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Shade tolerance is considered to be the central paradigm for understanding the succession and dynamics of temperate and tropical forests (Bazzaz, 1979; Pacala et al., 1996). Although the notion of shade tolerance dates back as far as the eighteenth century, there is still considerable debate as to what constitutes the salient features of shade tolerance (Sack & Grubb, 2001; Kitajima & Bolker, 2003; Niinemets, 2006), with two contrasting hypotheses. One hypothesis suggests that shade-tolerant and light-demanding species partition spatial and temporal gradients in irradiance because of a trade-off between survival and growth (Kitajima, 1994; Kobe et al., 1995). The alternative hypothesis suggests that species partition light gradients because of a trade-off in growth performance between low and high light (Shugart, 1984; Givnish, 1988). The reasoning behind the first hypothesis is that shade-tolerant species regenerate in the shaded forest understory where carbon gain proceeds at low rates. For such species, a high survival rate is thought to be important, if they are eventually to make it to the canopy. Indeed, temperate and tropical seedling studies under controlled conditions have shown that shade-tolerant species are characterized by tough, structurally reinforced leaves with a low specific leaf area (SLA; leaf area per unit leaf mass) (reviewed in Veneklaas & Poorter, 1998; Walters & Reich, 1999). This would allow them to deter potential herbivores (Coley, 1983), pay back the initial construction costs of the leaves (Poorter et al., 2006), reduce leaf turnover (King, 1994) and enhance plant survival (Poorter & Bongers, 2006). For light-demanding species that regenerate in the ephemeral, high-light conditions of gaps, a high growth rate is thought to be important. Seedlings of light-demanding species have been found to have high SLA, leaf area ratio (LAR; leaf area per unit plant mass) and assimilation rates (Veneklaas & Poorter, 1998; Walters & Reich, 1999). This would allow them to overshade and outcompete their neighbours, attain a position at the top of the re-growing gap vegetation, and achieve fast growth.
Several authors (Sack & Grubb, 2001; Lusk & Warton, 2007; Valladares & Niinemets, 2008) have argued that most of our knowledge on shade adaptations comes from work on small seedlings, and that the observed patterns may largely be driven by interspecific variation in seed size, as seed size is known to have large effects on seedling morphology (Grubb, 1998). Many light-demanding species have minute seeds with little reserves, and depend on photosynthetic carbon gain for onward autotrophic growth. As a result, they have a high biomass fraction in leaves, and high SLA and LAR. By contrast, many shade-tolerant species have large seeds, and form large seedlings with large leaves that need more structural reinforcement, and therefore have low SLA and LAR. Morphological differences between small-seeded light-demanding species and large-seeded shade-tolerant species are therefore largest just after germination, but may change dramatically over time when the light-demanding species catch up in size with the shade-tolerant species (Grubb et al., 1996; Sack & Grubb, 2001; Poorter & Rose, 2005). Lusk & Warton (2007) showed in a meta analysis that saplings (0.2–5 m tall) of evergreen species still showed a positive relation between SLA and regeneration light requirements, whereas for saplings of temperate winter deciduous species this relationship was reversed compared with seedlings. The winter sets a clear upper limit to the leaf lifespan of temperate deciduous shade-tolerant species, and for them it probably does not pay to structurally reinforce their leaves by having a low SLA, and instead, they make high-SLA leaves to enhance light interception. Large-scale comparative studies on leaf traits in later ontogenetic stages are scant. A study on the adult leaves of 63 tropical evergreen tree species found that light-demanding species had higher SLA compared with shade-tolerant species (Popma et al., 1992), whereas a study on 85 temperate deciduous species (Niinemets & Kull, 1994) found that light-demanding species had a lower SLA, paralleling the findings for saplings. Given the fact that SLA and LAR are strong drivers of interspecific variation in growth, this could have large repercussions for species growth performance along the light gradient for taller plants. Indeed, the second hypothesis suggests that shade-tolerant and light-demanding species may partition the light gradient because of a trade-off in growth performance between low and high light. According to this view, shade-tolerant species realize the fastest growth rates in the shade because of a maximization of light interception and low respiration (Givnish 1988), whereas light-demanding species realize the fastest growth rates in high light because of high photosynthetic carbon gain.
Given these recent findings, the question is whether the shade adaptations of tropical dry forest species parallel those of tropical evergreen species or those of temperate winter deciduous species. The importance of shade tolerance is likely to diminish in dry forests, which experience a more extreme dry season and have a seasonally open canopy (Lebrija-Trejos et al., 2008; Markesteijn et al., 2007). Wet tropical forests with a high leaf area index and an evergreen canopy cast a deep, persistent shade, whereas dry tropical forests with a low leaf area index and a seasonally deciduous canopy cast a lighter shade, which disappears during the dry season. The lighter shade could allow subcanopy trees to maintain a moderately positive carbon balance during the wet season, and the high light pulse could allow evergreens to make large carbon gains during the dry season when they are still physiologically active. It is therefore expected that plant adaptations to shade will be less pronounced in dry forests. Instead, the severe dry season may impose a strong environmental filter. Most species that can successfully survive this dry season will have a deciduous leaf habit, possibly leading to a smaller range of leaf lifespans, and to either a strong convergence of functional traits or to similar shade adaptations as found for saplings of temperate deciduous species. However, no data exist on how leaf traits are related to shade tolerance in dry tropical forest species.
In this study, the functional leaf traits of 39 moist forest species and 41 dry forest species are compared. The focus was on adult leaves, as it is argued that they should show different relationships with shade tolerance compared with seedling leaves (Grubb, 1998; Niinemets, 2006). The selected species represent the majority of stems in each community, thus providing insight into the spectrum of trait values among co-existing trees, and its implication for plant performance and niche differentiation (Reich et al., 2003). A suite of 26 functional traits have been selected that are important for the light capture, carbon gain and defence of leaves, and hence for the growth and survival rates of plants. Leaf traits were related to a continuous index of the regeneration light requirements of the species (Poorter & Kitajima, 2007), as light requirements in the regeneration stage are a better predictor of leaf traits of seedlings, saplings and adults than light requirements in the adult stage (Poorter, 2007). This is probably because the regeneration stage is the major bottleneck in the life cycle of the plant.
The aim of this study was to compare leaf adaptations to shade for moist and dry forest tree species. It was predicted that: (i) moist forest species would show more and stronger shade adaptations than dry forest species; (ii) for moist forest species SLA and associated leaf traits would increase, and leaf lifespan decrease with regeneration light requirements, whereas for dry forest species SLA and leaf lifespan would decrease with regeneration light requirements; and (iii) in the moist forest leaf traits underlying the growth–survival trade-off would be important for light partitioning, whereas in the dry forest leaf traits underlying the trade-off between low and high light growth might become more important.
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Most of the adult leaf traits evaluated (85%) were significantly correlated with juvenile CE (hereafter CE), at one or both sites (Table 1). More traits were significantly affected by CE in the dry forest than in the moist forest (16 vs 14 traits), but for these traits CE explained less of the variation (r2 is 0.17 vs 0.25, respectively; t-test on r2, t = 2.4, P = 0.024, df = 28). The leaf traits are discussed in four groups, related to leaf size (Table 1), leaf reinforcement (Fig. 1), leaf display at the metamer level (Fig. 2), and leaf chemistry (Fig. 3).
Figure 1. Relationship between leaf traits and juvenile crown exposure (CE) for moist forest species (n = 39, left panels) and dry forest species (n = 41, right panels). (a, b) Leaf density of the punch, (c, d) punch force and (e, f) leaf lifespan for saplings. For leaf lifespan the deciduous (open circles) and evergreen species (closed circles) are shown with different symbols, because it was expected that they might show different relationships with CE. Regression lines (continuous lines are significant, and broken lines are not significant), Pearson correlations, and significance levels are given. ns, P > 0.05; *, P < 0.05; **, P < 0.01; ***, P < 0.001.
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Figure 2. Relationship between leaf traits and juvenile crown exposure (CE) for moist forest species (n = 39, left panels) and dry forest species (n = 41, right panels). (a, b) Leaf mass fraction of the metamer, (c, d) specific leaf area (SLA) of the punch, and (e, f) leaf area ratio of the metamer (LARm). For SLA the deciduous (open circles) and evergreen species (closed circles) are shown with different symbols, because it was expected that they might show different relationships with CE. Regression lines (continuous lines are significant, and broken lines are not significant), Pearson correlations, and significance levels are given. ns, P > 0.05; *, P < 0.05; **, P < 0.01; ***, P < 0.001.
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Figure 3. Relationship between leaf traits and juvenile crown exposure (CE) for moist forest species (n = 39, left panels) and dry forest species (n = 41, right panels). (a, b) Nitrogen per unit mass (Nmass), (c, d) phosphorus per unit mass (Pmass), and (e, f) internode density. Regression lines (continuous lines are significant, and broken lines are not significant), Pearson correlations, and significance levels are given. ns, P > 0.05; *, P < 0.05; **, P < 0.01; ***, P < 0.001.
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Relative to shade-tolerant species, light-demanding species (with a high CE) had in both forests a large leaf area (Table 1) and internode cross-sectional area, long petioles, and a large biomass fraction in petioles (although for the PMFm of the dry forest this was at the edge of significance; P = 0.055). Light-demanding species were also characterized by a low internode density (Fig. 3e,f).
Six leaf traits were only correlated with CE in the moist forest, and nearly all these traits were related to leaf toughness and persistence. Shade-tolerant species (with a low CE) had a low SLA at the leaf and lamina level (Fig. 2c), and a high leaf dry matter content, leaf density (Fig. 1a) and leaf punch force (Fig. 1c). Species with a low CE had in both forests a long leaf lifespan (Fig. 1e,f). In the moist forest there was a significant interaction between leaf habit and CE for leaf longevity and SLA (ANCOVA; Table S2). Log(leaf lifespan) showed stronger relationships with CE for evergreen species (r = −0.85, P < 0.001, df = 24) than for deciduous species (r = −0.48, P = 0.09, df = 11), and the same applied for SLA at the leaf level (revergreen = 0.63, P < 0.001; rdeciduous = −0.13, P = 0.67).
Light-demanding species invested, in both forests, a low fraction of their biomass in leaves (LMFm; Fig. 2a,b). Light-demanding species in the moist forest compensated for this low LMFm by making leaves with a high SLA (Fig. 2c) and had, as a consequence, a high leaf area per unit metamer mass (LARm; Fig. 2e). By contrast, light-demanding species in the dry forest did not compensate for a low LMFm with their SLA (Fig. 2d), and they had, therefore, a low LARm (Fig. 2f).
Light-demanding species in the dry forest had high mass- and area-based N and P contents (Fig. 3b,d), whereas light-demanding species in the moist forest had only a high Nmass (Fig. 3a,c). Chlorophyll was only measured for the moist forest species. Chlmass was positively correlated with CE, whereas Chlarea was not correlated with CE (Table 1).
Nine leaf traits were correlated with CE only in the dry forest; light-demanding species had, amongst others, long internodes, thick leaves, and a high internode area to leaf area ratio.
To evaluate which leaf traits are the best predictors of CE, a multiple forward regression analysis was performed, including all measured 26 leaf traits (Table 2). In the moist forest, four traits explained 78% of the variation in CE. Leaf lifespan was first included in the analysis, and explained most (66%) of the variation. CE was negatively related to leaf lifespan, and positively related to internode cross-sectional area, SPL, and leaf mass fraction. In the dry forest four traits explained 67% of the variation in CE. CE was positively related to internode length, and negatively related to leaf lifespan, LARm, and deciduousness.
Table 2. Results of a forward multiple regression of 26 traits on the juvenile crown exposure of moist forest species and dry forest species
| ||b||r2|| ||b||r2|
|Constant||0.234|| ||Constant||3.206|| |
|Total|| ||0.78|| || ||0.67|