Popul Ecol (2001) 43:77–86
© The Society of Population Ecology and Springer-Verlag Tokyo 2001
SPECIAL FEATURE: ORIGINAL ARTICLE
Shoko Sakai
Phenological diversity in tropical forests
Received: September 8, 2000 / Accepted: January 30, 2001
Abstract One of the most intriguing and complex characteristics of reproductive phenology in tropical forests is high
diversity within and among forests. To understand such
diversity, Newstrom et al. provided a systematic framework
for the classification of tropical flowering phenology. They
adopted frequency and regularity as criteria with priority,
and classified plants in La Selva, Costa Rica, where most
plants reproduced more than once a year irregularly. Many
other studies have demonstrated annual cycles corresponding to rainfall patterns at the community level in Neotropical forests, including La Selva. On the other hand,
supraannual flowering synchronized among various plant
species, called general flowering, is known from aseasonal
lowland dipterocarp forests in Southeast Asia. Within both
forests, a wide spectrum of flowering patterns is found. This
range of patterns suggests the great potential of tropical
phenological studies to explore the selective pressures on
phenology. Various abiotic and biotic factors can be selective agents. The shared pollinators hypothesis suggests that
plant species sharing pollinators segregate flowering temporarily to minimize interspecific overlap in flowering times
and thus minimize ineffective pollination or competition for
pollinators, indicating strong phylogenetic constraints in
timing and variation of flowering. Comparison of phenology
within and among forests may help our understanding of
phenological diversity. Attempts are now being made to
develop a common language to communicate concepts and
render interpretations of data more compatible among investigators and to create a network to promote comparative
studies.
S. Sakai
Smithsonian Tropical Research Institute, Ancón, Republic of
Panama
Present address: Graduate School of Human and Environmental
Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo-ku,
Kyoto 606-8501, Japan
Tel. 181-75-753-6849; Fax 181-75-753-2999
Key words Plant reproductive phenology · General
flowering · Pollination · Predator satiation · Resource availability · Phylogenetic constraint
Introduction
Phenology is the study of the periodicity or timing of recurring biological events. What causes their timing with regard
to biotic and abiotic forces, and how does this timing affect
interrelation among phases of the same or different species?
In the case of plants, phenological events involve flowering,
fruiting, leaf flushing, and germination (Leith 1974). It is
certainly conceivable that the schedule of these events has
important effects on survival or reproductive success. Not
only abiotic environmental conditions such as temperature
and humidity, but also biotic factors including intraspecific
and interspecific competition for various resources, i.e., interactions with other organisms such as herbivores, pollinators, and seed dispersers, can be selective agents for plant
phenology. Some studies have showed experimentally that
germination, flowering, and leaf production out of season
caused low survivorship of seedlings (Tevis 1958), low seed
production (Augspurger 1981), and a high predation rate
(Aide 1992), respectively. On the other hand, plant phenology can greatly affect animals that use young leaves, flowers, and mature and immature fruits through temporal
changes in plant resource availability (van Schaik et al.
1993). Because of the importance and complexity of phenology, many studies have been conducted from various
points of view (reviewed in Rathcke and Lacey 1985;
Primack 1987; van Schaik et al. 1993), mostly in the temperate region (Newstrom et al. 1994a,b).
One principal characteristic of phenology in tropical
forests may be high diversity, partly because of the weaker
physical constraints on schedules of biological activities
(Gentry 1974; Janzen 1978; Sarmiento and Monasterio
1983; Newstrom et al. 1994a,b). Gentry (1974) may have
been among the first to indicate the existence of higher
diversity in phenology in tropical forests than among those
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of the temperate zone and to discuss its significance in relation to reproductive success. This study showed the great
potential of tropical phenological studies to explore selective pressures on phenology.
Few studies, however, have focused on phenological diversity among species. Most studies on plant phenology in
tropical forests have been conducted to describe community-level patterns of leafing, flowering, and fruiting, often
for purposes of studying resource availability for consumer
animals (Frankie et al. 1974; Croat 1975; Putz 1979; Opler
et al. 1980; Foster 1982; Koptur et al. 1988; Murali and
Sukumar 1994; Justiniano and Fredericksen 2000; Morellato et al., in press). From a botanical perspective, individual-level behavior has been analyzed in more detail in
population-level studies for rather short time periods, focusing on physiological releasing mechanisms (Augspurger
1981; Reich and Borchert 1982) and degree or effects of
synchronization within a population (Augspurger 1980,
1983; Primack 1980).
In this review, I first briefly introduce the framework for
studies on tropical phenology proposed by Newstrom et al.
(1994a,b). Although one problem concerned with phenological diversity is the difficulty of describing phenology and
confusion in terminology, a conceptual framework has been
proposed by Newstrom et al. (1994a,b) to improve communication. Second, I review two contrasting flowering patterns: flowering phenology in seasonal neotropical forests,
and the general flowering phenomenon in dipterocarp forests of Southeast Asia. Unfortunately, phenological patterns in other tropical regions have scarcely been studied. I
then mention potential factors that shape flowering phenology in tropical forests. Finally, I propose comparative
approaches to examine some possible causes for different
phenological behavior.
Description of phenology patterns
Classification of flowering phenology in tropical forests
has been attempted by different authors in different ways
(Gentry 1974; Frankie et al. 1974; Opler et al. 1980; Bawa
1983; Augspurger 1983). For example, categories used by
Opler et al. (1980) were based on duration and synchrony.
They categorized flowering behaviors of treelets and shrubs
into “continuous, “ “extended,” and “brief, “ and further
divided the latter two into “synchronous” and “asynchronous. “ Gentry (1974) classified the flowering phenology of
the Bignoniaceae into four flowering types: “steady state,”
“cornucopia,” “big bang,” and “multiple bang,” based on
duration, frequency, and amplitude, and discussed the ecological significance of the differences in phenology among
species in relation to pollination systems. These classifications, however, were not used by other authors for comparison with data from other forests, perhaps because
definitions of the terms were unclear or not sufficiently
quantitative. Furthermore, such classification covered only
a subset of the diverse patterns found in the field and therefore was not general.
Newstrom et al. (1994a,b) were the first to provide a
systematic framework for the classification of tropical flowering phenology. Because many terms had multiple connotations and a number of terms were used to indicate the
same phenomenon, they selected and explicitly redefined
terms for phenology patterns. For example, the word “seasonal” means the temporal association of an event with a
recognizable climatic season, according to Newstrom et al.
(1994b). Thus, changes in flowering species, or the proportions of flowering individuals during a year, cannot be called
seasonal, when association between the phenological event
and a particular climatic interval is not clear. Newstrom et
al. (1994a,b) suggested that phenological patterns could be
described with several indices, including frequency, duration, amplitude, synchrony, and regularity. When the event
is seasonal, the date of the event can be added. In contrast
with temperate forests, where most plants reproduce once a
year with high synchronization within and among individuals, these characters assume most importance in tropical
forests. Among these characters, Newstrom et al. adopted
frequency as a criterion with priority, and classified plants in
La Selva, a wet lowland tropical forests in Costa Rica.
The other argument by Newstrom et al. (1994a,b) is that
we must be conscious of hierarchical aspects of phenophases in tropical forests. A similar analysis has not been an
issue in temperate forests, where flowering is usually synchronized within a population, and the pattern is annual at
every level except for a small number of species with a
strong masting phenomenon. In the case of flowering
phenology, the lowest level of analysis can be an individual
flower on an inflorescence. The phenology of individual
flowers is summed to form patterns at higher hierarchical
levels. Such levels include the inflorescence, the branch, the
whole plant, the population, the guild, and the whole community. For example, flowering of Boesenbergia grandifolia
(Zingiberaceae) in Borneo showed irregular subannual
or annual flowering patterns at the individual level but
continuous flowering at the population level (Sakai 2000a).
For studies on selective forces for phenology, analyses at
the individual level are essential (Janzen 1978; Herrera
1998).
Annual cycles at the community level
in the Neotropics
One prominent theme in tropical community studies is the
periodicity or regularity of biological activities. In the temperate region, clear annual cycles in plant phenology predominate. Presumably, regular rhythms in temperature and
daylength and the existence of winter, which limits all biological activities, impose such patterns. In the tropics, seasonal fluctuation in mean temperature is often less than the
fluctuation within a single day, and changes in photoperiod
are very small.
In contrast to temperate forests, periodic change in rainfall caused by movements of the intertropical convergence
zone often plays an important role as proximate and ulti-
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mate factors for tropical plant phenology (van Schaik et al.
1993). Dry seasons within an annual cycle occur in most
tropical regions, and many studies have shown a correlation
between tropical plant phenology and rainfall (Augspurger
1981; Borchert 1983; Reich and Borchert 1984) demonstrating existence of annual patterns of plant reproduction even
in the tropics. Most neotropical forest communities studied
show flowering and fruiting peaks near the end of the dry
season (Janzen 1967; Croat 1975; Foster 1982; Frankie et al.
1974; Hilty 1980; Opler et al. 1980; Bullock and SolisMagallanes 1990; Justiniano and Fredericksen 2000). The
pattern may be caused by high insolation and photosynthesis in dry seasons or by enhancement of germination and
seedling survival by adjusting fruiting to precede the beginning of the wet season (van Schaik et al. 1993).
Examination at the species and population levels can
reveal wide variation in flowering phenology in a single
forest. In spite of the annual rhythm observed at the community level, only 29% of 254 trees showed an annual flowering pattern at La Selva in Costa Rica (Fig. 1) (Newstrom
et al. 1994b). The predominant flowering type was the
subannual pattern (flowering more than once a year, often
irregularly), accounting for 55% of the trees. This forest is
rather wet without a severe dry season, and monthly precipitation never drops to less than 100 mm (Sanford et al.
1994). Although comparative data are not available from
other neotropical forests, a higher proportion of annual
flowering species may occur in forests with stronger seasonality. Wright and Calderon (1995) analyzed flowering phenology of 217 species with 230 seed traps for 5 years on
Barro Colorado Island (BCI) in Panama. They found that
mean flowering dates of species were distributed throughout the year, and that concentration of flowering times (the
length of the mean vector in circular analysis [Batschelet
1981]) spanned the entire possible range.
Although many studies have suggested a correlation between rainfall and flowering or leaf flushing, external cues
have been experimentally demonstrated in only some plant
species. In some species, water conditions in the soil were
shown to play an important role by irrigation experiments
(Augspurger 1981; Reich and Borchert 1982; Wright and
Cornejo 1990a,b; Wright 1991; Tissue and Wright 1995).
However, a large-scale irrigation experiment (2.25 ha) in
BCI with a strong seasonal pattern in rainfall showed that
irrigation had no effect on the timing of leaf fall, leaf flush,
flowering, or fruiting for most species of canopy trees
(Wright and Cornejo 1990a,b). Deep-rooting canopy trees
possibly do not experience a water deficit, even in dry seasons (Steinberg et al. 1989). The mechanisms for synchronized flowering are still unknown for most species.
Little is known about long-term changes in plant behavior in seasonal tropical forests. Year-to-year fluctuations in
fruit production have been studied most intensively in
masting trees in temperate forests (reviewed by Kelly 1994;
Herrera 1998; Herrera et al. 1998). For this phenomenon,
predator satiation, i.e., starving the predators in low seed
years or swamping seed predators in high years (Janzen
1971), is one of the plausible explanations. In tropical
forests, long-term fluctuation in fruit production was best
Fig. 1. The proportion of subannual, annual, supraannual, and continual flowering types among trees at La Selva, Costa Rica (top) (254
trees; data from Newstrom et al. 1994b) and Lambir, Malaysia (bottom)
(187 tree species, data from Sakai et al. 1999) (modified from Sakai
2000b). In the graph, the general flowering type of Lambir is included
in supraannual type. Note that the graph of La Selva is on an individual
basis while that of Lambir is on a species basis. However, it may be
valid to compare flowering types between plants at La Selva and at
Lambir, because Newstrom et al. (1994b) stated the patterns found on
an individual basis are similar to that on a species basis
studied in BCI. According to 9.5-year seed trap data, yearto-year fluctuation of monthly total fruit production on
BCI was rather small (CV , 1; Wright et al. 1999) compared with the criteria of masting (CV . 1.5) proposed by
Silvertown (1980). Nevertheless, Wright et al. (1999) reported that extremely low fruit production at more than
10-year intervals brought about famines and regulated
mammal population density. They argued that El Niño
caused higher fruit production, which resulted in reduction
of stored energy of plants for reproduction. In the following
year, on the other hand, fewer stored reserves and the
cloudy dry seasons associated with La Niña depress reproduction and cause famine and abrupt reduction of
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fruigivore population densities. Such famine was observed
four times during 49 years.
Dominance of supraannual pattern in
a dipterocarp forest
In contrast with most neotropical forests, a large portion of
Asian tropical forests from Sumatra to the Philippines do
not have a clear annual cycle even in rainfall, partly because
both the northeast monsoon in summer and the southwest
monsoon in winter bring predominantly warm, humid air
masses and precipitation to this region (McGregor and
Nieuwolt 1998). In this equatorial monsoon region, precipitation patterns are dominated by intraseasonal fluctuation
with 30- to 60-day cycles (known as the 40- to 50-day tropical oscillation) and interannual fluctuation caused by the El
Niño Southern Oscillation and Quasi-Biannual Oscillation
(Yasunari 1995; McGregor and Nieuwolt 1998). Therefore,
fluctuation in rainfall is quite unpredictable. Periods of water deficit, which are often not evident from long-term average values, do occur but their frequency, duration, timing,
and severity vary from year to year (Whitmore 1984).
Interestingly, the phenomenon with multiyear intervals,
called general flowering (GF, or mass flowering), is known
from lowland dipterocarp forests in this region (Ashton et
al. 1988). The forests are characterized by dominance of the
plant family Dipterocarpaceae in the canopy and emergent
tree layers and high tree diversity (Whitmore 1984). GF
usually occurs every 2 to 10 years. During GF, many plant
species including most dipterocarp species and species of
other families flower sequentially for several months, but a
few flowers can be seen in non-GF periods (Sakai et al.
1999; Sakai 2000b). In other words, the forest has
supraannual seasonality at the community level. GF has
great effects not only on animals in the forests but also on
the local economy through production of illipe nuts (fruits
of Shorea, section Pachycarpae), an important commercial
item for export (Blicher 1994), and through increase of
edible fruits in the forests or on local farms. In spite of
the importance and uniqueness of this phenomenon, our
knowledge about GF is limited, although the phenomenon
has been known for a long time (Ridley 1901; Wood 1956;
Medway 1972; Janzen 1974; Cockburn 1975; Appanah 1985,
1993; Ashton et al. 1988; Ashton 1989; Corlett 1990).
Detailed long-term studies on GF, however, have recently come from Sarawak and West Kalimantan. The
Canopy Biology Program in Sarawak (CBPS; Inoue and
Hamid 1994, 1997) monitored about 300 plant species at
Lambir Hills National Park, Sarawak, and focused on pollination biology during three general flowering events in the
1990s (Momose et al. 1998b; Sakai et al. 1999; Kato et al.
2000). Curran and her collaborators monitored 54 species of
Dipterocarpaceae for more than 10 years, focusing on
seed survivorship and seedling recruitment during GF at
Gunung Palung National Park in West Kalimantan (Curran
et al. 1999; Curran and Leighton 2000; Curran and Webb
2000).
CBPS has monitored the phenological behavior of about
500 plants of various taxa and habits since 1992 using a
canopy observation system with tree towers and aerial
walkways constructed in an 8-ha permanent plot (Inoue
et al. 1995; Yumoto et al. 1996). When the censuses were
initiated, the forest was at the peak of fruit dispersal following GF in 1992. From 1993 to 1995, the proportion of flowering plants was very low, around 3%. However, in May
1996, the proportion increased dramatically to reach 17%
and 20% for individuals and species, respectively, and GF
was observed (Sakai et al. 1999).
The concentration of reproduction in GF is clear from
analyses at species and individual tree levels. Of 527 flowering events observed during 43 months from July 1993 to
December 1996, 57% occurred in 10 months of GF from
March to December 1996. Among species that flowered at
least once in the 43 months, 85% reproduced during the GF
period. Most species showed strict synchronization within
species, and major flowering periods of species were usually
less than 1 month.
Participation in GF was observed among various plant
groups, which confirmed that GF was a phenomenon operating at the community level. Sakai et al. (1999) classified
species into flowering types using flowering data of individual plants for the 43 months. The first is a GF type, which
flowers only in the GF period. Three additional categories
were based on flowering frequency: supraannual (flowered
once or twice in 43 months), annual (flowered three or
four times), and subannual types (flowered more than four
times). Species in which reproduction was not observed
during the 43 months were tentatively categorized as nonflowering. According to these criteria, 35% of 257 species
were of the GF type. Species of this GF type were found in
plants of different families and life forms, from epiphytic
orchids to emergent dipterocarp trees. Additionally, concentration of reproduction during a GF period was found
not only in plants of the GF type but also among annual and
supraannual plants (Sakai et al. 1999). Supraannual and
annual species also reproduced more actively during a GF
period than during non-GF years.
Responses of animal consumers of fruits and floral
resources to GF are most dramatic. Curran and Leighton
(2000) reported a drastic increase in encounter rate for
nomadic vertebrates such as bearded pigs (Sus barbatus)
and parakeets (Psittacula longicauda) following the fruiting
peak in two GF events, whereas they destroyed only small
portions of dispersed fruits because of high synchronization
within and among dipterocarp species. For bearded pigs,
GF may be essential for reproduction (Curran and Leighton
2000). On the other hand, giant honeybees (Apis dorsata)
are known to immigrate into dipterocarp forests in GF. In 8ha plot in Lambir, nests of giant honeybees were found only
during or just after GF (Nagamitsu 1998). The numbers of
giant honeybees caught by monthly light traps per night
were 0 during non-GF while the numbers can be nearly 200
in GF (T. Itioka, unpublished data). Stingless bees were
resident at Lambir, but establishment of new nests at
standard, artificial nesting sites were observed only in GF
(Nagamitsu 1998).
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It is obvious that some external factors trigger GF because GF occur irregularly. One possible candidate of the
cue may be the severe drought sometimes associated with
El Niño events. Correlation between drought and GF has
been reported from various locations (Wood 1956; Burgess
1972; Medway 1972; Janzen 1974; Whitmore 1984; Appanah
1985; van Schaik 1986; Kiyono and Hastaniah 1999). Correlations between El Niño and GF were reported from eastern Peninsular Malaysia (Ashton et al. 1988) and West
Kalimantan (Curran et al. 1999; Curran and Leighton 2000).
However, initiation of GF sometimes precedes drought,
and years of GF do not always coincide among geographic
regions (Ashton et al. 1988; Corlett and LaFrankie 1998;
Yasuda et al. 1999). On the other hand, Ashton et al. (1988)
analyzed 11-year climate data and occurrences of GF based
on illipe nut export records. They concluded that a drop of
daily minimum temperature was most likely to be the cue
for GF. Drops of temperature just before GF were observed
in different places (Ashton et al. 1988; Sakai et al. 1999;
Yasuda et al. 1998), but some GF events occurred without a
preceding temperature drop (Corlett and LaFrankie 1998).
More than one climatic signal may be a potential trigger for
GF. For further examination of the hypotheses, experimental approaches are essential because various climatic variables covary.
Evolutionary factors involved in GF are controversial.
Sakai et al. (1999) suggested three possible explanations:
predator satiation, promotion of animal pollination, and
paucity of climatic cues suitable for triggering flowering.
Predator satiation implies that long intervals between GF
limited the predator populations so that dipterocarp seeds
can escape from predation (Janzen 1974). Curran and
Leighton (2000) showed that seed predators destroyed most
dipterocarp fruits in a minor GF year whereas most of
the fruits survived in major GF years, thus supporting the
idea. Although the hypothesis has generally been accepted
(Ashton et al. 1988), Sakai et al. (1999) suggested that it
does not explain participation of plants rarely attacked by
vertebrate predators.
Promotion of pollination is one other possible factor for
GF, because observed fruit set was higher in GF than in
other years (Yap and Chan 1990; Sakai et al. 1999). Insect
populations and activities increase during GF (Nagamitsu
1998; Kato et al. 2000; T. Itioka, unpublished data), and thus
scarce pollinators may become more abundant. The last
explanation, paucity of climatic cues, explains synchronization among various species by adoption of the same flowering trigger due to paucity of potential climatic variables as
the flowering trigger under unpredictable and uniform
climatic condition. Even in tropical forests, where most
plant species show low population densities, outcrossing
is dominated in most plant species, as revealed by studies
using genetic markers (Gan et al. 1977; Hamrick and
Murawski 1994). For outcrossing, flowering synchronization with conspecifics is essential. Under aseasonal conditions, many unrelated plants may use the same, and most
clear, environmental signal as a flowering trigger. All the
hypotheses, which are not mutually exclusive, should be
explored.
What determines flowering phenology?
Timing
It is well accepted that reproductive phenology affects plant
fitness through reproductive processes such as pollination,
seed development, dispersal, and germination and seedling
survival (Table 1). Thus, flowering phenology is subject to
selection caused by seasonally variable biotic and abiotic
factors. Abiotic factors are mostly represented by various
climatic conditions, whereas biotic factors include pests,
herbivores, pollinators, and other plants that share pollinators, along with predators and dispersers of seeds and fruits.
Many studies conducted so far emphasize the adaptive
importance of flowering at a particular time (Table 1)
(reviewed in Rathcke and Lacey 1985; van Schaik et al.
1993).
For tropical forest plants, shared pollinators have received particular attention. The hypothesis suggests that
plant species sharing common pollinators segregate flowering temporally to minimize interspecific overlap in flowering times and thus ineffective pollination or competition for
pollinators (Stiles 1977; Appanah 1985; Ashton et al. 1988).
However, this hypothesis is rarely supported by experimental or field studies (Wheelwright 1985; Murray et al. 1987;
Wright and Calderon 1995). Most statistical tests of temporal flowering segregation have shown flowering to be aggregated (Poole and Rathcke 1979) or indistinguishable from a
random pattern (Wheelwright 1985). Different statistical
tests can give different results (Rathcke 1983). Null hypotheses for the tests still need further consideration, partly
because flowering phenology is thought to be under strong
phylogenetic constraints (see “Phylogenetic constraints”
section). Other studies suggested that synchronized flowering of different species could facilitate pollination through
increase of resource density and local pollinator attraction
(Schemske 1981; Sakai et al. 1999). Flowering may, however, be completely out of phase with pollinator abundance
(Zimmerman et al. 1989).
Variation in flowering patterns
Compared with timing of flowering, fewer studies have
focused on variation in flowering patterns such as duration,
frequency, and flowering intervals, which is in contrast to
recent progress in understanding of variation in leaf phenology with cost–benefit analyses (Kikuzawa 1991; Reich 1994;
Reich et al. 1991, 1992; Mulkey et al. 1995; Kitajima et al.
1997a,b).
Flowering duration of individual plants has often been
discussed as affecting pollination success of the plant
through regulation of pollen flow and foraging behavior of
pollinators (see Table 1) (Bawa 1983). Regulation of pollen
flow includes avoidance of self-pollination by reducing
flower number per day and promotes pollinator movement
among plants. Different pollinators with different foraging
behaviors favor different flowering patterns. For example,
plants pollinated by nonterritorial hummingbirds, which
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Table 1. Important hypotheses to explain different reproductive phenology in tropical forests
Phenological trait hypothesis
Importance
Literature for tropical phenology
Timing
Abiotic factors (climatic condition)
Radiation (resource limitation)
Water limitation
Wind seed dispersal
Some
Some
Some
van Schaik 1986; van Schaik et al. 1993
Reich and Borchert 1984; van Schaik et al. 1993
Frankie et al. 1974; Foster 1982; Gautier-Hion et al.
1985a
Frankie et al. 1974; Janzen 1967; Garwood 1983
Sakai et al. 1999
Germination and seedling survival
Availability of flowering cue
Biotic factors
Interaction with animals
Availability of animal pollinators
Availability of animal seed dispersers
Synchrony among plant species
Promotion of animal pollination
Promotion of animal seed dispersal
Predator satiation
Asychrony among plant species
Competition for pollinators
Competition for fruit dispersers
Interspecific pollen transfer
Relationship with other phenophases (e.g., leaf flushing)
Duration
Pollination
Predation
Resource availability
Frequency
Pollination
a
Some
Unknown
Some
Desgranges 1978; Feinsinger 1970; Zimmerman et al.
1989a
Baird 1980; Leigh et al. 1993; Levy 1988
Some
Rare?
Rare
Rare?
Schemske 1981; Koptur et al. 1988; Sakai et al. 1999
Wheelright and Orians 1982
Janzen 1974; Ashton et al. 1988; Curran and Leighton
2000
Rare?
Appanah 1985; Ashton et al. 1988; Stiles 1975;
Wheelwright 1985; Ratchke and Lacey 1985a; Ollerton
and Lack 1992a; Sakai 2000aa
Smyth 1970; Snow 1971; Gleeson 1981*; Rathcke and
Lacey 1985a
Rare
Unknown
Important
Borchert 1983; van Schaik et al. 1993
Probably important
Some
Unknown
Gentry 1974; Augspurger 1981; Bawa 1983
Augspurger 1981; Ims 1995
Bawa 1983
Probably important
Gentry 1974; Momose et al. 1998a
Reports with negative results or suggestions
regularly visit flowers of low-density plant species, continue
to open small numbers of flowers a day for a long time
(Stiles 1975). On the other hand, large display by strict
synchronization within and among individuals was important for attraction of bee pollinators in a tropical shrub
(Augspurger 1980). In addition to the pollinator aspects,
escaping from predators (Augspurger 1981) and spreading
the risk of uncertain pollination (Rathcke and Lacey 1985)
may also be important, but these aspects have rarely been
examined.
A few studies have examined differences in flowering
frequency among plants with different ecological characters
(Gentry 1974; Momose 1998a). For example, Momose et al.
(1998a) addressed theoretical differences in flowering intervals among the plants belonging to different forest strata
observed in a dipterocarp forest. The model assumes that
the flowering intervals of mature trees maximize visits by
pollinators, including opportunistic insects and social bees,
throughout their lifetimes after they reach their maximum
size. According to the model, trees in the highest canopy
layers reproduce at long intervals. It is their optimal strategy to delay flowering to make huge displays to attract
many opportunistic pollinators because they have low
mortality and high productivity. In contrast, the canopy or
subcanopy trees cannot wait so long between reproductive
episodes because of higher mortality. For these trees, it is
optimal to frequently produce smaller displays to attract
social bees, which recruit colony members when a display
exceeds a threshold size. The higher proportion of social
bee-pollinated plants in canopy and subcanopy trees than in
emergent trees also supports this idea. Like Gentry (1974),
Momose et al. (1998a) suggested pollinator behavior was an
important selective force for flowering phenology.
Phylogenetic constraints
Studies from tropical forests and other regions also show
that flowering phenology is a conservative trait within evolutionary lineages (Kochmer and Handel 1986; Johnson
1992; Ollerton and Lack 1992; Wright and Calderon 1995).
Kochmer and Handel (1986) observed that most of the
variation in the flowering times of the animal-pollinated
angiosperms of Japan (1575 species) and of North and
South Carolina (USA) (2298 species) was explained by
family membership. In addition, most families showed similar flowering times in Japan and Carolina. Wright and
Calderon (1995) examined quantitative (217 species) and
qualitative (1173 species) flowering data of plants on BCI,
and found that both the mean and the variance of flowering
times were similar among congeners and, although less significant, also present among confamilials. For most genera
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examined, the shared-pollinator hypothesis was rejected.
Although strong phylogenetic constraints detected by the
studies do not necessarily indicate absence of adaptation in
phenology, the diversity of tropical flowering phenologies
should be guided by phylogenetic perspectives. This means,
for example, that in the case of GF we may need to direct
attention to synchronization of flowering among species of
different families rather than within a family or Dipterocarpaceae, or we should study dipterocarps that do not share
GF phenology patterns.
Comparison of phenology
The first step in studying diversity of flowering patterns, to
which less attention has been paid, is the description of
phenology patterns. Descriptions enable us to compare
phenology among plants with different traits and thus to
examine factors that may affect flowering phenology. Comparison of phenology is sometimes very useful, because the
possibility of manipulating phenology and making experiments is limited in phenological studies. In addition, all
we can measure directly or manipulate are the relationships between phenology and proximate factors, largely
constrained by phylogenetic blueprints.
Comparison among species
Comparison among species within a community with different characteristics may help us to understand the effects of
these characteristics on flowering phenology. One does not
have to consider effects of climate, because all plants in the
community are basically under the same climatic condition.
One possible way to compare phenology patterns among
species is classification of phenology as proposed by
Newstrom et al. (1994a,b), which is primarily based on flowering frequency (see the section “Description of phenology
patterns”). With this classification, Newstrom et al. (1994b)
found a significant difference in flowering frequency between canopy and subcanopy trees and suggested that the
difference was caused by pollinator stratification (Bawa et
al. 1985). On the other hand, Momose et al. (1998a) examined the flowering frequency of trees of different height at
Lambir and suggested that these trees maximized pollinator
visits in their lifetime.
In the classification of Newstrom et al. (1994a,b), seasonality and periodicity, characteristics related to timing, are
not considered. One should bear in mind that flowering or
any events may not always occur annually or periodically,
as represented by the GF plants in dipterocarp forests.
Although circular analysis is often used to see synchrony,
periodicity, and seasonality (Zar 1996), it may not be appropriate when intervals of the focal events have irregular intervals or cycles other than 1 year. When periodicity is not
the issue, other analyses without assuming periodicity may
be better to test synchrony (Primack 1980; Augspurger
1983; Sakai et al. 1999; Sakai 2000a).
Comparison among communities
Comparison of reproductive phenology among communities is of interest for at least two reasons. Comparison
among communities under different climates is useful to
consider effects of climate. Van Schaik et al. (1993) compared timing of phenological activities at different tropical
forests of the world, based on 53 studies, and concluded that
peaks in irradiance were accompanied by peaks in flushing
and flowering unless water stress made this impossible.
Next, effects of plant reproductive phenology on animals
depending on flowers and fruits can be exmianed by comparison among forests. Janzen (1974) considered that
Malaysian dipterocarp forests maintained smaller mammal
populations than in the Neotropics, because dipterocarp
forests provided only a little food for mammals during nonGF periods (but see Sakai 2000b).
Comparisons of phenologies among different forests,
however, have rarely been attempted, partly because biologists monitor and describe plant activities with different
methods so that direct comparison is essentially impossible.
Studies with different goals adopt different methods of observation and analysis, providing different results with varying accuracy (Chapman et al. 1992, 1994; Zhang and Wang
1995).
For comparison among communities, again, classification based on flowering frequencies may be useful. This
approach clearly showed differences in phenology patterns
between La Selva and Lambir (see Fig. 1). There are advantages to using frequencies to compare phenology data from
different studies. First, flowering frequency can be calculated from most phenology data so long as the data distinguish individual plants. Second, frequency is robust against
variation of the census frequency. When flowering period is
very short compared with census frequency, reproduction
can be counted if parts of flower buds, flowers, or inflorescences after flowering are recognized by the observer. Finally, frequency is less affected by differences in threshold
levels. If the threshold level to recognize activities is different between two observers, the length of the event recorded
by the two may be different (Fig. 2). On the other hand, the
number of the event is one for both observers.
Monitoring of phenology with seed traps may be most
appropriate for direct comparison between sites. The
method is thought to be more objective, because with this
method one does not have to choose species and individuals
for observation. The data are usually quantitative, although
placement and the number of traps are issues in obtaining
data of high confidence. For example, whether dipterocarp
forests with GF, in which most large trees reproduce infrequently, produce fewer fruits than other forests dominated
by subannual and annual flowering species is an important
question to be answered by seed trap studies (Sakai 2000b).
Because this method does not distinguish individual
plants, it can be combined with direct observation of tagged
plants.
Seed traps provide useful data especially for seed dispersal and monitoring of floral and fruit resources. In spite
of relatively mild environments, contrary to earlier expecta-
84
References
Fig. 2. Diagram showing temporal change in multitude of phenological
events and duration of the event recorded by observers with different
methods. The threshold of observer B is higher than that of A; thus,
duration of the event recorded by B is shorter than A. The number of
the event, however, is one for both observers, unless the event is
strongly bimodal
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tropical forests is rather high (van Schaik et al. 1993). There
is no doubt that consumers are strongly affected by fluctuation of resource availability, but the frequency, severity, and
consequences of such fluctuations are just beginning to be
explored.
Concluding remarks
In this review, I have outlined diversity of flowering phenology in the tropics and pointed out that the plants often
flower without regularity and synchrony, in contrast to temperate forests. Examination of periodicity and seasonality,
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Corlett and LaFrankie 1998). Comparison of phenology
within and among forests may help our understanding of
phenological diversity and relevant changes in global patterns and processes. Attempts to develop a common language to communicate concepts and render interpretations
of data more compatible among investigators (Newstrom et
al. 1994b) and to create a network to promote comparative
studies may helpus to accomplish this goal.
Acknowledgments The author thanks W. Roubik and two anonymous
reviewers for constructive comments on the manuscript. This study was
partly supported by a Grant-in-Aid of the Japanese Ministry of Education, Science and Culture (09NP1501) and JSPS Research Fellowships
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