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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
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