General flowering in lowland mixed dipterocarp forests of South-east Asia

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1 Biological Journal of the Linnean Society, 2002, 75, With 5 figures General flowering in lowland mixed dipterocarp forests of South-east Asia SHOKO SAKAI* Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Ancón, Republic of Panama Received 27 November 2000; accepted for publication 4 October 2001 The general flowering (GF) events of forests in south-east Asia are perhaps the most spectacular phenomena in tropical biology. GF events occur at multiyear intervals. In GF, most dipterocarp species and many plants of other families come into flower and set fruit massively; these species and plants rarely flower except during GF events. GF is unique, because it can occur over thousands of kilometers and involve hundreds of plant species representing diverse families and lifeforms. It also involves strict mast fruiting. Satiation of generalist seed predators has been considered a primary force for GF. However, recent observations indicate that several selective agents rather than a single major factor may shape GF. In addition to the satiation of generalist predators, promotion of pollination could be one of the selective factors for GF, since synchronized flowering of many species causes an increase in pollinator activity through immigration and population growth. Although environmental prediction for better establishment of seedlings may also be involved in GF, no field data have been reported to support this idea. Longterm monitoring and further understanding of GF are essential for the conservation of this unique and diverse tropical forest in south-east Asia, especially in a period of global climatic change The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, ADDITIONAL KEYWORDS: Dipterocarpaceae environmental prediction masting plant reproductive phenology predator satiation promotion of pollination tropical forest. INTRODUCTION Reproductive synchrony among individuals in a population is a widespread phenomenon both in plants and in animals (Ims, 1990a). In seasonal environments, synchronization of reproduction among individuals occurs, in part, because a particular season is most favourable for reproduction and the survival of offspring. However, the extent of synchronization is usually much stronger than would be expected from the variability of climatic conditions. Extreme cases are provided by synchronized reproduction at long intervals in bamboos (Janzen, 1976) and cicadas (Lloyd & Dybas, 1966). Many plants in tropical forests experiencing less seasonal climatic changes also show high synchronization within populations (e.g. Primack, 1980; Augspurger, 1981). Many biologists *Current address: Graduate School of Human and Environmental Studies, Kyoto University, Sakyo, Kyoto, Japan sakai@bio.h.kyoto-u.ac.jp have investigated these phenomena to identify the primary causes of synchronization. In the case of plants, many studies have focused on high year-to-year variation in seed production, known as masting or mast seeding (Kelly, 1994). High annual variability of crops synchronized among individuals of single or closely related species has been reported for some plant species, especially in windpollinated trees in temperate forests. Recently, the hypothesis and concepts of masting have been critically reviewed (Kelly, 1994; Herrera et al., 1998; Herrera, 1998) and evaluated, both theoretically (Smith et al., 1990; Ims, 1990b) and by field observations (Norton & Kelly, 1988; Sork et al., 1993; Kelly & Sullivan, 1997; Shibata et al., 1998). Kelly (1994) suggested that economy of scale (i.e. larger reproductive efforts are more efficient) through promotion of wind pollination (Smith et al., 1990) and seed predator satiation (Janzen, 1971; Silvertown, 1980) was the most plausible primary selective force for plants to produce sporadic large crops rather than constant small ones. 233

2 234 S. SAKAI Figure 1. Changes in the percentage of flowering and fruiting species and individuals (237 species, 428 individuals) (Sakai et al., 1999b; Sakai et al. unpub. data). Lower seed-predation rates in masting years have been reported in trees such as Fagaceae (Sork, 1993; Crawley & Long, 1995) and Beturaceae (Shibata et al., 1998), and in grasses (Poaceae) (Kelly & Sullivan, 1997). There are also studies showing higher pollination success in masting years, which support the wind-pollination efficiency hypothesis from temperate forests (Nilssen & Wästljung, 1987; Allison, 1990; Shibata et al., 1998). The effects of possible factors differ among species and sites, and it is usually difficult to separate multiple factors and to evaluate their relative importance. General flowering (GF) or mass flowering in dipterocarp forests is perhaps the most spectacular phenomenon in tropical ecology (Ashton et al., 1988; Sakai et al., 1999b). It is observed in aseasonal, lowland tropical forests dominated by various dipterocarp species in south-east Asia. During GF, which occurs at irregular intervals of several years, nearly all dipterocarp species, together with species of other families, come heavily into flower, while only a few plants flower during intervening periods (Fig. 1). In contrast with masting in temperate forests, only limited information was available, until recently, for this type of forest (reviewed by Ashton et al., 1988; Appanah, 1993). Results of detailed long-term studies on GF at the community level have recently become available from Sarawak, and from West Kalimantan, in Borneo. The Canopy Biology Program in Sarawak (Inoue & Hamid, 1994, 1997) monitored ~300 plant species at Lambir, Sarawak, and focused on pollination biology in the 1990s (Momose et al., 1998; Sakai et al., 1999b). L. M. Curran and her collaborators monitored 54 species of Dipterocarpaceae for more than 10 years and focused on seed survivorship and seedling recruitment during GF in West Kalimantan (Curran et al., 1999; Curran & Leighton, 2000; Curran & Webb, 2000). These studies make this an appropriate time to review the causes and consequences of the GF phenomenon. GENERAL FLOWERING General flowering is a phenomenon unique to lowland dipterocarp forests. These forests are characterized by a high species diversity of trees. In particular, the lowland mixed-dipterocarp forests in Borneo are thought to be among the forests highest in tree species diversity in the world (Whitmore, 1984). Up to 10% of the species, and 80% of the emergent trees, are accounted for by various species of Dipterocarpaceae, which can reach 70m in height (Ashton, 1982). Several

3 GENERAL FLOWERING IN DIPTEROCARP FORESTS 235 Figure 2. Quantities of llipe nuts exports from Sarawak and Kalimantan. From data in Blicher (1994). dipterocarp species and genera usually grow together, so that a single species does not dominate. Seed production at multiyear intervals, synchronized among most dipterocarp species in the forests, has been recognized 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). It is well known by local people that a GF episode is reliably followed by abundant fruiting several months later. The longest record of dipterocarp seed production comes from the export statistics of illipe nuts (fruits of Shorea section Pachycarpae), an important commercial item of this region. The export quantity from Sarawak and Kalimantan fluctuates considerably, and mast years occur irregularly at 2 6 years intervals (Fig. 2). The area that a GF event covers can be as small as a single river valley, or as large as north-eastern Borneo or peninsular Malaysia (Ashton et al., 1988). The intensity of the event can differ depending on local topography (Yasuda et al., 1999). The annual coefficient of variation (CV) in dipterocarp fruit production in a particular area was calculated to be 2.2 based on data for a 14-year period from Kalimantan (Curran et al., 1999), which is one of the highest values shown by polycarpic woody plants (Herrera et al., 1998). Mast years can be clearly distinguished from normal years (Ashton et al., 1988), although flowering in nonmast years is sometimes observed (Yap & Chan, 1990). The clearest difference of GF from other masting phenomena is that not only dipterocarp trees but also many other plant species show flowering synchronized with dipterocarp trees (Medway, 1972; Appanah, 1985; Corlett, 1990; Sakai et al., 1999b). At Lambir in Sarawak, one third of 258 species of various families under observation reproduced only in a GF period. Those plants included epiphytic orchids and subcanopy trees such as Euphorbiaceae and Moraceae, in addition to emergent dipterocarp trees (Fig. 3). Moreover, annually flowering species flowered more intensively in a GF year (Sakai et al., 1999b). Supra-annual seasonality at the community level involving diverse plant species still has not been reported from other tropical forests. ASEASONAL CLIMATE AND FLOWERING TRIGGER The aseasonal climate of the region might play some role in the supra-annual seasonality of the forests with GF. Dipterocarp trees in relatively seasonal climatic conditions, with regular dry seasons, in Thailand, Sri Lanka and South India show annual or more frequent reproduction, though flowering intensity varies greatly among years and species (Holmes, 1942; Koelmeyer, 1959; Ashton, 1989; Dayanandan et al., 1990). In the equatorial region of the Asian tropics, annual dry seasons are not clear partly because both the summer and winter monsoons bring warm and humid air masses. The mixture of land and sea surfaces of the region, high sea-surface temperature in the oceans, and the predominant, dense rainforests on the islands also contribute to the high humidity. Periods of water deficit do occur, but they are often not evident from long-term average values due to their irregularity (Whitmore, 1984). Synchronization within a species is quite important to assure cross-pollination, particularly for outcrossing species with low population densities. The flowering trigger should be distinctive and reliable to ensure that individuals in various microhabitats sense it equally and exactly at the same time, and the switch is turned on at appropriate intervals. In the aseasonal tropical region, possible climatic cues may be limited and different plant species may adopt the same environmental variable as a flowering trigger. On the other hand, the existence of distinctive climatic cues with one year or shorter cycles may account for the domi-

4 236 S. SAKAI Figure 3. The proportions of the four flowering types (subannual, annual, supra-annual, and general flowering) and nonflowering species among all species observed at Lambir, Sarwak, taxonomic groups, pollination systems, and fruit types. Beetle pollination is divided into two subgroups, Dipterocarpaceae and plants of the other families. Numbers of species included are shown in parentheses (redrawn from Sakai et al., 1999b). nance of the annual or subannual pattern in other tropical regions. Several hypotheses have been proposed regarding the environmental trigger of GF. Association between GF and severe drought has often been reported from different forests (Wood, 1956; Burgess, 1972; Medway, 1972; Janzen, 1974; Whitmore, 1984; Appanah, 1985; van Schaik, 1986; Kiyono & Hastaniah, 1999). It is a reasonable consideration that reproduction is limited by resources, and that GF plants only reproduce in years in which they accumulate a certain amount of resources through photosynthesis. El Niño usually brings about droughts in the region (Leighton & Wirawan, 1986; Salafsky, 1994; McGregor & Nieuwolt, 1998), and correlation between ENSO and GF have been reported from eastern peninsular Malaysia (Ashton et al., 1988) and western Kalimantan (Curran et al., 1999; Curran & Leighton, 2000). On the other hand, Ashton et al. (1988) argued that drought itself is unlikely to be the trigger of GF for two reasons. Firstly, correlation between flowering intensity and local geography or water availability has not been observed. If water shortage itself was the flowering trigger, flowering should be affected by local topography, soil type, elevation, and so on. Secondly, there is no clear relationship between rainfall patterns and the timing of GF. For example, in eastern peninsular Malaysia and south-western Borneo the driest month is often observed in January, but GF in eastern peninsular Malaysia occurs from February to July while in western Borneo it occurs from August through November. Ng (1977) suggested a longer photoperiod as an alternative trigger that was not affected by soil

5 GENERAL FLOWERING IN DIPTEROCARP FORESTS 237 or topography, but it is not certain that an increase in hours of sunshine caused by less cloudiness can actually provide an effective cue for the synchronized flowering of dipterocarp species, given that the flowering of a single tree lasts only weeks (Ashton et al., 1988). In addition, Sakai et al. (1999b) reported that in 1996, GF in Sarawak was preceded by a decrease in solar radiation due to cloudiness. Wycherley (1973) proposed that some unusual temperature condition was the cue for GF and Ashton et al. (1988) suggested that this unusual temperature condition was actually a drop in the minimum temperature, a conclusion that was based on an analysis of meteorological records for 11 years. Drops in minimum temperature were also observed about one month before the onset of GF at Lambir in 1996 and 1997 (Fig. 4), and at Pasoh Forest Reserve in peninsular Malaysia in 1996 (Yasuda et al., 1999). However, GF was not preceded by a drop of temperature in Singapore in 1987, nor in Danum, Sabah, in 1987, nor in Gunung Palung NP, West Kalimantan, in 1987 or 1991 (Corlett & LaFrankie, 1998). In general, many meteorological factors, such as temperature, rainfall, humidity, and solar radiation, are closely related, and this makes it difficult to identify the exact factor that induces GF. Furthermore, species that respond to different environmental variables may flower at the same time due to a correlation among environmental variables. An experimental approach is needed to evaluate possible triggers. Is it possible to explain GF, that is, the synchronized reproduction of various species at irregular, multiyear intervals, with reference to an aseasonal climate alone? Figure 4 presents a running 30-day total of rainfall and daily minimum temperature between Lambir with GF and La Selva, where annually and subannually flowering species dominate (Newstrom et al., 1994a,b). The annual rhythms of both variables at Lambir are much more obscure than those at La Selva (Fig. 4). However, we must look more carefully into the seasonality of climatic conditions. Attempts have rarely been made to evaluate variation of seasonality among different tropical forests in relation to the phenology, or rhythms, of biological phenomena. It is doubtful that aseasonal climate is the major factor for GF for the following reasons. Phenomena such as GF are not known to occur in montane parts of the region, where the seasonality of the climate may be almost the same as in the lowlands. In addition, the reproduction of birds and population dynamics of insects show clear annual rhythms, even in forests with GF (birds: Fogden, 1972; insects: Kato et al., 1995, 2000). Some evolutionary factors may be involved. ULTIMATE FACTORS OF GENERAL FLOWERING Kelly (1994) evaluated theories for masting, and concluded that five of these theories could logically explain synchronized reproduction among individuals Figure 4. Climate data at Lambir and La Selva. Running 30 day total of rainfall, A: at Lambir; and B: at La Selva from 1985 to Daily minimum temperature, C: at Lambir from 1993 to 1998; and D: at La Selva from 1991 to Based on data from Sakai et al. (1999b), Sakai et al. (unpub. data), and OTS La Selva Biological Station (1999).

6 238 S. SAKAI with high annual variation in crop size. These five theories were as follows: (1) wind pollination; (2) predator satiation; (3) environmental prediction; (4) animal pollination; and (5) animal dispersal. In the case of GF, the wind pollination hypothesis is impossible because most plants in dipterocarp forests are pollinated by animal pollen vectors (Momose et al., 1998). Animal dispersal is also unlikely. Fruits of Dipterocarpaceae, the most important group in GF, are dispersed by wind, gravity and water, and secondary dispersal by animal vectors is rare. Besides, the proportion of the GF plants (plants flowering only in GF period) with animal-dispersed fruits was the smallest of three dispersal types (Fig. 3). In the following sections, I will consider the other three hypotheses. SEED PREDATORS Among the hypotheses to explain masting, predator satiation is most widely known (Janzen, 1971; Kelly, 1994). Kelly (1994) suggested two possible scenarios in which satiation was an effective means to reduce seed predation. The first scenario is that seed predator populations or losses of seeds are limited by the crop size in nonmast years. In this case, which may assume specialists as predators, populations limited by the small crop size of nonmasting years are much smaller than would be maintained by constant seed production. When seed losses by predators are a function of the crop size of the previous year, this may provide good evidence for the hypothesis (Kelly & Sullivan, 1997), although few studies have demonstrated such numerical responses. The occurrence of consecutive mast years, on the other hand, can be evidence against the hypothesis. The other scenario is that predator populations are limited by factors other than crop size, and that seed losses are limited by the number of seeds eaten per predator; this may assume generalists as predators. In this case, consecutive masting years are not against the hypothesis. On the other hand, when generalist predators switch their food depending on availability, synchronized fruiting may not be favoured (Ims, 1990b) and larger seed crops could possibly cause greater seed losses to predators (Kelly, 1994). Janzen (1974) was apparently the first to evaluate the ultimate causes of GF. He suggested that seed predators or herbivores, especially mammals and birds, which have general diets of fruits and seeds, could be the primary selective factor for synchronized flowering and fruiting of a variety of species. Satiation of specialist predators, mainly insects, does not explain GF, because satiation of predators that attack limited plant species does not require synchronized fruiting of unrelated species. Responses of generalist predators to GF have been reported in detail by a 10-year study from Kalimantan (Curran & Leighton, 2000; Curran & Webb, 2000). They showed that in 1986, a minor mast year, most dipterocarp seeds were consumed by resident and nomadic predators. On the other hand, in the GF years 1987 and 1991, resident vertebrates destroyed only 1.5% and 2.6% of the community s seed production. Most seeds also survived destruction by nomadic predators, since these arrived at the forest just before the end of seed dispersal, when most seeds had germinated. The authors suggest that dipterocarp seeds escape from vertebrate predators, rather than swamp them as assumed in the original formulation of the hypothesis, through two mechanisms, namely, interfamilial satiation of resident predators and regional escape from nomadic predators. At their study site, important resident seed predators were squirrels and primates. They preferred nondipterocarp seeds when they were available, and they rarely consumed dipterocarp seeds in major mast years because fruits of other families were also abundant in GF. On the contrary, nomadic predators such as bearded pigs and long-tailed parakeets concentrated their feeding on dipterocarp fruits if available. During GF they traveled for long distances and destroyed considerable quantities of dipterocarp seeds. Local communities escaped this seed destruction owing to the patchy distribution of nomadic predators, rather than to local, short-term satiation of predators. Seeds that escaped predation and vertebrate herbivory on postestablishment seedlings had a high survival ratio, showing that the availability of suitable microsites did not limit recruitment (Curran & Webb, 2000). Although the period when seeds are available is brief compared to the generation time of predators, the seeds consumed during GF are evidently essential for reproduction of some vertebrate predators, as their reproduction was observed only in GF years (Curran & Leighton, 2000). Bearded pigs are known for their large-scale population movement involving up to 300 individuals for hundreds of kilometers (Caldecott et al., 1993). They anticipate seed production and mate well before fruiting, rather than storing fat during GF. Local people predict GF by observing active mating behaviour of bearded pigs before major flowering events (K. Momose, pers. comm.). Curran & Leighton (2000) report high mortality and starvation of adult pigs in intermast years, and suggested that the length of the masting cycle was sufficient to depress their populations. However, there are two observations indicating that satiation of generalist predators alone can not explain GF at the community level. First, plants with different types of fruit and seed are involved in GF. Sakai et al. (1999b) examined the correlation between fruit

7 GENERAL FLOWERING IN DIPTEROCARP FORESTS 239 types and flowering types. The study categorized species into three fruit types based on characteristics of their dispersal unit (fruits when the seeds in the fruit are dispersed together, or seeds, when they are dispersed separately). These categories are as follows: (1) animal-dispersed species, which have rewards for dispersal agents; (2) large fruits, which have no special rewards and are >0.1 g in dry mass; (3) no special rewards and small fruits, <0.1g. A species with a large dispersal unit such as Dipterocarpaceae is likely to be damaged by generalist predators, while species with small dispersal units such as orchids, with tiny seeds, are not. If seed predation is an important factor in the evolution of GF, species with large fruits should be more strongly associated with GF than species with small fruits. Nevertheless, species with small fruits or seeds include as many GF species as species with large fruits (Fig. 3). Corlett (1990) also observed participation of many animal-dispersed species in GF, and pointed out that seed-predator satiation did not explain the synchronized flowering of the animaldispersed plants. In addition, consecutive GF events are observed rather frequently. Two flowering peaks were observed at Lambir in 1996, and GF was observed in three consecutive years from 1996 (Fig. 1). Ashton et al. (1988) reported several consecutive GF years, and two flowering events within a year were observed in peninsular Malaysia (Yap & Chan, 1990). In such cases, vertebrate predator populations might become very high several months or a year after the first fruiting peak, so that predator satiation would not be effective in the second masting. As discussed above, consecutive GF events are inconsistent with the hypothesis, because predator populations are then not limited by a lack of dipterocarp seeds. Janzen (1974) argued that the animal community should be limited by low fruit production in nongf years, and gave circumstantial evidence for a smaller biomass of birds and mammals in dipterocarp forests than in tropical forests in America and Africa. A few available data sets, however, do not support this argument. For example, the primates of Barro Colorado Island (BCI) in the Neotropics and Kuala Lompat in peninsular Malaysia have similar total biomass and similar proportions of fruits in their diets (Table 1). Bird biomass and fruit consumption were also similar between BCI and Semangoh in peninsular Malaysia (Table 2). At BCI, frugivore populations are also limited by the fruit production of the forest. Wright et al. (1999) showed that a late wet season and first month of the dry season, with extremely low fruit production, caused famine and abrupt reduction of frugivore population densities on BCI. Such famines were observed four times during 49 years. Extremely low fruit production at intervals longer than 10 years regulated mammal population density, while annual fluctuation of monthly total fruit production was rather small (CVs < 1, Wright et al., 1999). We need to consider carefully what the most optimal fruiting patterns are in relation to predator satiation, and why dipterocarp forests give up fruiting for years between GF events rather than one famine event in 10 years. Unfortunately, it is getting more difficult to study population densities and population dynamics in lowland dipterocarp forests because of decreases in mammal populations due to hunting, logging, and deforestation (Curran et al., 1999). Although satiation of specialist predators does not explain synchronized reproduction at the community level, it may strengthen synchronization within a Table 1. Primate biomass and consumption in Barro Colorado (Panama) and Kuala Lompat (Malaysia) Barro Colorado Kuala Lompat Number of species 5 5 Biomass (kg km 2 ) Total consumption [kg dry weight (ha year) -1 ] Proportion of diet (%) Flowers and fruits Arthropods 3 6 Leaves Reference Hladik & Hladik (1969) Raemaekers & Chivers (1980) Wright et al. (1994) Leigh (1999) Consumption, F (kg dry weight of food per year), of amimal of average weight (x) is caluculated from the regression F = x (Nagy, 1987).

8 240 S. SAKAI Table 2. Bird populations (numbers and biomass) and dry weight of food eaten by different. Categories of birds in Barro Colorado (Panama) and Semangoh (Malaysia) Barro Colorado Semangoh Bird population, no. (weight, kg) birds/ha Arboreal insectivores 14 (0.21) 10 (0.29) Other insecticores 5 (0.09) 7 (0.30) Omnicores 5 (0.15) 8 (0.23) Frugivores/granivores 2 (0.51) 9 (0.43) Total 26 (0.96) 30 (1.25) Dry weight of food [kg dry weight (ha year) -1 ] Folivorous insects Other insects 9 16 Fruit Reference Leigh (1999) Fogden (1976); Leigh (1999) group of plants. Some insect predators of dipterocarp fruits are known to attack more than one species within a genus or a family, and can cause considerable damage both in GF and nongf periods (Toy, 1991; Momose et al., 1996; Lyal & Curran, 2000). Momose et al. (1996) observed that more than 60% of immature fruits on twigs had been damaged by insects in early stages of their development. Little is known about the population dynamics, maintenance of populations during non-gf, and host specificity of insect predators. Apparently, some seed predators are specialized to GF events, and they never occur on a host tree flowering outside of GF (Lyal & Curran, 2000). POLLINATORS One of the most important problems related to GF is what pollinates plants that flower at multiyear intervals, because there are few floral resources to sustain pollinators during non-gf periods (Fig. 1). Most tropical plants are outcrossing in spite of the high species diversity and the low population density of each species (Gan et al., 1977; Hamrick & Murawski, 1990): and outcrossing is achieved by animal pollen vectors (Kress & Beach, 1994; Momose et al., 1998). From the viewpoint of animals foraging on floral resources, potential pollinators, the question becomes how to respond effectively to the drastic increase in resources during GF. Three tactics enable consumers to respond to an abrupt increase in floral resources in GF while maintaining their population during non GF periods. The three tactics are: (1) immigration; (2) stabilization of fluctuating resource availability by storing excess resource; and (3) shifting resource niches. Immigrating flower visitors are represented by Apis dorsata F. (giant honeybee, Hymenoptera, Apidae). The seasonal migration of A. dorsata over 100 km between montane and lowland areas reported from Sri Lanka (Koeniger & Koeniger, 1980) demonstrates their ability to migrate long distances. In lowland dipterocarp forests, they immigrate into the forest and build their nest as soon as GF starts. When the amount of floral resources drops to normal after GF, they leave the forest (Nagamitsu, 1998; Itioka et al., 2001). Other than A. dorsata, carpenter bees, birds, and bats are also thought to immigrate into forests from secondary growth in GF (Appanah, 1990). On the other hand, three other Apis bees and stingless bees are resident bees in the primary forests of Lambir (Nagamitsu & Inoue, 1997). Migration, or absconding, of stingless bees is rarely recorded (Michener, 1974). GF brings about a great increase of resources for stingless bees, which visit a wide variety of flowers irrespective of the principal pollinators. They store excess honey and pollen in their nests and produce new individuals. Successful establishment of new nests has been observed only in GF years (Nagamitsu, 1998). It is possible that changes in resource availability associated with GF promotes the coexistence of species. In GF, the intensity of interspecific competition among stingless bees was drastically decreased due to the lagged and slow response of their population increase to GF (Nagamitsu, 1998). During GF, stingless bees that are inferior in resource competition in nongf periods can get many more resources than usual. If these species have a better ability to raise colony workers or to find new nest sites than other species, then they can improve their position during GF. In general, high diversity in the environment is thought to promote the coexistence of species. In this case, GF increases temporal environmental diversity.

9 GENERAL FLOWERING IN DIPTEROCARP FORESTS 241 A feeding-niche shift was found in the beetle pollinators of Shorea parvifolia Dyer (section Mutica, Dipterocarpaceae) (Sakai et al., 1999a). The first pollination study of section Mutica was carried out by Appanah and Chan (Chan & Appanah, 1980; Appanah & Chan, 1981) at Pasoh Forest Reserve in peninsular Malaysia. They studied six species of section Mutica and reported that thrips (Thysanoptera) were pollinators of the plants. Thrips are tiny insects (body length ~1mm), most known as pests in relation to farm products. They are found on the flowers of most plant species, feeding on pollen and ovules, but rarely contributing to pollination. On Shorea species at Pasoh, thrips accounted for 97% of flower visitors, and they carried pollen. Thus, Appanah & Chan (1981) concluded that thrips were pollinators of the plants. They argued that thrips were ideal pollinators of Shorea, because they can maintain their population during nongf periods due to low host specificity. Besides, their short generation time (~8 days), and the abrupt increase in floral resources in GF, brought about a population explosion of thrips sufficient to provide pollination service. At Lambir, however, the density of thrips was much less (0.3 per flower) than that observed at Pasoh (2.4 per flower), and beetles visited as frequently as thrips (Sakai et al., 1999a). An experiment introducing beetles and thrips to bagged flowers showed a significant contribution of beetles to pollination, but not of thrips (Sakai et al., 1999a). Interestingly, some of the pollinator beetles are herbivores feeding on the new leaves of dipterocarp trees during non GF periods without dipterocarp flowers (Sakai et al., 1999a; M. Yamauti unpub. data). Monthly surveys using light traps, conducted from 1992 to 1998, constantly captured the beetles (T. Itioka unpub. data). In GF, however, they were observed foraging on the petals of the nocturnal flowers of many Shorea species. An increase in floral resources may cause a shift in their feeding niche. Competition for pollinators among beetle-pollinated Shorea species is one of the interesting subjects that have emerged for future studies. On the other hand, plants pollinated by specific pollinators tended to flower frequently. In contrast to beetles pollinating various species of Shorea, most beetle pollinators are known to feed on pollen and floral tissues of specific host plants such as Annonaceae and Araceae (Gottsberger, 1989a,b; 1990). Ficus species (Moraceae) also have a very specific relationship with their pollinator wasps (Agaonidae, Hymenoptera) (Galil & Eisikowitch, 1968; Compton et al., 1996; Harrison, 2000). The wasps hardly seem to respond to an increase in flowers other than those of their hosts, and their populations are not maintained if flowering of their hosts occurs at irregular and long intervals. At Lambir, the proportions of GF species in the Annonaceae and Ficus were the smallest of all the taxonomic groups (Fig. 3). Sakai et al. (1999b) suggested that aggregated flowering in GF promoted pollination, and that higher pollination success was one of the selective factors for GF. Higher fruit set in GF periods than in non-gf periods supports the idea (Sakai et al., 1999b). Yap & Chan (1990) report similar results in several species of Dipterocarpaceae. Why does synchronized flowering of different species promote pollination? Aggregated flowering of various species sharing common pollinators may promote the immigration and population growth of pollinators, and result in higher pollination success than isolated flowering. When the competition for pollinators can be reduced through such mechanisms as fine segregation in flowering time, synchronized flowering among species sharing the same pollinators will be advantageous for the plants. It was observed by a monthly survey using light traps that insects associated with floral resources increased dramatically during GF (Kato et al., 2000). Immigration of Apis dorsata may not occur when only a single honeybee-pollinated species flowers. Flowering synchronization among species with different pollination systems may also be promoted through interactions of plants and pollinators or flower visitors. Pollinators of some species visit but rarely pollinate other plants, and these plants would contribute to the population growth of nonpollinating flower visitors. Apis-pollinated plants are also exploited by stingless bees and contribute to the population growth of stingless bees. Thus, it may be advantageous to stingless-bee-pollinated species to flower together with Apis-pollinated plants. In turn, stingless-bee flowers may have the same effect on other insect populations. Such flower-visitor-mediated interactions between pollination guilds are symmetrical. Apis dorsata rarely visits small resource patches such as flowers pollinated by stingless bees, while stingless bees often visit Apis-pollinated species. Some pollinators do not have such interactions. In the case of plants with a very specialized relationship with pollinators, such as figs and Annonaceae, their pollinators rarely visit flowers except those of their host, and the flowering of other species does not affect their populations. This may partly explain why figs and Annonaceae show little or no increase in flowering intensity during GF. Our knowledge of the ecology of pollinators is insufficient to evaluate the promotion-of-pollination hypothesis. Plants are pollinated by a diverse variety of animals in GF, and how these animals survive during nongf, and how they respond to GF, differs among pollinators. Immigration of Apis dorsata does not occur without the huge floral resources of GF, but

10 242 S. SAKAI it is uncertain if flowering of a single Shorea species can bring about feeding-niche shifts in pollinator beetles. Though insect populations primarily dependent on floral resources may show clear population growth in GF, the responses of other pollinators, which may feed on vegetative parts of plants, such as most Lepidoptera, is unknown. ENVIRONMENTAL PREDICTION The environmental prediction hypothesis proposes that the plant can predict which years will be best for seedlings (Smith et al., 1990; Kelly, 1994). Although it is well documented in the case of masting induced by fire, which causes good nutrient conditions and reduction of competition (Payton & Brasch, 1978), Kelly (1994) suggested it is unlikely in the case of climate. The period between flower induction and seed germination is rather long, and it may be impossible for plants to predict climatic condition at the time of seed germination several months or one year later in terms of interyear variation. In equatorial regions under the effects of El Niño, however, the situation might be different. In a seasonal dry forest in Panama, annual fluctuation in fruit production is correlated with ENSO (Wright et al., 1999). In El Niño years, the high solar radiation causes higher fruit production than usual. Besides, Wright et al. (1999) suggest that more rainfall and favourable conditions for the establishment of seedlings in the following La Niña year could be an additional selective force towards the production of large crops in El Niño years. The idea that a series of climatic conditions associated with ENSO or other phenomena enhances interyear variation in plant phenology is more significant in aseasonal regions. In seasonal environments, most flowering cues assure not only synchronization among individuals, but also some prediction about future climate. For example, heavy rains after a long dry period induce Hybanthus flowering and indicate the start of the rainy season and 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 (Rathcke & Lacey, 1985). As the climate has an annual cycle, plants can anticipate climatic conditions at least in terms of annual means. In the case of GF, does the trigger indicate something about future climate and promote synchronization, or does it only function for synchronization? If a series of climatic conditions favourable for plant reproduction always follows a potential flowering cue, many plants may adopt the cue as a flowering trigger, and it may cause synchronized flowering among species. Careful examination of the relationships among various climatic variables is essential to address the problem. WHY IS GENERAL FLOWERING RESTRICTED TO THE ASIAN TROPICS? Comparison with other tropical forests illustrates the uniqueness of flowering phenology in dipterocarp forests. In coastal-plain and premontane forests of Atlantic Brazil, the proportion of species flowering at any one time is, on average, about 15%, and fluctuates between 2 and 32% (Morellato et al. in press). The proportion in a lowland wet tropical forest in Costa Rica ranges from 10 to 30% in overstory trees, and from 8 to 28% in a drier forest (Frankie et al., 1974). In montane forests, the proportion of flowering species is similar or larger. Koptur et al. (1988), Sun et al. (1996) and Hilty (1980) reported 20 60% from a montane forest in Costa Rica, 10 50% from Rwanda, and 25 40% from Colombia, respectively. In a forest with a severe dry season the proportion drops to 0% in the dry season, but 10 60% of the species are in bloom in the other seasons (Murali & Sukumar, 1994). Conversely, the percentage at Lambir is 0 3% in nongf period and even in a GF period the maximum is about 20%. A study from a dipterocarp forest in peninsular Malaysia shows similar results to Lambir, 0 7% in nongf and 35% in GF (Medway, 1972). The much smaller proportion of flowering species in lowland dipterocarp forests than in other tropical forests is caused by the longer flowering intervals and the aggregation of reproduction in GF periods. Newstrom et al. (1994a,b) show the distribution of flowering types among individual plants at La Selva. Although the data from Lambir are on a species basis and those from La Selva on an individual basis, it is possible to compare flowering frequency between plants in the two forests, as Newstrom et al. (1994a) suggest that the patterns found on an individual basis are not so different from those on a species basis. Though we could not assign flowering type to a fourth of the species because of a lack of flowering records during the 43-month study period, the difference is clear (Fig. 5). At La Selva, more than 50% of the individuals are subannual types. In contrast, only 3% are categorized as subannual in Lambir, and most species are of supra-annual types, including GF type (plant flowering only in GF period). Janzen (1974) suggests poorer soil fertility in Asian forests than in other tropics as a possible reason for longer intervals of reproduction. It may be true that different levels of soil nutrition cause different intervals of GF (Janzen, 1974). At Gunung Palung NP, dipterocarp trees in peat-swamp forests did not reproduce when most mature dipterocarp trees set fruits

11 GENERAL FLOWERING IN DIPTEROCARP FORESTS 243 Figure 5. The proportion of subannual, annual, supraannual and continual flowering types among trees at La Selva, Costa Rica (254 trees, Newstrom et al., 1994b) and Lambir (187 tree species, Sakai et al., 1999b). In the graph, GF type of Lambir is included in supra-annual type. in other habitats in major mast years (Curran & Leighton, 2000). However, no study has compared soils of tropical forests with and without GF. It is also unknown whether the long-term average of fruit production in forest with GF is lower than seasonal forests. It appears that the biogeographic characteristics of the forests, especially dominance and the evolutionary background of the dipterocarp trees in the forests, might have played an essential role in the establishment of synchronized flowering. Dominance of a single family in the canopy and emergent layers is rarely found in lowland tropical forests in other regions. Besides, dipterocarp species are different from most canopy species in other families in that they have large fruits dispersed by gravity or wind. This may cause aggregated distribution of each species through short dispersal distances (Condit et al., 2000). The family is thought to originate from rather seasonal tropical forests in Gondwana (Ashton, 1982; Ashton et al., 1988; Dayanandan et al., 1999), where they might have flowered annually in response to a drought-associated temperature drop as dipterocarp trees in South-east Asia and India do currently (Ashton, 1989). Their synchronized flowering, triggered by a drop of temperature in an aseasonal climate, may be largely a result of phylogenetic constraint, which serves as the core of GF. It is well accepted that phenology is strongly influenced by phylogeny (Kochmer & Handel, 1986; Wright & Calderon, 1995). Selection by fruit predation and/or pollination strengthen the synchronization within the family, and lead to the participation of plants of other families to form the observed phenomenon of GF. To examine this scenario, we need to know the palaeoclimate of Asian tropical forests. Reconstruction of past changes in climate and in plant phenology may also be important for predicting the effects of future climatic changes on phenology (Corlett & LaFrankie, 1998). CONCLUDING REMARKS GF provides a unique opportunity to study the causes and consequences of synchronized flowering among many species in the community at multiyear intervals under aseasonal climatic conditions. Considering the ecological and economic importance of the phenomenon, information on GF has been surprisingly limited. Recently, however, long-term studies on GF have been published, and new hypotheses have been proposed. Studies of GF involve a variety of subjects. To address the problems, collaboration of scientists from various fields, such as reproductive ecology, plant physiology, entomology, mammalogy, and meteorology, is required. Comparisons of phenology, productivity, and nutrient conditions between forests with GF and seasonal dipterocarp forests, or between seasonal or aseasonal forests in other regions, are useful for investigating the evolutionary cause of GF. Furthermore, theoretical studies of flowering and fruiting strategies and plant predator interactions would help to evaluate hypotheses explaining GF. The incidence of GF at multiyear intervals indicates the importance of longterm monitoring of biological phenomena. Field stations promote long-term monitoring, comparative studies among sites and the participation of scientists from different fields. It is quite probable that GF, which plays a central role in regeneration in dipterocarp forests, is vulner-

12 244 S. SAKAI able to changes of in the frequency and intensity of ENSO-associated conditions caused by global climatic change, as well as to changes in forest structure caused by logging and the impact of other human practices (Curran et al., 1999). Long-term monitoring and further understanding of GF are essential for the conservation of this unique and diverse tropical forest (Corlett & LaFrankie, 1998). ACKNOWLEDGEMENTS Discussions with Takuya Abe, Tamiji Inoue, Makoto Kato, Kuniyasu Momose, Hidetoshi Nagamasu, David W. Roubik and other members of SCBP helped develop the ideas in this paper. Tetsuzo Yasunari and Masatoshi Yasuda provided information about tropical climate and mammalogy, respectively. I thank S. Joseph Wright and Tohru Nakashizuka for constructive comments on earlier drafts. This study is partly supported by grants from the Japanese Ministry of Culture, Sports, Science and Technology (#09NP1501), JST-CREST Program and JSPS Research Fellowships for Young Scientists for S. Sakai. REFERENCES Allison TD Pollen production and plant density affect pollination and seed production in Taxus canadensis. Ecology 71: Appanah S General flowering in the climax rain forest of southeast Asia. Journal of Tropical Ecology 1: Appanah S Plant pollinator interactions in Malaysian rain forests. In: Bawa KS, Hadley M, eds. Reproductive ecology of tropical forest plants. Lancs: Unesco, Paris and The Parthenon Publishing Group, Appanah S Mass flowering of dipterocarp forests in the aseasonal tropics. Journal of Bioscience 18: Appanah S, Chan HT Thrips: the pollinators of some dipterocarps. Malaysian Forester 44: Ashton PS Dipterocarpaceae. Flora Malesiana Series 1. Spermatophyta 9: Ashton PS Dipterocarp reproductive ecology. In: Leigh H, Werger MJA, eds. Ecosystems of the world 14B: tropical rain forest. Amsterdam: Elsevier Scientific, Ashton PS, Givnish TJ, Appanah S Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. American Naturalist 132: Augspurger CK Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinator and seed predators on Hybanthus prunifolius (Vioraceae). Ecology 62: Blicher MU Borneo illipe, a fat product from different Shorea spp. (Dipterocarpaceae). Economic Botany 48: Burgess PF Studies of the regeneration of the hill forests of the Malay Peninsula. Malaysian Forester 35: Caldecott JO, Blouch RA, Macdonald AA The bearded pig (Sus barbatus). In: Oliver R, ed. Pigs, peccaries, and hippos: status, survey and conservation action plan. Gland, Switzerland: IUCN/SSC. World Conservation Centre, Chan HT, Appanah S Reproductive biology of some Malaysian dipterocarps. Malaysian Forester 44: Cockburn PS Phenology of dipterocarp in Sabah. Malaysian Forester 44: Compton SG, Wiebes JT, Berg CC The biology of fig trees and their associated animals. Journal of Biogioglaphy 23: Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S, Gunatilleke N, Hubbell SP, Foster RB, Itoh A, LaFrankie JV, Lee HS, Losos E, Manokaran N, Sukumar R, Yamakura T Spatial patterns in the distribution of tropical tree species. Science 288: Corlett RT Flora and reproductive phenology of the rain forest at Bukit Timah, Singapore. Journal of Tropical Ecology 6: Corlett RT, LaFrankie JV Potential impacts of climate change on tropical Asian forests through an influence on phenology. Climate Change 39: Crawley MJ, Long R Alternate bearing, predator satiation and seedling recruitment in Quercus robur L. Journal of Ecology 83: Curran LM, Caniago I, Paoli GD, Astianti D, Kusneti M, Leighton M, Nirarita CE, Haeruman H Impact of El Niño and logging on canopy tree recruitment in Borneo. Science 286: Curran LM, Leighton M Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs 70: Curran LM, Webb CO Experimental tests of the spatioscale of seed predation in mast-fruiting Dipterocapaceae. Ecological Monographs 70: Dayanandan S, Ashton PS, Williams SM, Primack RB Phylogeny of the tropical tree family Dipterocarpaceae based on nucleotide sequences of the chloroplast rbcl gene. American Journal of Botany 86: Dayanandan S, Attygalla DNC, Abeygunasekera AWWL, Gunatilleke IAUN, Gunatilleke CVS Phenology and morphology in relation to pollination of some Sri Lankan dipterocarps. In: Bawa KS, Hadley M, eds. Reproductive ecology of tropical forest plants. Lancs: Unesco, Paris and The Parthenon Publishing Group, Fogden MPL The seasonality and population of equatorial forest birds in Sarawak. Ibis 114: Fogden MPL A census of a bird community in tropical rainforest in Sarawak. Sarawak Museum Journal 24: Frankie GW, Baker HG, Opler PA Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology 62: