TROPICS Vol. 14 (4) Issued July 31, 2005

Fruit-frugivore interactions in a moist evergreen of in

1)＊ 2) 1) 1) 1) 3) Shumpei KITAMURA , Takakazu YUMOTO , Pilai POONSWAD , Phitaya CHUAILUA , Kamol PLONGMAI , Naohiko NOMA ,

4) 5) Tamaki MARUHASHI and Prawat WOHANDEE

1) Thailand Project, Department of Microbiology, Faculty of Science, Mahidol University, Rama 6 Rd, Bangkok 10400, Thailand 2) Research Institute of Humanity and Nature, Kyoto, 602-0878, Japan 3) School of Environmental Science, The University of Shiga Prefecture, Hikone, 522-8533, Japan 4) Department of Human and Culture, Musashi University, Nerima, Tokyo 176-8534, Japan 5) National Parks Division, Department of National Parks, Wildlife and Conservation, Phaholyothin Rd, Chatuchak, Bangkok 10900, Thailand ＊ Corresponding author. Department of Microbiology, Faculty of Science, Mahidol University, Rama 6 Rd., Bangkok 10400, Thailand E-mail address: [email protected], Tel: 66-2-201-5532, Fax: 66-2-644-5411

ABSTRACT by plays a crucial role in the tropics. Fruit-bearing serve not only as nutritional sources for frugivores, but also as seed sources for forest regeneration and as important foci for the re-establishment of other plant species by attracting seed-dispersing frugivores to their vicinity. However, opportunities for investigating the interactions between a diverse fruit flora and disperser fauna are rapidly disappearing in . We observed the behaviors of 28 species of frugivorous visitors to 15 fruit-bearing plant species in a moist evergreen forest in Khao Yai National Park, Thailand, to determine their potential quality as seed dispersers. Behavioral observations included the frequency and duration of visits by each forager and their fruit-handling techniques. The highest numbers of frugivores were recorded at strangler figs, confirming their role as an important resource for frugivores at Khao Yai. Mammals and non-passerine spent significantly more time at food plants than did passerine birds. Our study provides a preliminary inventory of plant-frugivore interactions that is comparable to other study sites in Southeast Asia. Since fruit-frugivore interactions may differ among the , these kinds of studies need to be replicated at faunally intact forests, as well as depleted forests, in Southeast Asia.

Key words: frugivore, frugivory, fruit characteristics, seed dispersal, seed predation

INTRODUCTION In the tropics, the majority of woody plant species bear -dispersed fruits (Howe & Smallwood 1982; Howe 1986; Fleming et al. 1987; Jordano 2000). These fruits may serve not only as resources to fulfill the nutritional requirements of frugivores (McKey, 1975), but also as seed sources for forest regeneration (McDonnell & Stiles, 1983; Elliott et al., 2002) and as important foci for the re-establishment of other plant species by attracting seed-dispersing animals to their vicinity (Alcantara et al., 2000; Schupp et al., 2002; Clark et al., 2004; Russo & Augspurger, 2004). In Southeast Asia, too, the species diversity of animal-dispersed plants is high (Ng, 1983) and most forest birds and mammals consume various kinds of fruits (Corlett, 1998b). Despite the massive anthropogenic habitat modifications in Southeast Asia (Laurance, 1999; Sodhi et al., 2004), studies on fruit-frugivore interactions are very limited (Corlett, 1998b). Information on fruit species’ preferences by most frugivorous animals may be insufficient to distinguish seed dispersal roles among particular frugivore species within an assemblage in many tropical forests in Southeast Asia. As many dispersal agents are highly vulnerable to hunting and habitat loss (da Silva & Tabarelli, 2000; Peres, 2000; Pattanavibool & Dearden, 2002), opportunities for investigating the interactions between a diverse fruit flora and an intact disperser fauna are rapidly disappearing in Southeast Asia (Corlett, 2002; Sodhi et al., 2004). Khao Yai National Park is regarded as one of the best conservation areas in Southeast Asia (Elliott, 2001). It still contains sizable populations of large frugivorous animals that were mostly depopulated in other areas of Thailand, as well as Southeast Asia. Most of the plants in the moist evergreen forest of Khao Yai National Park bear fleshy fruits and are thus potentially dispersed by animals (Kitamura et al., 2005). As a result of our previous work (Kitamura et al., 2002), interactions between fruits and frugivores in Khao Yai National Park is one of the best-studied examples in Southeast Asia. However, our previous approach was predicated on the assumption that frugivores within a single functional group 346 Shumpei KITAMURA, Takakazu YUMOTO, Pilai POONSWAD, Phitaya CHUAILUA, Kamol PLONGMAI, Naohiko NOMA, Tamaki MARUHASHI and Prawat WOHANDEE

consume similar plants and therefore disperse similar seeds. However, specific dietary information is required to assess the validity of this kind of approach (Moran et al., 2004). Furthermore, previous studies related to seed dispersal by animals in Khao Yai National Park concentrated on large frugivores such as gibbons (Whitington, 1990; Whitington, & Treesucon, 1991) and (Poonswad et al., 1998b; Kitamura et al., 2004a; Kitamura et al., 2004b; Kitamura et al., 2004c), without considering the seed-dispersing role of small frugivorous vertebrates that are diverse and abundant in Southeast Asia (Corlett, 1998b). The major aim of this study was to obtain data on fruit preferences of frugivores, including small frugivorous vertebrates that were mostly ignored in the previous studies conducted in Khao Yai National Park. To this end, the frequency and duration of frugivore visits to fruiting plants were recorded, and fruit-handling techniques are described. More specifically, we addressed the question of whether large-seeded plant species were visited by fewer disperser species than were plants with fruits or seeds that were more easily consumed in Khao Yai National Park. These trends are found mainly in Neotropical, African and temperate zone studies (Jordano, 1995), but there has been little work done on it in Southeast Asia. This study also provides a reference of fruit-frugivore interactions for ongoing ecological research and conservation in Khao Yai National Park, as well as Southeast Asia.

MATERIALS AND METHODS Study site This study was conducted in Khao Yai National Park (hereafter KY) in northeastern Thailand from June 1998 to August 1999. The park lies between 14º 05’‒14º 15’ N and 101º 05’‒101º 50’ E in the Dongruk mountain range, and covers an area of 2,168 km2 (Fig. 1). The elevation of the park ranges from 250 to 1,351 m. The study site is located in the area adjacent

�����

������� ������� ����

��������

��������

����������������������

Fig. 1. Location of Khao Yai National Park in relation to neighboring countries.

to the park headquarters and covers approximately 70 km2. The study site ranges from 600 to 800 m in altitude and was dominated by moist evergreen forest, which covered approximately 64 % of the total park area, or 1,375 km2, between 400 and 1,000 m in elevation (Smitinand, 1977). In KY, at least, 72 mammal species (25 % of species recorded in Thailand) and 340 species (37 % of bird species recorded in Thailand) have been reported (MUCDC, 1989; Lekagul & Round, 1991; Srikosamatara & Hansel, 1996). The dominant plant families in the forest include the Lauraceae, Cornaceae, Euphorbiaceae, , Elaeocarpaceae, , and . Kitamura et al. (2005) provided a detailed botanical inventory. The mean annual rainfall from 1993‒2002 was 2,360 mm, and the wet season usually occurs Fruit and frugivore assemblages in Thailand 347 from April to October. The dry season usually occurs from November to March (Kitamura et al., 2004a). The mean monthly temperature ranges from 21 ºC (December and January) to 32 ºC (April and May). Although some ripe fruits ( spp.) are available year-round (Poonswad et al. 1998a), fruit diversity and abundance are relatively high during the rainy season and reach a low point at the beginning of the dry season (Bartlett, 2003).

Plant observations We observed the feeding assemblages of frugivores during the peak fruiting period of 15 plant species (Table 1). These plant watches consisted of continuous 12-h observations (0600‒1800) of one individual plant per species. Plants were selected for study if frugivores had been observed to forage on them, or they had a ripe crop of fruit known, or suspected to be, attractive to arboreal frugivores. Since the most likely external variables to influence frugivore foraging

Table 1. Fruit and seed characteristics of the fruit-bearing plants selected for study. FL = fruit length (mm); FD = fruit diameter (mm); CO = color of fruit; NO = number of seeds per fruit; SL = seed length (mm); SD = seed diameter (mm). Fruit type: FT: D = dehiscent; I = indehiscent fruit with thin husk; T = indehiscent fruit with thick husk. Life form: LI = liana; ST = small (7−15 m); MT = medium- sized tree (15−30 m); TT = tall tree (> 30 m). Family Species FL FD CO NO SL SD FT LF Season Code Annonaceae Platymitra macrocarpa Boerl. 80.6 63.6 Brown 7 28.2 16.7 T TT Feb.99 1 Celastraceae robusta (Roxb.) Hou 18.6 11.2 Yellow 1 15.4 8.1 D TT Dec.98 2 Elaeagnaceae Elaeagnus conferta Roxb. 41.1 25.4 Red 1 33.0 9.9 I LI Jan.99 3 Elaeocarpacae Sloanea sigun (Blume) K. Schum. 10.3 6.3 Orange 1 8.8 5.9 I MT Dec.98 4 Euphorbiaceae Glochidion sphaerogynum (Mull.Arg.) Kurz 5.7 4.4 Red 9 4.9 3.4 D ST Jan.99 5 Euphorbiaceae Macaranga tanarius (L.) Mull. Arg. 5.9 5.4 Black 1 5.2 4.2 D ST Sep.98 6 Gnetaceae Gnetum montanum Markgr. 19.4 15.8 Red 1 20.7 12.7 I LI Jul.98 7 Lauraceae Cinnamomum subavenium Miq. 16.7 10.5 Black 1 14.2 8.1 I MT Feb.99 8 Magnoliaceae Michelia baillonii Finet & Gagnep. 9.8 7.4 Red 1 7.6 5.8 D TT Jul.98 9 Meliaceae lawii (Wight) C. J. Saldanha 25.2 15.7 Red 1 21.5 13.3 D MT May.99 10 Meliaceae (Miq.) S. S. Jain & Bennet 39.6 22.9 Red 1 31.4 20.3 D TT Jun.99 11 Moraceae Ficus altissima Bl. 21.5 18.3 Red 100 > 1.0 1.0 I TT Nov.98 12 Moraceae Ficus benjamina L. 18.8 18.1 Purple 100 > 1.0 1.0 I TT Jan.99 13 Moraceae Ficus subcordata Bl. 21.4 16.7 Purple 100 > 1.0 1.0 I TT Oct.98 14 Sapindaceae Nephelium melliferum Gagnep. 33.9 26.4 Red 1 22.4 12.7 T MT Apr.99 15 are the kinds and amounts of fruit available to frugivores within some area surrounding focal plants (Herrera, 1986), we selected the fruiting plants that were not surrounded by other fruiting plants during the observation period. Because we did not observe plants at night, we have no data on nocturnal frugivores such as fruit bats and flying squirrels. No observations were made on days with strong wind and rain. Observers were concealed on the ground in a position from which they could view as much of the focal plant canopy as possible through binoculars. Plant observations provided data on the animal species feeding on the plants and their handling behavior (swallowing fruit whole, pecking parts out of it, dropping fruit, and predating seed). Species visiting a plant without foraging were not considered in the analysis. Because it was impossible to identify most frugivores individually (especially in mixed-species flocks), repeat visits by the same individual had to be treated in the same way as visits by different frugivores. Very often, the precise moment when frugivores (especially small passerines such as white-eyes) arrived at or moved out of a focal plant could not be determined. Therefore, it was assumed that the presence and absence of a frugivore departed soon after its arrival were noticed soon after its entry or departure, so that the duration of all visits was scored to the nearest 1 min. To determine differences in visitation length among frugivores, we pooled results across all visited plant species. Although pooling the data may have masked important variability among focal plants, the sample sizes for most species of frugivores were too small to test such variability. Taxonomic nomenclature for plants, mammals, and birds followed Kitamura et al. (2002), Srikosamatara & Hansel (1996), and Lekagul & Round (1991), respectively.

Fruit characteristics In this study, we use the terms“ fruits” and“ seeds” in their ecological, not their anatomical sense (Herrera 1987). Ripe 348 Shumpei KITAMURA, Takakazu YUMOTO, Pilai POONSWAD, Phitaya CHUAILUA, Kamol PLONGMAI, Naohiko NOMA, Tamaki MARUHASHI and Prawat WOHANDEE fruits were collected beneath the focal plants during the observation periods. The following characteristics were recorded: length and transverse diameter of the fruit/seed, wet weight of the fruit/seed, ripe fruit color (for dehiscent fruits, the color of the inner part of the fruits displayed for animals was described), and number of seeds in a fruit. In the case of dehiscent fruits such as Aglaia spectabilis (Meliaceae), we treated the arillate seeds as the dispersal units, since they separate quite easily in the ripe fruit and are apparently removed by animals individually. These data were collected for at least 30 samples of each fruit species. Fruits with obvious damage were excluded from the measurements. No attempt was made to describe variation among individuals within species; samples were chosen to represent the typical size ranges. These measurements were performed within a day after fruits were collected. The life form of each species was defined as follows: liana (LI), small tree (7‒15 m tall; ST), medium-sized tree (15‒30 m; MT), and tall tree (> 30 m; TT). Fruit types of each species were defined according to Gautier-Hion et al. (1985) as dehiscent fruit (D), indehiscent fruit with a thin husk (I), or indehiscent fruit with a thick husk (T).

RESULTS Fruit characteristics of focal plants Fruit characteristics and growth forms of the focal plant species selected for this study, as well as time of year and species code for each species, are presented in Table 1. These 15 species belong to 12 genera of 11 families. The median values for fruit length, fruit diameter, number of seeds per fruit, seed length, and seed diameter were 19.4 mm, 15.8 mm, 1.0, 14.2 mm, and 8.1 mm, respectively. These characteristics were highly variable from small fruits to large fruits: the lightest fruit species was Macaranga tanarius (0.10‒0.13 g) and the heaviest fruit was Platymitra macrocarpa (74.5‒342.0 g).

Fruit use by the frugivore community In total, 22 species of birds and six species of mammals were observed foraging in 15 different species of fruit-bearing plants (Table 2). All frugivores, except Coracina fimbriata, Oriolus chinensis, and Eumyias thalassina, were resident in KY. Frequently observed frugivores were the birds , Bucerotidae, Megalaimidae, Pycnonotidae, Irena puella, and Gracula religiosa and the mammals, Macaca nemestrina, Hylobates lar, and the Sciuridae. The most widely consumed fruits were three species of strangler figs (Ficus spp., > 11 frugivore species), followed by Macaranga tanarius (nine species). The minimum number of frugivore species recorded for a given plant species was two for Platymitra macrocarpa and Bhesa robusta. Only mammal species were recorded feeding on P. macrocarpa, Elaeagnus conferta, and Nephelium melliferum. In contrast, only bird species were recorded feeding on B. robusta and Glochidion sphaerogynum.

Frugivore behavior at fruiting plants Three bird species, Zosterops palpebrosus (up to 13 individuals), Gracula religiosa (up to 13), and Treron curvirostra (up to ten), were commonly seen in flocks of varying size (Table 3). The other species typically arrived individually, although Megalaima spp. and most mammalian frugivores, except for Hylobates lar, arrived in pairs, or in small groups (up to four, although a flock of ten Anorrhinus austeni was once observed in Ficus subcordata). Several species of the Pycnonotidae were often seen together in mixed-species flocks moving through the canopy and staying in a particular fruiting tree such as Macaranga tanarius and Michelia billonii. Although pig-tailed macaques in our study site usually lived in a large troop, only a solitary male was observed during the study. Techniques of handling fruit varied among frugivore species, especially birds. Fruits were plucked and swallowed whole while the frugivore was perched (Columbidae and Bucerotidae) or mashed between the mandibles and then swallowed (Megalaimidae and Gracula religiosa). Pycnonotidae and Eumyias thalassina frequently took fruits on the wing, held them in the bill, and swallowed them whole after perching on a branch. In the case of Aglaia spectabilis, Megalaima faiostricta only consumed part of the aril without dispersing the seed; thus this species did not disperse any seeds during feeding. In some cases, fruit was picked and carried well out of sight (e.g., albirostris). Since most of the fruits were swallowed whole by most birds, we could not determine how the seeds were processed, i.e., defecated/regurgitated whole or digested/destroyed. In mammals, two species of squirrels (Ratufa bicolor and Callosciurus finlaysonii) mostly predated on the seeds of Elaeagnus conferta, Sloanea sigun, Macaranga tanarius, Gnetum montanum, and Michelia billonii. The squirrels Fruit and frugivore assemblages in Thailand 349

Table 2. Frugivore species, their status (R: resident, W: winter visitor, based on Lekagul & Round 1991) and fruit-bearing plant species in which they were observed foraging. See Table 1 for plant species codes. x: consumed by a frugivore species. Code of the plant species Family Scientific name Common name Status 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Total BIRDS Non-passerine Columbidae Treron curvirostra thick-billed pigeon R x x x 3 Ducula badia mountain R x x x x 4 Bucerotidae Anorrhinus austeni brown hornbill R x x x 3 Aceros undulatus R x x x 3 Anthracoceros albirostris R x x x x x x x 7 Buceros bicornis R x x x 3 Megalaimidae Megalaima lineata lineated barbet R x x x x 4 M. faiostrica green-eared barbet R x x 2 M. incognita R x x x x x x 6 M. australis blue-eared barbet R x x 2 Passerine Pycnonotidae Pycnonotus melanicterus black-crested R x x x 3 P. finlaysonii stripe-throated bulbul R x x x 3 Criniger pallidus puff-throated bulbul R x x x x x 5 Hypsipetes propinquus grey-eyed bulbul R x x x x x x 6 H. flavala ashy bulbul R x 1 Corvidae Oriolus chinensis black-naped oriole W x x 2 Coracina melaschista black-winged cuckoo-shrike W x 1 Irenidae Irena puella Asian fairy-bluebird R x x x x 4 Muscicapidae Eumyias thalassina verditer flycatcher W x x 2 Sturnidae Ampeliceps coronatus golden-crested myna R x 1 Gracula religiosa hill myna R x x x x x x 6 Zosteropidae Zosterops palpebrosus Oriental white-eye R x x 2 MAMMALS Cercopithicidae Macaca nemestrina pig-tailed macaque R x x x x x 5 Hylobatidae Hylobates lar white-handed gibbon R x x x x x x x 7 Viverridae Arctictis binturong binturong R x 1 Sciuridae Ratufa bicolor R x x x x x x x x x 9 Callosciurus finlaysonii variable squirrel R x x x x x x x x x x 10 Tamiops mcclellandi Cambodian striped tree squirrel R x 1 Number of bird species 0 2 0 7 6 7 1 4 7 5 4 12 8 10 0 22 Number of mammal species 2 0 3 1 0 2 3 3 1 1 2 3 4 4 4 6 Total 2 2 3 8 6 9 4 7 8 6 6 15 12 14 4 28 consumed the fruit pulp of Ficus spp., and both the fruit pulp and the seeds of other species (Platymitra macrocarpa, Aglaia spp., Cinnamomum subavenium, and Nephelium melliferum). For Hylobates lar, fruits were usually swallowed whole, or with the rind removed (P. macrocarpa, N. melliferum), if necessary. In contrast, Macaca nemestrina frequently stored the fruits in their cheek pouches while at the focal plants. The seeds were then separated from the fruit pulp and spat out (especially Cinnamomum subavenium). They also predated the seeds of G. montanum. During our observations, most frugivores tended to search for ripe fruits, except for squirrels and Macaca nemestrina. Those animals frequently consumed unripe fruit as well as ripe fruits.

Duration of visits Median visitation lengths of most avian frugivores (except for Treron curvirostra and Aceros undulatus) were less than 10 min, but those of mammalian frugivores, except for Callosciurus finlaysonii, were longer than 10 min (Table 3). Birds spent significantly less time per visit at focal plants than mammals did (Mann-Whitney U test, P < 0.001). Non-passerine species spent significantly more time per visit at focal plants than passerine species did (Mann-Whitney U test, P < 0.01). On occasion, extended visits could be observed (Table 3): one visit by Ratufa bicolor at Ficus subcordata lasted over 3 h. Similarly, a visit by Hylobates lar at Platymitra macrocarpa also lasted for 1 h. All long visits of these frugivores were 350 Shumpei KITAMURA, Takakazu YUMOTO, Pilai POONSWAD, Phitaya CHUAILUA, Kamol PLONGMAI, Naohiko NOMA, Tamaki MARUHASHI and Prawat WOHANDEE

Table 3. List of observed frugivore species, body size (body length for birds and head- body length for mammals), sample size, their group size (mean and standard deviation), and visit length (median and range) at focal plants in a moist evergreen forest of Khao Yai National Park in Thailand. NA: not available. Size Sample group size (n) Visit length (min) Scientific name (cm) (n) Mean SD Median Max Min Birds Non-passerine Treron curvirostra 27 27 6 9 11 36 1 Ducula badia 45 35 2 2 7 53 1 Anorrhinus austeni 74 13 3 3 5 31 2 Aceros undulatus 100 2 2 NA 11 NA NA Anthracoceros albirostris 70 88 2 1 6 14 1 Buceros bicornis 122 46 1 1 9 46 1 Megalaima lineata 29 10 1 0 4 13 1 M. faiostrica 24 6 1 0 4 46 1 M. incognita 23 53 1 0 7 53 1 M. australis 17 5 1 0 5 16 1 Passerine Pycnonotus melanicterus 19 46 1 1 2 15 1 P. finlaysoni 20 16 1 1 3 14 1 Criniger pallidus 24 53 2 1 2 14 1 Hypsipetes propinquus 19 92 1 0 3 11 1 H. flavala 20 30 2 1 3 18 1 Oriolus chinensis 27 4 1 0 10 16 1 Coracina fimbriata 23 11 2 0 5 16 1 Irena puella 25 25 1 1 3 30 1 Eumyias thalassina 17 21 1 0 4 52 1 Ampeliceps coronatus 22 1 2 NA 1 NA NA Gracula religiosa 30 28 3 3 5 17 1 Zosterops palpebosus 11 87 4 3 2 6 1 Mammals Macaca nemestrina 53 10 1 0 10 59 1 Hylobates lar 47 13 2 1 11 65 1 Arctictis binturong 65 1 1 NA 20 NA NA Ratufa bicolor 38 17 1 0 13 191 1 Callosciurus finlaysonii 22 64 1 1 6 33 3 Tamiops mcclellandi 11 6 1 0 20 31 2 mainly the result of long resting times between foraging bouts in the visited plants. In contrast, Megalaima spp. displayed relatively cryptic behavior throughout their visit. Moving slowly, these barbets searched for fruits, often interrupting the search with periods of rest in which they occasionally scanned their surroundings. Conversely, all passerine species actively searched for food throughout the duration of their visits.

Effect of the morphological characteristics of fruits and seeds The number of frugivorous species that served a given plant species declined with seed diameter (Fig. 2b; Spearman rank correlation, P < 0.001 for seed diameter); however, this correlation was not observed for fruit diameter (Fig. 2a; Spearman rank correlation, P = 0.26). Similarly, the number of frugivores that served a given plant species declined with seed diameter (Spearman rank correlation, P < 0.05), but not fruit diameter (Spearman rank correlation, P = 0.19). For eight plant species, the total number of frugivorous visitors observed exceeded 100 (Fig. 3). These plant species bore soft fruit pulp with many small seeds (Ficus spp.) or small-sized fruits (< 10 mm in diameter), except for Aglaia spectabilis. In the case of A. spectabilis, repeated visits by the same individual of Buceros bicornis, Anthracoceros albirostris, and Callosciurus finlaysonii were observed. These three species accounted for 92 % of all observations for this plant species. Fruit and frugivore assemblages in Thailand 351

12 12 ���� ����

8 8

4 4 ��������������������������� ���������������������������

0 0 0 15 30 45 60 75 0 5 10 15 20 25 ������������������� ������������������ Fig. 2. Number of frugivorous species plotted against (a) mean fruit diameter and (b) seed diameter of their diet species (N = 28 species).

100� ������ 80� �������������

60� ���������

40� ��������� 20�

0� 1 (5) 2 (5) 3 (2) 7 (9) 8 (49) 4 (102) 5 (132) 6 (477) 9 (134) 10 (38) 15 (13) 11 (135) 12 (149) 13 (123) 14 (182) ��������������������������������������� Fig. 3. Frequency of visits by frugivore groups (non-passerine birds, passerine birds, and mammals) to each of the plant species listed. The numbers in parentheses indicate the total number of visits by frugivores.

DISCUSSION Fruit and frugivore assemblage in Khao Yai In this study, we observed 22 bird and six mammal species eating fruit. This may be an underestimate, as our observation effort was limited (12 h for one individual per plant species), and we did not include nocturnal frugivores or consumers of fruits that had fallen beneath the focal plants. The question therefore arises whether our observations yield representative results when compared to long-term systematic observations such as those on Aglaia spectabilis (Kitamura et al., 2004a) and Ficus spp. (Poonswad et al., 1998a) in KY. In a seed dispersal study on A. spectabilis over three fruiting seasons with long-term observations of 300 h, eight animal species feeding on the arillate seeds in the canopy have been recorded (Kitamura et al., 2004a). In the present study, the recorded number of frugivore species in A. spectabilis was six (Table 2). These six species accounted for 95 % of all observations in the long-term study, and only rare visitors (Anorrhinus austeni and Ducula badia) were missed during our observations in the current study. In the case of fig consumers, our observations were apparently underestimates in terms of the number of frugivore species. As shown in Table 2, 12 species of birds and three species of mammals fed on Ficus altissima (57 % of bird species and 43 % of mammal species recorded by Poonswad et al., 1998a), and eight species of birds and three species of mammals fed on F. benjamina (only 24 % of bird species and 30 % of mammal species). In spite of the limited observations of figs in this study, however, several taxa, such as pigeons, hornbills, barbets, , primates, and squirrels, were also confirmed 352 Shumpei KITAMURA, Takakazu YUMOTO, Pilai POONSWAD, Phitaya CHUAILUA, Kamol PLONGMAI, Naohiko NOMA, Tamaki MARUHASHI and Prawat WOHANDEE as major fig consumers in KY (Poonswad et al., 1998a). Therefore, our results appear to be representative for the more frequent visitors to focal plants in KY. In general, fruits are eaten by a variety of animals (Table 2), although some fruit characteristics are more likely than others to attract a given group of potential dispersers. The number of frugivore species, as well as the abundance of the frugivores that served a given plant species, declined with seed diameter (Fig. 2). Large fruit/seed size apparently limits the number of avian frugivores, especially small passerine birds. The gape size of frugivorous birds limits the maximum seed diameter of fruits that they can swallow, while mammals have teeth and hands to eat larger fruits (Fleming et al., 1987; Corlett, 1998b). Furthermore, the very thick rinds of Platymitra macrocarpa and Nephelium melliferum apparently exclude all birds (Table 2, Fig. 3), as has been reported in other studies in KY (Whitington, 1990; Kitamura et al., 2002) and Southeast Asia (Leighton, 1982; Pannell & Koziol, 1987; Corlett, 1998b). Captive hornbills can manipulate indehiscent fruits with thick husks, such as Baccaurea ramiflora, Lansium domesticum, and Nephelium -ake, to remove the rind and gain access to the fruit pulp (S. Kitamura, personal observation), but we did not record such behaviors in the field during our study. Since squirrels mostly predated the seeds and the fruit pulp during their feeding, primates are considered to be the main seed dispersers for these plant species in KY. For this reason, in our study, as in most studies, birds seem to select smaller fruits than mammals (Gautier-Hion et al., 1985; Pizo, 2002; Bollen et al., 2004). Our results confirmed that frugivores are highly attracted to figs in KY. This was demonstrated by both the high diversity of frugivore species visiting fig plants (Table 2) and the high visitation rates of fig plants by frugivores (Fig. 3). Fruiting plants that provide important resources for frugivores have been called keystone plant resources (Terborgh, 1986). Figs (Ficus spp.) are considered to be keystone plant resources for many tropical forests such as those in Panama (Korine et al., 2000), South Africa (Bleher et al., 2003), Peninsular Malaya (Lambert & Marshall, 1991), (Kannan & James, 1999), and (Leighton & Leighton, 1983), but not in Madagascar (Goodman & Ganzhorn, 1997) and Gabon (Gautier-Hion & Michaloud, 1989). Since the soft flesh of figs can be penetrated by the bills of birds unable to swallow the fruit whole, there have been apparently no negative effects on the numbers of frugivore species for consumption of figs. Moreover, all fig species in this study were observed during the dry season, when other fruit resources were relatively limited (Whitington & Treesucon, 1991; Bartlett, 2003). Although the dominant frugivores at focal figs are non-passerine birds, such as hornbills and barbets in this study (Fig. 3), the easiness with which figs can be harvested by diverse assemblages of frugivores including small passerine birds, contribute to the unique role that Ficus plays in frugivore survival in KY. Our studies revealed that small passerine birds were the dominant frugivores for some plant species in terms of the number of species, as well as visitation rate (Fig. 3). Similar results are reported from India (Balasubramanian, 1996) and the Philippines (Heindl & Curio, 1999), where the most frequently observed frugivores are all passerine birds: Pycnonotus cafer, P. luteolus and Acridotheres tristis in India (Balasubramanian, 1996) and Hypsipetes philippinus, Zosterops montanum and Dicaeum bicolor in the Philippines (Heindl & Curio, 1999). These tendencies are also confirmed in the subtropical forests in Hong Kong (Corlett, 1996, 1998a) and Yakushima Island (Noma & Yumoto, 1997). These passerine birds either swallowed fruits whole, with or without prior handling, or they took bits of pulp from fruits that had many tiny seeds, so that even small pieces should contain at least some seeds for dispersal. The short visitation length of these passerine birds at the fruiting plant suggests their importance as effective seed dispersers. Although the duration of a visit at a fruiting plant is a clue to the dispersal quality of a given frugivore species only when it is related to the retention time of the frugivore (Wheelwright, 1991; Whitney et al., 1998; Holbrook & Smith, 2000), the observed visitation lengths in this study are shorter than the known seed passage times for passerine birds, such as bulbuls (Fukui, 1996, 2003). Furthermore, these passerine birds are among the last remaining seed dispersal agents in degraded landscapes and are apparently not target species for hunting in Southeast Asia (Corlett, 2002). This suggests that the role of these small passerine birds as seed dispersers has mostly been underestimated in Southeast Asia. The number of possible pairs of plants and frugivores is enormous in the tropics, but fruit-frugivore relationships are structured in a variety of ways, so only a subset of the possible interactions actually occurs (Primack & Corlett, 2005). This study provides a preliminary inventory of plant-frugivore interactions that are comparable to other study sites in Southeast Asia, but we still have very limited data on frugivores on the ground and at night in KY. Consumption of fallen fruit by nocturnal animals, such as civets, and secondary dispersal by rodents may be important processes of seed dispersal in Southeast Asia (Miura et al., 1997; Yasuda et al., 2000; Kitamura et al., 2004a; Yasuda et al., 2005). As fruit-frugivore interactions may differ among the forests in Southeast Asia, these kinds of studies need to be replicated at Fruit and frugivore assemblages in Thailand 353 faunally healthy forests, as well as depleted forests.

ACKNOWLEDGEMENTS We are grateful to the National Research Council of Thailand and National Park Division of the Royal Forest Department of Thailand, for granting us permission to conduct research activity in KY. We extend our hearty thanks to the staff in KY. In particular, we would like to thank B. Saengthong, S. Chuailua, S. Nakkuntod, S. Sanguanchat, N. Jirawatkavi and all staff members of the Thailand Hornbill Project for supporting our fieldwork, as well as their kind encouragement. Thanks to members of the plant ecology discussion group at the Center for Ecological Research, Kyoto University for providing useful suggestions and discussions. Two anonymous referees provided insightful comments on previous drafts of this paper. This research is partly supported by a Research Fund of the Japan Society for the Promotion of Science (#10041169).

REFERENCES Alcantara, J. M., Rey, P. J., Valera, F. & Sanchez-Lafuente, A. M. 2000. Factors shaping the seedfall pattern of a bird- dispersed plant. Ecology 81: 1937‒1950. Balasubramanian, P. 1996. Interactions between fruit-eating birds and bird-dispersed plants in the tropical dry evergreen forest of Point Calimere, South India. Journal of Bombay Natural History Society 93: 428‒441. Bartlett, T. Q. 2003. Intragroup and intergroup social interactions in white-handed gibbons. International Journal of Primatology 24: 239‒259. Bleher, B., Potgieter, C. J., Johnson, D. N. & Bohning-Gaese, K. 2003. The importance of figs for frugivores in a South African coastal forest. Journal of Tropical Ecology 19: 375‒386. Bollen, A., Elsacker, L. V. & Ganzhorn, A. W. 2004. Relations between fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach. Journal of Tropical Ecology 20: 599‒612. Clark, C. J., Poulsen, J. R., Connor, E. F. & Parker, V. T. 2004. Fruiting as dispersal foci in a semi-deciduous tropical forest. Oecologia 139: 66‒75. Corlett, R. T. 1996. Characteristics of vertebrate-dispersed fruits in Hong Kong. Journal of Tropical Ecology 12: 819‒833. Corlett, R. T. 1998a. Frugivory and seed dispersal by birds in Hong Kong shrubland. Forktail 13: 23‒27. Corlett, R. T. 1998b. Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) Region. Biological Reviews 73: 413‒448. Corlett, R. T. 2002. Frugivory and seed dispersal in degraded tropical east Asian landscapes. In: Levey, D. J., Silva, W. R. & Galetti, M. (Eds.) Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, Pp. 451‒465. CABI Publishing, New York. da Silva, J. M. C. & Tabarelli, M. 2000. Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404: 72‒74. Elliott, S. 2001. The National Parks and other wild places of Thailand. Asia Books Co. Ltd., Bangkok, Thailand. Elliott, S., Kuarak, C., Navakitbumrung, P., Zangkum, S., Anusarnsunthorn, V. & Blakesley, D. 2002. Propagating framework trees to restore seasonally dry tropical forest in northern Thailand. New Forests 23: 63‒70. Fleming, T. H., Breitwisch, R. & Whitesides, G. H. 1987. Patterns of tropical vertebrate frugivore diversity. Annual Review of Ecology and Systematics 18: 91‒109. Fukui, A. 1996. Retention time of seeds in bird guts: Costs and benefits for fruiting plants and frugivorous birds. Plant Species Biology 11: 141‒147. Fukui, A. 2003. Relationship between seed retention time in bird’s gut and fruit characteristics. Ornithological Science 2: 41‒48. Gautier-Hion, A., Duplantier, J. M., Quris, R., Feer, F., Sourd, C., Decoux, J. P., Dubost, G., Emmons, L., Erard, C., Hecketsweiler, P., Moungazi, A., Roussilhon, C. & Thiollay, J. M. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324‒337. Gautier-Hion, A. & Michaloud, G. 1989. Are figs always keystone resources for tropical frugivorous vertebrates: a test in Gabon. Ecology 70: 1826‒1833. Goodman, S. M. & Ganzhorn, J. U. 1997. Rarity of figs (Ficus) on Madagascar and its relationship to a depauperate frugivore community. Revue D Ecologie-La Terre Et La Vie 52: 321‒329. 354 Shumpei KITAMURA, Takakazu YUMOTO, Pilai POONSWAD, Phitaya CHUAILUA, Kamol PLONGMAI, Naohiko NOMA, Tamaki MARUHASHI and Prawat WOHANDEE

Heindl, M. & Curio, E. 1999. Observations of frugivorous birds at fruit-bearing plants in the north Negros forest reserve, Philippines. Ecotropica 5: 167‒181. Herrera, C. M. 1986. Vertebrate-dispersal plants: why they don’t behave the way they should. In: Estrada, A. & Fleming, T. H. (Eds.) Frugivores and seed dispersal, Pp. 5‒20. Dr W Junk Publishers, Dordrecht. Herrera, C. M. 1987. Vertebrate-dispersed plants of the Iberian Peninsula: a study of fruit characteristics. Ecological Monographs 57: 305‒331. Holbrook, K. M. & Smith, T. B. 2000. Seed dispersal and movement patterns in two species of Ceratogymna hornbills in a West African tropical lowland forest. Oecologia 125: 249‒257. Howe, H. F. 1986. Seed dispersal by fruit-eating birds and mammals. In: Murray, D. R. (Eds.) Seed Dispersal, Pp. 123‒189. Academic Press, Sydney. Howe, H. F. & Smallwood, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13: 201‒228. Jordano, P. 1995. Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant-animal interactions. American Naturalist 145: 163‒191. Jordano, P. 2000. Fruits and frugivory. In: Fenner, M. (Eds.) Seeds: The Ecology of Regeneration in Plant Communities, Pp. 125‒166. CABI Publishing, CAB International, Wallingford, UK. Kannan, R. & James, D. A. 1999. Fruiting phenology and the conservation of the Great Pied Hornbill (Buceros bicornis) in the of southern India. Biotropica 31: 167‒177. Kitamura, S., Suzuki, S., Yumoto, T., Chuailua, P., Plongmai, K., Poonswad, P., Noma, N., Maruhashi, T. & Suckasam, C. 2005. A botanical inventory of a tropical seasonal forest in Khao Yai National Park, Thailand: implications for fruit- frugivore interactions. Biodiversity and Conservation 14: 1241‒1262. Kitamura, S., Suzuki, S., Yumoto, T., Poonswad, P., Chuailua, P., Plongmai, K., Noma, N., Maruhashi, T. & Suckasam, C. 2004a. Dispersal of Aglaia spectabilis, a large-seeded tree species in a moist evergreen forest in Thailand. Journal of Tropical Ecology 20: 421‒427. Kitamura, S., Yumoto, T., Poonswad, P., Chuailua, P. & Plongmai, K. 2004b. Characteristics of hornbill-dispersed fruits in a tropical seasonal forest in Thailand. Bird Conservation International 14: S80-S88. Kitamura, S., Yumoto, T., Poonswad, P., Chuailua, P., Plongmai, K., Maruhashi, T. & Noma, N. 2002. Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecologia 133: 559-572. Kitamura, S., Yumoto, T., Poonswad, P., Noma, N., Chuailua, P., Plongmai, K., Maruhashi, T. & Suckasam, C. 2004c. Pattern and impact of hornbill seed dispersal at nest trees in a moist evergreen forest in Thailand. Journal of Tropical Ecology 20: 545‒553. Korine, C., Kalko, E. K. V. & Herre, E. A. 2000. Fruit characteristics and factors affecting fruit removal in a Panamanian community of strangler figs. Oecologia 123: 560‒568. Lambert, F. R. & Marshall, A. G. 1991. Keystone characteristics of bird-dispersed Ficus in a Malaysian lowland rain-forest. Journal of Ecology 79: 793‒809. Laurance, W. F. 1999. Ecology and management of fragmented tropical landscapes - Introduction and synthesis. Biological Conservation 91: 101‒107. Leighton, M. 1982. Fruit resources and patterns of feeding, spacing and grouping among sympatric Bornean hornbills (Bucerotidae). PhD thesis. University of California, California. Leighton, M. & Leighton, D. R. 1983. Vertebrate response to fruiting seasonality within a Bornean rain forest. In: Sutton, S. L., Whitmore, T. C. & Chadwick, A. C. (Eds.) Tropical Rain Forest: Ecology and Management, Pp. 181‒196. Blackwell Scientific Publications, Oxford, London. Lekagul, B. & Round, P. D. 1991. A guide to the birds of Thailand. Sahakarnbhaet Co., Ltd., Bangkok. McDonnell, M. J. & Stiles, E. W. 1983. The structural complexity of old field vegetation and the recruitment of bird- dispersed plant-species. Oecologia 56: 109‒116. McKey, D. 1975. The ecology of coevolved seed dispersal systems. In: Gilbert, L. E. & Raven, P. H. (Eds.) Coevolution of Animals and Plants, Pp. 159‒191. University of Texas Press, Austin and London. Miura, S., Yasuda, M. & Ratnam, L. C. 1997. Who steals the fruits? Monitoring frugivory of mammals in a tropical rain forest. Malayan Nature Journal 50: 183‒193. Moran, C., Catterall, C. P., Green, R. J. & Olsen, M. F. 2004. Functional variation among frugivorous birds: implications for rainforest seed dispersal in a fragmented subtropical landscape. Oecologia 142: 584‒595. Fruit and frugivore assemblages in Thailand 355

MUCDC 1989. Birds of Khao Yai National Park checklist. Conservation Data Center, Department of Biology, Faculty of Science, Mahidol University, Bangkok. Ng, F. S. P. 1983. Ecological principles of tropical lowland rain forest conservation. In: Sutton, S. L., Whitmore, T. C. & Chadwick, A. C. (Eds.) Tropical Rain Forest: Ecology and Management, Pp. 359‒375. Blackwell Soc. Publ., London. Noma, N. & Yumoto, T. 1997. Fruiting phenology of animal-dispersed plants in response to winter migration of frugivores in a warm temperate forest on Yakushima Island, Japan. Ecological Research 12: 119‒129. Pannell, C. M. & Koziol, M. J. 1987. Ecological and phytochemical diversity of arillate seeds in Aglaia (Meliaceae): a study of vertebrate dispersal in tropical trees. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 316: 303‒333. Pattanavibool, A. & Dearden, P. 2002. Fragmentation and wildlife in montane evergreen forests, northern Thailand. Biological Conservation 107: 155‒164. Peres, C. A. 2000. Effects of subsistence hunting on vertebrate community structure in Amazonian forests. Conservation Biology 14: 240‒253. Pizo, M. A. 2002. The seed-dispersers and fruit syndromes of Myrtaceae in the Brazilian Atlantic forest. In: Levey, D. J., Silva, W. R. & Galetti, M. (Eds.) Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, Pp. 129‒143. CABI Publishing, New York. Poonswad, P., Chuailua, P., Plongmai, K. & Nakkuntod, S. 1998a. Phenology of some Ficus species and utilization of Ficus sources in Khao Yai National Park, Thailand. In: Poonswad, P. (Eds.) The Asian Hornbills: Ecology and Conservation, Thai Studies in Biodiversity No 2, Pp. 227‒244. BIOTEC, NSTDA, Bangkok, Thailand. Poonswad, P., Tsuji, A., Jirawatkavi, N. & Chimchome, V. 1998b. Some aspects of food and feeding ecology of sympatric hornbill species in Khao Yai National Park, Thailand. In: Poonswad, P. (Eds.) The Asian Hornbills: Ecology and Conservation, Thai Studies in Biodiversity No 2, Pp. 137‒157. BIOTEC, NSTDA, Bangkok. Primack, R. & Corlett, R. T. 2005. Tropical rain forest: an ecological and biogeographical comparison. Blackwell Science Ltd, Oxford, UK. Russo, S. E. & Augspurger, C. K. 2004. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters 7: 1058‒1067. Schupp, E. W., Milleron, T. & Russo, S. E. 2002. Dissemination limitation and the origin and maintenance of species-rich tropical forests. In: Levey, D. J., Silva, W. R. & Galetti, M. (Eds.) Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, Pp. 19‒33. CABI Publishing, New York. Smitinand, T. 1977. Plants of Khao Yai National Park. New Thammada Press Ltd, Bangkok. Sodhi, N. S., Koh, L. P., Brook, B. W. & Ng, P. K. L. 2004. Southeast Asian biodiversity: an impending disaster. Trends in Ecology & Evolution 19: 654‒659. Srikosamatara, S. & Hansel, T. 1996. Mammals of Khao Yai National Park. Green World Foundation, Bangkok. Terborgh, J. 1986. Keystone plant resources in the tropical forest. In: Soule, M. E. (Eds.) Conservation biology: the source of scarcity and diversity, Pp. 330‒344. Sinauer Associates, Sunderland. Wheelwright, N. T. 1991. How long do fruit-eating birds stay in the plants where they feed. Biotropica 23: 29‒40. Whitington, C. 1990. Seed dispersal by white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand. Ms thesis. Mahidol University, Bangkok. Whitington, C. & Treesucon, U. 1991. Selection and treatment of food plants by white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand. Natural History Bulletin of the Siam Society 39: 111‒122. Whitney, K. D., Fogiel, M. K., Lamperti, A. M., Holbrook, K. M., Stauffer, D. J., Hardesty, B. D., Parker, V. T. & Smith, T. B. 1998. Seed dispersal by Ceratogymna hornbills in the Dja Reserve, Cameroon. Journal of Tropical Ecology 14: 351 ‒371. Yasuda, M., Miura, M. & Hussein, N. A. 2000. Evidence for food hoarding behaviour in terrestrial rodents in Pasoh forest reserve, a Malaysian lowland rain forest. Journal of Tropical Forest Science 12: 164‒173. Yasuda, M., Miura, S., Ishii, N., Okuda, T. & Hussein, N. A. 2005. Fallen fruits and terrestrial vertebrate frugivores: a case study in a lowland tropical rain forest in Peninsular . In: Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (Eds.) Seed fate: predation, dispersal and seedling establishment, Pp. 151‒174. CABI Publishing, Wallingford. Received 15th Feb. 2005 Accepted 2nd May 2005