Nomascus Gabriellae)Ina Lowland Tropical Forest

Received: 8 April 2016 | Revised: 2 March 2017 | Accepted: 18 March 2017 DOI: 10.1002/ajp.22667

RESEARCH ARTICLE

Feeding behavior and activity budget of the southern yellow-cheeked crested gibbons (Nomascus gabriellae)ina lowland tropical forest

Thanh H. Bach1,2,3 | Jin Chen1 | Minh D. Hoang4 | Kingsly C. Beng3,5 | Van T. Nguyen2

1 Key Lab of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, The southern yellow-cheeked crested gibbon (Nomascus gabriellae), an endangered species Chinese Academy of Sciences, Menglun, native to Vietnam and Cambodia, lives exclusively in undisturbed tropical forests and depends Mengla, Yunnan, China primarily on ripe fruit for food. Although this species is highly threatened, its ecology and 2 Cat Tien National Park, Vietnam conservation status remain relatively unknown. In order to understand how this heavily Administration of Forestry, Vietnam frugivorous primate adapts to the seasonal fluctuation of fruit resources in the forest, we 3 Kunming College of Life Science, University of Chinese Academy of Sciences, Beijing, China collected feeding behavior and ranging activity data on one group of southern yellow-cheeked 4 Southern Institute of Ecology, Vietnam crested gibbons in Cat Tien National Park, Vietnam, over 1-year period. We compared these Academy of Science and Technology, HCMC, data to information on phenological patterns at the site gleaned during a prior study. We found Viet Nam that the gibbons gathered most of their food from 69 different plant species and also consumed 5 Center for Integrative Conservation, insects and bird eggs. Fruits were the main dietary item (43.3%), followed by leaves (38.4%), Xishuangbanna Tropical Botanical Garden, flowers (11.6%), and other plant parts (6.0%). A significant seasonal shift in diet was observed; Chinese Academy of Sciences, Menglun, Mengla, Yunnan, China fruit generally dominated the diet in the rainy season and leaves in the dry season. The gibbons Correspondence often started daily activities very early (05:10 am) in the morning and also ended quite early Jin Chen, Key Lab of Tropical Forest Ecology, (16:45 pm) in the afternoon. Socializing was concentrated in the early morning, feeding had a Xishuangbanna Tropical Botanical Garden, bimodal pattern of high activity levels in mid-morning and mid-afternoon, and resting was most Chinese Academy of Sciences, Menglun, Mengla, Yunnan 666303, China. intense at the earliest and latest hours of the day and at midday, with proportionally less time Email: [email protected] used for traveling at these times. Averaged over the annual cycle, the gibbons spent 45% of their Funding information time feeding, 31.9% resting, 14.1% traveling, and 9.0% socializing. The percentage of time Xishuangbanna Tropical Botanical Garden; allocated to different activities varied significantly across months and between the dry and rainy University of Chinese Academy of Sciences seasons. Monthly variation in the activity budget was strongly related to changes in diet. In the rainy season, when the gibbons ate a higher percentage of fruit, they decreased their feeding time, while increasing traveling time in search of food; conversely, in the dry season, when they fed on a higher percentage of leaves, they decreased traveling time. Overall, our results show that the activity budget and diet of the southern yellow-cheeked crested gibbon are associated with seasonal shifts in climate. This study provides information relevant to the conservation and management of this endangered species by identifying important habitat conditions for reintroducing captive animals into the wild and providing insight into dietary needs, which may be relevant to the maintenance of animals in rescue centers.

KEYWORDS activity budget, behavior, Cat Tien National Park, crested gibbon, diet, Nomascus gabriella

1 | INTRODUCTION Foraging primates are forced to make decisions on which resources to exploit to ensure they obtain adequate nutrition and maintain a The determinants of feeding strategies of social primates have been sufficient body condition for survival, reproduction, and territory discussed in terms of costs and benefits of potential behaviors. maintenance. Consequently, many forest primates display varied

Am J Primatol. 2017;79:e22667. wileyonlinelibrary.com/journal/ajp © 2017 Wiley Periodicals, Inc. | 1of14 2of14 | BACH ET AL. feeding behavior in order to adapt to abundance of specific food items behavior, and activity patterns of southern yellow-cheeked crested (Di Fiore & Rodman, 2001; Fan, Fei, & Ma, 2012; Kim, Lappan, & Choe, gibbons. We then explored the relationships among diet, temper- 2012; McConkey, Ario, Aldy, & Chivers, 2003). On the other hand, ature, rainfall, and activity budgets. We tested three specific climate and available resources constrain activity budgets because predictions. First, since the availability of important food resources maintaining energy balance is contingent upon food availability and (e.g., edible fruits) in this forest is very seasonal, we predicted the the ability to exploit those resources. A central concept in life-history gibbons should have a very varied diet and consuming more fruits, theory is that individuals must allocate their energy to competing life- and a greater diversity of fruits, during the fruit rich season, while history traits such as investment in growth and body maintenance, switching to greater consumption of alternative foods during the territory maintenance, reproduction, and predator avoidance (Roff, season of fruit scarcity. Second, since energy intake is likely to 1993; Stearns, 1992). Most of the existing knowledge on activity be highly dependent on the availability of fruit resources, we budgets highlights seasonal variation associated with changes in the hypothesized gibbon should spend more time on more energeti- abundance, quality, or distribution of food resources (Altmann & cally costly activities such as traveling and socializing versus less Muruthi, 1988; Di Fiore & Rodman, 2001; Hanya, 2004; Vasey, 2005). costly activities such as resting during the fruit-rich season than Similarly, some studies have found that, as a consequence of seasonal duringtheseasonwithmorelimitedavailabilityoffruitresources. variation and reduced food availability, animals tend to rely on limited Finally, since time budgets reflect how animals interact with their stationary food resources (Joly & Zimmermann, 2007). environment temporarily in order to support resource acquisition The southern yellow-cheeked crested gibbon is one of seven andreproduction(Defler,1995;DiFiore&Rodman,2001;Fan,Ni, species of crested gibbons in the genus Nomascus (family: Sun, Huang, & Jiang, 2008), we predicted that during the period of Hylobatidae). Gibbons from this genus occur in southern China, food scarcity, gibbon may spend more time per day searching for Vietnam, Laos, and Cambodia. All are endangered or critically food and thus would wake up earlier and go to sleep later than endangered, mostly due to increases in habitat loss and hunting during the season of food abundance. (Geissmann et al., 2008; Groves, 2005; Rawson et al., 2011). Southern yellow-cheeked crested gibbons are distributed east of the Mekong River and south of the Srepok River in Cambodia, and 2 | METHODS south of the Ba River and Srepok River in Vietnam. It has been estimated that approximately 600 groups occur within protected | areas in Vietnam (Duc, Bang, & Covert, 2015; Duc, Bang, & Long, 2.1 Research protocols 2010; Rawson et al., 2011; Thinh, Craik, Thuong, Kha, & Ha Moc, This research was conducted after obtaining necessary permits from 2009), while at least 200 additional groups are estimated to occur Cat Tien National Park and the Vietnam Administration of Forest. The in forest remnants outside protected areas (Duc, Bang, Tinh, & research adhered to the American Society of Primatologists Principles Thang, 2014; Duc et al., 2015). Cat Tien National Park is one of for the Ethical Treatment of Non-Human Primates. the strongholds for this species in Vietnam, with 149 groups recorded and an estimated density of 0.52 (±0.47) and 0.72 2.2 | Study site (±0.08) groups per square kilometer for two different sectors, Cat Loc and Nam Cat Tien (Kenyon, 2008). This research was carried out in the lowland tropical rainforest at Cat Tien In comparison with other gibbon genera, information on the National Park (CTNP) (11°32′N, 107°23′E). This park was designated as a feeding ecology and behavior of Nomascus gibbonsisstillvery protected area in 1978 and upgraded to a National Park in 1992. It is located limited. Nomascus concolor remains the best studied taxon within in southern Vietnam and spreads across three provinces: Lam Dong, Dong the genus, with several studies addressing its feeding ecology Nai, and Binh Phuoc (Figure 1). This study focused on the southern Cat Tien (Chen, 1995; Fan, Ni, Sun, Huang, & Jiang, 2009; Lan, 1989; sector, which has one of the last remaining evergreen and semi-evergreen Sheeran, 1993). Data are also available for N. nasutus (Fan et al., rainforest habitats in Vietnam. It is located in the transitional zone between 2012; Fei et al., 2015; Fan, Fei, Scott, Zhang, & Ma, 2011; two major ecosystems in Vietnam: the southern end of the Dalat Plateau Geissmann et al., 2002), N. annamensis (Channa & Gray, 2009; Hon, and the Mekong Delta (Polet & Ling, 2004). The home range of our study 2016;Traeholt,Bonthoeun,Virak,Samuth,&Vutthin,2006),and group is mostly covered in tall (>40 m) evergreen and semi-evergreen N. hainanus (Liu,Zhang,Jiang,&Charles,1989;Turveyetal., forests, in which most canopy trees become defoliated during the dry 2015). N. leucogenys has had only two studies conducted on it,one season and most sub-canopy trees are evergreen (Forest Inventory and in the late 1980s (Hu, Xu, & Yang, 1990) and another recently Planning Institute, 1993). In the evergreen forest, the dominant tree species (Ruppell, 2013). For the southern yellow-cheeked crested gibbon, are in the genus Dipterocarpus (Dipterocarpaceae), and other important there is only a single, unpublished study, with limited detail species include Dalbergia bariensis, D. mammosa, Afzelia xylocarpa,and (Kenyon, 2008), while N. siki remains unstudied to date. Pterocarpus macrocarpus (all Fabaceae). In the semi-evergreen forest, where The aim of this study is to understand the feeding behavior and the soil is not as deep and is prone to drying, the dominant tree species are activity budget of southern yellow-cheeked crested gibbons living Lagerstroemia calyculata (Lythraceae), Tetrameles nudiflora (Tetramelaceae), in the lowland tropical forests of Vietnam. To address these topics, Anogeissus acuminata (Combretaceae), and Haldina cordifolia (Rubiaceae). we first characterized the diurnal and seasonal diet, feeding Lagerstroemia forms a closed upper canopy, whereas the middle story is BACH ET AL. | 3of14

FIGURE 1 Location and study site of the studied gibbon group in Cat Tien National Park. The photographs show the evergreen forest during the wet season and the semi-evergreen forest during the dry season more fragmented and open, and the understory is species rich, with a dense dry season from November through to April of the following year. ground cover of rattans, vines, shrubs, and grasses. Based on climate data recorded continuously during the study period by the CTNP Meteorological Station, mean annual temperature was 2.3 | Climate 25.0°C, the maximum temperature was 37.2°C (in March), and the The climate in CTNP is tropical with annual monsoons. There are two minimum temperature was 14.3°C (in February). Humidity averaged distinct seasons: A rainy season from May through to October and a 76.4% in the rainy season and 65% in the dry season. The annual 4of14 | BACH ET AL. precipitation was 2,240 mm, falling mainly during the rainy season 2.7 | Data analysis (90.5%). To avoid potential bias, we excluded all behavioral data collected during the 44 incomplete days in this study. Since the number of 2.4 | Study group sampling days varied considerably across months and the start and end time of sampling varied each day, we first converted all records into Three individuals of one gibbon group (one adult male, one adult percentages of the total number of scans recorded per 1 hr time female, and their offspring), which had been habituated to observers interval, day, month, season, and year before analysis. To assess if for 6 months, were monitored from their previous night’s sleeping site significant differences existed in preferred food sources, food items, to the sleeping site of the current day during 10–12 continuous days timing of activities, and seasonal variation, we used non-parametric per month for 12 consecutive months, from October 2014 to Kruskal–Wallis, t-test, multiple comparison Tukey HSD tests, and September 2015. We collected observations for a total of 1,390 hr ANOVA in the R statistical software [3.2.2, R Core Team 2015]. We 45 min during a total of 168 days of sampling, including 124 complete performed Spearman’s rank correlations to test the relationship (sleep tree to sleep tree) and 44 incomplete days. The incomplete days between monthly activity budgets, mean temperature, rainfall, and were primarily due to fighting with other groups, heavy rain, or dense dietary percentages variables. vegetation that prevented us from successfully following the gibbons for the entire day. All data were collected by the first author (Bach Thanh Hai) and two experienced field assistants (Nguyen Van Thuan and Bach Doan Ly). 3 | RESULTS

2.5 | Data collection 3.1 | Overall diet

Feeding, traveling, resting, and social activities of each group member Annually, the gibbon diet was dominated by plant material, although were recorded using scan sampling at 5 min intervals (Altmann, 1974). they occasionally fed on insects and bird eggs. During the study period, The location was recorded continually using a GPS receiver. At each we recorded a total of 69 plant species in 35 families consumed by scan point, we surveyed the group for a total of 1 min, recording the gibbons (appendix I). These included 43 trees (of which 11 species are behavior of all visible members. Each individual was observed for 5 s hemiepiphytic figs), 19 vines, and 7 epiphytes. Fruits were the most and the predominant activity during this interval was recorded. The common food item eaten (43.3%), followed by leaves (38.4%), flowers diet of the gibbons was compiled by directly observing the feeding (11.6%), and other plant parts (buds, petioles, shoots, and roots) (6%). gibbons and collecting food items. A voucher specimen of the plant Insects and bird eggs contributed only 0.5% to the overall diet. Figs being eaten was collected and later identified in the herbaria of the constituted 40.8% of the total fruits consumed. The most commonly Southern Institute of Ecology (Ho Chi Minh city, Vietnam) and the consumed plant species in each month are Ficus kurzii, Sphenodesma Xishuangbanna Tropical Botanical Garden (Yunnan, China). The main thorelii, Diospyros cf sumatrana, Garcinia oliveri, Lagerstroemia ovalifolia, gibbon activities recorded were traveling (brachiating, leaping, Calamus flagellum (appendix II). bridging, bipedal walking, quadrupedal climbing, and walking with Species diversity of the gibbon diet varied seasonally during our additional temporary use of the arms), resting (seating, hanging, study. The number of food species consumed averaged 8.5 ± 2.1 each leaning, lying, sleeping.), feeding (looking for food and water, eating, day, with the total number of species consumed each month averaging and drinking), and socializing (including playing, calling, and grooming). 21.2 ± 4.0. Individual plant species accounted for 0.03–45.9% of the diet each month, with the top three species each month constituting an average of 54.2% of the monthly diet (appendix II). 2.6 | Phenology of fruit production

Between June 2010 and May 2011, three transects 500 m by 1 m were 3.2 | Fruit production pattern randomly set within the southern sector of Cat Tien National Park by one of our co-authors Nguyen Van Thuan for another project. The The fruit availability varied across months and significantly differed numbers of fallen ripe and unripe fruits of all species seen on a 1 m strip between the dry and rainy seasons (t = 3.27, p < 0.01, N =6,t-test); the along transects were counted (for fruits >1 cm diameter) or estimated greatest amount of fruit along the transects occurred between June (for fruits <1 cm diameter). Counts were undertaken between the and September (during the rainy season), while the longest period of middle and end of each month. Only fresh fruits were counted and low fruit availability extended from the beginning of dry season to the fruits were not removed because they would no longer have been 2nd month of the rainy season (appendix III). There was no significant fresh, even if seen in subsequent months. Fruits which had been difference in fruit production among the three transects (H = 0.140, partially eaten, but were fresh, were also recorded. The total number p = 0.932, One Way ANOVA test). There were 50 plant species, total, of all types fruits counted per transect was calculated as the index of in the gibbons’ food species list producing fruits; 42 species (84%) fruit availability, these values were summed up per month (12 months) produced fruits during rainy season, and only 8 species produced fruits and then the index was compared between dry and rainy seasons. in the dry season (16%) (appendix I). Thus, our phenological data BACH ET AL. | 5of14 suggest that the rainy season is indeed a time of greater fruit production and higher fruit variety than the dry season.

3.3 | Feeding behavior

Feeding activity was not evenly distributed throughout the day; feeding activity was highest from 07:00 to 09:00 hr (13.84% and 13.23%), with the earliest feeding event at 05:40 hr and the latest at 16:10 hr (Figure 2). We found contrasting diurnal patterns of feeding during the dry and rainy seasons. During the dry season (Figure 3), when fruits were scarce, fruit was consumed first, while flowers and other plant items were increasingly consumed from morning to evening. By contrast, during the rainy season, when fruits were most available, there were two main peaks and one minor peak of fruit consumption, in the morning, midday, and afternoon (Figure 3). Gibbons started feeding relatively earlier in the morning in the rainy season and finished relatively later in the afternoon in the dry season. Overall, they spent more time feeding in the dry season (Figure 3). The percentages of feeding records allocated to different food items varied significantly among hours of the day (Kruskal–Wallis test, H = 1,221, p < 0.001). Gibbons were predominantly frugivorous during the early hours of the day and gradually reduced their consumption over the course of the day (Tukey HSD tests, morning vs. afternoon, q = 4.02, p < 0.05). In contrast, the proportions of flowers and other plant parts eaten increased from morning to late afternoon (Tukey HSD tests, afternoon vs. morning, q = 4.86, p < 0.05, and q = 4.88, p < 0.05, respectively). Consumption of leaves, insects, and bird eggs did not show any apparent diurnal trend, although they were eaten less in the earliest hours of the day (Figure 2). FIGURE 3 (a) Proportion of feeding time on different food types The percentages of feeding records allocated to different food in the dry season. The solid line with solid dots presents proportion items also varied significantly across months (Kruskal–Wallis test: of number records on all food types for each interval throughout H = 50.69, p < 0.001). Fruit and leaf consumption significantly the day (calculated from 6 month data, gibbon started feeding earlier in rainy season [5:40] and finished later in dry season [16:10]). (b) Proportion of feeding time on different food types in the rainy season. The solid line with solid dots presents proportion of number records on all food types for each interval throughout the day (calculated from 6 month data, gibbon started feeding earlier in raiy season [5:40] and finished later in dry season [16:10])

differed between the wet and dry seasons (Tukey HSD tests, q = 3.41, p <0.05, and q =3.34, p < 0.05, for fruit and leaves, respectively), with the gibbons consuming more leaves and less fruits and flowers in the dry season (Figure 4). The greatest proportions of fruit were eaten in July (75.4%), when ripe fruits of Calamus flagellum, Ficus kurzii,andSphenodesma thorelii were available, and in August (75.1%), when ripe fruits of Dracontomelon dao and Garcinia oliveri were available. High flower consumption FIGURE 2 Daily variation in the proportion of feeding time on corresponded with the flowering season of Sphenodesma thorelii in different food types throughout the day. Calculated from the January (24.5%) and Raphistemma pulchellum in February (35.1%). proportion of 5 min scan observations on each activity in each Leaves were consumed throughout the year, with a peak in interval (1 hr). The solid line with solid dots presents proportion of February (52.4%) and March (54.7%) (Figure 5). Feeding on other number records on all food types for each interval throughout the plant parts (buds, petioles, shoots, and roots) occurred during the day (calculated from whole year data, the smallest proportion of feeding time was 0.16% at 16:00–17:00 and the highest proportion transition period between the dry and rainy seasons and peaked in of feeding time was 13.84% at 8:00–9:00) October (13.6%) (Figure 5). 6of14 | BACH ET AL.

FIGURE 6 The percentage of time allocated to different activities during the day of the gibbon in Cat Tiennational park, Viet Nam, FIGURE 4 Seasonal variation in the proportion of food items by November 2014–September 2015 the southern yellow cheeked-crested gibbons in Cat Tien national park, Viet Nam, November 2014–September 2015: fruit and leaf – consumption differed between seasons (N = 60 Tukey test: df = 4, activities varied significantly across months (Kruskal Wallis test, q = 3.41, p < 0.05, and q = 3.34, p < 0.05). Lower case letters (a,b) H = 41,844, p < 0.001). Resting and social activities showed less indicate significant differences variation over the annual cycle than did either feeding or traveling (Figure 7). Traveling time was lowest in the fruit-scarce dry season, 3.4 | General activity patterns especially in February (7.3%) and was more than three times higher in the fruit rich rainy season (21.5% in August). In contrast, the gibbons Daily activities often began relatively earlier in the dry season than in spent more time feeding during the fruit scarce dry season, with a the rainy season (05:10 vs. 05:25) but ended relatively earlier in the maximum in November (53.4%), than during the fruit rich rainy season, rainy season than the dry season (16:20 vs. 16:45). Morning songs with a minimum in October (35.6%). typically began 30–60 min later than first activity, around dawn (from 05:50 to 07:00). Gibbons spent much time resting in the earliest and 3.5 | The relationships among diet, climate factors, latest hours of the day, and at noon. In contrast, feeding activities were and activity budgets very low during these times and reached peaks from 07:00 to 09:00 and 13:00 to 14:00 hr. Social activities were more intense in the early Across days, the dietary percentage of fruit was negatively correlated hours and at noon, and then reduced. Traveling was more frequent in with the proportion of time spent feeding overall but positively mid-morning and mid-afternoon (Figure 6). correlated with the proportion of time spent traveling (Table 1). By Averaged over the annual cycle, the study group spent 45% of contrast, the dietary percentage of leaves was positively correlated their time feeding, 31.9% resting, 14.1% traveling, and 9.0% in social with the proportion of time spent feeding, but negatively correlated activities. However, the percentage of time allocated to different with the proportion of time spent traveling and resting. Furthermore,

FIGURE 5 Monthly variation in the proportion of food items FIGURE 7 The percentage of time allocated to different activities eaten by the southern yellow cheeked-crested gibbons in Cat Tien across months of the gibbon in Cat Tien national park, Viet Nam, national park, Viet Nam, November 2014–September 2015 November 2014–September 2015 BACH ET AL. | 7of14

TABLE 1 Spearman correlation between dietary percentage and percentage of time budget allocated to different activities of the gibbons in Cat Tien National Park, Viet Nam, November 2014–September 2015 (N = 124 days)

Activity Fruit Leaves Flowers Others rprprprp Feeding −0.241 0.007** 0.371 0.000** −0.203 0.025* −0.060 0.505 Traveling 0.341 0.000** −0.422 0.000** 0.071 0.433 0.125 0.168 Resting 0.089 0.327 −0.183 0.043* 0.122 0.179 0.095 0.297 Socializing 0.062 0.496 −0.128 0.159 0.142 0.118 0.015 0.866

*Correlation is significant at p ≤ 0.05. **Correlation is significant at p ≤ 0.01. the dietary percentage of flowers was only negatively correlated with diet, feeding behavior, and activity budget of a group of individuals the proportion of time spent feeding. This means that the gibbons representing this endangered species. The diet was generally spent more time traveling and less time feeding when more of their dominated by fruits during the rainy season and leaves during the diet consisted of fruit, whereas they spent less time traveling and more dry season, with less consumption of flowers, and other plant parts time feeding when more of their diet consisted of leaves. (buds, shoots, petioles, and roots). This suggests that yellow cheeked- Our results also showed that there was significant relationship crested gibbons at this site are considerably more frugivorous and less between weather conditions and the amount of time allocated to folivorous than reported for other Nomascus species and are slightly different activities. Both daily ambient temperature and precipitation less frugivorous than Hoolock and Hylobates gibbons (Bartlett, 2007). were positively correlated with traveling time but negatively with Although trees are indispensable for the survival of gibbons, we found feeding time (Table 2). This suggests that the gibbons traveled more that this species also consumes plant items from epiphytes and vines, and decreased their feeding time when temperature and rainfall are as well as insects and bird eggs. higher. Daily ambient temperature and precipitation were also The gibbons in this study ate more fruits during periods of high associated the consumption of particular dietary items. Rainfall fruit availability and turned to leaves and other items during periods of positively correlated with fruit consumption but negatively with leaf low fruit availability, consistent with patterns observed elsewhere consumption, whereas temperature positively correlated with flower (Ahsan, 2000; Bricknell, 1999; Chivers, 1974; McConkey, Aldy, Ario, & consumption only (Table 2). Chivers, 2002; McConkey et al., 2003). Fruit is a comparatively rich energy source, containing relatively more carbohydrates per gram, and less fiber than leaves (Hamilton & Galdikas, 1994; Subramaniam, 4 | DISCUSSION 1981). Figs were highly abundant and diverse (11 species) (appendix 1) in our study site, making them a stable food source for gibbons during Using a comprehensive survey of gibbon activities and habitat use the dry season. Given that figs constituted ∼41% of the 43% fruit under natural conditions for 1 year, we were able to characterize the consumed, and that during 8 of the 12 months figs were recorded as the most common fruits consumed (appendix II), our results suggest that figs are essential food resources for this gibbon species, perhaps TABLE 2 Spearman correlation between monthly average because their asynchronous fruiting patterns guarantee a more temperature and precipitation with percentage of time budget reliable food source (Terborgh, 1986). Flowers and buds also are allocated to different activities and diet of the gibbons in Cat Tien likely to be important food items for gibbons as, at other sites (e.g., National Park, Viet Nam, November 2014–September 2015 (N = 124 McConkey et al., 2003), they constitute an important source of days) proteins and carbohydrates. Petioles (Epipremnum giganteum), roots Average temperature (°C) Precipitation (mm) (Epipremnum giganteum), and shoots (Bambusa blumeana) were eaten predominantly at the end of the dry and rainy seasons when other food rprp items and water supplies were scarce (March–April and September– Feeding −0.231 0.010** −0.783 0.001** November). N. gabriellae, like other Nomascus gibbons (N. nasutus, N. Traveling 0.301 0.000** 0.860 0.000** concolor, and N. leucogenys), occasionally ate insects and bird eggs, but − Resting 0.117 0.197 0.059 0.517 unlike some species of Hylobates (Bartlett, 2007) and N. concolor (Fan Socializing 0.004 0.965 −0.159 0.079 et al., 2009), we did not observe them preying on other vertebrates. Fruit −0.032 0.720 0.231 0.010** Large monthly variation in dietary proportions and diversity were Leaves 0.016 0.860 −0.289 0.001** found in the yellow checked crested gibbons, indicating that the taxon Flowers 0.256 0.004** −0.042 0.644 may adapt its feeding behavior to seasonal weather conditions. Others 0.056 0.538 −0.085 0.349 The southern yellow cheeked-crested gibbons ate more fruit

*Correlation is significant at p ≤ 0.05. (including figs) in the early hours of the day with reductions in amounts **Correlation is significant at p ≤ 0.01. through the course of the day. This diurnal pattern is consistent with 8of14 | BACH ET AL. findings from other gibbon species, including species of Hoolock, leaves (Nakagawa, 1989). During such periods, gibbons may spend Symphalangus, and Hylobates (Ahsan, 2000; Bartlett, 2007; Fan et al., less time singing and playing to conserve energy. Bartlett (1999) 2009). Being predominantly frugivorous during the early hours of the identified in lar gibbons a similar pattern of energy conservation day may allow gibbons to undertake energetically expensive activities during periods of fruit shortage. in the morning and mid-day, because the sugars in fruit are a rich In this study, gibbons decreased traveling time and increased source of energy that is readily and rapidly absorbed (Raemaekers, feeding time to decrease energy loss when the temperature and 1978; Vasey, 2005). This pattern was consistent with the daily rainfall was low. Traveling is energy-consuming (Bramblett, Quick, & patterns observed during both the dry and rainy seasons, providing Bramblett, 1976), and it is difficult to maintain an energy-conserving further support to previous findings that fruit provide readily posture while traveling (brachiating, jumping, or climbing) versus accessible energy immediately after sleep or rest (Clutton-Brock, resting periods (Bicca-Marques & Calegaro-Marques, 1998). Rainfall 1977; Oates, 1986). In contrast, flowers and other plant parts are was also strongly positively correlated with percentage of fruit eating eaten later and then increase in the late afternoon, while leaves, and negatively correlated with percentage of leaf eating. In summary, insects, and bird eggs tend to be eaten around midday. Consumption of the behavior (time allocation and diet) of the southern yellow-cheeked protein- and fiber-rich food items during the late afternoon allows time crested gibbon seems to shift seasonally along with climate factors and for their digestion overnight (Chapman & Chapman, 1991; Glander, fruit availability. 1982; Milton, 1979). Understanding feeding ecology and activity is important for the Resting and social activities showed less variation over the annual long-term conservation of the little known and highly threatened cycle than did feeding or traveling time, suggesting that the gibbons gibbons. The need to conserve remaining patches of mature forest and respond to climate seasonality and seasonal variation of food to protect favored trees that sustain wild populations of gibbons is a resources and water availability mainly by adjusting their time spent major priority. Our study provides a better understanding of the feeding and traveling. Many animals, including gibbons, adjust their behavior of yellow-cheeked gibbons, which can inform reserve feeding behavior based on temporal variation in available food managers of the season, time, and areas where increased patrolling resources (Asensio, Korstjens, & Aureli, 2009); when food is scarce, efforts may be needed. The data collected in this study also provide animals may pursue different coping strategies, such as changing their useful scientific information for assisting primate rescue centers in home range size (Brockman & van Schaik, 2005; Van Schaik, Terborgh, designing diet and feeding schedules for pre-release gibbons as well as & Wright, 1993). Feeding had a bimodal pattern of high activity levels time of release and habitat selection when reintroduction programs in mid-morning and mid-afternoon, whereas resting was most intense are undertaken for those rescued animals. at the earliest and latest hours of the day, and noon, with proportionally less time used for traveling. This pattern is consistent ACKNOWLEDGMENTS with that of agile gibbons (Gittins, 1982). This study was supported by Xishuangbanna Tropical Botanical Comparatively, N. gabriellae spent more time feeding (39%), Garden and University of Chinese Academy of Sciences. Our gratitude and less time traveling than two closely related species, N. concolor goes to Cat Tien National Park for allowing the research, Dr. Luu Hong (Fan & Jiang, 2008) and N. leucogenys (Ruppell, 2013). Though N. Truong for botanical identification, Bach Doan Ly for field assistance, ’ gabriellae s time spent resting is relatively shorter than N. concolor,it and Prof. Richard Corlett, Dr. Kim McConkey and Prof. Bert Covert is very similar to other gibbons (e.g., N. leucogenys). Feeding has for their valuable comments. Finally, we are grateful to Dr. Paul A. priority over other activities, and food is one of the most important Garber and anonymous reviewers for their valuable comments and ’ environmental factors that constrain an animal s activity budget editing of this manuscript. (Hanya, 2004; O’brien & Kinnaird, 1997). Our results reveal that significant monthly variation in activity budgets was strongly related to monthly changes in diet. There are fewer available calories per REFERENCES gram in fresh leaves than in ripe fruit pulp (Raemaekers, 1978). Agetsuma, N., & Nakagawa, N. (1998). 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APPENDIX I

Food Species Consumed and Months Consumed by the Southern Yellow Cheeked Crested Gibbons in Cat Tien National Park from November 2014 to September 2015: Life Form, Part Eaten, and Relative Proportion of Food Species During Study Period 12 of 14 | BACH ET AL.

Life form: T, tree; V, vine; E, epiphyte; T/H, tree or hemi epiphytes. Part eaten: Fr, fruit; YL, young leaves; L, mature leaves; FL, flowers; B, buds; S, shoots; P, petioles; R roots. Of the 50 plant species which produced fruits in the gibbons’ diet list, 42 species produced fruits during rainy season (84%). And of the 24 plant species which produced young leaves in the gibbons’ diet list, 20 species produced leaves during dry season (83%). BACH ET AL. | 13 of 14

APPENDIX II

Number of Plant Species Consumed, Main Food Species, and Their Percentages of the Feeding Records in Each Month

Month Number of hours observed Number of plants fed on Main food species Percentage of records Jan-15 141 hr 15 m 18 Ficus benjamina 23.8 Sphenodesma thorelii 24.5 Ficus sumatrana 13.3 Feb-15 46 hr 00 m 15 Raphistemma pulchellum 35.1 Sphenodesma thorelii 20.0 Rothmannia eucodon 11.8 Mar-15 144 hr 10 m 24 Sphenodesma thorelii 19.0 Carallia brachiata 16.6 Diospyros cf sumatrana 11.8 Afzelia xylocarpa 10.2 Apr-15 148 hr 45 m 30 Parabarium sp. 16.1 Unidentified vine (sp) 16.1 Diospyros cf sumatrana 12.8 Ochrocarpus siamensis 11.0 May-15 100 hr 50 m 24 Ficus kurzii 18.0 Diospyros cf sumatrana 16.6 Lagerstroemia ovalifolia 12.6 Afzelia xylocarpa 12.0 Jun-15 119 hr 10 m 21 Ficus kurzii 20.3 Calamus flagellum 18.5 Sphenodesma thorelii 14.5 Jul-15 97 hr 55 m 20 Calamus flagellum 24.5 Ficus kurzii 18.2 Xerospermum noronhianum 15.0 Aug-15 121 h 25 m 21 Dracontomelon dao 45.9 Garcinia oliveri 10.8 Ficus kurzii 10.1 Sep-15 86 hr 25 m 23 Garcinia oliveri 28.9 Ficus kurzii 13.2 Oct-14 95 hr 55 m 22 Ficus cf. costata 18.5 Rothmannia eucodon 13.1 Pothos scandens 12.6 Lagerstroemia ovalifolia 11.3 Nov-14 133 hr 20 m 20 Lagerstroemia ovalifolia 24.4 Ficus cf. costata 16.2 Grewia tomentosa 12.6 Sphenodesma thorelii 10.4 Dec-14 110 hr 35 m 16 Ficus benjamina 25.0 Lagerstroemia ovalifolia 19.8 Sphenodesma thorelii 10.4 Total 1,390 hr 45 m 69 14 of 14 | BACH ET AL.

APPENDIX III

Average Number of Fruit Counted per Transect During June 2010 to May 2011 in Cat Tien National Park