Ornithol Sci 8: 75–79 (2009)

SHORT COMMUNICATION Evidence of the consumption of fallen figs by Oriental Pied Anthracoceros albirostris on the ground in , Thailand

Shumpei KITAMURA1,2,#,*, Shunsuke SUZUKI3, Takakazu YUMOTO1,4, Prawat WOHANDEE5 and Pilai POONSWAD2

1 Center for Ecological Research, Kyoto University, 2-509–3, Hirano, Otsu 520–2113, Japan 2 Thailand Hornbill Project, Department of Microbiology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand 3 School of Environmental Science, The University of Shiga Prefecture, Hikone 522–8533, Japan 4 Research Institute of Humanity and Nature, Kamigamo-Motoyama 457–4, Kyoto, 603–8047, Japan 5 National Parks Division, Department of National Parks, Wildlife and Conservation, Phaholyothin Rd., Bangkok 10900, Thailand

Abstract (Bucerotidae) are large, canopy-dwelling birds in tropical ORNITHOLOGICAL forests that eat various kinds of fruits. We obtained conclusive evidence of the con- SCIENCE sumption of fallen figs Ficus stricta by Anthracoceros al- © The Ornithological Society birostris on the ground in Khao Yai National Park, Thailand, by using camera traps. of Japan 2009 At least one male Oriental Pied Hornbill was photographed removing sample figs from the ground around a fruiting . The use of cameras for the study of birds is generally impractical; however, this method can provide some useful baseline infor- mation on the behavior of certain avian species, as demonstrated in this study.

Key words Camera trapping, Feeding ecology, Ficus stricta, Moist evergreen forest

Hornbills (Bucerotidae) are the largest frugivorous ecdotal observations, it is difficult to determine ex- birds. Up to 9–10 species occur sympatrically in trop- actly what hornbills do on the ground. ical Asia. Of these, the Oriental Pied Hornbill An- In the study of wild animals, photographs not only thracoceros albirostris is one of the commonest, oc- provide confirmation of presence and identity, but curring in northern and eastern India, across South- also provide insights into species distribution, abun- east Asia, and on the Sunda Shelf islands (Kinnaird dance, population dynamics and behavior (O’Brien & & O’Brien 2007). Sympatric hornbills may partition Kinnaird 2008). Recent technological improvements resources in order to coexist if resources are limiting. have provided researchers with reasonably priced Because of its small body-size, the Oriental Pied ready-made camera traps equipped with tiny infrared- Hornbill may select different food items, differ tem- motion sensors, built-in-flash, and data packs (Swann porally in the use of resources, or forage in different et al. 2004). Camera trapping may be most appropri- strata in order to avoid competition with other sym- ate for large, ground-dwelling birds such as pheas- patric hornbill species. Asian hornbills typically for- ants, however, several studies have also unexpectedly age within the canopy, but some species including the recorded canopy-dwelling birds including hornbills Oriental Pied Hornbill has been reported descending on the ground (Dinata et al. 2008; O’Brien & Kin- to the ground to acquire food (Ali & Ripley 1987). naird 2008). Although it is difficult to determine what Because such records have usually been based on an- hornbills really do on the ground, camera trapping can be used effectively for recording such behavior (Received 16 June 2008; Accepted 16 March 2009) (O’Brien & Kinnaird 2008). # Corresponding author, E-mail: [email protected] In this study, by using camera traps, we were able * Present address: Laboratory of Animal Ecology, Department of Life Science, Faculty of Science, Rikkyo University, Nishi-Ike- to record evidence of the consumption of fallen figs bukuro 3–34–1, Toshima, Tokyo 171–8501, Japan Ficus stricta by Oriental Pied Hornbill on the ground,

75 S. KITAMURA et al. a behavior which, to our knowledge, has not previ- species that removed a particular sample could be ously been photographed in the field. identified, though several animals were either too fast or too slow to be detected by the sensor. Although METHODS fruits that were removed were not necessarily con- sumed, we assumed that most such figs were con- This study was conducted in November 2001 in sumed. Our assumption is practical. All of the animal Khao Yai National Park (14°10N, 101°20E, 780 m species recorded as removing sample figs in our above sea level), Thailand. Four species of hornbills study were previously known to be consumers of the inhabit the park: Buceros bicornis fruit of this fig species in Khao Yai (Poonswad et al. (130 cm in body length), Aceros 1998a). (Rhyticeros) undulatus (100 cm), Austen’s Brown Because the cameras were triggered every 10–15s Hornbill Anorrhinus austeni (80 cm), and Oriental while an animal or group of animals was within the Pied Hornbill (75 cm), which together consume more detectable area of the sensor, one picture does not than 80 species of fruits throughout the year. Further necessarily represent a single visit of a given animal details of the study site and resident hornbills are de- species. We regarded a picture as representing one scribed elsewhere (Poonswad et al. 2004). visit by a given species only when the picture was We installed an automatic photographic monitoring taken more than 30 minutes after the last picture of system (Sensor Camera Fieldnote; Marif Co., Ltd., the same species (O’Brien et al. 2003). Iwakuni, Yamaguchi, Japan) to monitor the animals that visited and ate fallen figs. The cameras were RESULTS equipped with built-in infrared motion sensors, built- in flashes, and data packs that stamped each photo- All sample figs in the trials disappeared from the graph with the time and date of the event. Color print feeding stations within two days. In total, we ob- film (ISO 400) was used in each camera. No photo- tained 186 photographs (74 [39.8%] from the East graphic delay interval was available for the model and 112 [60.2%] from the West). Of these, 166 pho- used. If an animal or a group of animals remained tographs included eight mammal species and three at the site, the camera was triggered every 10–15 s. bird species (Table 1), and the reminder contained no Each camera was wrapped tightly in a transparent images of any animals. From these photographs, two polypropylene bag for waterproofing and then en- species of animals, Oriental Pied Hornbill and Vari- cased in an open plastic box. able Squirrel Callosciurus finlaysoni were confirmed Camera trapping was conducted for 10 days be- to have removed sample figs (11 times and once, re- tween 18 and 27 November 2001 at sites baited with spectively). At least one male Oriental Pied Hornbill fallen fruits. Fallen fruits (mean weight 2.81.0 SD was observed removing sample figs from the ground g, N40) were collected from under a fruiting fig (Fig. 1). The activity period of Oriental Pied Horn- tree Ficus stricta (Miq.) Miq. situated along the for- est trail from Darn Chang to Bueng Phai. During each trial, 10 of these fruits were placed at feeding stations in the morning (ca. 0900 local time). As the crown area of this fig tree was very large, we estab- lished two feeding stations beneath the tree in order to be able to photograph visiting animals effectively. One feeding station was placed under the eastern edge of the tree’s crown (East), and the other was placed under the western edge (West). This camera system allowed us to monitor fruit consumption by animals on a 24-hour basis (Yasuda 2004). Decreases in the number of samples and the number of frames of film per day were recorded until no samples re- mained. After the samples had disappeared, the trials were repeated throughout the study period. From the Fig. 1. A male Oriental Pied Hornbill taking a fallen fig in photographs taken by the camera system, the animal moist evergreen forest, Khao Yai National Park, Thailand.

76 Consumption of fallen figs by Oriental Pied Hornbill

Table 1. Numbers of photographs of animal species obtained by camera traps at fallen figs Ficus stricta in Khao Yai National Park, Thailand. Species are listed in order of decreasing numbers of photographs. Note that percentages in parentheses may not add up to 100 due to rounding.

Species Common name No. of photographs (%) No. of independent visits (%)

Aves Anthracoceros albirostris Oriental Pied Hornbill 99 (53.2) 26 (40.0) Lophura diardi Siamese Fireback 20 (10.8) 12 (18.5) Gallus gallus Red Junglefowl 2 (1.1) 1 (1.5) Mammalia Callosciurus finlaysoni Variable Squirrel 23 (12.4) 10 (15.4) Maxomys surifer Yellow Rajah Rat 6 (3.2) 6 (9.2) Niviventer fulvescens Chestnut Rat 5 (2.7) 5 (7.7) Hystrix brachyura 4 (2.2) 1 (1.5) Muntiacus muntjak Common Barking Deer 3 (1.6) 1 (1.5) Tragulus kanchil Lesser Mousedeer 2 (1.1) 1 (1.5) Macaca nemestrina Pig-tailed Macaque 1 (0.5) 1 (1.5) Menetes berdemorei Indochinese Ground Squirrel 1 (0.5) 1 (1.5) No images of any animals 20 (10.8)

Total 186 (100.0) 65 (100.0)

bill, as determined from the time of the photographs, Therefore, compared with other species of hornbills ranged from 0847 to 1531 and peaked during the in Khao Yai, the Oriental Pied Hornbill has a rela- morning from 0930 to 1230 (62% of all photo- tively high potential to descend to the ground to eat graphs). fallen fruits. During intensive observations of fruit consumption DISCUSSION of the same fig tree in August 1999, fallen fig con- sumption by hornbills was not observed (Y. Kan- Camera trapping confirmed that the Oriental Pied bayashi unpublished data). Similarly, long-term ob- Hornbill consumed fruit that had fallen to the ground servations of fig consumers between June 1992 and around a fig tree. Although we did not conduct de- December 1993 (869 h) in the canopy as well as on tailed observation of fig consumption by hornbills in the ground in Khao Yai did not record any hornbills the canopy of the focal tree, all four species of horn- on the ground (Poonswad et al. 1998a). In a seed dis- bills were frequently observed eating figs. Of these persal study of large-seeded , spectabilis species, Great, Wreathed and Oriental Pied Hornbill from May to June in 2001 and 2002 (178 camera- have been reported to descend to the ground to days) and Canarium euphyllum from November to acquire food (Kemp 2001), however Great and December in 2000 and from September to November Wreathed Hornbill mostly forage in upper canopy in 2001 (175 camera-days) on the ground in Khao levels (Datta & Rawat 2003). Like Great and Yai, hornbills were never observed (Kitamura et al. Wreathed Hornbills, the main diet of the Oriental 2004; Kitamura et al. 2006). In addition, intensive Pied Hornbill consists of figs, but it also consumes a studies of fallen fruit consumption by terrestrial fru- wide range of terrestrial animals including scorpions, givores including the same fig species as in this study fish, and aquatic snails (Poonswad et al. 1998b). Fur- between July 2000 and June 2002 in Khao Yai did thermore, the Oriental Pied Hornbill is the only not include hornbills (Suzuki et al. 2006). Consider- species of hornbill in Khao Yai that uses mud (ob- ing our current results, the consumption of fallen tained from the ground) to seal its nest cavity en- fruits by hornbills must occur very rarely in Khao trance during the breeding season (Poonswad 1993). Yai, even for the Oriental Pied Hornbill. It has also been observed retrieving cicada ‘chim- One reason that this rare behavior was pho- neys’ (consisting of mud) from the ground for sealing tographed only during our study may be linked to the nest entrances (Pilai Poonswad personal observation). availability of fruit resources in November 2001.

77 S. KITAMURA et al.

Based on a long-term study of fruiting phenology at sity Press, Delhi. the community level in Khao Yai, our study period Datta A & Rawat GS (2003) Foraging patterns of sym- encompassed the second poorest fruit availability patric hornbills during the nonbreeding season in from 1996 to 2003 (Plongmai et al. 2007). Various , northeast India. Biotropica 35: groups of frugivores visited this fig tree during the 208–218. study period and most of the ripe figs in the canopy Dinata Y, Nugroho A, Haidir IA & Linkie M (2008) were consumed very quickly throughout the morning. Camera trapping rare and threatened avifauna in Dominance hierarchies at fruiting trees are governed west-central . Bird Conserv Int 18: 30–37. by a mass of frugivores, regardless of taxonomic af- French AR & Smith TB (2005) Importance of body size filiation (French & Smith 2005). The Oriental Pied in determining dominance hierarchies among diverse tropical frugivores. Biotropica 37: 96–101. Hornbill may also have been chased out of the Kemp AC (2001) Family Bucerotidae (Hornbills). In: canopy by fruit competitors, such as other larger del Hoyo J, Elliott A & Sargatal J (eds) Handbook of hornbills and primates (e.g. Pig-tailed Macaque the Birds of the World. Vol. 6. Mousebirds to Horn- Macaca nemestrina Hylo- and White-handed Gibbon bills. pp 436–520. Lynx Edicions, Barcelona. bates lar). Because most of the photographs of Orien- Kinnaird MF & O’Brien TG (2007) The ecology and tal Pied Hornbill were taken between 0930 and 1230, conservation of Asian hornbills: farmers of the forest. this species likely descends to the ground after the University Of Chicago Press, Chicago. disappearance of ripe figs from the canopy. As the Kitamura S, Suzuki S, Yumoto T, Poonswad P, Chuailua home range size of the Oriental Pied Hornbill (up to P, Plongmai K, Maruhashi T, Noma N & Suckasam C 2 15 km ) is much smaller than those of other sympatric (2006) Dispersal of Canarium euphyllum (Burser- hornbills in Khao Yai (Poonswad & Tsuji 1994), it aceae), a large-seeded tree species, in a moist ever- must display a higher degree of flexibility in the ex- green forest in Thailand. J Trop Ecol 22: 137–146. ploitation of food resources that other hornbills rarely Kitamura S, Suzuki S, Yumoto T, Poonswad P, Chuailua use. P, Plongmai K, Noma N, Maruhashi T & Suckasam C In most cases, the use of camera trapping solely for (2004) Dispersal of Aglaia spectabilis, a large-seeded the study of birds is impractical (Mohd-Azlan & tree species in a moist evergreen forest in Thailand. J Davison 2006); however, camera trapping can pro- Trop Ecol 20: 421–427. vide some useful information on the behavior of birds Mohd-Azlan J & Davison GWH (2006) Camera trap- and offer great potential for improving our under- ping as a tool to study ground dwelling birds? Malay standing of avian ecology in tropical forests. Nat J 57: 359–368. O’Brien TG & Kinnaird MF (2008) A picture is worth a thousand words: the application of camera trapping to ACKNOWLEDGEMENTS the study of birds. Bird Conserv Int 18: S144–S162. We are grateful to the National Research Council of Thai- O’Brien TG, Kinnaird MF & Wibisono HT (2003) land and the National Park Division of the Royal Forest De- Crouching tigers, hidden prey: Sumatran tiger and partment of Thailand, for granting us permission to conduct prey populations in a tropical forest landscape. Anim the study in Khao Yai. We extend our cordially thanks to the Conserv 6: 131–139. staff at Khao Yai. We thank T. Maruhashi, N. Noma, B. Plongmai K, Savini C, Poonswad P, Chuailua P, Kita- Saengthong, S. Chuailua, S. Nakkuntod, S. Sanguanchat, N. mura S & Wohandee P (2007) Nesting and flocking Jirawatkavi and all staff of the Hornbill Project for supporting behaviour in relation to phenology of non-fig hornbill our field work as well as their kind encouragement and hospi- food at Khao Yai National Park, Thailand. In: tality. We are also grateful to two anonymous reviewers who Kemp AC & Kemp MI (eds) The Active Management suggested useful improvements. We also thank Mahidol Uni- versity for general support. This research is partly supported of Hornbills and their Habitats for Conservation: by a Research Fund of the Japan Society for the Promotion of CD-ROM Proceedings of the 4th International Horn- Science (#1357006) and JSPS Research Fellowships for bill Conference. pp 371–380. Mabula Game Lodge, Young Scientists (DC1) for S. Kitamura. Bela Bela. Poonswad P (1993) Comparative ecology of sympatric hornbills (Bucerotidae) in Thailand. PhD Thesis. REFERENCES Osaka City University, Osaka. Poonswad P, Chuailua P, Plongmai K & Nakkuntod S Ali S & Ripley SD (1987) Compact handbook of the (1998a) Phenology of some Ficus species and utiliza- birds of Indian and Pakistan, 2 edn. Oxford Univer- tion of Ficus sources in Khao Yai National Park,

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