WITHIN-CROWN VARIATION IN THE TIMING OF LEAF

Transcription

1 American Journal of Botany 92(7): WITHIN-CROWN VARIATION IN THE TIMING OF LEAF EMERGENCE AND FALL OF MALAYSIAN TREES IN ASSOCIATION WITH CROWN DEVELOPMENT PATTERNS 1 NORIYUKI OSADA, 2,3,6,7 HIROSHI TAKEDA, 2 TOSHINORI OKUDA, 4 AND MUHAMAD AWANG 5 2 Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, Kyoto , Japan; 3 Nikko Botanical Garden, Graduate School of Science, University of Tokyo, Nikko, Tochigi , Japan; 4 National Institute for Environmental Studies, Ibaraki, Japan; 5 Faculty of Science and Environmental Studies, Universiti Putra Malaysia, Serdang, Malaysia; and 6 Graduate School of Life Sciences, Tohoku University, Aoba, Sendai , Japan 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 1 Manuscript received 15 July 2004; revision accepted 23 February 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 osadada@biology.tohoku.ac.jp 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 1210

2 July 2005] OSADA ET AL. WITHIN-CROWN VARIATION IN LEAF PHENOLOGY 1211 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, 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 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 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. For all of the studied trees, two sample branch units of about 1 m 3 were selected from the upper and lower parts of each crown. Because the size of the modular unit (i.e., leaves and branches that were produced in one flush timing) varied among species, the number of modular units within a sample branch unit differed among species (6 40 branches with leaves). No leaves were proximal (i.e., older) to the sample branch units. Light availability varied greatly among these trees primarily because of the difference in tree height. However, the upper crown generally received more light than the lower crown of each tree (Osada et al., 2001). 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 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 perbranch 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 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 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 TABLE 1. List of sample trees (Osada et al. 2001, 2003a). Nomenclature follows Kochummen (1997). Stature class follows Manokaran et al. (1992). Study period (mo) Stature class Height of branch unit (m) Upper Lower Lowest leaf height (m) Abbreviation Sample tree Family DBH (cm) Height (m) Et Elateriospermum tapos Bl. Euphorbiaceae Canopy Xs1 Xanthophyllum stipitatum Benn. Polygalaceae Canopy Ds Dipterocarpus sublamellatus Foxw. Dipterocarpaceae Emergent Pc Ptychopyxis caput-medusae (Hk.f.) Ridl. Euphorbiaceae Canopy Gs Ganua sp. 1 Sapotaceae Canopy Er Eugenia rugosa (Korth.) Merr. Myrtaceae Canopy Mf Mangifera foetida Lour. Anacardiaceae Canopy Cs Chionanthus sp. 1 Oleaceae Understory Xs2 Xanthophyllum stipitatum Benn. Polygalaceae Canopy Dm Diplospora malaccensis Hk.f. Rubiaceae Understory Ml Macaranga lowii King ex Hk.f. Euphorbiaceae Understory Mm Monocarpia marginalis (Scheff.) Sinclair Annonaceae Canopy So Santiria oblongifolia Bl. Burseraceae Canopy Hd Homalium dictyoneurum (Hance) Warb. Flacourtiaceae Canopy As Actinodaphne sesquipedalis Hk.f. & Thoms. Ex Meisn. Lauraceae Understory Mg Mallotus griffithianus Hk.f. Euphorbiaceae Treelet Ae Alangium ebenaceum (Clarke) Harms Alangiaceae Understory

3 1212 AMERICAN JOURNAL OF BOTANY [Vol. 92 Fig. 1. Examples of the phenology of leaf emergence (plus) and leaf fall (minus) for the upper and lower crowns of the tree species, Ptychopyxis caputmedusae, Ganua sp. 1., and Macaranga lowii. 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 TABLE 2. Phenological synchronizations of leaf emergence and leaf fall between the upper and lower crowns (Kendall s rank correlation, * P 0.05, ** P 0.01, *** P 0.001). Sample tree Leaf emergence Leaf fall Et 0.96*** 0.29** Xs1 0.55** 0.29* Ds 0.61*** 0.47*** Pc 0.59*** 0.30** Gs 0.65*** 0.41*** Er 0.40** 0.14 Mf 0.48** 0.58*** Cs 0.91*** 0.02 Xs2 0.67*** 0.09 Dm Ml 0.49*** 0.08 Mm So 1.00*** 0.60*** Hd 0.40** 0.27* As 0.85*** 0.47*** Mg 0.85*** 0.75*** Ae 0.88*** 0.19 far greater than expected at random (P , 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. Indices of leaf demography are shown in Fig. 2. Frequency of leaf emergence (FLE) and number of leaves emerged (NLE) were greater in the upper than in the lower crowns in 12 of 17 and 17 of 17 trees (P and P 0.001, respectively, sign test). Number of leaves emerged was less than one in some cases, because some of the shoots within branch units did not produce leaves even at the time of leaf emergence. Similarly, frequency of leaf fall (FLF) and number of leaves fallen (NLF) was greater in the upper than in the lower crowns in 10 of 17 and 16 of 17 trees (P and P 0.001, respectively). Thus, NLE and NLF were generally greater in the upper than in the lower crowns, but it was not always true for FLE and FLF. Here, most of the values of FLE and FLF were not exactly the same between the upper and lower crowns of the same trees (Fig. 2). As a consequence of these trends, leaf production was restricted to a few months, but a small number of leaves fell during most of the months in a year (Figs. 1 and 3). DISCUSSION 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

4 July 2005] OSADA ET AL. WITHIN-CROWN VARIATION IN LEAF PHENOLOGY 1213 Fig. 2. Indices of leaf demography of the two crown parts for 17 selected trees (FLE; frequency of leaf emergence [no./yr], NLE; number of leaves emerged [per one leaf emergence event], FLF; frequency of leaf fall [no./yr], and NLE; number of leaves fallen [per one leaf fall event]). Values of upper and lower crowns are connected by line for each tree. Fig. 3. Relationships between FLE (frequency of leaf emergence [no./yr]) and NLE (number of leaves emerged [per one leaf emergence event]), and between FLF (frequency of leaf fall [no./yr]) and NLF (number of leaves fallen [per one leaf fall event]) for the upper crowns of 17 selected trees. 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

5 1214 AMERICAN JOURNAL OF BOTANY [Vol. 92 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. LITERATURE CITED AIDE, T. 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