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’ as either in the forest in Tabin or local markets. Because Nephelium lappaceum, Nephelium rambutan-ake, or cultivated- rambutan fruits in the markets were larger Aglaia grandis in Tabin (Y. Nakashima, pers. obs.) than wild ones, we only selected the fruits whose fruit/ seed size was similar to wild ones when we fed them. Seed-handling and retention time To confirm the seed-handling methods of civets and Movement patterns and home ranges macaques, we fed the captive adult individuals rambutan The activity of the wild common palm civets was tracked fruits and observed their feeding behavior. The with radio-telemetry from December 2007 to December observations were conducted in August 2007 on the 2008 to determine their movement patterns. Seven Sandakan Crocodile Farm, where three adult common individuals (4 males and 3 females) were captured and palm civets (1 male, 2 females), one group of long-tailed fitted with radio collars (M2940B, Advanced Telemetry macaques (2 males, 2 females, and 1 infant) and pig-tailed Systems, inc, USA). Three individuals were captured in macaques (2 males and 2 females, 1 sub-adult, and 1 the Virgin Jungle Reserve (74 ha), where a small patch of infant) are kept in 2.0 × 3.0 × 2.3 m cages. N. lappaceum primary forest remains, one was captured near the oil fruit have a 3-4 cm indehiscent rind with soft hair (2-3 cm palm plantation, and three were captured near a gravel long) containing one arillate seed (25.0 × 15.2 × road. The mean collar weights were about 60 g, which is 10.1mm). The aril is firmly attached to the seeds and only 2.1- 3.5% of the animal body weights. The location of cannot be easily removed. In each feeding trial, we the radio-collared civets was estimated by triangulating randomly selected one focal macaque and civet from the bearings obtained by observers positioned at GPS adults in the cages and fed the former three rambutan (Garmin 76 CsX) mapping stations using receivers and fruits and the latter one fruit. We recorded the seed- hand-held two-element Yagi antennas (ATS3EL, Advanced handling methods and seed retention time. The seed- Telemetry Systems, inc, USA). Because we tried to handling methods were categorized into three criteria: approach in the tracking individuals as much as possible, swallow/spit/discard.‘ Spit’ means that the focal animals the error distance was relatively short (ca 15 m). spat out the seeds or discarded them by hands at least In preliminary research, radio-tagged individuals once putting them into their mouths or cheek pouches. were located every 30 minutes during two four-hour ‘Discard’ means they discarded the seed by hands after periods for each individual (2000 h to 2400 h). These data they consumed the fleshy parts in front of the mouth indicated that civet movement was slow, and they did not without putting the seeds into their mouths. Seed come back to the same place at least during two hours. In retention time was defined as the time the animals held the main tracking, radio-tagged individuals were located the fruits in their mouths or hands until they dropped or every two hours. Tracking was done from 1600 h to 0800 defecated the seeds. The final seed condition (broken/ h, after the civet was confirmed to be strictly nocturnal. not-broken) was also recorded. Seeds spat out or Civet location was estimated by triangulation using LOAS defecated by the civets or macaques were retrieved and (Ecological Software Solution, Inc., Sacramento, placed in Petri dishes containing moist filter paper to California). Cumulative ranges were analyzed using 95% confirm their germinability. The germination process was minimum convex polygon (MCP) methods (Mohr 1947) monitored at least once a week until seeds had and a 95% fixed kernel estimator (FK) with the Animal germinated, or seed death was obvious. Movement Extension (Hooge and Eichenlaub, 2000)) of For the civets, we also observed seed-handling Arc View® (version 3.2, Environmental systems Research methods and measured the seed retention time of four Institute, Inc., Redlands, California). To assume location wild individuals captured with local traps. These independency, locations obtained from continuous- individuals were only fed one complete fruit and only aril tracking data were not used for home range analysis. removed from the 20 fruits with water. We waited until the animals were satiated or for a maximum of 15 min of Estimation of dispersal distances feeding (Westcott et al. 2005). Feces deposited in the Dispersal kernels generated by common palm civets were holding cages were checked for seed presence at 15- estimated using movement data and seed retention time 224 Yoshihiro NAKASHIMA and Jumrafiha Abd. SUKOR

Table 1. Seed-handling methods for Nephelium lappaceum and seed retention time of Macaca fascicularis, M. nemestrina and Paradoxurus hermaphroditus in captive individuals. Seed retention time Seed-handlings Seed fate N of (mean ± SD) Species fruits Spit out (cheek b Spat or Swallow a Discard Not broken Broken Swallow pouch ) discarded 93 ± 39 Macaca fascicularis 30 0 19 (0) 11 28 2 - seconds 157 ± 74 M. nemestrina 30 0 25 (12) 5 24 6 - seconds Paradoxurus 155 ± 69 82 ± 21 30 20 10 0 30 0 hermaproditus minutes seconds aNumber of fruits stored in their cheek pouch. bDiscarded by hand after eating fleshy arils in front of mouth without inserting seeds.

Fig. 1. The seed retention time of common palm civets (Paradoxurus hermaphroditus) in their gut. Fifteen times trials were conducted both for males (3 individuals) and females (4 individuals). The mean retention time was 2.6 ± 1.1 h (mean ± SD).

Fig. 2. The estimated dispersal kernel of rambutan generated by common palm civets (Paradoxurus hermaphroditus) in Tabin Wildlife Reserve, Sabah, Malaysia. The dispersal kernel was estimated by combining data on frugivore movements and gut passage rates of seeds. Importance of Common palm civets as a long-distance disperser 225

Table 2. Home range size (ha) of Paradoxurus hermaphroditus in the Tabin Wildlife Reserve, Sabah, Malaysia.

b Home range (ha) a Travel distance (m) ID Sex Weight (kg) N of total locations Tracking times (mean ± SD) MCP (95%) Kernel (95%)

M525 M 1.8 142 43 50 5 1371 ± 541

M380 M 2.6 162 177 127 7 1500 ± 631

M345 M 2.1 191 50 73 12 1095 ± 295

M320 M 2.8 192 145 64 7 1297 ± 349

F543 F 1.8 257 35 30 14 1242 ± 161

F480 F 1.7 117 12 19 5 614 ± 194

F420 F 2.1 201 27 33 8 849 ± 230 aTravel distance (m) was the distance in which focal animals traveled during our trackings (1600h to 0800 h). bFor home range analysis, continuous-tracking data were not used to assume data independency.

in their guts following a method similar to Murray (1998) fleshy parts (19 fruits). Even when three fruits were and Holbrook and Smith (2000). First, we estimated the given at the same time, the focal individual consumed the distances from each estimated location to subsequent fruits one by one; they did not store fruits in their cheek every two- hour locations with Arc View®. Using the pouches any one time. Their seed retention time was minimum distance between the origin and each location short, only 93 ± 39 seconds. The pig-tailed macaques recorded for a given time interval, we calculated the also often did the same feeding behavior as the long-tailed probability that a civet would be in each of the following macaques: discarded seeds by hand (5 fruits) or put them distance categories: <100, 200, 300, 400, 500, 600, 700, > into their mouths and spat them out (25 fruits). However, 800. The probabilities of seed deposition within each unlike the long-tailed macaques, the pig-tailed macaques distance category were then summed over all time often stored fruits in their cheek pouches (12 times) after intervals to yield dispersal kernel. The final calculation is: removing the inedible rinds by hand, removed the fruit pd = ∑(adt*bt) individually from their mouths and consumed the fleshy where p = the probability of a seed being deposited aril while holding it in their hands. As a result, the mean at a particular distance category (d) from the parent tree, retention time was 157 ± 74 seconds, significantly longer a = the probability of a civet being within a particular than the long-tailed macaques (Mann-Whitney U-test: U = distance category (d) in time interval (t), and b = the 6,430,000, P = 0.05) with the longest time (312 seconds). probability of a seed being passed in that time interval. Neither macaques swallowed the rambutan seeds, We then plotted p against distance to give the probability although they sometimes masticated and destroyed them of seed deposition at 100-m intervals. Because it was (2 times for the long-tailed, 6 times for the pig-tailed). difficult to track the activity of this nocturnal animal so In contrast to the macaques, the civets often frequently, data of the same sex were combined and swallowed the rambutan fruits after removing of the fruit dispersal distances were estimated for each sex. rind by mastication (30 times), although they also spat out intact seeds (10 times) (Table 1). The mean seed retention time in their gut was 2.6 ± 1.2 h (mean ± SD); RESULTS 6.16 h was the longest time and 0.83 h was the shortest Seed-handlings and retention time time (Fig. 1). There was no significant difference between In total, we fed 30 fruits for the two species of macaques sexes in gut retention time (Mann-Whitney U-test: U = and 40 fruits for common palm civets. Seed-handlings 2,690,230, P = 0.84). The seed retention time was only 82 varied from species to species (Table 1). Long-tailed ± 21 seconds when the seeds were spat out. macaques ate the fleshy parts in front of their mouths The seeds spat out by the macaques or ingested by first (all 30 fruits) and discarded the seeds by hand (11 the civets had different germinability. Germination fruits) or put them in their mouths after consuming the probability was significantly higher in the seeds ingested 226 Yoshihiro NAKASHIMA and Jumrafiha Abd. SUKOR by the civets (85 %, n = 20) than the seeds spat out by removed them from their mouths and put them back in to macaques (40 %, n = 20) (Fisher’s Exact Test, P = 0.008). completely remove the fleshy parts from the seeds. If we had fed them more rambutans, the macaques might have Home ranges and movement patterns discarded the seeds sooner and consumed new fruits We conducted 5 to 14 times continuous trackings for each without the great effort to remove the fleshy parts. Thus, individual (Table 2) whose activity began at dusk our estimation time may not always accurately represent (17:30-18:00) and ended at dawn (4:30-6:00). The mean the time spent in the fruiting tree in the wild, where fruits travel distance per night was relatively long, 1258 ± 362 are much more abundant. m (mean ± SD) in males and 857 ± 327 m in females; The second point, however, suggests that pig-tailed and there was a significant difference between sexes macaques may hold seeds for several minutes even in the (Mann-Whitney U-test: U = 211, P = 0.003). wild, enabling them to move some distance from the In total, 117-257 locations were obtained per parent tree. Different from long-tailed macaques, pig- individual, and 82-159 locations were used for the home tailed macaques stored the rambutan fruits in their cheek range analysis (Table 2). The mean home range size was pouches. Although their movements during such times 69.9 ± 64.1 ha (mean ± SD, n = 7) in a 95% minimum are also likely to be affected by the abundance of available convex polygon and 56.8 ± 36.5 ha (mean ± SD, n = 7) fruits, some studies on similar-bodied macaques, the in the 95% kernel methods. Males have significantly Japanese macaques (M. fuscata yakui), showed that seeds larger home ranges (103.8 ± 67.4 ha, n = 4) than females held in cheek pouches are often dispersed over several (78.5 ± 33 ha, n = 3) (Mann-Whitney U-test: U = 8,946, P tens of meters (Yumoto et al. 1999; Tsujino and Yumoto, < 0.0001). 2009). Pig-tailed macaques have large cheek pouches, so their contribution to the dispersal of large-seeded plants Dispersal kernels may be greater than expected, Lucas and Corlett (1998) We confirmed that civets disperse seeds over several wrote that“macaques are probably best viewed as fruit hundred meters when they swallow them (Fig. 2). The thieves rather than mutualists”. mean estimated dispersal distance of all 7 individuals was Even when pig-tailed macaques carry large seeds 216 m. There was a large statistically-significant beyond the crown of the mother tree, the distance and difference between sexes in the dispersal kernel the number of dispersed seeds are necessarily limited. In (Kolmogorov-Smirnov: Z = 1.481, P = 0.0008), reflecting contrast, our first result suggests that civets can regularly the difference in their movements. The mean dispersal transport seeds beyond the mother trees. They often distance was longer in males (270 m) than in females (156 swallow fruits and hold the seeds in their guts for a m). relatively long time (2.6 h). Although we focused only on one primate fruit, rambutans, the observed difference of seed-handlings between macaques and civets is probably DISCUSSION applicable to other large-seeded plants. Lucas and Corlett Seed-handlings (1998) showed that long-tailed macaques have low Our feeding trials provided three important results; first, swallowing thresholds: They rarely swallow seeds larger there was a contrasting difference between macaques than 3 mm in seed diameter. Larger Japanese macaques and civets in seed-handlings. Civets regularly swallowed also never swallow seeds larger than 1 cm in diameter the rambutan seeds, but the two species of macaques (Otani and Shibata, 2005). In contrast, feces of common never did. Second, there was even a difference between palm civet often contained large seeds such as Aglaia the two species of macaques. The long-tailed macaques grandia (Meliaceae) (28.6 × 20.3 × 14.7mm), Arenga never stored fruits in their cheek pouches, but the pig- undulatifolia (Arecaceae) (28.0 × 19.4 × 13.6 mm) or tailed macaques often did. Third, seed retention time was Nephelium rambutan-ake (22.0 × 19.4 × 11.2 mm) in over one minute for both macaques. Tabin (Y. Nakashima, unpublished data). This indicates Concerning the third point, the relatively long that the civets have potentially higher capacity for retention time in both macaques was probably in part dispersal distance of large-seeded plants. caused by our experiment conditions and the fruit morphology of the rambutan. We fed only three rambutan Seed dispersal distance by common palm civets fruits at one time. Because the fleshy parts of rambutan Our estimation of dispersal distance showed that civets are firmly attached to the seeds, the macaques repeatedly actually disperse rambutan seeds over several hundreds Importance of Common palm civets as a long-distance disperser 227 of meters. This distance is much shorter than larger and contribute to the population persistence of large-seeded vulnerable frugivores such as Asian elephants (Campos- plants and vegetation recovery as long-distance seed Arceiz et al. 2008) or hornbills (Kinnaird and Timothy dispersal agents. 2008), but much longer than the longest distance reported in the cheek-pouch dispersal of macaques (Lucas ACKNOWLEDGEMENTS We thank EPU Malaysia, and Corlett, 1998; Yumoto et al. 1998; Tsujino and and Sabah Wildlife Department for granting us to conduct Yumoto, 2009). Other disturbance-tolerant frugivores research in Sabah, Malaysia. We are grateful to Dr. J. such as squirrels or rats may also disperse seeds in their Yamagiwa, Dr. N. Nakagawa, Dr. M. Nakamura, Dr. E. mouths, but at a maximum of several tens of meters in Inoue, Dr. G. Hanya, Dr. H. Matsubayashi, Dr. N. Kuze squirrels (Becker et al. 1985; Kitamura et al. 2008) and and Ms. M. Nakabayashi for their encouragement and rats (Yasuda, 2000; Kitamura et al. 2004).Several suggestions. This research was supported by a Research limitations of the accuracy of estimated distance arise Fund of Japan Society for the Promotion of Science, JSPS from the simplifications necessarily adopted in our study. Research Fellowships for Young Scientists for Y. N and The number of provided fruits and their captivity may by the Global COE Program A06 to Kyoto University. affect seed retention time in their gut (Campos-Arceiz et al. 2008), or the two-hour interval of locating animal positions may be too long to estimate their accurate REFERENCES movement patterns. 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Received 11th July 2009 Accepted 27th Sep. 2009