J Res (2008) 121:33–42 DOI 10.1007/s10265-007-0116-x

REGULAR PAPER

Size-related flowering and fecundity in the tropical canopy species, acuminata () during two consecutive general flowerings

Yoko Naito Æ Mamoru Kanzaki Æ Shinya Numata Æ Kyoko Obayashi Æ Akihiro Konuma Æ Sen Nishimura Æ Seiichi Ohta Æ Yoshihiko Tsumura Æ Toshinori Okuda Æ Soon Leong Lee Æ Norwati Muhammad

Received: 15 March 2007 / Accepted: 13 August 2007 / Published online: 18 October 2007 The Botanical Society of Japan and Springer 2007

Abstract We monitored the reproductive status of all 177 kg total dry matter mass of fruit (TDM) per tree). with diameters at breast height (dbh)[30 cm in a 40- Monotonic increases with increasing tree size were ha plot at Pasoh, west , and investigated the observed for flower production and TDM amongst trees up individual fecundity of 15 Dyer (Di- to 90 cm in dbh, but not for mature seed production or for pterocarpaceae) trees using seed-trapping methods during any of these parameters amongst larger trees. The pattern two consecutive general flowering periods in 2001 of reproductive investment during the two consecutive (GF2001) and 2002 (GF2002). The proportion of flowering reproductive events clearly differed between medium-sized trees was higher, and not dependent on size, in GF2002 and large trees; the former concentrated their reproductive (84.2%), than in GF2001 (54.5%), when flowering mainly investment in one of the reproductive events whereas the occurred in trees with a dbh £70 cm. Fecundity parameters latter allocated their investment more evenly to both of individual trees per event varied widely (221,000– reproductive events. Our results suggest size-related dif- 35,200,000 flowers, 0–139,000 mature seeds, and 1.04– ferences in the resource allocation pattern for reproduction.

Keywords Dry matter allocation Flowering magnitude Electronic supplementary material The online version of this Flowering probability Flower production article (doi:10.1007/s10265-007-0116-x) contains supplementary Seed production Seed set material, which is available to authorized users.

Y. Naito (&) M. Kanzaki S. Ohta Y. Tsumura Laboratory of Tropical Resources and Environments, Forestry and Forest Products Research Institute, Division of Forest and Biomaterials Science, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake, Sakyo, Kyoto 606-8502, Japan Present Address: e-mail: [email protected] S. Numata Center for Research and Development Strategy, S. Numata T. Okuda Japan Science and Technology Agency, Kojimachi Square Bldg, National Institute for Environmental Studies, Nibancho-3, Chiyoda-ku, Tokyo 102-0084, Japan 16-2 Onogawa, Tsukuba, Ibaraki 305-0053, Japan Present Address: K. Obayashi S. Nishimura Graduate School of Agricultural Science, Tohoku University, Center for Integrated Area Studies, Kyoto University, Naruko-onsen, Osaki, Miyagi 989-6711, Japan Yoshida-Honmachi, Sakyo, Kyoto 606-8501, Japan

A. Konuma Present Address: National Institute for Agro-Environmental Sciences, T. Okuda 3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, S. Nishimura S. L. Lee N. Muhammad Higashi-Hiroshima 739-8521, Japan Forest Research Institute Malaysia, Kepong, 52109 Kuala Lumpur, Malaysia 123 34 J Plant Res (2008) 121:33–42

Introduction that following a juvenile phase woody polycarpic begin to reproduce when they reach a certain size or age of Lowland tropical of are domi- onset of reproduction (reviewed in Harper and White 1974). nated by Dipterocarpaceae in the canopy and emergent strata Furthermore, their fecundity schedules had been thought to (Ashton 1982; Whitmore 1984). A striking feature of asea- comprise a period of increasing production, a plateau of sonal dipterocarp in this region is the phenomenon yield, and a subsequent steady decline in reproductive termed ‘‘general flowering (GF)’’, a community-wide activity (Harper and White 1974). However, the modes of intermittent mass reproduction, which usually occurs at reproduction after reproductive maturity, i.e., the relation- several-year intervals (Appanah 1985; Ashton et al. 1988; ship between tree size and fecundity, are diverse among Burgess 1972; Curran and Leighton 2000;Ng1977; Numata species (e.g., linear, modal, asymptotic; Greene and Johnson et al. 2003; Sakai et al. 1999; Yap and Chan 1990). This 1994), and no generalization has been made for long-lived supra-annual reproduction in the humid tropics is inferred to tree species. There have also been some studies examining be triggered by rare environmental cues such as prolonged the relationship between tree size and reproductive traits for drought and abnormally low temperatures, based on the dipterocarps (Appanah and Manaf 1990; Itoh et al. 2004; intense and/or long monitoring records of both plant phe- Thomas and Appanah 1995). However, these studies are nology and meteorological data (Ashton et al. 1988; Numata considered to have insufficiently illustrated species-specific et al. 2003; Sakai et al. 2006; Yasuda et al. 1999). During GF, size-dependence of reproduction because of integration of most dipterocarp species and many plant species of other species (Appanah and Manaf 1990; Thomas and Appanah families flower sequentially for several months (Sakai 2000; 1995) or small sample size (Itoh et al. 2004). Sakai et al. 1999). Previous studies have recorded large In this study we investigated the individual-based variations in flowering magnitude within dipterocarp popu- reproductive status (flowering or non-flowering) and lations between these reproductive episodes (Curran and fecundity (e.g., flower and mature seed production and dry Leighton 2000; Numata et al. 2003; Sakai et al. 2006). In matter allocation to fruit) of the typical ‘‘GF type’’ tree addition, long-term phenological data have shown that two species (Sakai 2001) Shorea acuminata Dyer (Diptero- GF events sometimes occur in close succession without carpaceae) during two consecutive GF events in 2001 and pause (Curran and Leighton 2000; Sakai et al. 2006). 2002. Using the data acquired on individual trees’ repro- However, although previous studies have elucidated the ductive traits across the two reproductive events we dynamics of reproductive phenology at the community level, addressed the questions: the manner and degree of change in the reproductive 1 Does the flowering behaviour of individual trees and behaviour of individual trees and species of dipterocarps the population relate to tree size? between GF events remains unclear. In particular, there have 2 Do fecundity, reproductive success, and the patterns of been no detailed studies of two consecutive reproductive reproductive investment to the two consecutive repro- episodes of dipterocarp trees. Since several hypotheses have ductive events relate to tree size? been proposed to explain the causes and the selective 3 How does adjacent reproduction affect flowering and advantages of supra-annual mass reproduction for tree spe- fecundity of individual trees? cies (e.g., the resource matching hypothesis (Norton and Kelly 1988), the predator satiation hypothesis (Janzen 1971), and the promotion-of-pollination hypothesis (Sakai 2002)), consecutive reproductive events of masting dipterocarps can Materials and methods be a good opportunity to test their assumptions. Therefore, studies on the reproductive dynamics of individual diptero- Study species carp trees during consecutive GF events may provide not only a better understanding of the reproductive ecology of Shorea acuminata Dyer (Dipterocarpaceae) is a common dipterocarp species but also a new perspective on the evo- canopy tree species that is widely distributed in mixed lutionary significance of general flowering/fruiting, which is dipterocarp forests of Malaya, Sumatra, and Lingga (Ash- a distinctive phenomenon in this region. ton 1982). The flowers are hermaphroditic and arranged in Reproduction is a critical phase for the maintenance and dense, semi-pendent, and paniculate inflorescences (Ap- growth of plant populations in the life history of plants. Many panah 1979; Chan and Appanah 1980). The shrimp-pink studies have shown that both plant size (e.g., Hirayama et al. flowers are about 1 cm in diameter, insect-pollinated 2004; Hirayama 2005; Shibata and Tanaka 2002; Thomas (Appanah 1979; Appanah and Chan 1981), and their petals 1996a, b; Wesselingh et al. 1997; Wright et al. 2005) and the are abscised the following morning (Appanah 1979). The amount of available resources (reviewed by Obeso 2002) are young sepals subsequently expand into full-sized wings closely related to plant reproduction. It is widely assumed (Ashton 1989), then the seeds grow rapidly and mature 123 J Plant Res (2008) 121:33–42 35 fully 3.5–4 months after anthesis. The fruit, with three long seeds of Shorea (section Muticae) fall within 10 m of their and two short wings, is one-seeded (Chan 1980; Y. Naito, mother trees (Chan 1980), we set seed traps up to 15 m from personal observation). Therefore, one fruit can be equated each focal tree to cover the dispersal range of immature with one seed. The dry mass of a fully developed fruit is seeds. Since the number of fallen seeds decreased approxi- usually ca. 0.2–0.4 g. mately two months after flowering, we replaced the small traps with larger ones (with an area of ca. 0.26 m2; hereafter ‘‘large traps’’) to obtain more accurate estimates of the spa- Study site and focal trees tial density of the fallen seeds. In addition, the range covered by the traps was extended from just beneath the trunk to 18 m This study was conducted in a 40-ha plot inside a primary from each focal tree, because the mature seeds were expected forest of the Pasoh Forest Reserve, Negeri Sembilan, to have a greater dispersal range than the immature seeds Malaysia. A detailed description of the study plot is (Chan 1980). A projection diagram was drawn for the five available in a previous report (Naito et al. 2005). Fieldwork focal trees inside plot 1 (which constitutes one part of the 40- was carried out during two GF periods—one from Sep- ha plot; for details, see Niiyama et al. 2003), and their crown tember 2001 to March 2002 (GF2001) and the other from areas were estimated using ArcView 3.1 software. The April 2002 to October 2002 (GF2002)—when two con- maximum observed canopy area (*280 m2) of the medium- secutive reproductive episodes of S. acuminata occurred at sized and large trees (Appendix) was equivalent to that of a the study site. The magnitude of the GF (i.e., the proportion circle of radius ca. 9.4 m, so we assume that the distances of flowering trees among observed trees with diameters at covered by the seed traps (i.e., 15 or 18 m from the focal breast height, dbh, [30 cm) in the Pasoh Forest Reserve trees) were sufficient to obtain estimates of the distributions was much larger in GF2002 than in GF2001; 55% versus of fallen seeds. The density of mature trees was sufficiently 24% of observed dipterocarp trees flowered in the study low (1.43 trees ha–1) that seed shadow overlaps were mini- plot in the respective periods (Numata et al. 2003). Before mized. However, if the seeds of a focal tree were inter-mixed these GF events, no major GF event had been reported in in the traps with those of other conspecific trees (judging the Pasoh Forest Reserve since 1996 (Numata et al. 2003). from the morphological characters of fruits), we excluded During this study, we observed the tree crowns of all S. those traps from further analysis. Seeds in both the small and acuminata trees with dbh [ 30 cm in the plot, from the large traps were collected and counted at least twice a week forest floor, using binoculars to determine the reproductive until the end of the mature seed dispersal period. To inves- status—non-flowering or flowering. To minimize obser- tigate the seed maturation process and dry matter allocation vation errors when determining their reproductive status, to fruit, up to 20 unbroken seeds were randomly chosen from the flowering (fruiting) census was conducted repeatedly at the samples of each focal tree almost once a week. These intervals of approximately 2–3 weeks until the end of seeds were weighed, after removing the wings from the fruits mature seed dispersal. The reproductive status of observed and oven-drying them at 60C for 2 days, and the average flowering or fruiting trees were counted as ‘‘flowering’’ in weight of the seeds produced by each tree was then calcu- this study. Among the reproductive trees ([30 cm dbh), 10 lated. Seeds with dry masses (here defined as the mass of the and 11 individuals of various sizes were chosen in GF2001 fruits without wings) ‡0.12 g, equivalent to ‡0.18 g fresh and GF2002, respectively (Appendix) as focal trees to weight, were considered mature based on a germination estimate individual-based fecundity parameters (flower and experiment that was conducted immediately after the seed seed production and dry matter allocation). Among the ten fall in GF2001 with seeds of various sizes (Y. Naito, focal trees in GF2001, six trees flowered consecutively in unpublished data). Furthermore, since seed fall rates often GF2002; they were monitored continuously to clarify the rapidly increased during the period of intense mature seed inter-event variation in reproductive output. Another five dispersal, we defined the onset of mature seed dispersal focal trees in GF2002 (G982, G1143, G1175, G1904, and based on seedfall phenology (i.e., the beginning of intense G2438) were selected from the non-flowering trees in mature seed dispersal) or seed size (the first day when the GF2001. Thus, in all, 15 trees were used in this study to average dry seed mass exceeded 0.12 g) for each tree. estimate individual-based fecundity parameters.

Seed trap placement and sample collection Estimation of individual-based fecundity parameters

Prior to anthesis we set small seed traps (plastic baskets) with To quantify the total number of seeds dispersed, the spatial an area of ca. 0.025 m2 at 3-m intervals (3, 6, 9, 12, 15 m) seed dispersal pattern (seedfall density as a function of from the base of each focal tree in four directions to deter- distance to a mother tree) for each focal tree was estimated mine the spatial pattern of seed fall. Since most immature from the seed trap data using a Weibull distribution model 123 36 J Plant Res (2008) 121:33–42

(Itoh et al. 2004). This model is a modification of the Size-dependence of flowering and fecundity mechanistic seed dispersal model described by Greene and Johnson (1989), which assumes that the distribution of wind To investigate the relationship between flowering probabil- speed along one direction follows a Weibull distribution. ity and tree size during each GF event, we fitted a nominal Since the frequency of wind speeds is known to often follow logistic curve to the flowering census data (dbh vs. flowering/ a Weibull distribution, this model can be applied theoreti- non-flowering) for each reproductive event using the maxi- cally to the dispersal pattern of wind-dispersed specimens, mum likelihood method with JMP 4.0 (SAS 2000). Loge- such as the winged seeds of S. acuminata. transformed dbh data were used as an explanatory variable Since the actual seed dispersal patterns in this study usu- for this logistic regression analysis. Furthermore, each of the ally had a mode at some distance from the focal trees, we three fecundity estimates (i.e., flower and mature seed pro- assumed that the Weibull distribution model provided a better duction and TDM) was used to examine the relationship fit to the observed data than other models (e.g., exponential, between tree size and fecundity. All other statistical analyses Gaussian, or 2Dt models; see Nathan and Muller-Landau were performed by use of the software SPSS 10.0 (2000). 2000) that assume seed density to be maximal directly under the mother tree. Accordingly, we assumed that seed density at x meters from a mother tree, q(x) (seed m–2), conformed to Results the Weibull distribution expressed by the equation: Size-dependence of flowering in each GF event hi N m x m qðxÞ¼ xm1 exp ; ð1Þ 1 m The flowering magnitude of the S. acuminata population 2paC m þ 1 a a was significantly higher in GF2002 than in GF2001 (when where N is the total seed production of the focal tree, a is a 84.2 and 54.5%, respectively, of the observed trees flow- scale parameter, and m is a shape parameter (Itoh et al. ered: P = 0.001; Fisher’s exact test). In addition, the 2004). The coefficients’ values and their standard errors proportion of flowering individuals was higher among were estimated by use of Delta Graph 4.0 (Deltapoint, larger (dbh) trees in GF2001 (Fig. 1; P = 0.0029; logistic USA) and R 2.4.1 (The R Development Core Team (2006): regression analysis), i.e., logedbh had a significant effect on nls function in statistical package) software using the least- flowering in this event (v2 = 7.59, P = 0.0059; Wald test squares method for non-linear regression analysis. for the coefficient of logedbh). In contrast, the proportion of Since the size and positions of the seed traps were flowering individuals in GF2002 was high, irrespective of changed once during the period of reproduction, and the the size class (P [ 0.05; logistic regression analysis). spatial dispersal pattern of mature seeds was expected to Over 96% of trees [30 cm dbh flowered during at least differ from that of immature seeds, we estimated three seed one of the two reproductive episodes. The proportion of dispersal curves for each focal tree: trees flowering in both GF events was greater in the large 1 a seed dispersal curve for immature seeds estimated tree size class ([70 cm dbh) (Fig. 1).

using small-trap data, q1(x); 2 a seed dispersal curve for immature seeds estimated Individual-based flower and seed production, using large-trap data, q (x); and 2 and dry matter allocation to fruit 3 a seed dispersal curve for mature seeds estimated using large-trap data, q (x). 3 Individual-based flower and mature seed production and

The numbers of fallen immature seeds (NFr1 and NFr2) TDM were estimated overall for 15 trees (Appendix, S1). and fallen mature seeds (NMature) were estimated by However, we failed to estimate these variables for a tree in applying the density functions q1(x), q2(x), and q3(x), GF2001 because of insufficient cover of seed shadows; respectively. In these estimations, the flower production they were treated as missing data. The estimates of each

(NFl) was regarded as being equivalent to the total number parameter varied enormously among the mother trees and of fallen immature seeds (NFr1 and NFr2) and mature seeds GF events—from 221,000 to 35,200,000 flowers for flower (NMature). Seed set was calculated as the ratio of mature production, from 0 to 139,000 seeds for mature seed pro- seed production (NMature) to flower production (NFl). duction, and from 1.04 to 177 kg for TDM per tree. Seed We also estimated the total dry matter mass of fruit set also varied among individuals, from 0.00 to 7.72%. (TDM) produced by each focal tree, as a measure of its Overall, the seed set ratio was higher in GF2001 (median: reproductive output during a monitored reproductive event, 1.21%) than in GF2002 (median: 0.19%) (Appendix), and by summing the product of its dry fruit mass and estimated the inter-event difference was statistically significant numbers of fallen fruits throughout that event. (U = 80.0, P = 0.020; Mann–Whitney U test).

123 J Plant Res (2008) 121:33–42 37

Both Either None addition, among the 14 focal trees for which complete sets of 30 100 fecundity data across GF2001 and GF2002 were collected, GF2002 Percent of trees flowering (lines) estimates of flower production and TDM showed significant, 25 80 negative rank correlations between GF2001 and GF2002 (Figs. 3a, c: q = –0.705, P = 0.005 for flower production; 20 GF2001 q = –0.693, P = 0.006 for TDM; Spearman’s rank correla- BothGF2001 & GF2002 60 15 tion). The correlation coefficient for mature seed production 40 was negative, but not statistically significant (Fig. 3b; q = 10 –0.522, P = 0.056). Furthermore, large trees (dbh [90 cm)

20 showed a tendency to reproduce more constantly than small 5 and medium-sized trees (30–90 cm in dbh), although all the

Number of trees in 40 ha (histogram) medium-sized trees that were examined concentrated their 0 0 30-50 50-70 70-90 90-110 110-130 reproductive investment in either one or other of the two Dbh class (cm) reproductive events (Figs. 3a–c).

Fig. 1 Size distribution and size-related flowering patterns of Shorea acuminata trees during the two general flowering (GF) events in 2001 (GF 2001) and 2002 (GF2002). Dark grey, light grey and un-shaded Discussion columns indicate trees that flowered in both, either, or none of the two flowering events, respectively. Broken lines indicate the proportion of Tree size and flowering probability in each GF event flowering trees in each dbh class for GF2001 and GF2002. The solid line indicates the proportion of trees flowering in both of the GF events The association between tree size and flowering differed Size-dependence and pattern of fecundity markedly between the relatively low (GF2001) and high intensity (GF2002) flowering events of S. acuminata. The Estimates of flower production and TDM increased with flowering probability of trees ([30 cm in dbh) in GF2001 tree size (dbh) up to 90-cm dbh in both GF2001 and was size-dependent, but it was high in GF2002, irrespective GF2002, but for the trees with larger dbh, size–fecundity of tree size, since an extremely high frequency of flowering patterns were different between the two GF events; flower trees with 30–70 cm dbh in GF2002 negated the size- production and TDM decreased with increasing tree size in dependence of flowering observed in GF2001 (Fig. 1). GF2001 but fluctuated irrespective of size in GF2002 Furthermore, at least another 15 smaller flowering trees (Figs. 2a, c). Although mature seed production in GF2001 (\30 cm dbh) were observed inside the study plot in showed a unimodal pattern similar to those in flower pro- GF2002, but none in GF2001 (Y. Naito unpublished data). duction and TDM in GF2001, no particular pattern was These results indicate that the relative frequency of the found in relation to tree size in GF2002 (Fig. 2b). Total smaller flowering trees (dbh £ 70 cm) determined the flower production and TDM during the two consecutive GF flowering magnitude of the whole S. acuminata population. events were low in small trees (30 cm \ dbh £ 40 cm), In addition, the results described above also suggest that the increased with tree size for the medium-sized trees larger trees ([ 70 cm dbh) flower more often, irrespective of (40 cm \ dbh £ 90 cm), and fluctuated but remained at the GF magnitude, compared with smaller trees (dbh £ 70 almost the same level as that of the medium-sized trees cm), which tended to flower mainly during a major GF event. among large trees (90 cm \ dbh) (Figs. 2d, f). However, Relationships between tree size and reproductive traits of total mature seed production fluctuated without any spe- this species will be discussed in the following section. cific relationship to tree size (Fig. 2e). There was no clear relationship between tree size and seed set. Relationship between tree size and fecundity

Inter-event variation and influence of adjacent In this study we evaluated three variables (i.e., flower and reproduction on flowering and fecundity of individual mature seed production and TDM) as measures of fecundity trees for each focal tree. Our results showed that both flower production and TDM in each reproductive event increased Among 29 trees that flowered during the GF2001 event, with increases in tree size up to 90-cm dbh, and their total 82.8% of trees (N = 24) flowered again in GF2002 (Table 1). across the two reproductive events also had similar patterns Four of the five trees that flowered only in GF2001 (Table 1) (Figs. 2a, c, d, f). However, for these variables in trees with were the focal trees that showed large fecundity in this study larger dbh ([ 90 cm), we did not observe a consistent size– (i.e., trees G557, G601, G1881 and G1891; Appendix). In fecundity pattern across the two reproductive events 123 38 J Plant Res (2008) 121:33–42

Fig. 2 Relationships between 108 108 dbh and each of the estimated a GF2001 Total d fecundity parameters for 15 GF2002 Shorea acuminata trees in 1 + 7 GF2001 and GF2002: a flower ) 7

e 10 10 e production, b mature seed r t production, and c total dry r e p

matter mass of fruit (TDM). The s r total fecundity for 14 trees with e 6 6 w 10 10 o a complete set of fecundity data l F during GF2001–GF2002 is also ( shown: d flower production, e mature seed production, and f 105 105 TDM 30 40 50 60 70 80 90 100 110 120 30 40 50 60 70 80 90 100 110

106 106 b e 105 105 1 +

)

e 4 4 e

r 10 10 t

r e

p 3 3

s 10 10 d e e s

2 2

e 10 10 r u t a

M 10 10 (

1 1 30 40 50 60 70 80 90 100 110 120 30 40 50 60 70 80 90 100 110

103 103 c f

102 102

10 10

1 1 Total dry matter mass of fruit per tree (kg) 30 40 50 60 70 80 90 100 110 120 30 40 50 60 70 80 90 100 110 Dbh (cm)

Table 1 Comparisons of reproductive status in Shorea acuminata (Figs. 2a, c). Since the total flower production and TDM also trees (dbh [ 30 cm) between GF2001 and GF2002 fluctuated widely among large trees (Figs. 2d, f), it was hard GF2001 GF2002 to derive the particular size–fecundity relationships for trees [90-cm dbh from the data acquired in this study. Even so, Flowering Non-flowering Total the observed size–fecundity patterns for total flower pro- Flowering 24 (6) 5 (4) 29 (10) duction and TDM (Figs. 2d, f) may suggest asymptotic or Non-flowering 23 (5) 2 (0) 25 (5) unimodal relationships rather than linearly increasing ones Total 47 (11) 7 (4) 54 (15) between tree size and these fecundity parameters. If the demography from flower to seed is similar among In all, 54 trees with a complete set of flowering census data during GF2001–GF2002 are shown. The numbers of focal trees used for individual trees, the size–fecundity pattern for mature seed estimating the individual-based fecundity parameters are also shown production should parallel that for flower production. However, in parentheses the relationships between tree size and mature seed production

123 J Plant Res (2008) 121:33–42 39

(N/tree) (N/tree) (kg/tree) 7 a Flower 5 b Mature seed c TDM 4*10 1.5*10 200 Large tree Large tree Large tree Medium-sized tree Medium-sized tree Medium-sized tree Small tree Small tree Small tree 7 3*10 150 1.0*105

7 2*10 100 GF2002 0.5*105 7 1*10 50

0 0 0 5 5 5 0 1*107 2*107 3*107 4*107 0 0.5*10 1.0*10 1.5*10 0 50 100 150 200 GF2001

Fig. 3 Inter-event variation and trade-off in fecundity between Crosses, filled triangles, and open circles indicate small trees GF2001 and GF2002 for 14 Shorea acuminata trees. Graphs show (30 cm \ dbh £ 40 cm), medium-sized trees (40 cm \ dbh £ 90 each of the three estimated fecundity parameters in GF2001 and cm), and large trees (90 cm \ dbh), respectively GF2002: a flower production, b mature seed production, and c TDM. were inconsistent (Fig. 2b), and the size–fecundity patterns for Martinez-Ramos 1992; Thomas 1996a). However, this mature seed production were different from those for flower assumption is not always applicable to long-lived polycarpic production (Figs. 2b, e; cf. Figs. 2a, d). This discrepancy of tree species. In the case of S. acuminata, a monotonic size–fecundity patterns between flower production and mature increase with increasing tree size only appeared to be valid seed production was due to the large variations in the pre-dis- for flower production and TDM in trees up to 90 cm in dbh. persal demography of seeds, which stochastically affected the Similarly, Greene and Johnson (1994) showed that a production of mature seeds independently of tree size. In fact, monotonic increasing relationship between fecundity (seed there were large differences both in the abortion rates (i.e., the production) and tree size can only be assumed for trees with a proportions of the early abscission of immature seeds to flowers; basal area of less than *0.4 m2 (equivalent to ca. 35-cm ranges 90.0–99.1% (GF2001) and 95.6–99.6% (GF2002)) and dbh); for trees with larger basal areas, a wide variety of in the rates of pre-dispersal seed predation after the mass responses (linear, modal, and asymptotic) were found among abortion of seeds (ranges 11.7–52.6% (GF2001) and 27.9– nine canopy tree species in North America. Some recent 74.9% (GF2002)) among individual trees (Naito et al. in prep- studies also suggest that relationships between tree size and aration). Moreover, higher rates of early abscission (mean: fecundity vary among species (modal or asymptotic: Soe- 96.0% in GF2001 vs 98.4% in GF2002) and pre-dispersal pre- hartono and Newton 2001; linear or asymptotic: Hirayama dation (mean: 35.4% in GF2001 vs. 53.7% in GF2002) lowered 2005; Hirayama et al. 2004), and that no generalizations can the seed set and seed output in GF2002 (Naito et al., in prepa- be made about the size–fecundity relationship across mul- ration). Some external factors such as a lack of cross pollination tiple tree species. As stated by Thomas (1996a), both a (Ghazoul et al. 1998) and seed consumption by insects and theoretical approach and more data on forest tree species are mammals (Chan 1980; Momose et al. 1996; Nakagawa et al. required to identify which aspects of life history might allow 2005; Maycock et al. 2005) have been reported as being closely quantitative predictions of fecundity across species. related to the pre-dispersal mortality of seeds in various dip- Although we did not find sufficient evidence to differ- terocarp species. These external factors stochastically influence entiate between the total fecundity of medium-sized trees the survival of pre-dispersal seeds among individual trees and/or and large trees in this study (Figs. 2d–f), the pattern of reproductive events, thereby making the size–fecundity pattern reproductive investment during the two consecutive GF for mature seed production different from that for flower pro- events clearly differed between medium-sized and large duction. The mature seed production depended more on the pre- trees. As shown in Figs. 3a–c, medium-sized trees con- dispersal demography of seeds than tree size. centrated their reproductive investment in only one of the General models of size–fecundity relationships in plants reproductive events whereas the large trees tended to have been based on the assumption that reproductive output allocate their investments more evenly in both reproductive increases with increasing plant size. In fact, many studies events (at least on the basis of the numbers and mass of have demonstrated monotonically increasing relationships reproductive parts examined). Resource allocation between plant size and reproductive output for a wide variety dynamics of the individual trees should be clarified in of herbaceous species (Samson and Werk 1986; Shipley and further studies to confirm the observed size-related changes Dion 1992) and some tree species (Alvarez-Buylla and in allocation pattern for reproduction.

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Influence of adjacent reproduction on individual trees’ Moreover, stored phosphorus is assumed to play an impor- flowering and fecundity tant role in the reproduction of dipterocarps, because of its drastic decrease during dipterocarps’ flowering and fruiting The significant negative correlations observed in flower (T. Ichie, Kochi University, personal communication). production and TDM between GF2001 and GF2002 indicate Therefore, adjacent reproduction might critically drain the there were significant trade-offs in the investment in repro- stored resources such as phosphorus, which might cause the duction between the two consecutive reproductive events absence of reproduction and decreased fecundity in the (Figs. 3a, c). No focal trees displayed large reproductive subsequent reproductive event of S. acuminata. Further outputs in both of the events examined in this study. Fur- studies are required to clarify the physiological mechanisms thermore, although most of the reproductive trees in GF2001 of flowering and the decisive factors regulating the occur- flowered again in GF2002 (Table 1), the four focal trees that rence and frequency of flowering of both dipterocarp exhibited the highest fecundity in GF2001 failed to flower in individuals and populations. GF2002 (Appendix). Similarly, Burgess (1972) found that individuals of some Shorea species flowered in 1968 but did Acknowledgments The authors would like to thank Dr K. Niiyama for permission to use his 6-ha plot (plot 1), Dr A. Itoh for providing not flower in 1970 when heavy-fruiting years occurred in his unpublished manuscript, and Dr M. Yasuda for many advisory close succession. These results indicate that resource limi- comments about this study. We also thank Mr A. Hussein and Mr A. tations attributable to large resource consumption during Nyak for their assistance during this study, and all local staff of this adjacent reproduction affected the flowering and fecundity project who helped us greatly in the field. This study was a part of a joint research project of FRIM, Universiti Putera Malaysia, and the of current reproduction among individual trees. Thus, a National Institute for Environmental Studies of Japan (Global Envi- tree’s nutritional status may play some role in floral induc- ronment Research Program supported by the Ministry of Environment tion of dipterocarp individuals. Ichie et al. (2005) concluded in Japan, Grant No. E-4). that storage of carbohydrate resources might not be a deci- sive factor in the occurrence or frequency of flowering in the masting dipterocarp species, aromatica Ga- Appendix ertn. f., because the total non-structural carbohydrates were continuously present in all organs, even after flowering. Table 2

Table 2 Tree size and Tree dbh Crown Tree Year Flower Mature Seed Total fecundity of 15 Shorea no. (cm) area size of production seed set dry acuminata trees during the (m2) GF (·103) production (%) matter general flowering periods in event (·103) mass 2001 and 2002 of fruit (kg)

G221 106.0 271 Large 2001 403 14.5 3.60 7.38 2002 2,300 25.6 1.11 26.4 G557 87.1 229 Medium 2001 9,240 56.9 0.62 75.1 G601 52.9 N/A Medium 2001 1,800 139 7.72 57.5 G855 108.0 N/A Large 2001 370 4.47 1.21 2.85 2002 35,200 76.0 0.22 177 G982 70.8 111 Medium 2002 12,500 2.74 0.02 38.2 G1143 65.4 147 Medium 2002 6,840 12.7 0.19 31.2 G1175 82.4 277 Medium 2002 25,900 32.9 0.13 109 G1516 32.2 N/A Small 2001 221 1.59 0.72 1.96 2002 298 1.25 0.42 1.79 G1881 45.9 N/A Medium 2001 3,720 70.1 1.88 42.7 G1891 57.8 N/A Medium 2001 4,410 94.6 2.15 72.5 G1904 34.1 N/A Small 2002 307 0 0.00 1.04 Trees were assigned to one of G2438 50.1 N/A Medium 2002 2,150 32.2 1.50 21.0 three size categories (small, medium, or large) based on their G2816 115.9 N/A Large 2001 – – – – dbh: small, 30–40 cm; medium, 2002 6,720 10.6 0.16 18.7 40–90 cm; large, [90 cm G2824 96.1 N/A Large 2001 3,580 35.8 1.00 28.9 – Indicates that estimates could 2002 708 10.9 1.54 5.18 not be made because of G2959 103.7 N/A Large 2001 1,640 2.37 0.14 6.75 insufficient cover of the seed 2002 1,190 1.76 0.15 4.16 shadow

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