLA and sapling light environment (DSF) for Cecropia (●) and Bellucia (○) (a); Tachigali (●) and Cariniana (○) (b); and Capirona (●) and Theobroma (○) (c). LAR and LMF are given for the initial measurement, SLA for the final measurement. Continuous regression lines refer to the filled symbols, and broken regression lines to the open symbols. Regression lines are only shown if they are significant; + P < 0·054; * P < 0·05; ** P < 0·01; *** P < 0·001.
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An increase in RGR with irradiance was closely paralleled by an increase in NAR (Fig. 1); the GRCNAR of the species ranged from 0·88 to 1·23 (Fig. 2a), and was significantly different from zero in all cases. For four species, an increase in LMF with irradiance led to an increase in RGR (and positive GRCLMF; Fig. 2c). This was counterbalanced by a decrease in SLA with irradiance and a negative GRCSLA. As a consequence, adjustments in LAR had little effect on RGR, and GRCLAR values were close to zero (Fig. 2b).
Figure 2. Growth response coefficient (GRC) (mean ± SE) of net assimilation rate (NAR) (a); leaf area ratio (LAR) (b); leaf mass fraction (LMF) (c); and specific leaf area (SLA) (d) for six rain forest tree species. LAR and LMF are taken as the average over the growth interval. Species are ordered along the X-axis according to their shade tolerance, with the most shade-tolerant species on the right. * indicates whether the GRC is significantly different from 0 (P < 0·05). Note that the scaling of the Y-axis differs between graphs.
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Species tended to differ in their GRCs, but this was only significant for GRCSLA (GRCNAR, F = 2·0, P = 0·089; GRCLAR, F = 2·1, P = 0·081; GRCLMF, F = 2·2, P = 0·071; GRCSLA, F = 3·1, P = 0·016). The two pioneer species, Cecropia and Bellucia, had the largest GRCLMF and GRCSLA (Fig. 2), but overall, the GRCs were not correlated with the whole-plant light compensation point of the species (Spearman’s rank correlation between GRCs and LCPNAR of the six species: GRCNAR, r = − 0·17, P > 0·10; GRCLAR, r = 0·17, P > 0·10; GRCLMF, r = 0·78, P = 0·066; GRCSLA, r = − 0·32, P > 0·10).
Species differed considerably in their LPR (one-way anova, F5,64 = 4·74, P < 0·001). On average, Cecropia had the greatest LPR (92%), and Theobroma had the smallest (17%) (Fig. 3a). Species also had different leaf lifespans (one-way anova, F5,63 = 5·6, P < 0·001), from 0·4 years for Cecropia to 3·2 years for Tachigali (Fig. 3b). LPR was negatively correlated with irradiance and RGRn, although correlations were stronger with RGRn (three significant relationships) than with DSF (two significant relationships) (Fig. 4, Table 5). The leaf lifespan of Cecropia and Tachigali was related negatively to light environment (Table 4); plants in shade had leaf lifespans which were, on average, half (Cecropia) to three times (Tachigali) longer than plants in a high-light environment (data not shown).
Figure 3. Interspecific variation in leaf partitioning ratio (LPR) and leaf lifespan for six rain forest tree species. Back-transformed logarithmic means and corresponding standard errors are shown. Bars with a different letter were significantly different at P = 0·05 (Student Newman–Keuls test). Species are ordered along the X-axis according to their shade tolerance. Only saplings with a direct site factor < 30% were included.
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Table 5. Correlation between leaf partitioning ratio (LPR), the light environment (DSF) and carbon balance (RGRn) of saplings of six rain forest tree species. Pearson’s correlation coefficient and significance levels are shown
| ||LPR (g g−1)|
|Species||DSF (%)||RGRn (mg g−1 d−1)|
|Bellucia|| 0·18 ns|| 0·19 ns|
|Tachigali||−0·44 ns||−0·49 ns|
|Theobroma||−0·05 ns|| 0·20 ns|
Figure 4. Leaf partitioning ratio (LPR) vs sapling RGRn for Cecropia (●) and Bellucia (○) (a); Tachigali (●) and Cariniana (○) (b); and Capirona (●) and Theobroma (○) (c). Continuous regression lines belong to the filled symbols, and broken regression lines belong to the open symbols. Regression lines are only shown if they are significant; * P < 0·05; ** P < 0·01; *** P < 0·001. Note that the scaling of the X-axis differs between graphs.
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