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Ecology |
2Faculty of Environmental and Symbiotic Sciences, Prefectural University of Kumamoto, Kumamoto 862-8502, Japan; 3Faculty of Agriculture, Hasanudin University, Makassar 90245, Indonesia; 4Faculty of Science, Kagoshima University, Kagoshima 890-0065, Japan
Received for publication February 16, 2004. Accepted for publication September 16, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: allometry • architecture • coexistence • Indonesia • interspecific comparison • Pterospermum diversifolium • Pterospermum javanicum • regeneration niche • Sterculiaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Tree architecture has long been of interest, and its adaptive significance for growth and survival has been discussed by many researchers. Horn (1971)
demonstrated mathematically that a monolayer arrangement of foliage within a crown is effective for assimilation under closed canopies, whereas multilayer arrangements are more effective in canopy gaps. Kohyama (1987)
and King (1990)
emphasized the importance of tree architecture from the viewpoints of static functioning (which optimizes leaf display under current light conditions) and dynamic functioning (which enhances the opportunistic use of light following disturbance).
Understanding these functions led researchers to two important findings concerning tree architecture. First, sapling architectures are related to the mature height of a species (King, 1990
; Aiba and Kohyama, 1997
). Because static functioning is more important for permanent understory shrubs, they should have an architecture that leads to increased leaf area while minimizing self-shading within their crowns. In contrast, dynamic functioning is more important for young saplings of canopy species, and they should have an architecture that reduces the biomass requirement per unit of height growth. Second, temporal and spatial fluctuation in the understory light environment induces allometric variations among coexisting understory saplings and promotes the coexistence of different species at equilibrium by accelerating the diversification of regeneration niches (Grubb, 1977
). Kohyama (1991)
demonstrated this phenomenon mathematically, and Aiba and Kohyama (1997)
did it empirically. These research efforts led to broad acceptance that architectural and allometric variations influence the growth and survival of tree species and can lead to their coexistence at equilibrium. Hence, information about tree architecture can be a strong tool in assessing species' growth strategies.
However, most previous research has compared the architecture of trees belonging to different taxonomic groups. Interspecific comparisons should be done using closely related species for two reasons. The first reason is that the coexistence of closely related species with similar ecological and physiological characteristics is central to our understanding of the maintenance of biodiversity (Ashton, 1988
). The second reason is phylogenic constraint. A hierarchically structured phylogeny undermines the comparison of two phenotypes across two higher taxa, and can lead to serious statistical problems (Felsenstein, 1985
). Interspecific comparisons within a genus are most likely to weaken this phylogenic constraint. Furthermore, previous researches compared species architectures only for juveniles, not for the entire development trajectory through to maturity. Only a few researchers have studied a species' growth trajectory from the juvenile stage to reproductive maturity (Alvarez-Buylla and Martinez-Ramos, 1992
; Thomas, 1996
; Yamada and Suzuki, 1996
; Aiba and Kohyama, 1997
). As Poorter and Werger (1999)
pointed out, the outcome of interspecific comparisons is very sensitive to the choice of ontogenetic trajectory reflected in the comparison, and thus the entire development trajectory from seedling to reproductive maturity should be studied.
This paper analyzes interspecific differences in whole-plant developmental trajectories from seedlings to reproductive maturity for two sympatric congeneric species, Pterospermum diversifolium Bl. and P. javanicum Jungh. (Sterculiaceae) in a floodplain rain forest in Indonesia. We characterize the growth strategies of the two species from the viewpoint of their individual growth trajectories and propose mechanisms for the coexistence of the two congeneric species within a forest community in terms of their different growth strategies.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). According to Kochummen, these species are fast-growing, light-demanding trees that regenerate only in canopy gaps and on the fringes of forests. However, in our study site in the Indonesian tropical floodplain forest, we found many Pterospermum trees under closed canopies. In particular, we found two species (P. javanicum and P. diversifolium) growing under these conditions. These species form part of a continuous canopy at about 30 m aboveground and can become part of the emergent layer.
Study site
We performed our study in an equatorial floodplain forest in Labanan (Berau, East Kalimantan, Indonesia; latitude 1°52'30'' N, longitude 117°12'00'' E). The forest was designated as a 100 ha forest reserve in the Labanan concession of PT. Inhutni I, Indonesia. Records of precipitation at the Tanjun Redeb airport (ca. 20 km from the study site) from 1971 to 2000 give an average annual precipitation of 2012 mm.
A 100 x 100 m permanent sample plot was established within the forest in 2002 at an altitude of 30 m, and all trees greater than 4.8 cm DBH (diameter at breast height, 130 cm above the ground) were tagged with an aluminum number plate; the trees were then identified, their DBH was measured, and their location was mapped (E. Suzuki, Faculty of Science, Kagoshima University, unpublished data). Endertia spectabilis Steenis & de Wit of the Fabaceae (Caesalpinioideae) was abundant within the plot. Dipterocarp trees from the genera Shorea, Dryobalanops, Parashorea, and Anisoptera were also present. Numerous species belonging to the Euphorbiaceae, Ebenaceae, Annonaceae, Sapindaceae, and many other families formed the main continuous canopy at a height of about 30 m. P. javanicum was the fifth most abundant tree species in the plot; P. diversifolium was the 34th most abundant species. We found 97 and 265 individuals of P. diversifolium and P. javanicum, respectively, in the 1-ha plot. The values of the index of skewness for the frequency distribution of tree heights in the plot were positive for each species, which suggests that some big trees were present with many small trees, generating the inverse J-shaped frequency distribution typically observed for shade-tolerant species with plentiful regeneration.
Nondestructive sampling
All Pterospermum trees in the plot were identified to the species level, then were tagged using numbered plastic tapes. Each tree's location was mapped, and tree height was measured in August 2002. Tree height was defined as the height of the top of the crown for trees greater than 4.8 cm in DBH. For smaller trees, the same value was defined as stem height. In addition, the diameters at ground level and the crown widths of all Pterospermum trees that appeared to be sound and that showed no evidence of past breakage were measured by averaging two measurements, and the height at the lowest leaf (or branch, if present) was recorded. We also recorded the presence or absence of branches. To increase our sample of large trees, we added 11 trees that lay outside the plot and measured tree height, height at the lowest leaf (or branch), the stem diameter at ground level and crown diameter (again, using two measurements). The stem diameter (D, in centimeters) and crown width (Cr, in meters) were defined as the geometric mean of two measurements of the respective diameters. The crown depth (Cd, in meters) was defined as the difference between tree height (H, in meters) and the height of the lowest leaf (or branch).
Destructive sampling
Thirty-five and 28 trees of P. javanicum and P. diversifolium, respectively, with stem heights ranging from 20 to 150 cm, were destructively sampled to permit a detailed analysis of allometric relationships for the juvenile trees. These samples were collected from around the plot under closed canopies. Only trees that appeared sound were selected for sampling. All sampled P. diversifolium lacked branches (hereafter, these are referred to as "monoaxial"), but 89% of the sampled P. javanicum had branches. A crown projection photograph (top view) of all samples was taken before sampling. The juvenile trees were then cut at ground level, and the following parameters were measured: stem height, stem diameter at ground level and crown diameter (two measurements each, as described in the previous section), height at the lowest leaf and branch (whichever one occurred first), number of branches originating at the main stem, number of leaves on the tree, and length (from petiole base to leaf tip) of the longest leaf on the tree. The leaf area and the dry masses of petioles, leaf blades, stems, and branches were also measured. Stem height and the length of the longest leaf on the tree were measured for an additional 14 trees for P. diversifolium with heights ranging from 200 to 600 cm. To determine the leaf size of the mature trees, we measured the lengths of 10 leaves from a mature tree taller than 30 m for each species. From these data, we determined stem height, stem diameter, crown width, crown depth, oven-dry stem mass (Ms, in grams), leaf mass (Ml, in grams), support mass (Msup = petiole dry mass + branch dry mass, in grams), and total mass (M = Ms + Ml + Msup, in grams) for each sample tree.
Data analysis
We compared the allometric relationships for the two species for development of the entire plant using data derived from nondestructive sampling. To examine interspecific differences in juvenile allometric relationships in more detail, we used data derived from destructive sampling. For our analysis of the juvenile allometries, we examined three combinations of allometric pairs: (1) length dimensions (the top three pairs in Table 2), (2) length and mass dimensions (the fourth and fifth pairs in Table 2), and (3) mass dimensions (the sixth through eighth pairs in Table 2). For the analysis of whole-plant development, we lacked mass data and thus examined only allometries relating to length dimensions.
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 | (1) |
; Niklas, 1994
). The nonlinearity model for an allometric relationship used a generalized allometry (Aiba and Kohyama, 1996
, 1997
; Thomas, 1996
):
 | (2) |
). The expanded allometry has fewer degrees of freedom because of more constants, and the RSS in Eq. 2 is smaller than that in the simple allometry (Eq. 1).
We examined the linearity and nonlinearity of the allometric relationships by means of an ordinal extension of the analysis of variance (Snedecor and Cochran, 1980
):
; Thomas, 1996
).
Because the F test showed that all the juvenile allometries were linear or provided a better fit by means of simple allometry than by using expanded allometry, we used the simple allometry for our interspecific comparison. For this comparison, we applied an ordinal ANCOVA test, which is commonly used to compare allometric relationships (Kohyama, 1987
; Kohyama and Hotta, 1990
; Kohyama and Grubb, 1994
). Although this test is based on the Model I regression method, we chose to use it for two reasons: (1) we were not interested in specifying the values of the regression parameters, but rather in detecting differences in parameters between the species, and (2) the related species would presumably show similar errors or deviations.
The differences in the slope (b) of the allometric line were tested first to detect homogeneity of slopes. If the slopes did not differ, the difference in the adjusted Y intercept of the allometric line was tested using the same slope for both species. Species with a greater slope show a greater increase in Y per increment of X, and species with a greater Y intercept (for the same slope) have a greater Y for any particular value of X.
Because the F test showed that all allometric relationships for whole-plant development, with the exception of the D–Cr relationship for P. diversifolium, were nonlinear or provided a better fit by means of the expanded allometry, we compared allometric relations for the two species using the expanded allometries. For this comparison we used an ordinal extension of the analysis of variance:
n – 3).
Evaluation of self-shading
We adopted a simplified approach to empirical measurement of the degree of self-shading (DSS) caused by upper leaves within a crown (Chazdon, 1985
; Yamada et al., 2000a
). The DSS value (expressed as a percentage) is defined as the ratio of the sum of overhead projections of the leaf area of all leaves within a crown to the sum of projected areas of leaves overlapped (shaded) by upper leaves; a crown with no leaves shaded by upper leaves would have a DSS value of 0%. This ratio is based on the simple assumption that a given leaf undergoes no self-shading if no upper leaves overlap it horizontally (i.e., if their vertical projection does not overlap that of the lower leaf).
We calculated DSS values for each of the destructively sampled trees. These samples had grown under closed canopies, and under these conditions light coming from angles nearer to the horizon is likely to be intercepted by the stems and crowns of neighboring trees. Most of the light captured by a tree's leaves, therefore, would come from angles nearer to the vertical, and reducing the extent of self-shading could significantly increase the tree's whole-crown carbon gain.
Leaf margins of all leaves in photographs of the crowns taken from directly overhead were traced onto tracing paper, and the leaves drawn on the tracing paper were painted. Leaf margins of shaded parts were likewise traced and painted. Leaves completely shaded by upper leaves and not visible in these views were accounted for by photographing the crowns with the shading leaves removed. All these papers were scanned, and the total area and total shaded leaf area for all leaves within a crown were determined by counting painted pixels using an area meter programmed in Photoshop 5.0 (Adobe Inc., San Jose, California, USA).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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). The monoaxial growth habit is considered to be an adaptation that favors rapid height growth because it reduces the amount of energy allocated to horizontal growth (Givnish, 1978
). Because a large part of the strength of the petiole and rachis derives from turgor pressure and fibrous materials, development of these structures consumes less energy than the production of woody branches bearing the same load. Therefore, a monoaxial growth habit with large, expendable leaves (Givnish, 1984
) maximizes the amount of energy available for vertical growth at a given stem height and thus promotes rapid height growth. Consequently, juvenile P. diversifolium that retained a monoaxial growth habit for longer (until a larger tree size) than P. javanicum and deployed large leaves directly on the stem during monoaxial growth, follow a dynamic function of tree architecture to enhance the opportunistic use of light after a disturbance rather than a static function that optimizes leaf display under current lighting conditions.
The observed D–H and M–H relationships for juveniles support the hypothesis that P. diversifolium's growth strategy emphasizes height growth. Curves for this species have a significantly higher slope for the D–H and M–H relationships than P. javanicum. This means that P. diversifolium attains more height growth than P. javanicum for a given increment in D and M. The slopes of the D–H curves for P. diversifolium and P. javanicum were 1.90 and 1.33, respectively. These values are much greater than the values for models based on constant stress or elastic similarity, which are 0.50 and 0.67, respectively (McMahon, 1973
; Sposito and Santos, 2001
). This means that the safety margin for stem rigidity (i.e., the ratio of actual stem diameter to the theoretical calculated minimal diameter to prevent elastic buckling) decreased with increasing tree size. Similar trends have been reported for other tropical Sterculiaceae (Yamada et al., 2000b
, 2001
) and for many other tree taxa (King, 1990
; Sposito and Santos, 2001
). Rapid height growth would be favored over stem stability by juvenile trees in tropical forests, in which vertical gradients in relative light availability are steeper than in forests outside the tropics (Yoda, 1974
).
Juvenile P. diversifolium had smaller crown widths and higher values of DSS than P. javanicum. Because monoaxial growth must initially expand crown width by displaying larger leaves, horizontal growth is limited compared with trees that adopt a branching growth habit. Furthermore, the monoaxial growth habit develops large leaves toward the stem's leader, leading to significant self-shading of lower leaves. Consequently, the static function of tree architecture of P. diversifolium is inferior to that of P. javanicum. Unlike P. diversifolium, P. javanicum branched well starting at a younger age. The branching growth habit expands crown area by making and expanding branches with small leaves, thereby distributing the leaves more widely to achieve a low DSS and create a monolayer crown shape. Therefore, P. javanicum's architecture is more effective in terms of increasing survival at a given height or under darker conditions than is the case for P. diversifolium.
Growth trajectories
Many researchers have suggested that a nonlinear function for the generalized allometry would better fit observed D–H relationships for whole-plant development (Aiba and Kohyama, 1996
; Thomas, 1996
). The maximum heights we estimated using a generalized allometry for D–H relationships were lower for P. diversifolium than for P. javanicum. This is because the architecture of juvenile P. diversifolium is suitable for rapid initial height growth, but height growth ceases when these trees reach the canopy layer and the trees rarely pass through the layer to become emergents. King (1996)
found that long-lived species showed a greater increase in crown diameter when they reached the upper end of their height range. Yamada et al. (2001)
observed a switch from stem elongation to radial growth with increasing tree size in another tropical species in the Sterculiaceae (Scaphium longiflorum Ridley); small trees elongated rapidly but thickened less during rapid stem elongation, whereas large trees elongated relatively little but thickened rapidly to strengthen the stem's mechanical stability. The relative importance of rapid height growth and stem stability for a tree would depend on tree size. An alternative explanation of the nonlinearity of the D–H relationship involves the relationship's dependence on reproductive maturity (Thomas and Ickes, 1995
; Thomas, 1996
). The D–H relationship, leaf proliferation, and leaf size are all known to show pronounced allometric discontinuities associated with the onset of reproduction (Alvarez-Buylla and Martinez-Ramos, 1992
; Thomas and Ickes, 1995
; Thomas, 1996
). More studies are needed to assess the allometric discontinuities related with reproductive onset and to identify the size at which reproductive onset occurs for various species.
Pterospermum javanicum continued height growth after reaching the continuous canopy layer and passed through this layer to become emergent. In contrast with D–H relationships, P. javanicum ceased crown expansion after reaching the canopy layer, although juveniles allocated considerable energy to expanding their crown area. The asymptotic maximum crown width for P. javanicum, estimated using a generalized allometry, was smaller than that of P. diversifolium. Thus, the allometric strategies adopted by juveniles appear to be largely independent of those adopted by larger trees. This suggests that diverse pathways to reaching maturity should exist among tropical trees, a finding that would not have been revealed had we analyzed only juvenile architectures and allometries. The study of whole-plant development trajectories is strongly recommended for researchers interested in clarifying the diverse growth strategies that may be adopted by tropical trees passing from the seedling stage to maturity.
Coexistence mechanisms for two congeneric species within a community
Differentiation of growth strategies between P. diversifolium and P. javanicum, assessed by means of tree architecture, can be expected to lead to equilibrium coexistence in a community if the two species differ in their regeneration niche as a function of understory light conditions. This is because each phenotype potentially provides competitive advantages, and these advantages depend on understory light conditions. In the competition for growth and survival between these two species, P. diversifolium is hypothesized to outperform P. javanicum in bright microsites because its architecture is better adapted to rapid height growth. In contrast, P. javanicum is hypothesized to outperform P. diversifolium in shaded microsites because its architecture is better adapted to light assimilation under those conditions. Therefore, we can expect that the spatial distribution of P. diversifolium in a forest community will be restricted to brighter microsites, whereas P. javanicum will be more widely distributed where understory light is limited. Furthermore, stem elongation by P. diversifolium in bright microsites is likely to be more rapid than that of P. javanicum. To verify these hypotheses, further comparative studies of spatial distribution, survival, and growth in relation to understory light conditions will be needed.
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FOOTNOTES |
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5 Author for correspondence (tyamada{at}pu-kumamoto.ac.jp
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Poorter L. M. J. A. Werger 1999 Light environment, sapling architecture, and leaf display in six rain forest tree species. American Journal of Botany 86: 1464-1473
Snedecor G. W. W. G. Cochran 1980 Statistical methods, 7th ed. Iowa State University Press, Ames, Iowa, USA
Sposito T. F. A. M. Santos 2001 Scaling of stem and crown in eight Cecropia (Cecropiaceae) species of Brazil. American Journal of Botany 88: 939-949
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Thomas S. C. K. Ickes 1995 Ontogenetic changes in leaf size in Malaysian rain forest trees. Biotropica 27: 427-434[CrossRef][ISI]
Yamada T. Y. Kumagawa E. Suzuki 2001 Adaptive significance of vegetative sprouting for a tropical tree, Scaphium longiflorum (Sterculiaceae), in a peat swamp forest in Central Kalimantan. Ecological Research 16: 641-647[CrossRef][ISI]
Yamada T. T. Okuda M. Abdullah M. Awang A. Furukawa 2000a The leaf development process and its significance on reducing self-shading of a tropical pioneer tree species. Oecologia 125: 476-482[CrossRef][ISI]
Yamada T. T. Yamakura H. S. Lee 2000b Architectural and allometric differences among Scaphium species are related to microhabitat preferences. Functional Ecology 14: 731-737[CrossRef][ISI]
Yamada T. E. Suzuki 1996 Ontogenetic change in leaf shape and crown form of a tropical tree, Scaphium macropodum (Sterculiaceae) in Borneo. Journal of Plant Research 109: 219-225[CrossRef][ISI]
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= monoaxial Pterospermum diversifolium, 
= branched P. javanicum, and x = monoaxial P. javanicum. Leaf length is defined as the sum of the blade and petiole lengths
