ORIGINAL ARTICLE

Fruiting behavior of dipterocarps in two consecutive episodesof general flowering in a Malaysian lowland rain forest

Shinya Numata • Ryo O. Suzuki • Sen Nishimura •

Yoko Naito • Akihiro Konuma • Yoshihiko Tsumura •

Naoki Tani • Toshinori Okuda • Md Noor Nur Supardi

Received: 17 July 2010 / Accepted: 17 May 2011 / Published online: 8 October 2011

� The Japanese Forest Society and Springer 2011

Abstract We examined fruiting behaviors of 24 dip-

terocarp species in a lowland rain forest of Peninsular

Malaysia during two consecutive episodes of general

flowering (GF). The first GF episode (GF2001) occurred

from August 2001 to February 2002, and the second GF

episode (GF2002) followed immediately, from March to

September 2002. The magnitude of GF2002 was greater

than that of GF2001 at the community level. Significant

positive size dependence of fruiting behavior at the com-

munity level was found in both GF2001 and GF2002, but

there was no significant association between the fruiting

behaviors in GF2001 and GF2002 except for one species.

These results imply that tree size was one of the explana-

tory factors for fruiting behavior of dipterocarp species, but

there was no evidence that adjacent reproduction caused

the absence of reproduction and decreased fecundity in the

subsequent fruiting event. In contrast, strong spatial

aggregation of fruiting trees was found in GF2001, sug-

gesting that external factors may affect fruiting behavior of

dipterocarps in a minor GF episode. Among the 12 study

species, there were large variations in fruiting behavior, but

growth type (e.g., fast-growing or slow-growing) did not

simply explain the inter-specific pattern of fruiting behav-

ior. Thus, tree size may account for fruiting behavior of

dipterocarps during the consecutive GF episodes through

species-specific differences in phonological responses to

internal and external conditions.

Keywords Dipterocarpaceae � Peninsular Malaysia �Reproductive phenology � Size dependency �Spatial distribution pattern

S. Numata � T. Okuda

Biological Environment Division, National Institute

for Environmental Studies, Tsukuba,

Ibaraki 305-8506, Japan

S. Numata (&)

Graduate School of Urban Environmental Sciences,

Tokyo Metropolitan University, Minami-Osawa 1-1,

Hachiouji, Tokyo 192-0397, Japan

e-mail: nmt@tmu.ac.jp

R. O. Suzuki

Sugadaira Montane Research Center, University of Tsukuba,

Sugadaira-kogen 1278-294, Ueda, Nagano 386-2204, Japan

S. Nishimura � M. N. Nur Supardi

Forestry Division, Forest Research Institute Malaysia,

52109 Kepong, Selangor, Malaysia

Y. Naito

Graduate School of Agriculture, Kyoto University,

Kitashirakawa Oiwakecho, Kyoto, Kyoto 606-8502, Japan

A. Konuma

National Institute for Agro-Environmental Sciences,

3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan

Y. Tsumura

Forestry and Forest Products Research Institute,

Matsunosato 1, Tsukuba, Ibaraki 305-8687, Japan

N. Tani

Japan International Research Center for Agricultural Sciences,

Ohwashi 1-1, Tsukuba 305-8686, Japan

T. Okuda

Graduate School of Integrated Arts and Sciences,

Hiroshima University, 1-7-1 Higashi-Hiroshima,

Hiroshima 739-8521, Japan

123

J For Res (2012) 17:378–387

DOI 10.1007/s10310-011-0308-z

Introduction

The family Dipterocarpaceae, known as useful timber

trees, is widely distributed in lowland rain forests of the

aseasonal Southeast Asia (Ashton 1982; Maury-Lechon

and Curtet 1998; Symington et al. 2004). Many dipterocarp

species represents a unique rhythm of reproductive phe-

nology known as general flowering (GF), followed by mast

fruiting (Appanah 1985; Ashton et al. 1988; Sakai et al.

1999; Yasuda et al. 1999; Sakai 2002; Numata 2004). Even

though this region has little seasonal weather variation, GF

represents supra-annual synchronization of reproduction

across diverse tree species including dipterocarps at irreg-

ular intervals of 1–10 years. A previous study showed that

70% of emergent trees and 40% of canopy trees have been

regarded as GF species that flowered only during GF

periods in Borneo (Sakai et al. 1999). It was also reported

that at least 27 genera in 24 families restricted their

reproduction to the GF episodes in Bornean forests

(Cannon et al. 2007).

Since GF plays a central role in the successful regen-

eration of dipterocarp forests in the tropics of Southeast

Asia (Ashton et al. 1988; Sakai et al. 2006), an under-

standing of reproductive behavior of GF species will pro-

vide important information on forest dynamics and help in

forest management. However, very little is known about

variation in reproductive behavior among GF species due

to the difficulty of population-scale phenological observa-

tion of widely scattered trees in dipterocarp forests (Naito

et al. 2008).

In general, plant size is a key element to understand

variation in reproductive behavior of plants. A few studies

have examined the relationship between tree size and

reproductive traits of dipterocarps in terms of plant internal

and external conditions. Regarding the internal factors in

relation to tree size, tropical rain forest trees in particular

require a certain period to accumulate sufficient resources

for reproduction in a tropical rain forest with poor soil

ferterily (Burgess 1972; Janzen 1974; Kelly 1994; Itoh

et al. 2003). Naito et al. (2008) showed the size-related

differences in the resource allocation pattern for repro-

duction of a Shorea species in two GF episodes. If repro-

duction critically drains stored resources, we can expect

size dependence of reproduction and the absence of

reproduction or decreased fecundity in consecutive fruiting

events.

Concerning the external factors, many studies have

focused on meteorological cues, including low tempera-

tures, strong solar radiation and/or prolonged drought

1–2 months before the beginning of a GF (e.g., Ng 1977;

Ashton et al. 1988; Sakai et al. 1999, 2006; Yasuda et al.

1999; Numata et al. 2003). Of these meteorological cues,

two climatic factors have been proposed as GF triggers:

drought and drops in minimum temperature (Ashton et al.

1988; Yasuda et al. 1999; Sakai 2002; Numata et al. 2003;

Sakai et al. 2006; Brearley et al. 2007). In relation to the

tree size, Appanah and Manaf (1990) reported that small-

sized dipterocarp trees could fruit in recently logged forests

where canopies are more exposed, but not in undisturbed

primary forest with closed canopies. If large-sized trees are

likely to have more exposed canopies than small-sized

trees on the basis of allometric relationship (e.g., Okuda

et al. 2003, 2004), it is reasonable to assume a positive size

dependence of reproduction in terms of both external and

internal conditions, such as sensitivity to meteorological

change and competition for light and nutrients. Moreover,

Itoh et al. (2003) suggested that some site conditions, i.e.

elevation, slope inclination and soil texture, are possibly

responsible for the population-scale variation in fruiting of

a dipterocarp species without reference to tree size.

Population level analyses on reproductive behavior are

important in order to tackle the question of how dipterocarp

species produce their fruits and seedlings through a GF

episode. In the present study, we investigated fruiting

behavior of 24 dipterocarp species in two consecutive GF

episodes during August 2001 to September 2002. Firstly,

we describe features of the two GF episodes on the basis of

the fruiting status of individual trees. Subsequently, at both

the community and population levels, we examined size

dependence of reproductive behavior and its interspecific

difference. To reveal the effect of resource availability on

reproductive behavior, we examined how adjacent fruiting

affects subsequent fruiting behavior. Spatial distribution

patterns were compared between fruiting and sterile trees

in each GF episode to examine whether the occurrence of

fruiting was randomly distributed or spatially aggregated.

Materials and methods

Study site

This study was conducted in a lowland rain forest, Pasoh

Forest Reserve, Negri Sembilan state, Peninsular Malaysia

(2�590N, 102�190E, altitude 75–150 m). Since land use of

this region has changed rapidly from forest to mostly

agricultural plantation, the Pasoh Forest Reserve has

unfortunately become an example of the now rare undis-

turbed lowland rainforests in Peninsular Malaysia. The

reserve has a total area of 2,450 ha. It is surrounded on

three sides (north, south, and west) by oil palm plantations

and to the east by virgin hill dipterocarp forests. The main

part of the reserve consists of a lowland dipterocarp forest

of the Keruing–Meranti type (Appanah and Weinland

1993). The core area (ca. 200 ha) is surrounded by

regenerating forests that were logged in the early 1950s and

J For Res (2012) 17:378–387 379

123

is generally homogenous in topography and community

structure, with no evidence of large-scale human distur-

bance (Manokaran and Swaine 1994; Numata et al. 2006).

The climate in this region is aseasonal tropical rain forest

(average annual rainfall approximately 2,000 mm), but

there are generally two weak dry seasons (July and January)

each year (Numata et al. 2003).

A 40-ha ecological plot (500 m 9 800 m) has been

established for the phenological observation and gene flow

study of dipterocarp trees since 2000 (Konuma et al. 2000;

Takeuchi et al. 2004; Naito et al. 2005, 2008; Tani et al.

2009). All dipterocarp trees ([30 cm in diameter at breast

height, DBH) in the plot were mapped and tagged, and tree

size in DBH was measured. All the target individual trees

were identified based on flower sample, if present, or

leaves, bark and timber characteristics. The study plot

involves primary forest stands as well as regenerating

forest stands after selective logging in 1958 (Numata et al.

2006). The primary forest contains stands at various stages

of maturity, from canopy gaps to climax forest topped by

emergent trees with heights of 50–60 m. Some parts of the

primary forest are seasonally swampy.

Observation of fruiting behavior in dipterocarp trees

We focused on trees of Dipterocarpaceae that play a central

role in a GF episode. In 2001 and 2002, a great number of

canopy and emergent trees including non-dipterocarp spe-

cies also bore flowers and fruits. We monitored flowering

and fruiting behaviors of all dipterocarp species (Diptero-

carpaceae) in the 40-ha plot. Thus, 2 Anisoptera (A. laevis

Ridl. and A. megistocarpa V. Sl.), 5 Dipterocarpus (D.

cornutus Dyer., D. costulatus V. Sl., D. crinitus Dyer., D.

kunstleri King., and D. sublamellatus Foxw.), 2 Hopea (H.

dryobalanoides Miq. and H. sangal Korth.), 1 Neobalan-

ocarpus (N. heimii King.), 1 Parashorea (P. densiflora V.

Sl. et Sym.) and 13 Shorea species (S. acuminata Dyer., S.

bracteolata Dyer., S .guiso (Blanco) Blume, S. hopeifolia

(Heim) Sym., S. lepidota Korth., S. leprosula Miq., S.

macroptera Dyer., S. maxwelliana King., S. multiflora

Sym., S. ochrophloia E. J. S. ex Sym., S. ovalis Korth. S.

parvifolia Dyer., and S. pauciflora King.) were used for the

study.

Observations of reproductive status were carried out in

2001 and 2002 (Table 1). Observations of individual trees

were made with binoculars from the forest floor by three or

four experienced observers. For identification and recon-

firmation of species, flowers and fruit samples of each

individual tree were collected and housed at the field sta-

tion near the Pasoh Forest Reserve. Fruiting behavior

(fruiting or sterile) was evaluated for each tree in each GF

episode in this study. To assess whether a tree had fruited,

we looked for fruit in the canopy and searched for fallen

fruit on the ground. Several trees flowered, but did not

produce fruits in each GF episode. In this case, these

abortive trees were regarded as ‘‘sterile’’. Trees whose

fruiting was observed only once throughout a GF episode

were regarded as ‘‘sterile’’ to minimize observation errors.

To quantify fruiting intensity of individual trees, mature

fruit density on the ground and of each canopy was visually

evaluated and classified into two classes based on the result

of monitoring of flower and fruit production of individual

trees (e.g., Naito et al. 2008): low density (ca. \5 mature

fruits m-2) or high density (ca. C5 mature fruits m-2). For

each fruiting tree, fruiting intensity (high or low) was

determined by the classification of the density of mature

fruits.

Data analysis

In total, 24 dipterocarp species, 818 individual trees were

chosen for the study (Table 2). For the population level

analysis, 12 species (D. cornutus, D. sublamellatus, N.

heimii, S. acuminata, S. lepidota, S. leprosula, S. mac-

roptera, S. maxwelliana, S. multiflora, S. ovalis, S. parvi-

folia, and S. pauciflora) with sufficient number of samples

([20 individuals) were chosen.

All statistical analyses were conducted by R 2.9.2 (R

Development Core Team 2009). Chi-square test was used

to compare proportion. Fisher’s exact test for independence

was used to test whether the fruiting behavior (fruiting or

sterile) and fruiting intensity (high, low, or sterile) in

GF2002 associate with those in GF2001. Analysis of var-

iance (ANOVA) was used for comparisons of several

variables. The effect of tree size (DBH) on the fruiting

behavior in GF2001 was evaluated using generalized linear

model (GLM) with binomial error structure and logit link

function. For GF2002, we also analyzed effects of tree size

and adjacent fruiting (fruiting behavior in GF2001) on the

fruiting behavior in GF2002. Level of significance was

assessed by Wald test. The interspecific relationship

between percentages of fruiting trees in GF2001 and

GF2002 was analyzed using Spearman’s rank correlations.

At the community level, univariate spatial patterns

(aggregation/regularity) of fruiting trees were analyzed

using Ripley’s K(t) function for all individuals ([30 cm in

DBH) (see Suzuki et al. 2009). Species-specific spatial

patterns were analyzed for the 12 species with sufficient

number of samples (n [ 20). The K(t) function is defined

as the expected number of plants within distance t from a

randomly chosen plant, under complete spatial randomness

K(t) = pt2 (Diggle 1983; Haase 1995). When L(t) is

defined as H[K(t)/p] - t, under complete spatial random-

ness, the expected value of L(t) is zero. L(t) was calculated

at 10-m intervals up to 250 m. We tested a null hypothesis

of ‘‘random reproduction’’ that assumes that the spatial

380 J For Res (2012) 17:378–387

123

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J For Res (2012) 17:378–387 381

123

distribution of sterile trees or fruiting trees does not differ

from that expected if fruiting was a spatially random event.

A random distribution expected from the null hypothesis

was generated by a randomization procedure that the

observed spatial distribution of plants keep constant, the

fruiting event (fruited or non-fruited) of individuals were

permuted at random, and L(t) of spatial patterns of the

randomly fruiting and sterile trees were calculated,

respectively. The 95% confidence envelopes of L(t) func-

tion were estimated from 500 randomization procedures.

When the observed L(t)values were larger or smaller than

the envelopes of the expected L(t) under the null hypoth-

eses, the spatial pattern (aggregation/regularity) of trees

was statistically significant at the distance t, respectively, in

the fruiting event of trees.

Results

GF episodes in 2001 and 2002

The first GF occurred from August 2001 to February 2002

(GF2001). The flowering of A. laevis, D. costulatus, S.

lepidota, and S. macroptera started in August 2001, and

many mature fruits of many species were dispersed in

January and February 2002. The second GF (GF2002)

started from March 2002, and mature fruits were dispersed

in August and September 2002. The flowering sequence of

the dipterocarp species in GF2001 was roughly consistent

with that in GF2002 (Table 1). It was noteworthy that 43

small-sized reproductive trees (B30 cm in DBH) were

found in the study plot in GF2002 (Table 2).

Table 2 Summary of fruiting behavior of 24 dipterocarp species in the 40-ha plot of the Pasoh Forest Reserve in GF2001 and GF2002

Species n Mean

DBH

(cm)

SD Nut

weighta

(g)

GF2001 GF2002

% Fruiting

trees

% Fruiting

trees

% Consecutive

fruiting trees

% Sterile

trees

Number of fruiting

trees with small

size (B30 cm) in

GF2002

Anisoptera laevis 5 89.4 22.2 1.5 20.0 40.0 20.0 60.0

Anisoptera megistocarpa 2 70.1 18.6 1.2 0.0 100.0 0.0 0.0

Dipterocarpus cornutusb 110 53.7 17.7 3.7 21.8 71.8 21.8 28.2 3

Dipterocarpus costulatus 10 66.7 29.4 2.0 40.0 50.0 20.0 30.0

Dipterocarpus crinitus 4 94.4 37.3 0.8 100.0 75.0 75.0 0.0

Dipterocarpus kunstleri 8 73.4 21.0 2.5 12.5 62.5 12.5 37.5

Dipterocarpus sublamellatusb 41 63.1 21.0 3.0 26.8 39.0 17.1 51.2

Hopea dryobalanoides 13 38.3 7.2 0.8 46.2 61.5 15.4 7.7 5

Hopea sangal 1 43.2 – 0.4 100.0 0.0 0.0 0.0

Neobalanocarpus heimiib 45 78.2 40.3 2.5 31.1 68.9 26.7 26.7

Parashorea densiflora 8 58.9 23.4 3.0 0.0 12.5 0.0 87.5

Shorea acuminatab 58 57.9 25.1 0.6 44.8 84.5 39.7 10.3 10

Shorea bracteolata 9 40.4 12.3 1.0 33.3 77.8 22.2 11.1 2

Shorea guiso 2 48.7 6.4 0.5 0.0 0.0 0.0 100.0

Shorea hopeifolia 3 87.3 47.3 1.2 66.7 33.3 0.0 0.0

Shorea lepidotab 47 46.5 17.9 1.1 6.4 66.0 4.3 31.9 7

Shorea leprosulab 64 52.5 15.9 1.3 39.1 45.3 15.6 31.3 1

Shorea macropterab 96 49.4 15.6 1.2 25.0 66.7 18.8 27.1 5

Shorea maxwellianab 133 63.5 22.1 1.5 6.8 56.4 4.5 41.4 1

Shorea multiflorab 24 44.4 15.5 1.2 0.0 41.7 0.0 58.3 6

Shorea ochrophloia 1 45.4 – 1.0 0.0 0.0 0.0 100.0

Shorea ovalisb 26 49.7 16.3 1.3 3.8 7.7 0.0 88.5

Shorea parvifoliab 70 47.4 19.7 0.7 57.1 24.3 7.1 25.7 3

Shorea pauciflorab 38 61.7 26.7 1.2 2.6 26.3 0.0 71.1

Total 818 54.7 23.4 – 24.4 54.6 14.4 35.3 43

DBH diameter at breast heighta Data taken from Ashton (1982)b Species with sufficient number of samples (n [ 20)

382 J For Res (2012) 17:378–387

123

Over all species, the magnitude of GF was greater in

GF2002 than GF2001 (Fig. 1; Table 2). The proportion of

fruiting trees in GF2002 (54.6%) was significantly different

from that in GF2001 (23.8%) (v2 test: df = 1, X2 = 162.8,

P \ 0.0001). At the species level, 79% (19 species) and

88% (21 species) of the study species produced fruits in

GF2001 and GF2002, respectively. The proportion of

fruiting trees with high fruiting intensity in GF2002

(31.4%) was also significantly different from that in

GF2001 (11.5%) (v2 test: df = 1, X2 = 96.4, P \ 0.0001).

In total, 13.9% of trees (114 trees of 15 species) produced

fruits both in GF2001 and GF2002 (consecutive fruiting

trees), and 35.5% (290 trees) of the trees produce fruits

neither in GF2001 nor GF2002 (sterile trees). Fisher’s

exact test for independence indicated that the fruiting

behavior and fruiting intensity in GF2002 were signifi-

cantly independent from those in GF2001 (P = 0.25 for

the fruiting behavior and P = 0.12 for the fruiting inten-

sity) (Table 3).

Size dependence of fruiting and effect

of adjacent fruiting

Fruiting was observed at the various size classes of trees in

both GF2001 and GF2002 (Fig. 1). The mean size in DBH

of fruiting trees was 62.8 cm in GF2001 and 60.0 cm in

GF2002, while the mean size of sterile trees was 53.9 cm

in GF2001 and 51.1 cm in GF2002. The consecutive

fruiting (in both GF2001 and GF2002) was also observed

for the various size classes and the mean size was 69.1 cm

(Fig. 2). Significant differences in tree size were found

between the sterile trees, the fruiting trees in either GF2001

or GF2002 and the consecutive fruiting trees (ANOVA:

F = 26.4, P \ 0.0001).

Results from GLM with fruiting behavior (fruiting or

sterile) as a responsible variable are shown in Table 3. At

the community level, fruiting behavior of trees in 24 dip-

terocarp species was significantly positively related to tree

size in DBH in both GF2001 and GF2002 (Fig. 2; Table 4).

At the species level, five species (D. cornutus, D.

sublamellatus, N. heimii, S. acuminata, S. macroptera)

showed significant positive size dependence of fruiting

behavior in GF2001. In GF2002, two species (N. heimii

and S maxwelliana) showed significant positive size

dependence of fruiting behavior (Table 4). At the com-

munity level, GLM analysis did not indicate significant

effect of adjacent fruiting on the subsequent fruiting

behavior (Table 4). However, only S. parvifolia showed

significant negative effects of adjacent fruiting on sub-

sequent fruiting behavior, and fruiting intensity of this

species in GF2002 was significantly associated with that in

GF2001 (Fisher’s exact test: P = 0.01).

Spatial distribution pattern of fruiting trees

For the 12 dipterocarp species with sufficient numbers of

samples (n [ 20), spatial distribution patterns of fruiting

trees were compared among different fruiting behaviors:

either GF2001 or GF2002 and consecutive fruiting trees in

GF2001 and GF2002 (Table 5). Of 35 distribution patterns

Fig. 1 Size distributions of numbers and proportion (upper) of

fruiting trees in the 40 ha plot of the Pasoh Forest Reserve in GF2001

(a) and GF2002 (b). DBH Diameter at breast height

Table 3 Comparison of fruiting intensity of trees ([30 cm in

diameter at breast height) between GF2001 and GF2002

GF2001 GF2002 Total

High fruiting

intensity

Low fruiting

intensity

Sterile

High fruiting intensity 29 18 47 94

Low fruiting intensity 38 143 290 101

Sterile 190 29 34 623

Total 257 190 371 818

Fig. 2 Tree size and fruiting behavior of trees in the 24 dipterocarp

species. Proportions of sterile trees, fruiting trees in either GF2001 or

GF2002 and consecutive fruiting trees are shown. DBH Diameter at

breast height

J For Res (2012) 17:378–387 383

123

analyzed, significant aggregation, significant regularity,

and random patterns were 6 (17%), 1 (3%), and 28 (80%),

respectively. Of these significant aggregation patterns,

strong significant aggregation patterns (P \ 0.01) were

observed for fruiting trees of S. leprosula (Fig. 3a), S.

parvifolia (Fig. 3b), and all 24 species in GF2001 (Fig. 3c),

but the others were very weak and marginally significant

(P [ 0.01). These strong aggregation patterns of fruiting

trees were found in only two species (S. leprosula and S.

parvifolia), and they greatly contributed to the community-

level spatial aggregation of fruiting in GF2001.

Inter-specific pattern of fruiting behavior

Among the 12 dipterocarp species, percentage of fruiting

trees highly varied from 0% (S. multiflora in GF2001) to

84.5% (S. acuminata in GF2002) during the two GF epi-

sodes (Table 2). In GF2001, S. parvifolia showed the

highest percentage of fruiting trees (57.1%) while S. mul-

tiflora, S. pauciflora, S. ovalis showed lower percentages of

fruiting trees (0, 2.6, and 3.8%, respectively). Shorea ac-

uminata and D. cornutus showed the highest percentages of

fruiting trees in GF2002 (84.5 and 71.8%, respectively).

Percentage of consecutive fruiting trees varied from 0%

(S. multiflora, S. ovalis and S. pauciflora) to 39.7%

(S. acuminata). No significant rank correlation was found

between percentages of fruiting trees in GF2001 and

GF2002 across the 12 species (q = 0.29, ns) (Fig. 4).

However, the species with high percentages of fruiting

trees in GF2001 marginally tended to have a high pro-

portion of fruiting trees in GF2002, except S. parvifolia

which showed significant negative effects of adjacent

reproduction on fruiting behavior in GF2002 (q = 0.59,

P = 0.06).

Discussion

Although the sequential flowering pattern did not differ

much between GF2001 and GF2002, the magnitude of

GF2002 was 1.4 times greater than that of GF2001. We

also found that the proportion of trees with the high fruiting

intensity was significantly greater in GF2002 than in

GF2001. However, the magnitudes of these episodes may

not be particularly large compared with past GF episodes in

this region, because an earlier study which investigated the

reproductive phenology of dipterocarps species showed

that the magnitude of GF which occurred in 2005

(GF2005) was 1.8 times greater than GF2002 in terms of

the percentage of flowering trees (Sun et al. 2007).

Table 4 Results from generalized linear model using with binomial error structure and logit link function

Species n Fruiting behavior in GF2001 Fruiting behavior in GF2002

Intercept Tree size Intercept Tree size Fruiting behavior

in GF2001

Dipterocarpus cornutus 110 -3.372*** 0.037** -0.409 0.020 17.750

Dipterocarpus sublamellatus 41 -3.679** 0.040* -3.017* 0.358 0.957

Neobalanocarpus heimii 45 -2.680** 0.023* -2.162* 0.043** 0.617

Shorea acuminata 58 -1.537* 0.023* 1.659 -0.004 0.622

Shorea lepidota 47 -4.310** 0.031 0.723 -0.001 0.053

Shorea leprosula 64 -1.065 0.011 -0.671 0.012 -0.394

Shorea macroptera 96 -2.863*** 0.034* -1.600 0.048* 0.142

Shorea maxwelliana 133 -4.094*** 0.022 -1.185* 0.023** 0.227

Shorea multiflora 24 0.000 0.000 -2.083 0.039 NA

Shorea ovalis 26 -0.304 -0.067 -6.019 0.063 -13.966

Shorea parvifolia 70 -0.804 0.024 -0.068 -0.008 21.486*

Shorea pauciflora 38 -36.610 0.322 -2.117* 0.018 -16.404

All trees (24 species) 818 -2.064*** 0.016*** -0.690*** 0.015*** 0.104

The effect of tree size and fruiting behavior (for GF2002) on fruiting behavior (fruiting or not) as a response variable were evaluated. This

analysis was conducted only for species for which there were more than 20 individuals ([30 cm in diameter at breast height). Level of

significance was assessed by Wald test. Significant positive size dependence of fruiting behaviour and significant negative effect of adjacent

fruiting on subsequent fruiting behaviour shown in bold

NA not applicable

* P \ 0.05

** P \ 0.01

*** P \ 0.001

384 J For Res (2012) 17:378–387

123

Factors affecting fruiting behavior

Regardless of GF magnitude, positive size dependence of

fruiting behavior was found both in GF2001 and GF2002

(Table 4). This result suggests that tree size is one of the

explanatory factors for fruiting behavior of the dipterocarps

in a GF episode. However, with the exception of S. par-

vifolia, there was no evidence that adjacent reproduction

caused the absence of reproduction and decreased fecun-

dity in the subsequent fruiting event. These results indicate

that the internal resource condition of trees may not be a

primary determinant whether they bear fruits in consecu-

tive GF episodes. Since some Dipterocarpus species tend

to flower and fruit more frequently (e.g., Ashton 1982), it is

likely that internal resource condition does not directly

affect fruiting behavior of dipterocarps even in consecutive

GF episodes at the community level. However, our results

were clearly inconsistent with the several studies that have

suggested that intensity of reproduction was strongly

influenced by adjacent reproductive status in dipterocarp

species (Burgess 1972; Naito et al. 2008). One of the

reasons may be the lack of detailed quantitative data on

flowering and fruiting intensities of individual trees in this

study. On the other hand, Shorea parvifolia showed the

highest proportion of fruiting trees (57.1%) in GF2001

among the 12 species (Table 2). The direct reason for this

is unclear, but species-specific fruiting behavior may also

be indirectly related to the responses to resource avail-

ability. Further study is needed to examine how resource

availability affects fruiting behavior at the community and

species levels.

Our results show that fruiting of S. leprosula and S.

parvifolia in the minor GF episode was spatially aggre-

gated with respect to the total population (relative spatial

aggregation). The two species may respond to relatively

weak meteorological cues at some specific site conditions

Table 5 Summarized results of the spatial pattern analysis to test ‘random reproduction’ hypothesis that assumes that the spatial distribution of

fruiting trees do not differ from that expected if flowering was a spatially random event

Species 2001 2002 Consecutive reproduction

Pattern Dmax Significant

distances

Pattern Dmax Significant

distances

Pattern Dmax Significant

distances

Dipterocarpus cornutus r – – r – – r – –

Dipterocarpus sublamellatus r – – R 170 140–210 A 250 240–250

Neobalanocarpus heimii r – – r – – r – –

Shorea acuminata r – – r – – r – –

Shorea lepidota r – – r – – r – –

Shorea leprosula A 70 20–250 r – – r – –

Shorea macroptera r – – r – – r – –

Shorea maxwelliana r – – r – – r – –

Shorea multiflora a – – r – – a – –

Shorea ovalis r – – r – – a – –

Shorea parvifolia A 30 20–120 r – – r – –

Shorea pauciflora r – – A 20 20 a – –

All trees (24 species) A 80 0–190 A 240 240–250 r – –

This analysis was conducted only for species for which there were more than 20 individuals ([30 cm in diameter at breast height). Significant

departures from the null hypothesis of ‘random reproduction’ are considered at the P \ 0.05 significance level based on 500 simulations.

Significant distances indicate distances for which L(t) was significant. Dmax represents the ‘‘scale’’ of spatial patterns, which is defined as the

distance with maximal deviation between the significant L(t) values and the mean L(t) of 500 simulations under the null hypothesis

A Aggregation pattern, R regular pattern, r random patterna Spatial patterns were not analyzed because there were no fruiting plants

Fig. 3 Representative spatial patterns that were remarkably signifi-

cant by spatial pattern analysis. a Fruiting trees of Shorea leprosula in

2001, b fruiting trees of Shorea parvifolia in 2001, and c fruiting trees

of all species in 2001. Solid line observed L(t) values, broken and

dotted lines 95 and 99% confidence envelopes, respectively, derived

from 500 simulations of the random reproduction hypothesis, which

assumes that the spatial distribution of sterile or fruiting trees does not

differ from expected if flowering was a spatially random event. Upper

deviation from the confidence intervals indicates that spatial distri-

bution of plants significantly aggregated at the spatial scales

J For Res (2012) 17:378–387 385

123

in a minor GF episode. In fact, both minimum air tem-

peratures and minimum soil moistures before GF2002

(January–March 2002) were lower than those before

GF2001 (June–August 2001) in forest understory of the

Pasoh Forest Reserve (GF2001: 20.5�C and 20.6%;

GF2002: 17.6�C and 6.9%; M. Adachi, National Institute

for Environmental Studies of Japan, unpublished results).

On the other hand, Itoh et al. suggested that spatial fruiting

aggregation of a dipterocarp species repeatedly occurred in

the Lambir Hills National Park. This may reflect a differ-

ence of elevation within a plot between the Lambir Hills

National Park (ca. 140 m) and our study site (ca. [20 m)

(Lee et al. 2004; Manokaran et al. 2004). A further study

on habitat association with topography and soil condition is

needed to determine how topographic and soil heteroge-

neity of the microenvironments affect fruiting behavior of

GF species in a lowland rain forest.

Inter-specific pattern of fruiting behavior

of dipterocarp species

We found large differences in fruiting behavior among the

12 species (Table 2). Except for S. parvifolia which showed

significant effects of adjacent reproduction on fruiting in

GF2002, percentages of fruiting trees in GF2001 marginally

positively correlated with that in GF2002 across the 12

species (Fig. 4). What explains such inter-specific differ-

ences in fruiting behavior among the dipterocarp species in

a GF episode? It is well known that rainforest tree species

can be classified into several types of guilds, strategies or

functional groups (e.g., climax and pioneer species in

Whitmore and Burnham 1984). Suzuki et al. (2009)

examined growth strategies of 11 dipterocarp species in the

50-ha plot of the Pasoh Forest Reserve, and classified the

species into fast-growing species with high mortality rates

and slow-growing with low mortality rates. Six species

(S. acuminata, S. lepidota, S. leprosula, S. ovalis, S. par-

vifolia, and S. pauciflora) in our study were regarded as fast-

growing. However, percentages of fruiting trees varied

greatly even among the six species in both GF2001 and

GF2002 (Fig. 4; Table 2). Therefore, the ecological growth

type of dipterocarp species does not simply explain the

inter-specific pattern of fruiting behavior.

Instead of growth types of trees, we assume that fruiting

behavior of dipterocarp species in a GF episode may be

related to the other reproductive traits, because there are

differences in reproductive frequency, flower and fruit

characteristics, production volume, and pollination system

even among the study species (Ashton 1982; Suzuki and

Ashton 1996). For example, the three species (S. paucifl-

ora, S. maxwelliana and S. lepidota) which showed lower

numbers of fruiting years during observations over a cer-

tain period (Yap and Chan 1990; Numata et al. 1999) had

low percentages of consecutive fruiting trees in this study.

Thus, reproductive traits may also be important in

accounting for species-specific differences in phonological

responses to internal and external conditions in dipterocarp

species. Comprehensive studies including fruiting behavior

as well as the other reproductive traits during the regen-

eration stage are important to understand reproductive

behavior of dipterocarps in GF phenomena.

Acknowledgments The authors particularly thank K. Obayashi who

arranged the establishment of the 40-ha plot. We also thank N. Kachi

and anonymous reviewers for valuable comments and suggestions.

We thank field assistants, Tompol, Ating, Data, Boo, Ali-Satu,

Semping, Ali-Dua, Kesiong, Wak, Dan, Tajam, and Omar for their

help in performing the fieldwork. The present study was a part of a

joint research project between the Forest Research Institute of

Malaysia, Universiti Putra Malaysia, and National Institute for

Environmental Studies of Japan (Grant no. E-4 from the Global

Environment Research Program, Ministry of Environment of Japan).

All the research reported here was conducted in compliance with the

laws of the relevant countries.

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