TROPICS Vol. 18 (4) Issued April 30, 2010 Importance of common palm civets (P a r a d o x u r u s hermaphroditus ) as a long-distance disperser for large- seeded plants in degraded forests ＊ Yoshihiro NAKASHIMA and Jumrafiha Abd. SUKOR Faculty of Sciences, Kyoto University, Oiwake-cho, Kitashirakawa, Sakyo-ku, 606-8502 Kyoto City, Kyoto, Japan *Corresponding author, Tel: +81-75-753-4085, Fax: +81-75-753-4115, E-mail: [email protected] ABSTRACT Information on the dispersal distance achieved by disturbance-tolerant frugivores INTRODUCTION is critical for predicting the possibility of plant Seed dispersal distances greatly influence plant species population persistence and the speed of vegetation persistence in habit fragments (Cain et al. 2000; Johst et recovery in degraded forests. We estimated the al. 2002) and on vegetation recovery after human impacts dispersal kernel of one large-seeded plant with (Wunderle, 1997). As deforestation and fragmentation ‘ primate fruits ’ rambutans (N e p h e l i u m increase, plants must migrate to survive because the lappaceum ), generated by common palm civets environments in disturbed habitats are less stable and (Paradoxurus hermaphroditus ) in the degraded more unpredictable than undisturbed habitats (Saunders forest in the Tabin Wildlife Reserve, Sabah, et al. 1991). Since seed dispersal distance determines the Malaysia. We predicted that for the dispersal potential area to which plants can migrate, such distance, civets are superior to macaques, which information is critical for predicting the possibility of are another potential disperser for large-seeded plant population persistence and the speed of vegetation ‘primates fruit’ in degraded forests. Observations recovery in degraded sites (Weir and Corlett, 2007). on feeding trials showed that the civets often Despites its importance, our knowledge of the potential swallowed seeds, but both the macaques never did. dispersal distance is limited, particularly in rainforest Thus the mean seed retention times of the civets, (Weir and Corlett, 2007). 2.6 h, were much longer than those of macaques: In fleshy-fruited plants, seed dispersal distance is 75 seconds for the long-tailed macaques and 156 largely determined by disperser foraging behavior in seconds for the pig-tailed macaques. Radio tracking fruiting trees and animal movement pattern after feeding the activity of the common palm civets (4 males and (Westcott et al. 2005). Many studies have estimated the 3 females) demonstrated that they traveled several dispersal kernels generated by particular animals by hundreds of meters during gut passage time. The combining information on frugivore movements and the estimated mean dispersal distance was 216 m. gut passage rates of seeds (Murray, 1988; Westcott et al. Male dispersed the seeds in significantly longer 2005; Weir and Corlett, 2007; Campos-Arceiz et al. 2008). distance (270 m) than female (156 m), reflecting However, these studies have concentrated on large the difference in home range size between sexes. frugivores such as hornbills (Holbrook and Smith, 2000; These results indicated that common palm civets Kinnaird and Timothy, 2008), elephants (Campos-Arceiz play an important role in the dispersal of large- et al. 2008), or primates (Yumoto et al. 1999; Russo et al. seeded plants as long-distance dispersers, probably 2006). Such large frugivores, which are highly susceptible surpassing macaques. to habitat fragmentation or hunting, have been typically rare or eliminated from disturbed habitats (Sodhi et al. Keywords: Civets; Large-seeded plants; Macaques; 2004; Cardillo et al. 2005). To determine the potential Seed dispersal; Southeast Asia dispersal distance in disturbed habitats, information on the capacity of tolerant frugivores is more important. The loss or decline of large frugivores is not likely to equally affect the dispersal distance of all plant species. 222 Yoshihiro NAKASHIMA and Jumrafiha Abd. SUKOR Recent studies showed a negative correlation between confirm this hypothesis, first, we observed the seed- seed size and the number of frugivores that consume handling behavior of captive common palm civets and two those fruits (Corlett, 1998; Kitamura et al. 2002); large- species of macaques, long-tailed (Macaca fascicularis) seeded plants rely on fewer and larger-bodied birds or and pig-tailed (M. nemestrina), and confirmed possible mammals, and small-seeded fruits can be dispersed by a differences in their seed-handling methods. Second, we wide variety of frugivores, including smaller ones. Large actually estimated the dispersal kernels generated by seeds may be discarded by hand or spat out even by large common palm civets with methods similar to Murray frugivores (Corlett, 1998). This suggests that the (1988) in the Tabin Wildlife Reserve, Sabah, Malaysia. dispersal distance of large-seeded species is more Through these investigations, we demonstrated the susceptible to change in diversity and the abundance of importance of common palm civets in the dispersal frugivores in degraded habitats. Thus, a study on the distance for large-seeded plants in degraded forests. capacity of tolerant frugivores in the dispersal of large- seeded plants has immediate priority. In the rainforests of Southeast Asia, there are some METHODS large-seeded plants whose fruits have inedible and Study site indehiscent rinds containing sugar-rich aril and large This study was conducted in the Tabin Wildlife Reserve seeds (e.g. Aglaia, Diospyros, Garcinia, Melodinus, (hereafter Tabin) from August 2007 to February 2009 in Nephelium) (Corlett, 1998). Since these fruits are the Malaysian state of Sabah on the island of Borneo. preferred and dispersed by such primates such as Tabin (5ﾟ05’ – 5ﾟ22’ N, 118ﾟ30’ – 118ﾟ55’ E) has 122,539 orangutans, gibbons, or macaques, they are called ha and is located 50 km northeast of the town of Lahad ‘primate fruits’ (Leighton and Leighton, 1984; Corlett Datu, in eastern Sabah. Tabin is almost exclusively 1998), although other mammalian frugivores also often surrounded by large agricultural areas planted with oil consume them (Leighton and Leighton, 1984). The plant palms (Elaeis guineensis). Most parts of Tabin have been species with primate fruits are most susceptible to human heavily logged and are dominated by pioneer species impact, because mammalian frugivores including such as Duabanga moluccana (L ythraceae) and primates are highly vulnerable to habitat degradation in Neolamarckia (Anthocephalus) cadamba (Rubiaceae) this region (Sodhi et al. 2004). (Mitchell 1994), except for a core area (8,616 ha) located In this study, we estimated the dispersal kernel of in central Tabin and seven other smaller Virgin Jungle one primate fruit, rambutans (Nephelium lappaceum, Reserves. Sapindaceae), generated by a tolerant but non-primate This study was conducted near the basecamp located disperser, the common palm civet (Paradoxurus on the western boundary of Tabin. The study area was hermaphroditus, Viverridae) in the Tabin Wildlife heavily logged in the 1980s at least twice (Mitchell, 1994). Reserve, Sabah, Malaysia. Civets are Old World Only a small patch of primary forest remains at Virgin Carnivora, and fruit, including primate fruit (Leighton Jungle Reserve No. 83 (74 ha) around Mud Volcano, and Leighton, 1984), is a significant component of their which is a mound of mud heaved up through overlying diet (Rabinowitz, 1991; Joshi et al. 1995; Corlett, 1998; sediments (Mitchell, 1994). The undergrowth is thick and Mudappa, 2001; Zhou et al. 2008). They swallow large dominated by tangles of climbers, giant herbs, and thorny fruits whole and defecate seeds intact (Mudappa, 2001). creepers. A comprehensive description of the natural They are also known to persist well or even thrive in vegetation in the study area is available in Mitchell (1994). human modified areas (Corlett, 1998; Corlett, 2002). As The topography in the study area was gently undulating such, civets can be regarded as potentially important at an elevation of about 120 m a.s.l. dispersers for ‘primate fruits', along with tolerant Most terrestrial megafauna remain in Tabin, such as primates, macaques in degraded forests (Corlett, 1998). Asian elephants (Elephas maximus) or Asian two-horned We focus on civets, instead of macaques, because we rhinoceros (Dicerorhinus sumatrensis), but such large hypothesized that civets are superior to macaques in the arboreal frugivores as Borneo orangutans (Pongo dispersal distance for large-seeded plants. Different from pygmaeus) or Mueller’s gibbon (Hylobates muelleri) are civets, macaques spit out large seeds or discard them by rare or not abundant around the basecamp. All seven hand (Lucas and Corlett, 1998). This seed-handling species of Viverridae inhabiting the lowlands of Borneo difference creates differences in seed retention time, have been confirmed (Rajaratnam, 2000; Yasuma and which can result in different seed dispersal distances. To Andau, 2000). The sighting frequency was highest for Importance of Common palm civets as a long-distance disperser 223 common palm civets (Paradoxurus hermaphroditus), minute intervals. These procedures were repeated followed by Malay civets (Viverra Tangalunga), and several times a night, and the captured animals were banded palm civets (Hemigalus derbyanus) (Y. released after radio collars were attached to them. Nakashima, unpublished data). Common palm civets In both feeding trials, we obtained rambutan fruits were frequently observed to eat such‘ primate fruit’