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Tropical Biology |
2Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan; 3Nikko Botanical Garden, Graduate School of Science, University of Tokyo, Nikko, Tochigi 321-1435, Japan; 4National Institute for Environmental Studies, Ibaraki, Japan; 5Faculty of Science and Environmental Studies, Universiti Putra Malaysia, Serdang, Malaysia; 6Graduate School of Life Sciences, Tohoku University, Aoba, Sendai 980-8578, Japan
Received for publication July 15, 2004. Accepted for publication February 23, 2005.
ABSTRACT
In aseasonal tropics, timing of leaf emergence and leaf fall may differ between the shoots of different crown parts within a tree. This is important for the efficient development of crowns because leaves should be produced as soon as enough carbohydrates are accumulated. This hypothesis was tested by investigating leaf demography over a 44-mo period for 17 Malaysian trees and comparing the timings of leaf emergence and fall between the upper and lower crowns. The timings of leaf emergence were synchronized between the upper and lower crowns, but those of leaf fall were less synchronized in most trees. Greater rates of leaf production in the upper than in the lower crowns were attributable to the differences in the number of leaves that emerged per leaf emergence event, rather than differences in frequency of leaf emergence per year. Timings of leaf emergence and leaf fall were mainly simultaneous in the upper and lower crowns, but unsynchronized leaf production and leaf fall also occurred. Such limited plasticity of leaf demography within crowns may be the result of physiological integration of branches or the compromise between the advantages of satiating herbivores and effective crown development in the trees of aseasonal tropics.
Key Words: crown development • leaf emergence • leaf fall • leaf phenology • Malaysia • tropical trees
In tropical regions, leaf phenology and demography are highly diverse across various tree species (e.g., Osada et al., 2001
; Reich et al., 2004
). Because leaf phenology and demography strongly influence forest productivity and plant–animal interactions, these traits have been investigated in various tropical forests (e.g., Medway, 1972
; Frankie et al., 1974
; Reich and Borchert, 1984
). In these studies, leaf phenology has been related to abiotic factors such as seasonalities in rainfall or water stress (e.g., Reich and Borchert, 1984
; Borchert, 1994
) and irradiance (e.g., van Schaik et al., 1993
; Wright, 1996
) and biotic factors such as reducing herbivory (e.g., Aide, 1993
). In aseasonal tropical rain forests, water stress would not be the main factor affecting leaf phenology (e.g., van Schaik et al., 1993
; Wright, 1996
). Alternatively, irradiance seasonality and the effects of herbivores have been emphasized as the main factors (e.g., Aide, 1993
; van Schaik et al., 1993
). However, most of these studies have concentrated on leaf phenology at the levels of forest community, species, and/or an individual tree, and variations in leaf phenology and demography within crowns of an individual tree have received much less attention.
Tall trees have large crowns, and the light microenvironments vary widely within crowns (e.g., Parker, 1995
; Niinemets et al., 1999
). Such variations in light microenvironment are expected to affect the shoot growth patterns and leaf phenology within crowns. For efficient crown development, the enhancements of shoot extension and associated leaf production are more important for sunlit parts than for shaded parts of the crowns (Sprugel et al., 1991
; Takenaka, 1994
; Stoll and Schmid, 1998
). In accordance with this, leaf production rate was greater in the upper than in the lower crowns for most trees in a Malaysian rain forest (Osada et al., 2001
). In aseasonal forests, seasonality in meteorological factors would not regulate the phenology, and the timing of leaf production may depend on the accumulation of carbohydrates of the shoots. Actually, leaf production phenology was not related to any meteorological factors at the population level, and the frequency of leaf emergence (per year) was greater in saplings in higher light in a tropical tree, Elateriospermum tapos (Osada et al., 2002
). Leaf phenology and demography are thus expected to differ even within crowns, depending on the light microenvironment of the shoots.
On the other hand, the timing of leaf emergence may be synchronized within a whole crown because of the physiological integration of tree crowns (Watson and Casper, 1984
). This phenological synchrony may be adaptive by satiating herbivores (Aide, 1993
) and by producing flowers synchronously to attract pollinators (Osada et al., 2002
). Osada et al. (2002)
showed synchronous leaf production after leaf fall in tall canopy trees of E. tapos, but it is not clear whether this pattern prevails across various tree species. Moreover, the differences in leaf phenology between saplings and tall trees observed for E. tapos brought about another hypothesis that leaf phenology changes depending on tree height.
In this study, we investigated the leaf phenology and demography for the upper and lower crowns of 17 trees of various heights in Pasoh Forest Reserve, Peninsular Malaysia, for which we have already reported basic leaf demography (Osada et al., 2001
) and leaf phenology (Osada et al., 2003a
). Using the same data set, we looked for general patterns in the leaf demography between the upper and lower crown parts that differ in light microenvironment. Particular attention was paid to the question of whether the timing of leaf emergence and of leaf fall is synchronized within crowns and how leaf phenology and demography are related to the patterns of crown development.
MATERIALS AND METHODS
Study site
The study was carried out in the Pasoh Forest Reserve, Peninsular Malaysia (2°59' N, 102°18' E). The Pasoh Forest Reserve is a lowland dipterocarp forest that belongs to the Red Meranti-Keruing type and 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 is 20–30 m (Manokaran and Swaine, 1994
).
The reserve is located in the Jelebu district, which has the lowest annual rainfall in Peninsular Malaysia. Annual rainfall at Kuala Pilah (37 km south of the Reserve) averages 1850.2 mm/yr, with two peaks in April–May and November–December. The mean monthly temperature ranges from 26.0°C to 27.7°C (Manokaran and Swaine, 1994
).
A canopy walkway system, built in April 1992, consists of three towers (two 32 m and one 52 m tall), which are joined by 20-m walkways 32 m above the ground. Because the system is situated on a hill, the top of the 52-m tower is the highest place in the reserve, except for the eastern boundary.
Measurement of leaf demography
Seventeen trees of 16 species of various heights were selected as sample trees to measure leaf demography (Table 1; Osada et al., 2001
, 2003a
). All the trees are classified as shade tolerant.
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). All sample branch units were tagged and sketched in September 1995 to analyze branch number, leaf number, and position of leaves. The number and position of fallen leaves and those of newly emerged leaves were recorded monthly from October 1995 through May 1999. Although the census period was shorter in some trees, it was at least 29 mo (Table 1).
Data analysis of the general pattern of leaf demography within a crown
Because the examined branch numbers were different between the sample branch units of the upper and lower crowns of each sample tree, the number of leaves emerged or fallen could not be compared directly. Therefore, number of leaves emerged and fallen during each month was standardized to a per-branch basis at the beginning, i.e., divided by the number of branches at the beginning of the census. Synchronization of the timing of leaf emergence or leaf fall between the two crown parts was examined for each of the 17 trees by Kendall's rank correlation (JMP ver. 4.0, SAS, Cary, NC, USA).
Leaf production rate (per year; LPR) and leaf loss rate (per year; LLR) were greater in the upper than in the lower crowns in most trees (Osada et al., 2001
). In this study, LPR was divided into frequency of leaf emergence per year (FLE) and number of leaves emerged (per leaf emergence event; NLE) (Osada et al., 2002
): LPR = NLE x FLE. Similarly, LLR was divided into frequency of leaf fall per year (FLF) and number of leaves fallen (per leaf fall event; NLF): LLR = NLF x FLF. These indices for the upper were compared to the lower crown for each tree.
The position of walkways restricts the sampling procedure, and thus one or two sample trees could be selected for each species. Accordingly, we investigated the general patterns of leaf demography within crowns that was found in most trees and did not focus on the species' specific patterns. Because the selection of trees was not random but depended on the position of walkways, the data may not be representative of all trees. Regardless, this study is quite important because within-crown variation in leaf phenology has seldom been investigated previously.
RESULTS
Examples of the phenology of leaf emergence and leaf fall during the census period are shown in Fig. 1. Timing of leaf emergence was synchronized between the upper and lower crowns for 15 of 17 trees (Table 2; Fig. 1). This proportion is far greater than expected at random (P = 0.0012, binomial test). On the contrary, timings of leaf fall were synchronized within crowns for only 10 of 17 trees (P = 0.48). The trees usually produced new leaves synchronously between the upper and lower crowns, but leaf fall was not always synchronous.
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Timings of leaf emergence were synchronized within crowns for most trees. However, FLE (frequency of leaf emergence) differed between the upper and lower crowns for most trees, indicating that the timing of leaf emergence was not completely simultaneous within a crown. Thus, in addition to the synchronized leaf production within crowns (major leaf production), other minor differences in timing of leaf production also occurred in the crown parts. In contrast, NLE (number of leaves emerged per leaf emergence event) was greater in the upper than in the lower crowns of all trees. Greater rates of leaf production in the upper than in the lower crowns (Osada et al., 2001
) are, therefore, mainly attributable to the differences of NLE, rather than those of FLE. Such patterns are found irrespective of differences in tree species and height, suggesting that these patterns are general, at least for the trees of greater than 5 m in height. This result is in contrast to saplings of E. tapos, in which a greater value of FLE was important in increasing the leaf production rate under higher light (Osada et al., 2002
). Thus, leaf demography of branches of tall trees in different light microenvironments may not be described simply by extrapolating the leaf phenology of saplings under different light environments.
It is interesting to note that FLE was not always greater in the upper than in the lower crowns. In accordance with this, minor leaf emergence event was not restricted to upper crowns, but also was found in various crown parts (N. Osada, personal observation). Nonstructural carbohydrate of branches declined during the seasons of leaf production in various tropical tree species (Tissue and Wright, 1995
; Lovelock et al., 1999
; Newell et al., 2002
). We therefore predicted that, because the competition for better-lit space is severe in these studied aseasonal forests, each branch within the crowns should produce leaves and extend new stems as soon as enough carbohydrates accumulate. However, independent leaf production of the shoots within crowns may be impossible because of the physiological integration of branches within crowns. Or rather, the major leaf emergence events may be important to satiate herbivores, and two modes of leaf production, major and minor leaf productions, may be the result of such trade-off relationships between the adaptive significance of synchronous and asynchronous leaf production.
In contrast to leaf production, leaf fall was less synchronous within crowns. Leaf fall was synchronized with those of leaf production in most of the studied trees (Osada et al., 2003a
). These results suggest that leaf fall events can be divided into (1) internally regulated events synchronized with the timings of leaf production and (2) accidental events that occurred during the whole period. To maximize the shoot productivity, nitrogen of older leaves, which were situated in more shaded positions, should be reallocated to well-lit new leaves (Field, 1983
; Hirose and Werger, 1987
; Hikosaka, 2003
; Osada et al., 2003b
). According to this view, synchronous leaf fall with new leaf production is important for maximizing shoot productivity (Hikosaka, 2003
). Such phenological patterns would be possible only in aseasonal forests such as the studied site. In contrast, water stress in dry seasons strongly regulates the leaf phenology in tropical dry forests, with most of the leaves being dropped during dry seasons (e.g., Reich and Borchert, 1984
; Borchert, 1994
). As causes of accidental leaf fall, herbivore attack and physical disturbance are considered important. Herbivores are particularly important for reducing the newly emerged leaves that are less tough and less defended (Lowman 1992
, Aide 1993
). In addition to this, physical damage occurred throughout the seasons. Because we only investigated the appearance and disappearance of the leaves, these two factors could not be distinguished. The number of leaves fallen per leaf fall event was greater in the upper than in the lower crowns, suggesting that either or both of these two types of events are more common in the upper crowns. As a consequence, FLF became greater than FLE, while NLF became smaller than NLE.
As shown in this study, leaf emergence and leaf fall were primarily simultaneous within crowns, but unsynchronized leaf production and leaf fall also occurred in most trees in the Malaysian rain forest. Such limited plasticity of leaf demography within crowns may be the result of physiological integration of branches or the compromise between the advantages of satiating herbivores and effective crown development in the trees of tropical rain forests, where moderate seasonalities in meteorological factors do not regulate the leaf phenology.
FOOTNOTES
1 The authors thank A. Furukawa, M. Yasuda, and the members of the Laboratory of Forest Ecology, Kyoto University, for their valuable suggestions. The present study is a part of a Joint Research Project between Forest Research Institute Malaysia, Universiti Putra Malaysia, and 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 JSPS Research Fellowships for Young Scientists for N. O. 
7 E-mail: osadada{at}biology.tohoku.ac.jp
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