Primates (2009) 50:45–49 DOI 10.1007/s10329-008-0110-5
ORIGINAL ARTICLE
Predation on giant flying squirrels (Petaurista philippensis) by black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China Peng-fei Fan Æ Xue-long Jiang
Received: 5 December 2007 / Accepted: 14 October 2008 / Published online: 18 November 2008 Ó Japan Monkey Centre and Springer 2008
Abstract Predation on vertebrates is infrequent in gibbons. In a 14-month field study of the central Yunnan black crested gibbon (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China, we observed gibbons attacking, killing and eating giant flying squirrels (Petaurista philippensis). During 845 h of observation on one study group, the gibbons attacked giant flying squirrels 11 times, and succeeded in 4 cases. Although all members of the group attempted to attack the squirrels, all four successful attacks were made by the same adult female. The victims were infants in three cases and a juvenile or sub-adult in one case. Black crested gibbons also attacked adult giant flying squirrels by grabbing their long tails and throwing them from the canopy, but they failed to catch or kill the prey in three cases observed. Passive meat sharing occurred in three out of four successful cases. Besides hunting giant flying squirrels, the black crested gibbons also ate eggs or chicks in two birds’ nests and one lizard.
P.-f. Fan X.-l. Jiang (&) Kunming Institute of Zoology, Chinese Academy of Sciences, 32 Jiaochang Donglu, Kunming, 650223 Yunnan, People’s Republic of China e-mail:
[email protected] Present Address: P.-f. Fan College of Life Science and Chemistry, Dali University, 671000 Yunnan, People’s Republic of China e-mail:
[email protected]
Keywords Food sharing Meat eating Nomascus concolor jingdongensis Petaurista philippensis Predation
Introduction Gibbons (lesser apes) are arboreal primates, restricted to tropical, seasonal rain forests and sub-tropical evergreen forests in Southeast Asia. They mostly eat ripe, sugar-rich juicy fruits and also large quantities of figs (Leighton 1987; Bartlett 2007). Siamangs (Symphalangus syndactylus) and black crested gibbons (Nomascus concolor) are more folivorous, and spend the same or more time feeding on leaves as on fruit (Chivers 1984; Fan 2007). Animals, usually insects, are also included in their diet, but account for a small part (usually not more than 15% of the total diet) (Bartlett 2007), with the exception of the Kloss gibbon (Hylobates klossii), which spends 26% of its feeding time on insects (Whitten 1982). Among the great and lesser apes, predation and meateating behavior have been reported in different populations of chimpanzees (Pan troglodytes) (Stanford et al. 1994; Mitani and Watts 2001; Watts and Mitani 2002), in the bonobos (P. paniscus) (Badrian and Badrian 1977; Ihobe 1992), in the orangutans (Pongo pygmaeus) (Sugardjito and Nurhuda 1981; Utami and van Hooff 1997), and possibly in the gorilla (Gorilla gorilla) (Fossey 1983). Until recently, there was only one possible case of predation on a hen (Newkirk 1973) and one on bird’s eggs (Carpenter 1940) by gibbons (Hylobates lar). In a 14-month study of the ecology and behavior of a habituated group of central Yunnan black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China, we observed several cases of attacking, killing
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and eating vertebrates including mammals, birds and a reptile by the gibbons.
Methods The study was carried out at Dazhaizi (24°210 N, 100°420 E) on the western slope of Mt. Wuliang, a national nature reserve in Jingdong County, central Yunnan, China. Primary semi-humid evergreen broadleaved forests and midmountain humid evergreen broadleaved forests cover most of the study area, and the canopy is well connected. The precipitation from April 2005 to March 2006 was 1,607 mm, and 96% of the rainfall fell between May and October. The average temperature during the study period was 16°C (range -2 to 31°C; Fan and Jiang 2008). The study group was a polygynous group with two breeding females. One adult female with a blackish belly (FB-female) gave birth in February 2004, and the other, who has a yellowish belly (FY-female), gave birth in July 2005. Besides the two adult females and their dependents, the group consisted of one adult male, one sub-adult male and one juvenile. After 2 years of prior observation from March 2003, the group was finally habituated in March 2005. We then conducted a 14-month ecological and behavioral study from March 2005 to April 2006. We followed the group for 6–13 days each month—totally 125 days and 845 h during the study period (Fan and Jiang 2008). This group ranged between 1,900 and 2,700 m above sea level. In addition to regular instantaneous scan sampling, with a 5-min interval between scans (Altmann 1974), we used ad libitum sampling to record behavior as predation occurred. All predation cases were observed at a distance of no more than 20 m. A pair of 8 9 42 binoculars was used to help identify the prey. We also tried to collect remnants of the prey to take measurements and photos. Two species of giant flying squirrels (Petaurista philippensis and P. elegans) occur in this area. The giant flying squirrel P. philippensis is 2.5–3.0 kg, 44–51 cm in head– body length, 54–62 cm in tail length, and 4.5–5.0 cm in ear length (based on three specimens at the Kunming Institute of Zoology). Dorsal pelage is gray with white hair-tips and the tail is dull dark. P. elegans is smaller than P. philippensis, at 37 cm in head–body length and 37.5 cm tail length (Corbet and Hill 1992). Its dorsal pelage is redbrown with bold white spots, normally confined to the head and center of the back; its tail is bright red-brown. It is easy to distinguish the two species in the wild by their fur color. P. philippensis is more common than P. elegans in the study area, and all the prey attacked in this study were P. philippensis.
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Results In a total of 845 contact hours, we observed seven successful cases of predation on vertebrates, including four cases on giant flying squirrels (P. philippensis), two cases on eggs or chicks in nests of two different birds, and one on a lizard (Table 1). Detailed information is given below. Case 1 (17 September 2005) The juvenile uttered wo-wo vocalization, and jumped around in a tree about 25 m in height and 30 cm diameter at breast height (DBH) when the group was foraging at 1350 h. FB-female moved to the tree quickly and also uttered wo-wo vocalization. This vocalization is very similar to the soft grunts described by Chivers (1974, p. 222). Gibbons usually produce it in the initial stages of an alarm response to a source of potential danger outside the group. They also produce it occasionally when they find fruit trees. FB-female then grabbed the long tail of an adult giant flying squirrel from a hole about 14 m above ground and threw it down into a smaller tree nearby of about 10 m in height. The adult male, sub-adult male and FY-female also moved quickly to the big tree, and the adult male tried to strike the squirrel, which managed to escape and glide away. In the meantime, FB-female caught a young squirrel from a tree hole and started to eat it. The juvenile and the dependent infant of FB-female bit small parts from the body while it was held by the FB-female. The adult male, sub-adult male and FY-female stayed near FB and watched but did not touch the squirrel. After 15 min, FB-female threw down the remnants, a small part of skin with little meat, without bones and tail, about 12 cm in length. Case 2 (18 September 2005) FB-female was the last individual in the travel sequence when the group was foraging at 1230 h. Suddenly, adult male, sub-adult male, FYfemale and juvenile moved back to a 15 m high tree where the FB-female had remained. FB-female, about 10 m above the ground, was eating a giant flying squirrel about 15 cm in head–body length. FY-female and juvenile sat near FB-female and had already taken a small part of the meat and were eating when we first saw them. Adult male and sub-adult male stayed 3 m away from FB-female, and did not beg for meat. FY-female left the tree at 1238 h, and the sub-adult male sat close to the FB-female. The body of the giant flying squirrel was separated into two parts at 1243 h. Sub-adult male drew one part from FB-female’s hand and ate it in 2 min. The other part of the body was taken by the dependent infant. No remnant was thrown onto the ground in this case. Case 3 (26 September 2005) When the group had finished a feeding session, they began to forage in the forest and encountered a giant flying squirrel nest made of leaves
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Table 1 Summary of successful predation cases by black crested gibbons at Wuliang Mountain from March 2005 to April 2006 Date
Time of day (h)
Predator
Prey
Food sharing
17 September 2005
1350
FB-female
Giant flying squirrel
Juvenile, dependent infant of FB
18 September 2005
1230
FB-female
Giant flying squirrel
FY-female, juvenile, sub-adult male, dependent infant of FB
26 September 2005
1233
FB-female
Giant flying squirrel
Not sure
9 January 2006
1334
FB-female
Giant flying squirrel
Adult male, FY-female, juvenile
15 April 2006
1000
Adult male
Chicks
None
19 April 2006
1030
Adult male
Eggs or chicks
None
15 April 2006
1027
Juvenile
Lizard
None
located between branches about 12 m above the ground, at 1233 h. FB-female smashed the nest with her right hand five or six times and pulled from the nest a giant flying squirrel infant about 10 cm in head–body length. She bit the infant, killing it, and began eating. FY-female and juvenile sat close to the FB-female, but the adult male and sub-adult male stayed 5 m away. The juvenile moved away from FB-female at 1237 h and came back 1 min later; he grabbed and pulled the carcass towards him but FB-female refused to share it. FB-female ate nearly the whole body and threw a small part of the skin to the ground, but we could not find it. Case 4 (9 January 2006) FB-female left the fig tree the group was feeding in while the other three individuals remained feeding (sub-adult male was not with the group at that time). Suddenly FB-female uttered a wo-wo vocalization and one giant flying squirrel glided from her tree at 1334 h. The other three individuals moved quickly toward her. FB-female had destroyed a giant flying squirrel’s nest made of leaves and caught a juvenile or larger-size squirrel. The adult male and FY-female fed on the squirrel for about 2 min from 1338 to 1340 h and the juvenile ate from the carcass held by the FB-female from 1338 to 1349 h. FBfemale moved 4 m away at 1349 h and the adult male and juvenile followed her, but FB-female did not share the meat again. FB-female moved again at 1351 h but the others did not follow. FB-female continued to eat meat and dropped the remnants at 1356 h, which we retrieved. They consisted of a small part of the skin with one ear and no tail, head–body length 23 cm and 2.4 cm in ear length. The following seven cases were unsuccessful attempts at predation on squirrels: Case 5 (17 June 2005) The sub-adult male struck an adult giant flying squirrel’s back with his hand, but the squirrel glided away. Case 6 (16 September 2005) An adult giant flying squirrel was thrown from a high tree when the group was foraging at 1355 h, but we did not see who carried out the attack.
Case 7 (25 September 2005) FY-female struck the back and tried to grab the tail of an adult giant flying squirrel, but it glided away. She then carefully searched and destroyed the nest of leaves in the same tree but could not find any young. Case 8 (22 October 2005) At 1155 h FY-female uttered wo-wo vocalization and threw an adult giant flying squirrel to the ground from a height of 25 m. The squirrel lay motionless on its back for about 10 s, then turned over and climbed into a tree. The adult male quickly moved to the tree and attacked the squirrel but it escaped. Case 9 (22 October 2005) At 1310 h the adult male approached and attacked an adult giant flying squirrel but could not catch it. Case 10 (5 March 2006) At 0900 h the juvenile caught the tail of an adult giant flying squirrel, and the squirrel turned its head and tried to bite the juvenile. The gibbon loosened its grip and the squirrel glided away. Case 11 (19 April 2006) At 1325 h the juvenile approached an adult giant flying squirrel, but the squirrel climbed up another tree. The juvenile chased it and pursued the squirrel across several trees, then gave up. The last three cases deal with other vertebrate species: Case 12 (15 April 2006) At 1000 h the adult male found a bird’s nest 1 m above the ground when the group was foraging. The male climbed down and picked up the nest, then sat on a branch 2 m above the ground and ate the nestlings. Case 13 (19 April 2006) While the group was foraging in the forest at 1030 h, the adult male found a nest in a trunk 15 m above the ground, seized it and ate the eggs or chicks in the nest. Besides these two cases, another uncertain case was observed on 19 April. FB-female threw a destroyed nest from a tree at 1027 h but we could not see whether the FBfemale had acquired any food from the nest. From the
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materials and sizes of the three nests, they were evidently built by different species of birds. Case 14 (15 April 2006) The juvenile ate a lizard about 15 cm in length when the group was foraging at 0915 h. He ate the body and insides of the lizard and threw away the vertebrae. We could not find the remains.
Discussion Prey Predation on vertebrates is an uncommon behavior, with few cases reported in gibbons (Newkirk 1973; Carpenter 1940). In this paper, we report seven cases of predation and meat-eating behavior. Of the prey, nestlings or eggs in birds’ nests were the easiest for the gibbons to capture. Most birds in the study area build nests and began to reproduce in April, so more birds’ eggs and chicks were available during this month (personal observations). Giant flying squirrels are nocturnal and arboreal. Adult individuals usually spend the day in hollow trees or branches (personal observations), and infants always stay in nests inside tree holes (Case 1) or made of leaves (Case 2– 4). Such behavior makes it possible for gibbons to find and attack them. All four victims were babies or juveniles based on body size and skin size of the remnants, although the gibbons also tried to attack adults. This predation behavior occurred in the breeding season of the flying squirrels; three cases occurred in late September when the infants had no ability to defend themselves or escape. The young squirrels would still be highly vulnerable during December and January (Case 4). Although no adult giant flying squirrels were killed by gibbons, group members attacked adults in 9 out of the 11 cases. We are confident that the gibbons wanted to catch and eat the adult squirrels and not just chase them away, because they pursued them when no young squirrels were present. Attacks on adult giant flying squirrels were dangerous because they have powerful claws and incisors, and can even hurt local hunters. Gibbons always attempted to catch the squirrels by the tail and throw them down. This method might severely injure or kill an adult if it fell on a rock [one adult grey leaf monkey (Trachypithecus phayrei) died in the study area after it fell on a hard stone; P.F.F., unpublished data). The gibbons would have to descend to the ground and retrieve the squirrel quickly, however. Although on seven occasions we have observed black crested gibbons walking on the ground, the presence of the observers might have prevented them from rapidly coming to the ground in most predation attempts that we witnessed.
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Food sharing All four successful predation cases on giant flying squirrels were performed by the FB-female, although all other group members showed attacking behavior. After FB-female killed the prey, she always ate it near the site of predation. Passive meat sharing occurred in at least three cases (1, 2 and 4) (Table 1). Of 38 primate species that have been observed to hunt and/or eat vertebrates, only baboons and chimpanzees have been known to share meat (Butynski 1982). Offspring survival may be enhanced by the additional nutrition, and indeed most food transfers in primates usually occur from adults to young (Feistner and McGrew 1989). Food sharing is uncommon in gibbons (Nettelbeck 1998). In this study, only the FB-female was successful in predation and she shared primarily with her dependent infant and the juvenile. However, it was notable that FBfemale also shared meat with the FY-female. The study group was different from other gibbon groups because it is polygynous. Previous studies have suggested that aggression between females prevents males from acquiring new mates (Brockelman and Srikosamatara 1984). Jiang et al. (1999) suggested that the tolerance between adult black crested gibbon females was one reason why some groups consisted of two adult females. Further observations supported this view (Fan et al. 2006): two adult females could feed in the same tree, sing great calls synchronously, groom and be groomed with adult males, and groom each other. Meat-sharing behavior between the two adult females provides new support for the high degree of tolerance between these reproductive females. Prey size also influenced meat sharing. FB-female shared meat with several members when she killed a large prey in Case 4, but refused to share with others when she killed a small prey in Case 3. Acknowledgments This study was carried out at the Black Crested Gibbon Monitoring Station on Mt. Wuliang and was supported by the National Natural Science Foundation of China (#30670270), the National Basic Research Program of China (#2003CB415103) and Knowledge Innovation Program of the Chinese Academy of Sciences (#KSCX2-SW-119). Many thanks are given to anonymous reviewers for their comments and suggestions to improve the manuscript. We would like to thank the staff from the Jingdong Nature Reserve Management Bureau for their much needed support. We also acknowledge our field assistants, Mr. Liu Yekun and Mr. Liu Yeyong for their kind help.
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