Mammal Study 28: 161–165 (2003) © the Mammalogical Society of Japan Short communication

Arboreal fruit visitors in a tropical forest in Sri Lanka

Palitha Jayasekara1,*, Seiki Takatsuki2, Udayani R. Weerasinghe3 and Siril Wijesundara4 1 Faculty of Agriculture, Gifu University, Yanagido 1-1 Gifu 501-1193, Japan 2 The University Museum, the University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan 3 Royal Botanic Gardens, Peradeniya, Sri Lanka

Tropical forests exhibit extremely high biodiversity, and ified forests. The topography, vegetation, and climate of provide complex habitats for wildlife (Harrison 1962). the area have been described in detail by De Zoysa and More than 60% of woody plants in the tropical forest Raheem (1990) and Gunatilleke and Gunatilleke (1996). bear fruits, which are important foods for birds and In brief, however, the forest is dominated by trees mammals (Fleming 1979). Recent studies on frugivory belonging to the family Dipterocarpaceae (Gunatilleke have revealed that birds and primates are the main fruit and Gunatilleke 1996). Rainfall ranges from 3,000 mm consumers (Terborgh 1990; Wrangham et al. 1994; Dew to 6,000 mm per year and temperature ranges from 19°C and Wright 1998). However, past studies have been con- to 31°C. ducted during the daytime, thus it is possible that many Since biodiversity is high in tropical forest, it was nocturnal animals have been overlooked, leaving infor- expected that various species of animals might be mation on frugivores incomplete and biased to diurnal observed visiting various types of fruits. We focused on animals (with the exception of bats, which have been mammalian frugivores, and so selected 10 large fleshy relatively well studied (Thomas 1984; Banack 1998; Eby fruit species belonging to nine families representative of 1998). This bias is the result of methodological limita- different strata of the forest (Table 1). The trees selected tions. varied in height from approximately 20 m to 40 m, and Using traditional observational methods, it has been in fruit color, pulp type, and size (18.4–137.0 mm3) and difficult to study animals, particularly in tropical forests, weight (3.9–328.5 g). Fruit type was defined following technological developments, however, such as automatic Bell (1991) and the color of the external surface was cameras, are helping to overcome these limitations (e.g. used to categorize the color of the fruit. However, for Miura et al. 1997; Yasuda 1998). Miura et al.’s (1997) dehiscent fruits the color of the external surface of the and Yasuda’s (1998) studies pioneered such techniques edible part was used. in Asian tropical forests, but focussed on ground dwell- To identify fruit consumers, wooden platforms were ing species. This research, also using automatic cam- set on branches in the study tree, and fully ripened fruits eras, therefore aimed to expand studies of frugivores into harvested from the same tree were placed in a clump on the arboreal layers of a tropical forest in Sri Lanka. This the platform. Only one fruit species was used per fruit study also aimed to describe differences of fruit types, clump. The number of fruits placed on the platform which might affect fruit users, and so contribute to a varied according to the fruit size (Table 2). better understanding of frugivory in the tropical forest. Automatic camera systems (Marif Co., Japan) were used for recording visitors. These consisted of an auto- Methods matic camera with a built-in far-infrared sensors and auto-quartz timepieces to record the time of animal Fieldwork was carried out in the Sinharaja tropical visits. Cameras were placed 15–20 m up on the trunks rain forest in Sri Lanka during two periods: from June or branches of selected trees. Cameras were automati- 2000 to January 2001, and from July to December 2001. cally triggered by the far-infrared rays radiated by ani- The 88 km2 Sinharaja forest consists of natural and mod- mals visiting fruit. If an animal remained at the fruit,

*To whom correspondence should be addressed. Present address: c/o The University Museum, the University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan. E-mail: [email protected] 162 Mammal Study 28 (2003)

Table 1. Fruit species used in the study and their fruit characteristics.

Species Family Fruit type Colour Protection Pulp type Fresh weight (g) Seed size (mm3) Artocarpus nobilis Moraceae compound brown thick husk juicy fibrous 287.7 13.6 Coscinium fenestratum Menispermaceae drupe brown thick husk juicy soft 5.2 17.1 Cullenia ceylanica Bombacaceae schizocarp white no aril 69.5 20.8 Cullenia rosayroana Bombacaceae schizocarp white no aril 328.5 28.0 Diospyros racemosa Ebenaceae drupe green no juicy fibrous 11.2 15.2 Dysoxylum ficiforme Meliaceae drupe brown thin husk juicy soft 10.5 16.7 Garcinia hermonii Clusiaceae drupe green no less juicy fibrous 115.2 27.2 Myristica dactyloides Myristicacea schizocarp orange no aril 28.7 24.3 Podadenia thwaitesii Euphorbiaceae drupe green thick husk juicy soft 21.5 17.6 Semecarpus walkeri Anacardiaceae achine red no less juicy fibrous 3.0 10.1

Table 2. Number of fruits and duration of the experiment. (rats and mice), were recorded making 479 visits to fruit Experiment duration during the study period (Table 3). Nine taxa were identi- Fruit species Number of bait fruits (days) fied to the species level and one was identified to the Artocarpus nobilis 516genus level. It was difficult, or impossible, to identify Coscinium fenestratum 35 12 murids, bats, and loris even to the generic level. Since Cullenia ceylanica 715bats visited fruit baits, it is likely that they were fruit Cullenia rosayroana 322bats, but there remains the possibility that other bats also Diospyros racemosa 40 12 visited opportunistically. It is also known that two loris Dysoxylum ficiforme 40 21 species belonging to the genera Loris and Nycticebus Garcinia hermonii 34 15 occur in the area, but we were unable to identify them Myristica dactyloides 30 26 from photographs. Among the animals recorded, eight Podadenia thwaitesii 20 14 were mammals (four species of Rodentia, two Primates, Semecarpus walkeri 50 12 one Carnivora, one Chiroptera) and four were birds (Table 3). Miura et al. (1997) have previously recorded the camera was triggered every five seconds. all of these animal groups on the ground in Pasoh forest The cameras were set in the morning and checked at in peninsula Malaysia, which suggests that these animals an interval of two to three days to minimize human dis- move between arboreal layers and the ground. They turbance. The numbers of fruits eaten were recorded, reported 35 animal species. Only the loris (species and fruits damaged by insects or pathogens, or consumed unidentified) was newly recorded during this study as a by animals, were replaced with new ones. Data were nocturnal arboreal frugivore. collected continuously over two to three weeks per fruit species (Table 2) and at least two rolls of film (24 shots Timing of visits per roll) were used per fruit species in each selected tree. Our study was able to reveal not only diurnal animals One photograph was considered to represent one visit. but also nocturnal animals visiting fruit (Table 3). Because the duration of the experiment differed among Among the animals recorded, seven species visited fruits the fruit species (Table 2), frequency of visits was during daytime, and the others (4 species and murids) expressed per day to avoid this bias. The animals at night. The major diurnal visitors were: the western recorded were identified according to Kotagama and purple–faced leaf monkey Trachypithecus vetulus, the Karunarathna (1983) and Kotagama and Fernando western giant squirrel Ratufa macroura melanochra, the (1994). Sri Lanka mynah Gracula ptilogenys, and the Sri Lanka grey hornbill Ocyceros gingalensis (Table 3). The Results and discussion major nocturnal visitors were: the small flying squirrel Petynomys fuscocapillus layardi and a bat (Table 3). Visitor composition Five fruit species, Artocarpus nobilis, Coscinium fenes- A total of twelve different taxa were identified, and in tratum, Cullenia rosayroana, Diospyros racemosa, and addition several unidentified species of murid rodents Semecarpus walkeri were visited during both day and Jayasekara et al., Frugivores in a Sri Lankan forest 163

Table 3. List of frugivore species taken by automatic cameras. * bold letters show nocturnal visits, and plain letters show diurnal visits.

Group Common name Abbreviations Scientific name Number of visits Rodentia Murids Murid 28 Jungle squirrel J. squirrel Funambulus sublineatus obscurus 21 Western giant squirrel G. squirrel Ratufa macroura melanochra 65 Small flying squirrel F. squirrel Petynomys fuscocapillus layardi 88 Primates Purple face leaf monkey L. monkey Trachypithecus vetulus 90 Loris Loris Loris sp. or Nycticebus sp. 19 Chiroptera Bats Bat 41 Carnivora Golden palm civet G. civet Paradoxurus zeylonensis 9 Mammal total 361 Birds Sri Lanka mynah Mynah Gracula ptilogenys 60 Sri Lanka grey hornbill Hornbill Ocyceros gingalensis 40 Ashy headed laughing thrush Thrush Garrulax cinereifrons 9 Sri Lanka orange billed babbler Babbler Turdoides rufescens 9 Bird total 118 Grand total 479

Table 4. Frequency of visit (/day) to each fruit by each frugivores. See Table 3 for animal name abbreviations.

Fruit species Murid J. squirrel F. squirrel G. squirrel L. monkey G. civet Loris Bat Mynah Hornbill Babbler Thrush Total Artocarpus nobilis —— — 1.5— 1 1—————3 Coscinium fenestratum 1.5— — 3 — ———————2 Cullenia ceylanica —— 1 — — ——1.4————2 Cullenia rosayroana — — 3 — 1 — 0.5 — — — 0.4 0.4 5 Diospyros racemosa — 0.9 — — 1.1 — — 1.5 — — — — 3 Dysoxylum ficiforme —— — — 2.4———————1 Garcinia hermonii 0.9— — — — ———————1 Myristica dactyloides —— — — — ———2.31.5——2 Podadenia thwaitesii —— — — 1.1———————1 Semecarpus walkeri — 1 1.3— — ———————2 Number of species visited 2 2 3 2 4 1 2 2 1 1 1 1 Number of visits 2.4 2 5.3 4.5 5.6 1 1.5 2.9 2.3 1.5 0.4 0.4 night. The fruits of Dysoxylum ficiforme, Myristica rus zeylonensis, a member of the Carnivora, also visited dactyloides, and Podadenia thwaitesii were visited only the fruits, indicating that they are omnivorous (see also during daytime, while those of Cullenia ceylanica and Boonsong and McNeely 1988; Miura et al. 1997). Two Garcinia hermonii were visited only at night. species of insectivorous birds, the ashy headed laughing thrush Garrulax cinereifrons and the Sri Lanka orange- Dominant animal species billed babbler Turdoides rufescens also visited the fruits, Mammals accounted for 361 of the 479 visits to fruit suggesting that they consume fruits opportunistically. (Table 3), and most of these (243 of 361) were made by leaf monkeys, flying squirrels, and giant squirrels. Birds Fruit preferences made fewer visits than mammals, presumably because The leaf monkey visited four fruit species, but made the fruits we used were large, and only two species (the most visits to Dysoxylum ficiforme (Table 4). The fruit mynah and the hornbill) accounted for most of the visits of D. ficiforme is brown, and contains juicy, soft pulp, (100 of 118). and has fruit protection (Table 1). Fruits with such It is noteworthy that the golden palm civet Paradoxu- characters are known as typical monkey-preferred fruits 164 Mammal Study 28 (2003)

(Gautier-Hion et al. 1985). The flying squirrel visited likely to be biased and misleading without due consider- three fruit species (Cullenia rosayroana, Cullenia ation of nocturnal animals. ceylanica, and Semecarpus walkeri), but visited C. rosayroana most frequently (Table 4). Acknowledgments: We are grateful to the Forest Depart- Murids visited two fruit species, Coscinium fenestra- ment of Sri Lanka, for granting permission to work in tum and Garcinia hermonii, both of which contained the Sinharaja forest. The Forest Department Office of relatively small amounts of pulp. The giant squirrel, the the Sinharaja forest reserve supported us in numerous dusky-striped jungle squirrel Funambulus sublineatus ways. Professors I. A. U. N. Gunatilleke and C. V. S. obscurus and a loris species visited fruits with very dif- Gunatilleke at Peradeniya University gave many valu- ferent characters. For example, the giant squirrel visited able suggestions and advice. Without Mr. Rupasinghe’s both Artocarpus nobilis and Coscinium fenestratum tree climbing to set cameras in the canopy layer, this (Table 4). A. nobilis produces large compound fruit with study would have been impossible. Dr. M. Yasuda large amounts of juicy fibrous pulp, while C. fenestratum advised us on automatic camera mechanics. Professor produces small drupes with very little juicy, soft pulp T. Kikuchi of Yokohama National University, and Pro- (Table 1). Thus the giant squirrel chooses widely fessor H. Koizumi of Gifu University encouraged us varying fruit types. The jungle squirrel visited both throughout this study. We also thank Dr. Monika Diospyros racemosa and Semecarpus walkeri, and it Shaffer-Fehre, Dr. Mark Carine, and Dr. Mark A. Brazil seems that both the jungle squirrel and the loris species for helpful comments on the manuscript. This study was take widely varying fruit types. partly supported by the Nagao Foundation (Japan) and Among the birds, both the mynah and the hornbill the Centre for International Development at Harvard visited specifically Myristica dactyloides. The aril of University, USA. which is bright orange. Such colorful fruits are known as typical bird preferred fruits (Knight and Siegfried 1983). References Cullenia rosayroana was visited by five different frugivores (Table 4). It produces dehiscent fruits that Banack, S. A. 1998. Diet selection and resource use by flying foxes seem easier to handle and eat for animals that have (Genus Pteropus). Ecology 79: 1949–1967. Bell, A. D. 1991. Plant Form: An Illustrated Guide to Flowering Plant neither special morphology nor skills. This type of fruit Morphology. Oxford Univ. Press, Oxford, 341 pp. may be used by various frugivores, thus it is a generalist Boonsong, L. and McNeely, J. A. 1988. Mammals of Thailand. Saha in terms of attracting frugivores. Karn Bhaet, Co., Bangkok, 758 pp. Dew, L. J. and Wright, P. 1998. Frugivory and seed dispersal by By contrast, Dysoxylum ficiforme, Podadenia thwait- four species of primates in Madagascar’s eastern rain forest. esii, and Garcinia hermonii were visited by a limited Biotropica 30: 425–437. numbers of animals. Dysoxylum ficiforme and P. thwait- De Zoysa, N. and Raheem, R. 1990. Siharaja: A Rain Forest in Sri esii were visited only by the leaf monkey, and Garcinia Lanka. March for Conservation. Colombo, Sri Lanka, 61 pp. Eby, P. 1998. An analysis of diet specialization in frugivorous hermonii was visited only by murids (Table 4). They are Pteropus poliocephalus (Megachiroptera) in Australian subtropical specialists in attracting frugivores. It is likely that pro- rainforest. Australian Journal of Ecology 23: 443–456. tection of D. ficiforme, for example, limits visitors other Fleming, T. H. 1979. Do tropical frugivores compete for food? American Zoology 19: 1157–1172. than leaf monkeys, which have strong fingernails, and Gautier-Hion, A., Duplanter, J.-M., Quris, R., Feer, F., Sourd, C., these fruit characters attract particular animals that have Decoux, J.-P, Dubost, G., Emmons, L., Erard, C., Hecketsweiler, special morphology or skills to consume them (Turner P., Moungazi, A., Roussilhon, C. and Thiollay, J.-M. 1985. Fruit 2001). However, the functional aspects of these fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324–337. characters are mostly unknown. Gunatilleke, I. A. U. N. and Gunatilleke, C. V. S. 1996. Sinharaja World Heritage Site. Sri Lanka. Natural Resources and Science Authority of Sri Lanka 47/5 Maitland place, Colombo 7, 22 pp. Conclusions Harrison, J. L. 1962. The distribution of feeding habits among animals in a tropical rain forest. Journal of Animal Ecology 31: The present study has confirmed that a considerable 53–63. number of species of frugivores may be active in the Knight, R. S. and Siegfried, W. R. 1983. Inter-relationships between arboreal layers in tropical forests at night as well as type, size and color of fruits and dispersal in Southern African trees. Oecologia 56: 405–412. during daytime. Clearly, conclusions concerning the Kotagama, S. W. and Fernando, P. 1994. A Field Guide to the Birds arboreal frugivore community of a tropical forest are of Sri Lanka. Wildlife Heritage Trust of Sri Lanka, 95 Cotta Jayasekara et al., Frugivores in a Sri Lankan forest 165

Road, Colombo 8, Sri Lanka, 224 pp. Turner, I. M. 2001. The Ecology of Trees in the Tropical Rain Forest. Kotagama, S. W. and Karunarathna, G. P. B. 1983. Checklist of the Cambridge University Press, Cambridge, 298 pp. mammals (Mammalia) of the Sinharaja MAB Reserve, Sri Lanka. Wrangham, R. W., Chapman, C. and Chapman, L. J. 1994. Seed Forester 16: 29–25. dispersal by forest chimpanzee in Uganda. Journal of Tropical Miura, S., Yasuda, M. and Ratnam, L. C. 1997. Who steals the fruits? Ecology 10: 355–368. Monitoring frugivory of mammals in a tropical rain forest. Yasuda, M. 1998. Community ecology of small mammals in a tropi- Malayan Nature Journal 50: 183–193. cal rain forest of Malaysia with special reference to habitat prefer- Terborgh, J. 1990. Seed and fruit dispersal – commentary. In (K. S. ence, frugivory and population dynamics. Ph D Thesis, Graduate Bawa and M. Heandley, eds.) Reproductive Ecology of Tropical School of Agricultural and Life Sciences, The University of Tokyo. Forest Plants. Pp. 181–190. The Parthenon, Paris, France. Thomas, D. W. 1984. Fruit intake and energy budgets of frugivorous Received 5 May 2003. Accepted 16 October 2003. bats. Physiological Zoology 57: 457–467.