American Journal of Botany 93(8): 1134–1139. 2006.

IRREGULAR DROUGHTS TRIGGER MASS FLOWERING IN
ASEASONAL TROPICAL FORESTS IN ASIA

1SHOKO SAKAI,2,10 RHETT D. HARRISON,3 KUNIYASU MOMOSE,4 KOICHIRO KURAJI,5 HIDETOSHI NAGAMASU,6TETSUZO YASUNARI,7 LUCY CHONG,8 AND TOHRU NAKASHIZUKA3,92

Center for Ecological Research, Kyoto University, Otsu 520-2113, Japan; 3Research Institute for Humanity and Nature, Kyoto
602-0878, Japan; 4Department of Agriculture, Ehime University, Matsuyama 790-8566, Japan; 5University Forest in Aichi,
University of Tokyo, Seto, Aichi, 489-0031, Japan; 6The Kyoto University Museum, Kyoto 606-8501, Japan; 7Hydrospheric
Atmospheric Research Center, Nagoya University, Furo-cho, Nagoya 464-8601, Japan; 8Forest Research Center, Forestry
Corporation, Kuching 6 Mile Road, Sarawak 93250, Malaysia; 9Graduate School of Life Sciences, Tohoku University,
Sendai 980-8577, Japan

General flowering is a community-wide masting phenomenon, which is thus far documented only in aseasonal tropical forests
in Asia. Although the canopy and emergent layers of forests in this region are dominated by species of a single family,
Dipterocarpaceae, general flowering involves various plant groups. Studying proximate factors and estimating the flowering
patterns of the past and future may aid our understanding of the ecological significance and evolutionary factors behind thisphenomenon. Here we show that this phenomenon is most likely triggered by irregular droughts based on 10 years ofobservations. In the aseasonal forests of SE Asia, droughts tend to occur during transition periods from La Niña to El Niño, which
results in an irregular 6–7-yr cycle involving a dry period with several droughts and a wet period without droughts. The magnitudeof a flowering event also depends on the timing of droughts associated with the El Niño southern oscillation (ENSO) cycle, withthe largest events occurring after an interval of several years with no flowering. Because most plant species can only reproduce
successfully during large flowering events, changes in the ENSO cycle resulting from global warming, may have serious
ramifications for forest regeneration in this region.
Key words:

Borneo; dipterocarp forests; Lambir; mass flowering; masting; Malaysia; phenology; Sarawak.

Masting is the intermittent production of large seed crops bya plant species synchronized within a population (Kelly, 1994).
The phenomenon has attracted the attention of biologists andhas been studied intensively, especially in temperate canopy
tree species such as oaks and beeches. In many cases,
fluctuations in fruit production are partly or mostly due tofluctuations in flower production. Although variation in flower/
fruit production may be explained by resource matching (e.g.,
crops sizes vary simply in response to environmental
variation), in most cases the fluctuation is much larger than
anticipated. Thus, evolutionary factors that favor large
fluctuation are thought to be involved. Promotion of windpollination, predator satiation, and animal dispersal are often
suggested as selective agents (Kelly, 1994).
General flowering (GF), one of the most spectacular andmysterious phenomena in tropical biology, is a masting
phenomenon unique to Asian dipterocarp forests. It is unique
in involving the synchronization of flowering thus fruiting
across diverse plant groups (Ashton et al., 1988; Sakai, 2002).
GF occurs at irregular intervals of less than 1 year to several
years. During such an event, most dipterocarps and many otherplants, from shrubs to emergent trees to epiphytic orchids,
1

Manuscript received 6 December 2005; revision accepted 26 May 2006.

The authors thank R. Johan for helping with field observations, theSarawak Forestry Department and Sarawak Forestry Corporation for
permission and logistic support, the Department of Irrigation andDrainage, Sarawak, Malaysia, for providing rainfall data, and T. Inoueand other members working in Lambir Hills National Park for help andsupport in various ways. This study was partly supported by the ResearchInstitute for Humanity and Nature Project (P2–2) in Japan, the Ministry of
Education, Science, Sports, and Culture (no. 16405006), and the Grant for
the Biodiversity Research of the 21st Century COE (A14), Japan.
10
Author for correspondence (e-mail: shoko@ecology.kyoto-u.ac.jp)

flower over roughly a 3-mo period. Conversely, flowers are
scant between GF events especially in the canopy and emergent
layers, while many understory herbs and treelets may flower
more frequently. The timing and extent of GF appears to be
unpredictable. GF occurs in different seasons at the same sites
and may be widespread, for example extending across theentire Sunda region, or it may be localized (Ashton et al.,1988). Thus, in the lowland dipterocarp forests of SE Asia,
many taxa respond to the same flowering trigger, but thetrigger occurs at irregular intervals, at various times of the year,
and over both large and small areas. The situation is very
different to that in the equatorial regions of the Americas where
small annual changes in sunrise and sunset trigger floweringand leaf flushing (Borchert et al., 2005).
Several hypotheses for the evolution of GF have been
proposed, including the most widely accepted one of seed
predator satiation. Recently, two groups (Sakai, 2002;
Williamson and Ickes, 2002) have independently suggested
the potential role of ‘‘environmental prediction’’ in theevolution of GF. They hypothesize that plants can predict
which years will be best for the survival of seedlings, thensynchronously flower and produce seeds only in such years.
While the hypothesis may not hold true for masting in seasonal
climates, except for some special cases (Kelly, 1994), it may be
more significant in aseasonal climates. In seasonal climates,
most flowering triggers of annually flowering plants cause not
only synchronization among individuals, but also signal thestart of a new climatic condition or season. For example, heavy
rain after a long dry period induces the flowering of tropical
shrubs, and the rain also indicates the start of wet conditions
lasting for several months (Augspurger, 1981). Many
temperate woody species flower at the same time of the year
in response to temperature or cumulative heatsums (Rathcke1134

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S AKAI ET AL .—D ROUGHTS TRIGGER GENERAL FLOWERING

and Lacey, 1985). Because the climate has an annual cycle,
plants can anticipate climatic conditions at least in terms ofannual averages. On the other hand, whether flowering triggers
also signal some future climatic condition and whether plants
have evolved to flower in favorable periods for pollination or
the establishment of seedlings in aseasonal climates, often withmore prominent supra-annual rhythms than annual ones, haverarely been investigated.
Proximate factors of general flowering have been the subjectof controversy over the last decades. Identification of thetrigger is considered to be important for evaluating roles ofclimatic conditions as a determinant of phenology, and toassess why community-wide masting phenomenon does notoccur in other tropical regions. In addition, such information isessential for the management and conservation of anendangered ecosystem, especially to explore effects of climatechanges on forest regeneration. Two climatic factors have been
proposed as GF triggers: drought and a temperature drop, bothof which may be associated with the El Niño Southern
Oscillation (ENSO) (Ashton et al., 1988; Yasuda et al., 1999;
Curran et al., 1999; Wich and van Schaik, 2000; Sakai, 2002).
Prolonged droughts (e.g., Appanah, 1985) or an increase insolar radiation associated with dry conditions (Ng, 1977; van
Schaik, 1986) have repeatedly been reported for GF years. On
the other hand, Ashton et al. (1988) argued, based on 11-yr
records of flowering from Pasoh, Malay Peninsula, that a dropin the daily minimum temperature always preceded flowering
events. Temperature drops preceding GF were also confirmed
for later flowering events at that site (Yasuda et al., 1999;
Numata et al., 2003) and other sites (Sakai et al., 1999). Manyof these researchers presented data from single environmental
cues and GF records or only casually mentioned an association.
Yasuda et al. (1999) and Numata et al. (2003) examined
temperature and rainfall in parallel, but as they discussed, there
was a correlation between the two climatic variables, which
prevented distinguishing between the two hypotheses.
In this paper, we examine GF triggers based on observations
over a 10-yr period, comprising four GF years. We also present
temporal patterns of flowering triggers over a period of 19 yr
and meteorological conditions associated with the triggers.
Finally, we discuss hypotheses for the evolution of GF in thelight of meteorological characteristics of the identified triggers.
MATERIALS AND METHODS
Study site—Our study was carried out in a lowland dipterocarp forest at
Lambir Hills National Park, Borneo (4820 0 N, 113850 0 E, 150–250 m above sea
level) (Roubik et al., 2005). Rainfall data were collected at the Bukit Lambir
Station of the Department of Irrigation and Drainage (DID), Sarawak,
Malaysia, within the park approximately 3 km northwest of the study site.
From 1985–2003, the average annual rainfall was 2722 mm and ranged from2044 mm to 3822 mm. Seasonal variation was significant but low, and the area
occasionally had droughts with biological consequences (Harrison, 2000;
Nakagawa et al., 2000; Delissio, 2003; Potts, 2003; Ititoka and Yamauti, 2004).
Plants were observed using a canopy observation system (tree towers andwalkways) constructed at the center of the Canopy Biology Plot (8 ha, 200 3
400 m) (Roubik et al., 2005) and another tree tower constructed as a tourist
attraction. The Canopy Biology Plot includes humult and udult soils (sandy
clay, light clay, or heavy clay in texture), several ridges and valleys, and closed(mature-stage) forests and canopy gaps. The tower for tourists is situated alonga stream on yellow sandstone, 2 km northeast of the Canopy Biology Plot.
Because the plant reproductive phenology did not differ significantly between
the two sites, we treated them together throughout this paper.

1135

Meteorological data—We calculated the 30-d moving rainfall total toidentify droughts (defined as ,40 mm total rainfall for more than 30 d).
Meteorological rhythms in the tropical part of the Indian monsoon area (Asia,
Australia, and the West Pacific) tend to generate dry spells of 15–30 days
(Yasunari, 1979), and hence a 30-d period best links flowering patterns to theoccurrence of drought. From 1993 to 1998, temperature was monitored every
30 min (temperature/humidity sensor, E7050–10, Yakogawa Weathac Corp.,
Tokyo, Japan) from a tower 35 m above the ground located at our study site,and since 2000 every 10 min on a different tower 50 m above the ground(VHE-Z23, Vaisala K. K., and Hobo H8Pro, Onset). Also in 2000, a solar
radiometer (MS401, EKO, Tokyo, Japan) was installed on the top of a canopy
crane 85.8 m above the ground. Readings were taken every 5 s and averaged
over 10 min (CR10X data logger, Campbell Scientific, Logan, Utah, USA).
Both temperature and radiation data sets have missing values due to mechanicalproblems.
Because droughts are known to be associated with ENSO in this region, we
examined the relationship of droughts from 1985–2003 at Lambir Hills and theTroup southern oscillation index (SOI), which is the standardized anomaly ofthe difference in mean sea level pressure between Tahiti and Darwin. Sustained
negative values of the SOI indicate El Niño episodes.
Monitoring plant reproduction—We have monitored reproductive
activities of trees, lianas, and epiphytes since 1993 (Sakai et al., 1999). Our
sampling of the plants did not directly reflect the number of individuals of eachlife form, but was weighted toward larger plants (i.e., canopy and emergent
trees). Due to the death of some of the monitored plants and an incomplete dataset, we used data from 309 individuals of 178 species for this study, including
114 dipterocarps of 40 species (Appendix S1, see Supplemental Dataaccompanying online version of this article). Flowering phenology in the GF
of 1996, 1997, and 1998 of three dipterocarp genera, Dipterocarpus (N ¼ 26),
Dryobalanops (N ¼ 15), and Shorea (N ¼ 67), and two other families,
Burseraceae (N ¼ 17) and Euphorbiaceae (N ¼ 34), were compared to examine
the correlation between meteorological factors and flowering patterns.
Flowering in 2001 was not shown because the flowering sequences were notclear, probably due to successive flowering triggers within a short period.
Plant phenology was monitored twice a month and, in this paper, we reportresults from July 1993 up to the end of September 2003. At each census,
reproductive organs (flower buds, flowers, and fruits) were observed, and theintensity of reproductive activity for each individual was recorded as one of fivegrades: 0, nonreproductive; þ, very few flowers or fruits covering ,1% of thecrown; 1, .1% and ,50% of the crown covered with flowers or fruits; 2,.50% and ,80% of the crown covered with flowers or fruits; 3, flowers or
fruits covering .80% of the crown.
Flowering and fruit set of Dipterocapaceae in different years—For
dipterocarps, we define a reproductive event as a series of plant reproductive
activities from flowering to fruit dispersal. Indices of flowering and fruiting
were determined as the maximum grade of intensity of plant reproductive
activities, as defined earlier, throughout the period with flowers and mature
fruits, respectively. Therefore, these two variables (e.g., indices of floweringand fruiting) were divided into four categories (þ, 1, 2, and 3, as described).
Very minor reproductive events in which the maximum grade of the intensity of
reproductive activities throughout the event was þ, usually indicating theflowering of only one branchlet on a large tree, were excluded from thefollowing analysis.
We classified the events based on the year when the event started (the firstdate of observed flowering or fruiting). Reproductive events in 1993 and 2003
were excluded from the analysis due to incomplete coverage in those years. We
defined an index of the magnitude of GF (1, 2, and 3) based on the number ofreproductive events for Dipterocarpaceae in each year (see Results), rather than
all reproductive events. This was done because the flowering phenology ofDipterocarpaceae showed the strongest association with GF (Sakai et al., 1999),
and because reproductive events of Dipterocarpaceae could be more clearly
identified. In taxa with very short reproductive events or, conversely, those thatare flowering or fruiting most of the time, it can be difficult to distinguish
reproductive events. To evaluate relationships among the three variables(magnitude of GF, intensity of flowering, and intensity of fruiting), we
calculated the Spearman correlation coefficients for all paired combinations.
Because there were correlations between all three variables, we further
evaluated the correlation between the magnitude of GF and the fruit set bycalculating the Spearman partial correlation coefficients for the magnitude of
GF and the intensity of fruiting controlled by the intensity of flowering. Then1136

A MERICAN J OURNAL OF B OTANY

Fig. 1. Plant reproductive phenology and climatic variables over 10
yrs at Lambir Hills National Park, Sarawak, Malaysia. Vertical dotted lines
indicate the timing of drought peaks. (a) Temporal changes in the
proportion of flowering (thick line) and fruiting (thin line) in all
individuals monitored in this study (see Appendix S1 in Supplemental
Data with online version of this article; N ¼ 309). (b) Changes in the
proportion of flowering (thick line) and fruiting (thin line) individuals of
Dryobalanops aromatica and D. lanceolata (Dipterocarpaceae) (N ¼ 15).
(c) Changes in total rainfall over the proceeding 30-d period. The
horizontal line indicates 40 mm, the maximum rainfall for our definition ofdrought. (d) Daily minimum temperature monitored on top of tree towers
at our study site. (e) Daily changes in average net daily radiation over 10d and monitored from the top terrace of a canopy crane.

we tested if the coefficients deviated significantly from zero. The analysis was
conducted using program SAS (SAS Institute, Cary, North Carolina, USA).

RESULTS
Flowering patterns and meteorological data—During the
10 years, we observed a relatively large GF in 1996 and small
GFs in 1997, 1998, and 2001 (Fig. 1). GF in 1996 clearly had
two peaks, and in each peak, the composition and sequence offlowering species were similar. Two flowering peaks, withconsiderable overlap, could also be discerned in 1998 and in2001 (Fig. 1).
A close association between temperature drops and droughts
was not observed. Significant temperature drops preceded GF
in 1996 and 1997, by 3 and 4 months, respectively (Fig. 1d).
However, no temperature drop was observed in 2001. On theother hand, on every occasion that the 30-day total rainfall[Vol. 93

Fig. 2. Changes in the proportion of flowering individuals in three
genera Dipterocarpus (N ¼ 26), Dryobalanops (N ¼ 15), and Shorea (N ¼67) (Dipterocarpaceae), and the two families Burseraceae (N ¼ 17) andEuphorbiaceae (N ¼ 17) over three general flowering events in 1996 (a),1997 (b), and 1998 (c). The arrow indicates the timing of the drought ineach case.

dropped below 40 mm, either a small or a large GF occurred(Fig. 1c). All flowering peaks were also preceded by a drought,with one exception. In 2001, two rather indistinct floweringpeaks were observed, but only one drought (30 day rainfall
total , 40 mm) was recorded. However, an additional dry spell(30 day rainfall total ¼ 70.5 mm) did occur 1.5 months before
flowering. Fluctuations in radiation are roughly correlated with
rainfall patterns (Fig. 1e). However, in 2001 three peaks ofsolar radiation of similar strength were observed, but only thelast one was followed by a relatively large flowering.
Therefore, the strength of radiation and the magnitude offlowering did not correlate well, and the temporal match ofincreased radiation with the onset of flowering was variable.
From these results, we concluded that drought is the mostplausible trigger of GF.
Close examination revealed a very constant temporal
relationship between the timing of droughts and flowering(Fig. 2). The interval between a drought and flowering wasvery short. In 1996, the first observed flowering ofDryobalanops was recorded on 26 March, 4 days after theend of a drought. In 2001, Dryobalanops was observed
flowering on July 31, 10 days after the end of the minor
drought mentioned. Flowering sequences in the four GFs of
1996, 1997, and 1998 did not vary significantly. Euphorbia-

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S AKAI ET AL .—D ROUGHTS TRIGGER GENERAL FLOWERING

Fig. 3. Occurrence of droughts (30-d rainfall total , 40 mm) (arrows)
and the 3-mo moving average of the southern oscillation index (SOI). Dry
periods with droughts are shaded. Negative SOI values indicate El Niñoconditions.

ceae usually started flowering well before other groups, andflowering peaked when the 30-day total rainfall was lowest or
when the drought ended (Fig. 2, indicated by arrows). About 1
month after the end of a drought, flowering peaks wererecorded for Dryobalanops, Dipterocarpus, and Burseraceae.
In all 3 years, Burseraceae had two flowering peaks; the two
peaks included both some of the same and some different
species. Shorea always flowered last.
Nineteen-year southern oscillation index and droughtrecords—From 1985 to 2003, droughts (measured as total
rainfall , 40 mm for 30 d) occurred 14 times (Fig. 3): three
from 1985–1988, five from 1990–1993, and five from 1996–
1998. Droughts most often occurred when the SOI waschanging from positive to negative, indicating transition
periods from La Niña to El Niño.
Magnitude of fruiting—From 1994 to 2002, 269 dipterocarp reproductive events were recorded. The numbers of
reproductive events in 1996, 1997, 1998, and 2001 were 82,
45, 59, and 57, respectively. In other years, there were six
events or less. Thus, three categories for GF year were
determined: 1, non-GF years (1994, 1995, 1999, 2000, and2002); 2, small-GF years (1997, 1998, and 2001); and 3, largeGF year (1996) (Fig. 4). The three variables (e.g., category of
GF year, intensity of flowering, and intensity of fruiting) weresignificantly correlated (category of GF year and flowering, P¼ 0.001; category of GF year and fruiting, P , 0.001;
flowering and fruiting, P , 0.001). The partial correlation
between category of GF year and fruiting intensity controlled
by flowering intensity was both positive and highly significant(r ¼ 0.162, P ¼ 0.008).
DISCUSSION
Trigger of general flowering—From our studies in Borneo
over a 10-yr period, we conclude that drought is the mostplausible trigger for GF. We recorded a large GF in 1996 andsmaller flowering events in late 1997, 1998, and 2001 (Fig. 1).
All flowering peaks were preceded by dry periods, except one in2001 preceded by a weak dry spell (discussed in the next
section), and every drought (30-d rainfall total , 40 mm, seeMaterials and Methods section) was followed by a flowering.
The different plant taxa examined had a similar sequence offlowering in different GF events, supporting the view that they
are responding to a common trigger. A previous study among

1137

Fig. 4. Proportion of flowering trees with over 50% of crown (a)flowering and (b) fruiting in different years from 1994 to 2002 plottedagainst the total number of dipterocarps flowering over the year. The
numbers of trees flowering in 1996, 1997, 1998, and 2001 were 82, 45, 59,
and 57, respectively. In other years, fewer than six trees flowered. Thus,
the years were categorized into three general flowering categories; high(1996), low (1997, 1998, and 2001), and non-general flowering (1994,
1995, 1999, 2000, and 2002).

Shorea species on the Malay Peninsular also confirmed similar
flowering sequences in different flowering events (LaFrankie
and Chan, 1991). Interestingly, minor droughts were found to
trigger leaf flushing in several species (Ichie et al., 2004).
Flower induction is basically the transformation of leaf buds toflower buds (Syamuswida and Owen, 1997). Thus, these results
suggest plants initiate buds when dry conditions start andproduce either leaves or flowers depending on the severity of thedrought. Conversely, neither temperature nor solar radiation
was clearly correlated with flowering. Although our temperature
data have some gaps and temperature drop cannot be examinedin some years, we can safely say that GF can occur without
a preceding drop in temperature as shown by the flowering in
2001. For solar radiation, however, we may need further data
and analysis to evaluate its role as a flowering trigger because
data are available for only a relatively short period.
One of the subjects for future studies is how the plants
respond to the drought so quickly. Some species start flowering
before the peak of the drought (Fig. 2). Because the end of thedrought is actually the start of rainfall, the observed patternindicates that at least some of the plants start flowering in
response to drought rather than to the rain after the drought.
Nevertheless, the interval between the start of drought and thatof flowering is still shorter than the time usually required forflower development in many other plants (Salisbury, 1963).
Careful anatomical observation of flower development may berequired before we conclude that drought is a sufficientcondition for flower initiation (Syamsuwida and Owens, 1997).
Dry conditions in SE Asia are associated with the El Niñocycle (Popelewski and Halpert, 1987). From 1985 to 2003, the14 droughts fell into three periods from 1985 to1988, from1990 to 1993, and from 1996 to 1998. There may be an
irregular 6–7-yr cycle involving a dry period with several
droughts and a wet period without droughts. Droughts occurred
during transition periods from the La Niña to El Niño, or at the
beginning of an El Niño period. The five droughts associatedwith the 1996–1998 period triggered four successive flowerings in three years and similar patterns have been reported fromother sites (Yap and Chan, 1990; Curran et al., 1999). Becauseof the dry–wet cycles, flowering intervals are very irregular,
and earlier studies have tended to overlook the shorter intervals(e.g., Janzen, 1974).

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Magnitude of flowering and fruiting—Correlation between
the strength of a drought and the magnitude of a GF event does
not seem to be very simple. The magnitude may be affected by
the level of accumulated resources in addition to the strength of
the trigger. During the 1996–1998 period, the first flowering
episode in 1996 was much bigger than the subsequent
flowerings. Stored phosphorus, rather than carbon or nitrogen,may be a determinant of the magnitude because it is known that
phosphorus in dipterocarp trees dramatically decrease during
flowering and fruiting (T. Ichie, Kochi University, personalcommunication). The level of accumulated resources may also
affect the response threshold to the trigger. For example, thefirst of two flowering peaks in 2001, which occurred after 3
years without flowering, was preceded by a relatively weak dry
period (30-d rainfall total ¼ 70.5 mm). We think that a relatively
long wet period before the drought increases the sensitivity ofthe plant to the trigger.
Magnitude of GF may strongly affect reproductive successof individual trees. In our study, many individual trees
produced a large number of flowers in both small and large
flowering events, but fruit crops were smaller in small GF
events (Fig. 4). The partial correlation between the category of
GF year and flowering intensity was positive and significant (P¼ 0.008), meaning that more large-flowering events resulted inlarge fruit crops during a big GF year than in smaller GF years.
These results could be explained by either increased pollination
success (outcrossing opportunities or pollinator facilitation) or
increased pre-dispersal seed survival during larger flowering
events or a combination of both factors. In several studies,increased postdispersal seed and seedling survival during larger
flowering events has also been demonstrated (Curran andLeighton, 2000). Only the first flowering event of a wet period
may contribute to regeneration of GF plants.
Implications to evolutionary factors—The most parsimonious explanation of general flowering is simply the irregularoccurrence of the flowering trigger. For most of theirevolutionary history, the lowland dipterocarp forests of SE
Asia have experienced a drier, more seasonal climate (Ashton
et al., 1988). Today, flowering normally occurs toward the endof the dry season or beginning of the wet season in seasonal
forests in Asia. Hence, it is not unreasonable to suggest that at
the onset of humid, aseasonal conditions 7000 years ago,species were physiologically committed to waiting for a dryseason trigger, thus irregular occurrences of drought has led to
the GF phenomenon. This historically based hypothesis would
also explain why GF is a community-wide phenomenon,
affecting many different taxa and ecological types, which
would be a surprising result for most of the other hypotheses.
Nevertheless, one or more selective factors, such as seed
predator satiation, pollination facilitation and/or environmental
prediction, are believed to have played a role in the evolution
of GF because of such strong synchronization of reproduction
among various plant species.
Association among flowering trigger, magnitude of fruiting,and ENSO revealed by this study has important implications
for understanding the evolutionary factors behind GF. For
example, it has been postulated that the onset of rain following
a drought should indicate the start of a long wet period before
the next drought, and hence more seedlings will survive (Sakai,2002). However, this is clearly not the case when droughts insuccessive years are common, and the first flowering event ina series usually results in successful mass fruiting (see the[Vol. 93previous section). On the other hand, droughts or clear weather
may be favorable for pollination and accumulation of resources
for reproduction (van Schaik et al., 1993). The current
photosynthates, rather than stored assimilates, are considered
to be the major carbon source for fruit development in
dipterocarp trees (Ichie et al., 2005). Williamson and Ickes(2002) proposed that droughts that trigger flowering provide
a favorable environment for seedling recruitment by improving
light conditions on the forest floor because the drought also
caused substantial defoliation and mortality of canopy trees. On
the other hand, repetition of consecutive masting andnonflowering periods suggests that the resource matching
hypothesis (Kelly, 1994) and the strict resource thresholdmodel (Isagi et al., 1997) do not explain the timing of GF
events. GF, when we do not consider variations in magnitude,
seems to be governed by triggers rather than resources.
By far the most popular hypothesis proposed to explain GF
is that of ‘‘seed predator satiation’’ (Janzen, 1974; Curran et al.,
1999; Curran and Leighton, 2000): Populations of seed
predators are reduced during periods of low seed production,
so that in a masting the seed predator population is quickly
satiated and a high proportion of seeds escape. As applied to
GF, the hypothesis assumes that the interval between flowerings is long, so that the high populations of seed predators
generated during one masting event decline before the next.
The hypothesis is supported by a decline in viable seed andseedling establishment during a minor flowering event
compared with that during a major event (Curran and Leighton,
2000). The present study suggests, however, that in addition to
the magnitude of fruiting, the intervals between flowerings may
also influence the effectiveness of seed predator satiation
because the length of the time intervals are highly variable.
Further studies on the intensity of fruiting, population
dynamics of seed predators, and survival of seeds and seedlings
are needed to understand efficiency of predator satiation in GF.
Implications for conservation—A recent increase in theintensity and frequency of droughts has been reported forseveral places in Borneo (Harrison, 2005) and other tropicalregions (Condit, 1998). This may be due to global climatechange (Timmermann et al., 1999), a decrease in forest cover,or long-term periodic changes in ENSO frequency andmagnitude. However, the effect of these changes on theecology of dipterocarp forests is unknown (Corlett and
LaFrankie, 1998). ENSO-related droughts are thought to haveoccurred in Borneo throughout the Late Pleistocene andHolocene periods, but estimates of the frequency andmagnitude have varied considerably. From 15 000 to 7000 yr
BP ENSO is thought to have had a cycle of about 15 yr, while
it is 2–8.5 yr at present (Robell et al., 1999). There have also
been substantial changes in the extent of lowland forests in SE
Asia, as a result of sea-level fluctuations, and their seasonality.
Changes in drought frequency and magnitude may have serious
consequences for the long-term viability of these forests,
although it may not be very apparent at the moment, especiallyin the face of other anthropogenic changes such as deforestation. For example, the results of this study suggest thatchanges in the ENSO cycle, may have serious ramifications forforest regeneration in this region, because most plant species
can only reproduce successfully during large flowering events
after wet periods for several years. A greater effort should bemade to coordinate studies among sites to further theunderstanding the GF phenomenon.

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