AOBPreview originally published online on November 13, 2002
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Annals of Botany 91: 55-63, 2003
© 2003 Annals of Botany Company
Branch Architecture, Light Interception and Crown Development in Saplings of a Plagiotropically Branching Tropical Tree, Polyalthia jenkinsii (Annonaceae)
1 Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
* For correspondence at: Nikko Botanical Garden, Graduate School of Science, University of Tokyo, 1842 Hanaishi, Nikko, Tochigi 321-1435, Japan. Fax +81 288 543178, e-mail ss29326{at}mail.ecc.u-tokyo.ac.jp
Received: 10 May 2002; Returned for revision: 18 June 2002; Accepted: 3 October 2002 Published electronically: 13 November 2002
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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To investigate crown development patterns, branch architecture, branch-level light interception, and leaf and branch dynamics were studied in saplings of a plagiotropically branching tree species, Polyalthia jenkinsii Hk. f. & Thoms. (Annonaceae) in a Malaysian rain forest. Lengths of branches and parts of the branches lacking leaves (‘bare’ branches) were smaller in upper branches than in lower branches within crowns, whereas lengths of ‘leafy’ parts and the number of leaves per branch were larger in intermediate than in upper and lower branches. Maximum diffuse light absorption (DLA) of individual leaves was not related to sapling height or branch position within crowns, whereas minimum DLA was lower in tall saplings. Accordingly, branch-level light interception was higher in intermediate than in upper and lower branches. The leaf production rate was higher and leaf loss rate was smaller in upper than in intermediate and lower branches. Moreover, the branch production rate of new first-order branches was larger in the upper crowns. Thus, leaf and branch dynamics do not correspond to branch-level light interception in the different canopy zones. As a result of architectural constraints, branches at different vertical positions experience predictable light microenvironments in plagiotropic species. Accordingly, this pattern of carbon allocation among branches might be particularly important for growth and crown development in plagiotropic species.
Key words: Annonaceae, branch-level light interception, crown development, leaf dynamics, Malaysia, Pasoh Forest Reserve, plagiotropic species, Polyalthia jenkinsii.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A tree crown develops through the repetitive production of shoots, i.e. branches and leaves (Maillette, 1982; Room et al., 1994). Crown architecture directly determines the pattern of leaf arrangement and thus affects light capture efficiency in the crown (e.g. Pearcy and Yang, 1996); it also restricts the direction of future growth (Room et al., 1994). Crown development patterns can therefore be described through the dynamics of the shoot population (Maillette, 1982). Recent studies of crown development have focused on relationships between branch light level and branch development within crowns (Stoll and Schmid, 1998; Takenaka, 2000; Henriksson, 2001). They have revealed the importance of correlative inhibition, i.e. export of photosynthate from low-light branches to high-light branches within individuals, on crown development of various trees. However, the light microenvironment of each leaf on the branches was not investigated; this information is essential to determine the carbon gain of the shoots. On the other hand, by computing the light microenvironment of each leaf in the crown, other studies have investigated the importance of crown architecture and leaf display on efficient light capture at the crown level (Ackerly and Bazzaz, 1995; Pearcy and Yang, 1996, 1998; Muraoka et al., 1998; Yamada et al., 2000; Takenaka et al., 2001). However, only static aspects of crown architecture were measured in these studies and they were not related to the dynamics of crown development.
Tropical forest understoreys are characterized by light resource limitations, and seedlings and saplings of shade-tolerant tree species require physiological and morphological mechanisms to survive and grow effectively in such light-limited environments. Plagiotropic branches, in which leaves grow two-dimensionally along horizontal stems (Hallé et al., 1978), may enhance light capture efficiency, and are considered preferable to orthotropic branches in shaded environments (Givnish, 1984; King and Maindonald, 1999). In plagiotropically branching species (referred to as ‘plagiotropic species’ hereafter), however, there is a conflict between vertical and horizontal growth, because vertical growth is critical to successful regeneration, whereas horizontal leaf dispersion is necessary for efficient light capture (Zipperlen and Press, 1996). King et al. (1997) found that branch spacing increased with increased growth rates and light levels in various plagiotropic species, but these authors did not consider the effects of branch architecture on the growth patterns of these species. Zipperlen and Press (1996) found that saplings of Shorea leprosula maximized height growth, whereas the more shade-tolerant Dryobalanops lanceolata tended to produce long branches that increased light interception.
From a dynamic point of view, however, lower plagiotropic branches are inevitably shaded by newly produced upper branches. Accordingly, even if plagiotropic branches are expanded in small saplings, these branches will be shed during the course of growth and will not contribute to the architecture of later stages of the tree. Thus, there may be an optimal strategy for the growth of plagiotropic branches in different vertical positions within saplings; assimilated carbon may be exported from lower branches to upper branches to expand new leaves, as well as to the main stem and roots. Since tall saplings should produce a larger leaf area than smaller saplings in order to cope with the larger proportion of non-photosynthetic organs (e.g. Shukla and Ramakrishnan, 1984; Ardhana et al., 1988), the optimal strategy for the growth of plagiotropic branches and leaf display may also change with increasing sapling height. Tall saplings may produce longer branches and a larger leaf area per branch than smaller saplings by changing the number of leaves and/or the individual leaf area.
In this study, branch architecture, branch-level light interception, and leaf and branch dynamics were analysed in saplings of a shade-tolerant tree species, Polyalthia jenkinsii Hk. f. & Thoms., in a Malaysian rain forest. This species produces plagiotropic branches along a vertical main stem during the sapling stage. The following questions were addressed. (1) Do branch architecture and leaf and branch dynamics differ among branches at different vertical positions within saplings and among saplings of different heights? (2) How are these factors related to the light interception capacity of the leaves on these branches?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Study site and species
The study was conducted at the Pasoh Forest Reserve, Peninsular Malaysia (2°59'N, 102°18'E). The Pasoh Forest Reserve is a lowland dipterocarp forest of the Red Meranti–Keruing type, which is dominated by Shorea spp. (Red Meranti group) and Dipterocarpus spp. (Keruing; Manokaran et al., 1992). The emergent layer averages 46 m and the height of the main canopy ranges from 20 to 30 m (Manokaran and Swaine, 1994). Branch architecture, leaf and branch dynamics, and light interception of saplings of a shade-tolerant tree species, Polyalthia jenkinsii Hk. f. & Thoms. (Annonaceae), were studied. During the sapling phase, this species grows vertical main stems with expanding plagiotropic branches and is, therefore, considered to be a typical plagiotropic species.
Data collection
In April 1997, saplings of P. jenkinsii (n = 11) in a shaded understorey were selected to investigate leaf and branch dynamics. Saplings of various heights (30–240 cm) were chosen to investigate the effect of sapling height. First-order branches and leaves were tagged, and tree architecture and leaf positions were sketched to allow for the identification of each leaf. The number and position of missing and newly emerged leaves and branches were recorded monthly from May 1997 to May 1999.
In addition, nine individuals of P. jenkinsii (30–210 cm tall) were chosen in the shaded understorey in September 2000 on which the following variables were measured: length of first-order branches; length from branch base to the oldest leaves (length of ‘bare’ branches); length from the oldest leaves to the branch tip (length of ‘leafy’ branches); average angle of a first-order branch from the horizontal; number of leaves on all first-order branches; and lengths of leaf blades and internodes. Furthermore, geometric measurements of architectural characters were carried out for four of the nine saplings of various heights (32, 70, 132 and 210 cm). For each node, lengths, angles and azimuths of the petiole, leaf surface and internode extending from this node, and the azimuth of the midrib were recorded using a ruler, level and compass. Angles and azimuths were almost constant for all internodes within most plagiotropic branches and were therefore recorded once for each of these branches. For branches that had an obvious bend, length, angle and azimuth measurements were taken for the portions above and below the bend. For each leaf, the azimuth of the normal to the surface, the angle of the surface from the horizontal, and the azimuth of the midrib and the leaf blade length from the petiole attachment point to the tip were also measured. Coordinates for leaf-blade shape were obtained by tracing representative leaves on to graph paper and then recording the x- and y-coordinates for points on the leaf margins, starting with x = y = 0 at the point of attachment of the petiole, with the midline of the leaf as the y-axis.
Data analysis
Leaf population dynamics were expressed as changes in leaf number, which is a result of the birth and death of leaves on a branch. Changes in leaf number were expressed as the net leaf gain rate (number per year), and this rate was divided into two components: the leaf production rate (number per year) and the leaf loss rate (number per year; Bongers and Popma, 1990; Osada et al., 2002). All indices were calculated on a per first-order branch basis, and only branches that existed from the beginning of the census were used in the analyses. In addition, the rate of branch increase (number per year) was calculated for each first-order branch; this accounted for the death of that branch and the emergence of any second-order branches, i.e. the branch increase rate was zero when the first-order branch died, whereas it was >1 when new second-order branches emerged within the first-order branch system. The rate of increase in the number of first-order branches (number per year) was also calculated.
First-order branches of each individual sapling were categorized into classes based on their vertical position at the beginning of the census, i.e. upper, intermediate and lower parts of the crown. The indices of branch architecture and leaf and branch dynamics were averaged for the branches in each position class of each sapling. As we were interested in changes in the patterns of crown development with increasing sapling height, analysis of covariance (ANCOVA) was used to investigate relationships between sapling height and indices of branch architecture, and leaf and branch dynamics among branches in different position classes. In the ANCOVA model, relative branch position (upper, intermediate and lower) was a factor, and sapling height a covariate. The interaction between branch position and sapling height was used to test for differences in slopes among branches in different positions. If height yielded consistently parallel gradients of the indices, then there would be a significant covariate effect in the ANCOVAs. A significant interaction term, on the other hand, would indicate that the slopes of the relationships varied among branches in different positions. If there was no significance in the covariate analysis then the significance of differences among branches at different positions was evaluated using ANOVA.
The three-dimensional computer model ‘Y-plant’ (Pearcy and Yang, 1996; Valladares and Pearcy, 1999) was used to simulate light interception of each leaf of four saplings on which geometric measurements had been taken. Branch and petiole diameters were assumed to be 1 mm, and leaf absorptance and transmittance of the adaxial surfaces were assumed to be 0·85 and 0·10, respectively. Fractional diffuse light absorption (DLA) was estimated for each leaf. Simulations of DLA were based on vectors for 160 different sky sectors (eight azimuth and 20 angle classes). To investigate the generality in the patterns of light interception for the leaves of branches in different vertical positions, simulations were conducted for the open canopy (no hemispherical photographs) and for the average understorey light environment. The average understorey light environment was calculated from 25 hemispherical photographs taken under closed forest canopy in the same forest (CoolPix 910 with FC-E8 fisheye converter; Nikon, Tokyo, Japan), which took into account the small contribution of light from a low angular altitude relative to the total light. Images of hemispherical photographs were analysed using Hemiview ver. 2·1 (Delta-T Devices, Cambridge, UK). Both simulations showed similar results, so only the results obtained from the open canopy (no hemispherical photographs) are presented here. Fractional DLA was multiplied by the relative leaf area of each leaf within each individual sapling, and was then summed for all leaves on a branch to investigate the relative light interception of each branch. Relative light interception at the branch level was also averaged for branches in each vertical position class (upper, intermediate and lower parts of the crown) for each sapling. Moreover, to investigate the effects of branch number on light interception, the relative light interception of total branches within each positional class was also calculated.
Theoretically, plagiotropic branches should expand horizontally to capture light efficiently. A hypothetical architecture was therefore constructed on a computer by changing the angles of first-order branches to be horizontal, and relative light interception was then calculated for the simulated saplings. Values of relative light interception were compared for real and simulated saplings.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Branch architecture
Figure 1 shows the differences in branch architecture in relation to sapling height for branches at different vertical positions. An interaction between height and branch position was detected for branch length and length of bare branches (Table 1). Branch length and bare branch length were larger in tall saplings than in small saplings, particularly in the lower branches, whereas these lengths remained almost constant in the upper branches, irrespective of sapling height (Fig. 1). In contrast, leafy branch length was larger in intermediate branches than in upper and lower branches, and larger in tall saplings. The branch angle (measured from the horizontal) was larger in upper than in lower branches, but was not related to sapling height (Table 2). Leaf number per first-order branch was larger in intermediate than in upper and lower branches, and was not related to height (Table 2). Leaf and internode lengths were not related to branch position, but were larger in tall saplings, although the relationship between leaf length and height was only marginally significant [Table 1; Li = 0·0814H + 18·28, r2 = 0·221; Ll = 0·225H + 118, r2 = 0·137, n = 27, where Li is internode length (mm), H is height (cm), and Ll is leaf length (mm)]. The number of first-order branches also increased with height (B = 0·0598H + 3·68, r2 = 0·687, n = 11, where B is the number of first-order branches). Thus, as saplings grew taller, the lower branches increased in length while the length of leafy parts decreased, and they had fewer leaves than intermediate branches. In contrast, the upper branches were short and had few leaves, irrespective of the height of the sapling.
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Light interception
Diffuse light absorption of individual leaves changed with sapling height but not with branch position (Fig. 2; Table 1). Maximum DLA was not related to height or branch position (Table 1); in contrast, minimum DLA was related to height, being reduced for tall saplings. Consequently, the range of DLA was also related to height, and was greater in tall saplings (Fig. 2; Table 1).
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Relative light interception at the branch level was larger in intermediate than in upper and lower branches, and was smaller in tall saplings (Fig. 3; Table 1). This indicates that relative light interception at the branch level was influenced more by the difference in standing leaf number on the branch than by DLA of individual leaves within the branch. Relative light interception of total branches within each branch position class (upper, intermediate and lower branches) was larger in intermediate than in upper and lower classes, but was not related to height because the number of first-order branches was larger in tall saplings (Fig. 3; Table 1). The relative contribution of light interception was, thus, similarly larger in intermediate branches than in upper and lower branches within a crown irrespective of sapling height.
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According to the branch-angle simulation experiments, the relative light interception of the four saplings was slightly but consistently higher in the simulated horizontally fixed branches than in actual branches at all branch positions (Fig. 3). This indicates that variations in the branch angles of real saplings do not increase light capture efficiency.
Leaf and branch dynamics
The rate of leaf production was higher and that of leaf loss was smaller in upper than in lower branches (Fig. 4; Table 1). Moreover, leaf production and loss rates were higher in tall saplings (Fig. 4; Table 1). Consequently, net leaf gain rate was not related to sapling height, and was larger for upper than for lower branches (Table 2).
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The rate of increase in the number of branches was not related to sapling height. However, it was larger in upper than in lower branches, and it was less than one branch per year for most of the intermediate and lower branches because of the death of branches (Fig. 5; Table 2). Almost all first-order branches produced during the census period were in the upper crown, and the production rate of the new first-order branches was higher in tall saplings (Fig. 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Branch architecture was clearly related to the relative vertical positions of branches and to sapling height. Branch length indicates the trajectory of past growth, and was larger in lower than in upper branches of tall saplings, whereas it was almost the same in small saplings. The length of bare branches, an index of the number of leaves that have dropped, tended to be larger in lower than in upper branches of tall saplings. The length of leafy branches was larger and there were more leaves on intermediate branches than on lower branches, irrespective of sapling height, suggesting that growth declines in the lower branches because of shading by highly developed intermediate branches, whereas the upper branches are still in an early stage of development. Because leaf and internode lengths were not related to branch position, differences in leaf size did not affect the patterns of branch architecture within crowns. In contrast, an increase in leaf size may be important for increasing the total leaf area at the branch level in tall saplings, since leaf size increased as saplings grew taller, whereas the number of leaves per branch was not related to height. Accordingly, the length of intermediate and lower branches increased with increasing sapling height, indicating that crowns became wider as sapling grew taller. This may be important for increasing light interception at the sapling level as saplings grow taller.
Although the maximum DLA of individual leaves was not related to height or branch position, the minimum DLA was smaller and the range of DLA was larger for tall saplings. This suggests that the leaves of tall saplings suffer severe mutual shading compared with those of small saplings. It is not clear why small saplings were unable to maintain leaves with lower DLA. Although all the saplings studied were in a shaded understorey, subtle differences in light environment might affect this pattern. Relative light interception at the branch level was higher in intermediate than in upper and lower branches. This indicates that carbon gain at the branch level may be larger in intermediate than in upper and lower branches within saplings, not as a result of differences in DLA, but instead because of differences in the standing number of leaves on branches. Owing to the increase in branch number, relative light interception at the branch level was smaller in tall saplings than in small saplings, but relative light interception per total number of branches within each branch position class was not related to height. Thus, the relative contribution of light interception of branches of different vertical position classes was similar for saplings of different heights.
Branch angles were steeper in upper branches and were nearly horizontal in lower branches, irrespective of sapling height. Yamada et al. (2000) showed that unbranched saplings of Macaranga gigantea, a tropical pioneer species, produce new leaves near their orthotropic trunks, whereas they deploy old leaves further from the trunks by increasing petiole length and increasing the deflection angle of the petiole relative to the trunk in order to capture light efficiently. The branch architecture of P. jenkinsii can be compared with the leaf morphology of M. gigantea: the length of the bare part of first-order branches in P. jenkinsii is analogous to petiole length, and the length of the leafy part is analogous to leaf blade length in M. gigantea. The crown projection area of the horizontally fixed petiole angle was slightly larger than that of actual plants in M. gigantea (Yamada et al., 2000). Similarly, the actual branch angle did not increase light capture efficiency in P. jenkinsii compared with hypothetical branches that were fixed horizontally. Yamada et al. (2000) attributed this to the increasing height growth rate in actual plants by elongating petioles vertically in young leaves. However, this explanation does not apply to P. jenkinsii, since the angles of upper branches are only about 30° from the horizontal and their effect on increasing height is almost negligible. Changes in branch angle with decreasing vertical branch position within crowns may thus be a developmentally constrained process in P. jenkinsii. It would be difficult and costly to keep branch angles strictly horizontal, and this would only bring minor benefits.
Since the rates of leaf production and loss were higher in tall saplings but net leaf gain rate was not related to height, leaf turnover was faster in tall saplings. As internode length was also larger in tall saplings, crown development was more rapid in tall saplings. Moreover, the rate of leaf production was higher and that of leaf loss was lower in the upper branches than in the lower branches. Leaf dynamics did not, therefore, correspond to branch-level light interception, and upper branches grew more vigorously than intermediate and lower branches. Senescence of lower branches was also evidenced by the low leaf production rate and by the very low branch increase rate (a branch increase rate <1 represents a decrease in the number of branches). Furthermore, new first-order branch production was restricted to the upper crowns, indicating crown expansion upwards. Thus, the ratio of carbon used within the branch (including imported carbon) to carbon fixed by leaves on the branch, which is an estimate of carbon allocation, was higher in upper branches than in intermediate and lower branches. This pattern of carbon allocation parallels that of temperate seedlings that have orthotropic stems with a spiral leaf arrangement: photosynthate from recently matured upper leaves is primarily translocated to developing leaves, but that from lower leaves is mainly translocated to lower stems and roots (Isebrands and Nelson, 1983; Dickson, 1986). Correlative inhibition, i.e. photosynthate export from low-light branches to high-light branches within individuals was recently found in various orthotropic species (Stoll and Schmid, 1998; Takenaka, 2000; Henriksson, 2001). Light environments were measured at the branch level in these studies, but the authors did not take into account the branch-level light interception, i.e. the product of the light environment and the leaf area of the branches. Thus, the results for P. jenkinsii do not contradict the results of these studies. In addition, the present results are the first to describe the relationship between light interception at the leaf level and leaf and branch dynamics in the crown. This approach is important in understanding the patterns of crown development in relation to crown architecture, because the highly diverse architectures found in tropical trees (Hallé et al., 1978) may be related to differences in regeneration strategies.
Owing to architectural constraints, branches at different vertical positions experience predictable light microenvironments in plagiotropic species. If branches were strictly autonomous in carbon allocation in saplings of P. jenkinsii, then lower branches would consistently grow and produce more leaves than upper branches, and the crown width would be larger and sapling height smaller than measured values. The cost of carbon allocation would be reduced in such saplings compared with that in actual saplings. However, this strategy is not adaptive because (1) the light environment generally increases with height (Yoda, 1978; Parker, 1995), (2) tree saplings should grow taller to mature and reproduce, and (3) branches cannot extend indefinitely because of mechanical constraints and the high density of small saplings in a forest understorey. Accordingly, the pattern of carbon allocation among branches at different vertical positions found in P. jenkinsii may be particularly important for growth and crown development in plagiotropic species.
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ACKNOWLEDGEMENTS |
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We thank R. W. Pearcy for critical comments on the manuscript, and A. Furukawa, M. Awang, T. Okuda, M. Yasuda, N. Osawa, Makmom and Shamsuddin and members of the Laboratory of Forest Ecology, Kyoto University, for valuable suggestions. The present study is a part of a Joint Research Project between the Forest Research Institute Malaysia, Universiti Putra Malaysia and the National Institute for Environmental Studies of Japan (Global Environment Research Program granted by Japan Environment Agency, Grant No. E-1). This study was partly supported by a JSPS Research Fellowship for Young Scientists to N.O.
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