Ranging Behavior of Eastern Hoolock Gibbon (Hoolock Leuconedys) in a Northern Montane Forest in Gaoligongshan, Yunnan, China

Home , Black crested gibbon, Eastern hoolock gibbon, Ficus neriifolia

Primates (2014) 55:239–247 DOI 10.1007/s10329-013-0394-y

ORIGINAL ARTICLE

Ranging behavior of eastern hoolock gibbon (Hoolock leuconedys) in a northern montane forest in Gaoligongshan, Yunnan, China

Dao Zhang • Han-Lan Fei • Sheng-Dong Yuan • Wen-Mo Sun • Qing-Yong Ni • Liang-Wei Cui • Peng-Fei Fan

Received: 17 December 2012 / Accepted: 17 October 2013 / Published online: 13 November 2013 Ó Japan Monkey Centre and Springer Japan 2013

Abstract Generally, food abundance and distribution was patchily distributed within their total (14-month) home exert important influence on primate ranging behavior. range, and during most months they used only a small portion Hoolock gibbons (genus Hoolock) live in lowland and of their total home range. In order to find enough food, the montane forests in India, Bangladesh, Myanmar and China. group shifted its monthly home range according to the sea- All information about hoolock gibbons comes from studies sonal availability of food species. To satisfy their annual on western hoolock gibbons (Hoolock hoolock) living in food requirements, they occupied a total home range of lowland forest. Between August 2010 and September 2011, 93 ha. The absence of neighboring groups of gibbons and the we studied the ranging behavior of one habituated group of presence of tsaoko cardamom (Amomum tsaoko) plantations eastern hoolock gibbon (H. leuconedys) living in a seasonal may also have influenced the ranging behavior of the group. montane forest in Gaoligongshan, Yunnan, China. Results Further long-term studies of neighboring groups living in show that the study group did not increase foraging effort, intact forests are required to assess these effects. calculated in this study as the daily path length, when fruit was less available. Instead, the gibbons fed more on leaves Keywords Home range size Daily path length and decreased traveling to conserve energy. They relied Monthly home range Behavioral adaptation heavily on a single food species in most study months which Seasonal forest

D. Zhang and H.-L. Fei contributed equally to this paper. Introduction D. Zhang H.-L. Fei W.-M. Sun P.-F. Fan (&) Institute of Eastern-Himalaya Biodiversity Research, Studies of habitat use and ranging behavior (home range size, Dali University, Dali, Yunnan 671000, daily path length, and home range use etc.) provide important People’s Republic of China e-mail: [email protected] insights into wildlife behavior and ecology. Generally, food abundance and distribution play the most inﬂuential roles in D. Zhang S.-D. Yuan W.-M. Sun L.-W. Cui (&) shaping primate ranging behavior (Di Bitetti 2001). Key Laboratory of Forest Disaster Warning and Control in Numerous studies have documented that primates adjust Yunnan Province, Southeast Forestry University, Kunming, Yunnan, People’s Republic of China their ranging behavior in response to seasonal variation in e-mail: [email protected] food availability and distribution (Clutton-Brock 1975;Di Bitetti 2001; Di Fiore 2003; Fan and Jiang 2008; Bartlett D. Zhang 2009). This relationship holds more strongly for frugivorous School of Resources and Environmental Engineering, Anhui University, Hefei, Anhui 230601, primates such as gibbons than for folivorous primates People’s Republic of China (Clutton-Brock 1977) because of the higher spatial and seasonal variance in the availability of fruit compared to Q.-Y. Ni leaves (Janson and Chapman 1999) and the shorter digestion College of Animal Science and Technology, Sichuan Agricultural University, Yaan, Sichuan 625014, People’s time required for fruit than for leaves (Demment and Laca Republic of China 1991). Supporting this view, several studies have shown that 123 240 Primates (2014) 55:239–247

Table 1 Study site and home range size for different gibbon species Species Site Latitude (N) Altitude (m) Home range Reference (ha)

Hoolock hoolock Sibsagar district, Assam 26.7 119 22 Tilson (1979) Lawachara, Bangladesh 24.5 20 35 Islam and Feeroz (1992) Lawachara, Bangladesh 24.5 20 63 Ahsan (2001) Chunati, Bangladesh 22.9 15 26 Ahsan (2001) Hylobates agilis Sungai Dal, Malaysia 4.8 500 29 Gittins (1982) H. klossii Paitan, Siberut, Indonesia 1.4 33 Whitten (1982) H. lar Krau Game, Malaysia 3.7 50 57 Raemaekers (1979) Mo Singto, Khao Yai, Thailand 14 800 23 Bartlett (2009) H. moloch Gunung Halimun-Salak, Java, 6.7 1,000 37 Kim et al. (2011) Indonesia CALS, Java, Indonesia 7.7 100 15 Malone (2007) H. albibarbis Sabangau, Kalimantan, Indonesia 2.5 15 47 Cheyne (2010) H. muelleri 9 agilis Barito Ulu, Kalimantan, Indonesia 0.2 200 45 McConkey et al. (2003) Symphalangus syndactylus Krau Game, Malaysia 3.7 50 47 Raemaekers (1979) Nomascus concolor Dazhaizi, Wuliang Mt. China 24.4 2,200 151 Fan and Jiang (2008) N. nasutus Bangliang, Guangxi, China 22.9 700 130 Fan et al. (2010) N. hainanus Bawangling, Hainan, China 19.1 1,000 400 Liu et al. (1989) frugivorous primate species, including gibbons, increase annual home range to satisfy their food requirements in their daily path length (DPL) and consequently their monthly different seasons. This may also be the case for gibbons. home range size when fruits comprise a greater proportion of Home range sizes of northern Nomascus gibbon populations their diet, or when fruit is more abundant (Cercocebus al- living in seasonal forest are substantially larger than those of bigena: Olupot et al. 1997; Ateles chamek: Wallace 2006; more southerly or lowland gibbon populations (Table 1). Nomascus concolor: Fan and Jiang 2008; Hylobates lar: Javan gibbons in higher elevation habitats have larger home Bartlett 2009). However, some other primate species have ranges than lowland conspecific groups (Kim et al. 2011; not shown the same responses to fruit abundance or con- Malone 2007; Table 1). However, the home range sizes of sumption (Kaplin 2001; Di Fiore 2003; Buzzard 2006). northern hoolock gibbons living in lowland forests are similar Kaplin (2001) found that neither overall abundance of fruit to those of southern gibbon populations (Table 1), probably resources in the home range nor overall proportion of fruit in due to the high density of fruit trees in lowland forests. the diet, but rather temporal and spatial availability of spe- The eastern hoolock gibbon (Hoolock leuconedys) is now cific fruit species, was related to ranging behavior in her considered a separate species from the western hoolock study groups of Cercopithecus lhoesti and C. mitis doggetti. gibbon (H. hoolock), based on distinctive fur coloration Di Fiore (2003) found ranging behavior of two highly fru- (Mootnick and Groves 2005). The eastern hoolock gibbon givorous woolly monkey (Lagothrix lagotricha poeppigii) occurs in China, Myanmar and India, east of the Chindwin groups was not related to habitat-wide abundance of ripe River (Groves 1967, 1972; Das et al. 2006; Brockelman et al. fruit, but to insect prey abundance. Buzzard (2006) sug- 2009; Fan et al. 2011). A recent survey in China recorded gested that the ranging behavior of Tai guenons (C. camp- only 40–43 groups and the total population was estimated to belli, C. petaurista, and C. diana) was more likely influenced be fewer than 200 individuals (Fan et al. 2011), although by resource monitoring and territorial defense. several thousands of the species may still occur in Myanmar Fruit productivity decreases with increasing latitude and and India (Das et al. 2006; Chetry et al. 2008; Brockelman altitude (Hanya and Aiba 2010), and fruiting seasonality also et al. 2009). This small population in China lives in an area increases with latitude (Ting et al. 2008). Primates living in situated at high altitude (1,600–2,700 m above sea level) and seasonal forests have shown seasonal variation in home northern latitude (N: 24°49–25°480) (Fan et al. 2011). range use as the distribution and abundance of their main This area is the most northerly location where gibbons are food sources changed seasonally (Cebus apella nigritus:Di known to live, and represents an extreme habitat for gibbons. Bitetti 2001; Callimico goeldii: Porter et al. 2007; R. bieti: During our study period, the annual mean temperature was Grueter et al. 2008; Ren et al. 2009; R. roxellana: Li et al. 13.3 °C and the forest was covered by snow on some days 2000, Tan et al. 2007). As a result, these groups used a large (Fan et al. 2013). Fruit productivity decreased nearly to zero

123 Primates (2014) 55:239–247 241 between December and February 2010 (Fan et al. 2013). track and observe both GA and female B. This research Therefore, ranging behavior from this population may pro- focused only on the family group GA, because it was very vide important insights into the behavioral adaptation of difficult to follow female B for full days (Fan et al. 2013). gibbons to an extreme habitat. In this paper, we report on the Because of the large home range and low frequency of ranging behavior of one habituated eastern hoolock gibbon singing, it was difficult to find the gibbons. In total, we group living in a high montane forest in Nankang, Gaoli- observed GA for 853 h over 103 days (monthly range gongshan, between August 2010 and September 2011. We 4–12, mean = 7.4 days), 63 of which (monthly range 2–6, tried to elucidate how the group adjusts its home range in mean = 4.5 days) were full-day follows, starting when the response to seasonal variations in food availability and dis- gibbons left their sleeping trees until they settled to sleep in tribution. However, an important feature that needs to be the evening. The sample size was comparable to most borne in mind is the isolation of this group, without any gibbon studies regarding ranging patterns (Gittins 1982; neighboring groups that might affect its range boundaries. Whitten 1982; Islam and Feeroz 1992; Ahsan 2001; McConkey and Chivers 2007; Bartlett 2009; Fan and Jiang 2008; Kim et al. 2011) and other primate studies (Kaplin Methods 2001; Zhou et al. 2007). We recorded GA’s location every half hour using a Study area portable GPS. A scan sampling method (Altmann 1974)at 5-min intervals (Lappan 2009; Bartlett 2009; Cheyne 2010) This study was conducted in Nankang Nature Park (24°490– was used to record the diet of gibbons. When an individual 24°500 N, 98°450–98°460 E, 1,330 ha), which has been man- was feeding, we recorded the food species and food type aged as part of the Gaoligongshan National Nature Reserve (figs, other fruits, leaves, flowers, animals, and others) (Fan since 1996 (Fan et al. 2013). The elevation of the study site et al. 2013). We marked and recorded the location of all ranges between 1,800 and 2,300 m asl. The vegetation is food trees in which at least one gibbon consumed food montane humid evergreen broad-leaved forest dominated by items for more than 10 min, which we defined as ‘impor- members of Lauraceae, Fagaceae, Theaceae, and Magnoli- tant food trees’. In total, we recorded 283 important food ceae (Zhang et al. 2008). In many valleys, local people have trees, representing 35 different species. cut trees and cleared the undergrowth to grow tsaoko cardamom (Amomum tsaoko). Recurrent clearings have fragmented Data analyses the forest in a dendritic pattern with the negative effect of reducing the density of the tree canopy and consequently Full-day observations (N = 63) were used to calculate the increasing the distance between fruit trees visited by gibbons. DPL as the sum of the straight-line distances (in meters) The annual mean temperature was 13.3 °C between between consecutive GPS points during a full day. Step- October 2010 and September 2011. The lowest monthly wise linear regression was used to evaluate the effects of mean temperature was 6.4 °C in January and the highest daily diet (expressed as the proportion of different food 20.3 °C in August 2010 (Fan et al. 2013). The annual rainfall types), mean temperature during the gibbons’ active time was 1,801.4 mm. Rainfall was higher than 200 mm in each and rainfall between 0800 and 2000 h, on the variation of rainy season month from May to October, except in September DPL. 2011 (198.1 mm), while lower than 100 mm in each month of We reported the monthly most important food species the dry season from November to April (Fan et al. 2013). based on the contribution to the group’s monthly diet. We imported all locations of important food trees on a topo- Study animals graphic map using ArcGIS 9.2. We emphasized the locations of monthly most important food species within the There was only one group (GA) and a single solitary group’s home range. female (B) living in the park during the study period. GA All group locations were added to the same topographic consisted of one adult male, one adult female, and one map. We tested three methods for analyzing the total and infant which became fully independent in October 2010. monthly home range size of the group. First, we superim- All members in GA were fully habituated to human posed a 100 9 100 m grid system on the topographic map observers before this research. and estimated home range size by counting the number of grids used by gibbons each month (monthly home range Data collection size) and throughout the whole study period (total home range size) (Buzzard 2006; Kaplin 2001; Fan and Jiang We worked 11–30 days every month between August 2010 2008; Zhou et al. 2007). Second, we also used the mini- and September 2011, totalling 328 days in the forest, to mum convex polygon (MCP) method to calculate home 123 242 Primates (2014) 55:239–247

Fig. 1 Distribution of important food trees within the study group’s home range range size, defined here as the area included within a Results minimum convex polygon encompassing all locations recorded in each month (monthly home range size) and Daily path length throughout the study (total home range size) (Kaplin 2001). Given that the MCP method is sensitive to outliers and During the 63 full-day observations, GA moved likely to overestimate home range somewhat (Burgman 345–2,606 m per day, with a mean distance of 1,162 m. and Fox 2003; Grueter et al. 2009), we repeated the ana- Using a stepwise linear regression to tease apart the effects lysis using the 95 % MCP method. The grid method and of the rainfall, temperature and daily diet of fruits, flowers, the regular 100 % MCP method gave nearly identical total figs and leaves on gibbon DPL, we found that gibbons home range areas (93 and 93.6 ha, respectively), and the decreased DPL when their diet included more leaves 95 % MCP method was about 6 % lower. Both 100 and (Y = 1574.076 - 11.204X, P \ 0.001, N = 63). 95 % MCP boundaries are shown in Fig. 1, suggesting that there are few if any outliers in gibbon ranging paths. To Food distribution test if the group shifted their monthly home range in response to food distribution, we computed centroids of The important food trees visited by the gibbon group were monthly home range as averages of x and y coordinates of not evenly distributed within the study group’s home 95 % GPS locations in the month (Brockelman et al. in range; more trees were located in the western part of the press). In addition, we overlaid all monthly polygons and home range than the east (Fig. 1). The group heavily relied distinguished areas covered by different numbers of on a single food species in each study month and they monthly layers (Ramos-Fernandez et al. 2013; Brockelman normally fed on the same species for 2 months and then et al. in press). We conducted all statistical analyses via changed to a different species (Table 2). Six species were SPSS 17.0 for Windows. identified as monthly most important species, which were

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Table 2 Most important food species of the study group Table 3 Monthly home range, estimated by the 95 % convex polygon method, used by an eastern hoolock gibbon group at Nankang, Date Number of Most important Percentage Yunnan, China food species food species of records Date Home Proportion to Mean daily 10-Aug 16 Ficus neriifolia 60 range (ha) the total path length (m) 10-Sep 8 Ficus neriifolia 60 home range 10-Oct 16 Cayratia japonica 43 10-Aug 18.4 0.21 930 10-Nov 22 Cayratia japonica 46 10-Sep 41.5 0.47 1,815 10-Dec 25 Embelia floribunda 25 10-Oct 37.1 0.42 1,403 11-Jan 14 Embelia procumbens 41 10-Nov 21.1 0.24 1,219 11-Feb 12 Embelia procumbens 47 10-Dec 17.7 0.2 717 11-Mar 10 Schefflera minutistellata 39 11-Jan 10.6 0.12 508 11-Apr 18 Schefflera minutistellata 37 11-Feb 12.3 0.14 765 11-May 17 Cerasus trichostoma 22 11-Mar 21.2 0.24 934 11-Jun 18 Ficus neriifolia 18 11-Apr 21.2 0.24 897 11-Jul 23 Embelia procumbens 52 11-May 61.5 0.7 1,324 11-Aug 14 Ficus neriifolia 65 11-Jun 36.9 0.42 1,202 11-Sep 17 Ficus neriifolia 49 11-Jul 24.5 0.28 842 11-Aug 21.9 0.25 1,434 11-Sep 51 0.58 1,926 patchily distributed. Ficus neriifolia, Embelia procumbens Total 88.1 and Cayratia japonica were mostly located in the western part of the home range, Schefflera minutistellata was distributed in the middle, and Cerasus trichostoma occurred in not to be influenced by the distribution of the monthly most the eastern part (Fig. 1). Four trees bearing the liana important species visited in such months (Fig. 1). The total Embelia floribunda were scattered in different parts of the home range size using the 95 % MCP method was 88.1 ha home range. (Table 3).

Monthly home range Discussion We recorded 59–156 group locations each month, for a total of 1,515 locations. The group used a relatively small Impacts of diet on daily path length part of its home range in any given month (Table 3; Figs. 2 and 3). Monthly home range size was positively correlated DPL represents the foraging effort of the group in 1 day. with monthly mean DPL (Spearman correlation r = 0.818, The mean DPL of the study group was 1,162 m, which is P \ 0.001, N = 14). The centroids of monthly home range within the range of other studied gibbon species, including clearly shifted from month to month and the maximum hoolock gibbons living in lowland forest (reviewed in shift in range centroids over the year was 719 m (mean Bartlett 2007). This suggests that, on a daily scale, our 205 ± 184 m; range 17–719 m; N = 13) (Fig. 2). No core study group did not travel for longer distances in search of area was used in all 14 months and five small areas were food than other gibbon species, though they live in a used in 11 months (Fig. 3). The group heavily used the northern montane forest with relatively fewer fruit trees. To north-west part when it relied on Ficus neriifolia during satisfy their food requirements, they changed their diet by August and September in both 2010 and 2011 and on feeding more on leaves (Fan et al. 2013), like N. concolor Cayratia japonica in October and November. The gibbons living in a montane forest at Wuliang Mountain (Fan et al. moved to the southern part when their diet relied on 2009) and N. nasutus living in a degraded karst forest (Fan Embelia procumbens in January, February and July and on et al. 2012). Overall, however, they fed relatively less on Schefflera minutistellata in March and April. In May, the fruits and figs than other gibbons (Bartlett 2007). group extended its home range to the east in order to feed We found an inverse relationship between the degree of on three trees of Cerasus trichostoma. In December, May, folivory and DPL of the study group. When fruit was less and June, the group fed on many different species and the available gibbons changed their diet to leaves (Fan et al. contribution of the most important food species to the 2013) and decreased their travel (present study). Other monthly diet was not so high (Table 2); therefore, the studies have shown that this behavior is common in gib- centroids of monthly home range in these months seemed bons, as well as in other primates (e.g., Cebus apella: 123 244 Primates (2014) 55:239–247

Fig. 2 Monthly home range of the study group. Centroids of monthly home range shifted from month to month

Zhang 1995; Pan troglodytes verus: Doran 1997; M. fus- Impacts of food distribution on home range use cata: Hanya et al. 2006; Ateles chamek: Wallace 2006; Nasalis larvatus: Matsuda et al. 2009). Both lar gibbons Notable seasonality in plant phenology and variation of (Hylobates lar) and siamangs (Symphalangus syndactylus) food availability has been reported in the study site (Fan in Kuala Lompat, Malaysia reduce their travel during the et al. 2013). During most months the group heavily relied months when the abundance of their main food is low on a single species which represented more than 35 % of (Chivers 1974; Raemaekers 1980). Similarly, at Khao Yai, the monthly diet. Because food trees were patchily dis- Thailand, lar gibbons reduce their travel during the cool tributed within its total (14-month) home range, the group dry season when fruit availability is low (Bartlett 2009). occupied on a monthly basis a small portion of the total Western black crested gibbons (N. concolor) in Wuliang home range. With the seasonal changes in fruit availability, Mountain decrease traveling when they eat more leaves they fed on different food species distributed in different during cold months (Fan and Jiang 2008). Physical effort is parts of the home range (Fig. 1). Therefore, the group probably decreased because of the poor nutritional content shifted its monthly home range to meet dietary require- (cal/g) provided by fresh leaves compared to fresh fruit ments. For example, in order to forage on the fruit of pulp (Raemaekers 1978). On the other hand, gibbons may Cerasus trichostoma, the group extended its home range to not need to travel far because leaves are believed to be a the east in May. We observed the group in August and dense and relatively predictable food supply (Kaplin 2001, September in both 2010 and 2011 and the group used the personal observation). When the study group spent more same area in different years when they ate Ficus neriifolia time feeding on leaves in January (81.9 %) and February heavily during the period. These results suggest that the (79.3 %) (Fan et al. 2013), they traveled less and used only distribution of important food species is the main deter- a small portion of their 14-month home range (Table 3). minant of home range use of the group.

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Fig. 3 Spatial variation of monthly home range. The different shades represent the number of monthly layers (overlaps)

Why did the study group use a relatively large home several other primate species (Cebus apella nigritus:Di range? Bitetti 2001; Callimico goeldii: Porter et al. 2007; R. bieti: Grueter et al. 2008; Ren et al. 2009; R. roxellana: Our study group occupied a larger total home range than Li et al. 2000, Tan et al. 2007). All these species live in most lowland gibbon groups, but similar to that of northern heterogeneous and/or seasonal forest and feed on dif- Nomascus gibbons (Table 1). In principle, home ranges ferent species distributed in different areas or habitat should be large enough to accommodate a ﬂuctuating fruit types. Therefore, they need to move every month and resource base (Di Bitetti 2001; Fan and Jiang 2008), so if a consequently occupy large annual home ranges to cover population’s resource is patchily distributed both spatially the distribution of all important food species. The present and temporally, the home range required would naturally study highlights the impacts of food distribution on tend to be larger. ranging patterns of gibbons. The ranging pattern of our group was different from that of a white-handed gibbon (Hylobates lar) group in Other factors might inﬂuence the ranging behavior Khao Yai Park, Thailand (Bartlett 2009; Brockelman of the group et al. in press) and two siamang (Symphalangus syndactylus) groups in Malaysia (Chivers 1974). Although Except for the single female (B), there was only one family those groups used different food species over the group living in Nankang. Intergroup competition was months, monthly home range shifted relatively little over therefore absent. Low group density and decreased inter- the year, probably due to the relatively greater homo- group competition might result in a larger home range, as geneity in the distribution of feeding trees (Chivers we observed in the study group. On the other hand, the lack 1974; Bartlett 2009; Brockelman et al. in press). How- of neighboring groups might free the group from the ever, a similar shifting pattern has been reported in obligation of territory defense, consequently resulting in a

123 246 Primates (2014) 55:239–247 smaller home range. However, we are unaware of studies Brockelman WY, Nathalang A, Greenberg DB, Suwanvecho U (in that have given direct evidence of this. press) Evolution of small-group territoriality in gibbons. In Yamagiwa J, Karczwaski L (eds) Primates and cetaceans: field In Nankang, tsaoko cardamom plantations are widely studies and conservation of complex mammalian societies. distributed in most valleys within the group’s home range Springer, Japan which might decrease the overall food density and increase Burgman MA, Fox JC (2003) Bias in species range estimates from the influence of fragmentation of food species distribution minimum convex polygons: implications for conservation and options for improved planning. Anim Conserv 6:19–28 on the group’s ranging behavior. Further studies on larger Buzzard PJ (2006) Ranging patterns in relation to seasonality and populations living in protected forest should help clarify frugivory among Cercopithecus campbelli, C. petaurista, and C. the effects of tsaoko cardamom plantations, important food diana in the Taı¨ forest. Int J Primatol 27:559–573 tree density, and low group density on the ranging behavior Chetry D, Chetry R, Das A, Loma C, Panor J (2008) New distribution records for Hoolock leuconedys in India. Primate Conserv of hoolock gibbons. 23:125–128 In summary, this is the first report on the ranging Cheyne SM (2010) Behavioural ecology of gibbons (Hylobates behavior of hoolock gibbons living in a montane forest. albibarbis) in a degraded peat-swamp forest. In: Gursky-Doyen This study demonstrates that food availability and distri- S, Supriatna J (eds) Indonesian primates. Springer, New York, pp 121–156 bution are the main determinants of the group’s ranging Chivers DJ (1974) The siamang in Malaya: a field study of a primate behavior. The group did not increase foraging effort despite in a tropical forest. Contr Primat 4:1–335 the cold, seasonal habitat in which it lives. When fruit was Clutton-Brock TH (1975) Ranging behavior of red colobus (Colobus less available, the group fed more on leaves (Fan et al. badius tephrosceles) in the Gombe National Park. Anim Behav 23:706–722 2013) and decreased travel to conserve energy. They usu- Clutton-Brock TH (1977) Some aspects of intra-specific variation in ally relied on a single food species in each study month and feeding and ranging behaviour in primates. In: Clutton-Brock used a small portion of their total home range in most TH (ed) Primate ecology: studies of feeding and ranging months. They shifted their monthly home range in order to behaviour in lemurs, monkeys and apes. Academic Press, London, pp 539–556 find enough food which was distributed in different loca- Das J, BI Swas J, Bhattacharjee PC, Mohnot SM (2006) First tions, and they therefore occupied a large total home range distribution records of the eastern hoolock gibbon (Hoolock of 93 ha. hoolock leuconedys) from India. Zoo’s Print J 21:2316–2320 Demment MW, Laca EA (1991) Herbivory: the dilemma of foraging Acknowledgments This study was supported by the National Nat- in a spatially heterogenous food environment. In: Palo RT, ural Science Foundation of China (#31160424), Rufford Small Grant, Robbins CT (eds) Plant defenses against mammalian herbivory. Provincial Natural Science Foundation of Yunnan (2009ZC124 M), CRC Press, Boca Raton, pp 29–44 and Fauna and Flora International. All research methods adhered to Di Bitetti MS (2001) Home-range use by the tufted capuchin monkey the Chinese legal requirements. We would like to thank Mr. Ai Huai- (Cebus apella nigritus) in a subtropical rainforest of Argentina. Sen, Lin Ru-Tao, Li Jia-Hong, and Shi Xiao-Chun from Gaoligong- J Zool Lond 253:33–45 shan National Nature Reserve for their needed support. We are very Di Fiore A (2003) Ranging behavior and foraging ecology of lowland grateful to Dr. Warren Brockelman and two anonymous reviewers for woolly monkeys (Lagothrix lagotricha poeppigii) in Yasunı´ their valuable comments. Dr. Matthew B. Scott and Mr. Davide National Park, Ecuador. Am J Primatol 59:47–66 Fornacca helped us to edit the English. Doran D (1997) Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. Int J Primatol 18:183–206 Fan PF, Jiang XL (2008) Effects of food and topography on ranging References behavior of black crested gibbon (Nomascus concolor jingdong- ensis) in Wuliang Mountain, Yunnan, China. Am J Primatol Ahsan MF (2001) Socio-ecology of the hoolock gibbon (Hylobates 70:871–878 hoolock) in two forests of Bangladesh. In: The apes: challenges Fan PF, Ni QY, Sun GZ, Huang B, Jiang XL (2009) Gibbons under for the 21st century. Conference proceedings. Brookfield Zoo, seasonal stress: the diet of the black crested gibbons (Nomascus Brookfield, pp 286–299 concolor) on Mt. Wuliang, Central Yunnan. Primates 50:37–44 Altmann J (1974) Observational study of behaviour: sampling Fan PF, Fei HL, Xiang ZF, Zhang W, Ma CY, Huang T (2010) Social methods. Behaviour 49:227–267 structure and group dynamics of the cao vit gibbon (Nomascus Bartlett T (2007) The hylobatidae, small apes of Asia. In: Campbell nasutus) in Bangliang, Jingxi, China. Folia Primatol 81:245–253 CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Fan PF, Xiao W, Huo S, Ai e HS, Wang TC, Lin RT (2011) Primates in perspective. Oxford University Press, New York, Distribution and conservation status of Hoolock leuconedys in pp 274–289 China. Oryx 45:129–134 Bartlett T (2009) The gibbons of Khao Yai: seasonal variation in Fan PF, Fei HL, Ma CY (2012) Behavioral responses of cao vit behaviour and ecology. Allyn & Bacon, Boston 170 p gibbon (Nomascus nasutus) to variations in food abundance and Brockelman WY, Naing H, Saw C, Moe A, Linn Z, Moe TK, Win Z temperature in Bangliang, Jingxi, China. Am J Primatol (2009) Census of eastern hoolock gibbons (Hoolock leuconedys) 74:632–641 in Mahamyaing Wildlife Sanctuary, Sagaing Division, Myanmar. Fan PF, Ai HS, Fei HL, Zhang D, Yuan SD (2013) Seasonal variation In: Lappan S, Whittaker DJ (eds) The gibbons, new perspectives of diet and time budget of eastern hoolock gibbons (Hoolock on small ape socioecology and population biology. Springer leuconedys) living in a northern montane forest. Primates Science?Business Media, LLC, New York, pp 435–452 54:137–146

123 Primates (2014) 55:239–247 247

Gittins SP (1982) Feeding and ranging in the agile gibbon. Folia McConkey KR, Ario A, Aldy F, Chivers DJ (2003) Influence of forest Primatol 38:39–71 seasonality on gibbon food choice in the rain forests of Barito Groves CP (1967) Geographic variation in the hoolock or white Ulu, Central Kalimantan. Int J Primatol 24:19–32 browed gibbon (Hylobates hoolock). Folia Primatol 7:276–283 Mootnick AR, Groves CP (2005) A new generic name for the hoolock Groves CP (1972) Systematics and phylogeny of gibbons. In: gibbon (Hylobatidae). Int J Primatol 26:971–976 Rumbaugh DM (ed) Gibbon and siamang, vol 1. Karger, Olupot W, Chapman CA, Waser PM, Isabirye-Basuta G (1997) Switzerland, pp 1–89 Mangabey (Cercocebus albigena) ranging patterns in relation- Grueter CC, Li DY, van Schaik CP, Ren BP, Long YC, Wei FW ship to fruit availability and the risk of parasite infection in (2008) Ranging of Rhinopithecus bieti in the Samage Forest, Kibale National Park, Uganda. Am J Primatol 43:65–78 China. I. Characteristics of range use. Int J Primatol Porter LM, Sterr SM, Garber PA (2007) Habitat use and ranging 29:1121–1145 behavior of Callimico goeldii. Int J Primatol 28:1035–1058 Grueter CC, Li DY, Ren BP, Wei FW (2009) Choice of analytical Raemaekers JJ (1978) Changes through the day in the food choice of method can have dramatic effects on primate home range wild gibbons. Folia Primatol 30:194–205 estimates. Primates 50:81–84 Raemaekers JJ (1979) Ecology of sympatric gibbons. Folia Primatol Hanya G, Aiba S (2010) Fruit fall in tropical and temperate forests: 31:227–245 implications for frugivore diversity. Ecol Res 25:1081–1090 Raemaekers JJ (1980) Causes of variation between months in distance Hanya G, Kiyono M, Yamada A, Suzuki K, Furukawa M, Yoshida Y, traveled daily by gibbons. Folia Primatol 34:46–60 Chijiiwa A (2006) Not only annual food abundance but also Ramos-Fernandez G, SmithAguilar SE, Schaffner CM, Vick LG, fallback food quality determines the Japanese macaque density: Aureli F (2013) Site fidelity in space use by spider monkeys evidence from seasonal variations in home range size. Primates (Ateles geoffroyi) in the Yucatan Peninsula, Mexico. Plos ONE 47:275–278 8:e62813. doi:10.1371/journal.pone.0062813 Islam MA, Feeroz MM (1992) Ecology of hoolock gibbon of Ren BP, Li M, Long YC, Wu RD, Wei FW (2009) Home range and Bangladesh. Primates 33:451–464 seasonality of Yunnan snub-nosed monkeys. Integr Zool Janson CH, Chapman CA (1999) Resources and primate community 4:162–171 structure. In: Fleagle JG, Janson CH, Reed KE (eds) Primate Tan CL, Guo ST, Li BG (2007) Population structure and ranging communities. Cambridge University Press, Cambridge, patterns of Rhinopithecus roxellana in Zhouzhi National Nature pp 237–261 Reserve, Shanxi, China. Int J Primatol 28:577–591 Kaplin BA (2001) Ranging behavior of two species of guenons Tilson RL (1979) Behaviour of hoolock gibbon (Hylobates hoolock) (Cercopithecus lhoesti and C. mitis doggetti) in the Nyungwe during different seasons in Assam, India. J Bombay Nat Hist Soc forest reserve. Rwanda. Int J Primatol 22:521–548 76:1–16 Kim S, Lappan S, Choe JC (2011) Diet and ranging behavior of the Ting S, Hartley S, Burns KC (2008) Global patterns in fruiting endangered Javan gibbon (Hylobates moloch) in submontane seasons. Global Ecol Biogeogr 17:648–657 tropical rainforest. Am J Primatol 73:270–280 Wallace RB (2006) Seasonal variations in black-faced black spider Lappan S (2009) Flowers are an important food for small apes in monkey (Ateles chamek) habitat use and ranging behavior in a southern Sumatra. Am J Primatol 71:1–12 southern Amazonian tropical forest. Am J Primatol 68:313–332 Li B, Chen C, Ji W, Ren B (2000) Seasonal home range changes of Whitten AJ (1982) Home range use by kloss gibbons (Hylobates the Sichuan snub-nosed monkey (Rhinopithecus roxellana)in klossii) on Siberut Island, Indonesia. Anim Behav 30:182–198 the Qinling Mountains of China. Folia Primatol 71:375–386 Zhang SY (1995) Activity and ranging patterns in relation to fruit Liu ZH, Zhang YZ, Jiang HS, Southwick C (1989) Population utilization by brown capuchins (Cebus apella) in French Guiana. structure of Hylobates concolor in Bawanglin Nature Reserve, Int J Primatol 16:489–507 Hainan, China. Am J Primatol 19:247–254 Zhang XY, Zhou W, Wu JP, Bai B, Li ZB (2008) Food selection of Malone NM (2007) The socioecology of the critically endangered hoolock gibbon (Hoolock hoolock) at Nankang Mt. Gaoligong in Javan gibbon (Hylobates moloch): assessing the impact of spring. Zool Res 29:l74–l80 anthropogenic disturbance on primate social systems (Ph. Zhou QH, Huang CM, Li YB, Cai XW (2007) Ranging behavior of D. Dissertation). Eugene: University of Oregon the François’ langur (Trachypithecus francoisi) in the Fusui Matsuda I, Tuuga A, Higashi S (2009) Ranging behavior of proboscis Nature Reserve, China. Primates 48:320–323 monkeys in a riverine forest with special reference to ranging in inland forest. Int J Primatol 30:313–325 McConkey KR, Chivers DJ (2007) Influence of gibbon ranging patterns on seed dispersal distance and deposition site in a Bornean forest. J Trop Ecol 23:269–275

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