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Dietary Adaptations of Assamese Macaques (Macaca Assamensis) in Limestone Forests in Southwest China

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Dietary Adaptations of Assamese Macaques (Macaca Assamensis) in Limestone Forests in Southwest China American Journal of Primatology 77:171–185 (2015) RESEARCH ARTICLE Dietary Adaptations of Assamese Macaques (Macaca assamensis)in Limestone Forests in Southwest China ZHONGHAO HUANG1,2, CHENGMING HUANG3, CHUANGBIN TANG4, LIBIN HUANG2, 5 1,6 2 HUAXING TANG , GUANGZHI MA *, AND QIHAI ZHOU ** 1School of Life Sciences, South China Normal University, Guangzhou, China 2Guangxi Key Laboratory of Rare and Endangered Animal Ecology, Guangxi Normal University, Guilin, China 3National Zoological Museum, Institute of Zoology, Chinese Academy of Sciences, Beijing, China 4College of Forest Resources and Environment, Nanjing Forestry University, Nanjing, China 5The Administration of Nonggang Nature Reserve, Chongzuo, China 6Guangdong Institute of Science and Technology, Zhuhai, China Limestone hills are an unusual habitat for primates, prompting them to evolve specific behavioral adaptations to the component karst habitat. From September 2012 to August 2013, we collected data on the diet of one group of Assamese macaques living in limestone forests at Nonggang National Nature Reserve, Guangxi Province, China, using instantaneous scan sampling. Assamese macaques were primarily folivorous, young leaves accounting for 75.5% and mature leaves an additional 1.8% of their diet. In contrast, fruit accounted for only 20.1%. The young leaves of Bonia saxatilis, a shrubby, karst‐ endemic bamboo that is superabundant in limestone hills, comprised the bulk of the average monthly diet. Moreover, macaques consumed significantly more bamboo leaves during the season when the availability of fruit declined, suggesting that bamboo leaves are an important fallback food for Assamese macaques in limestone forests. In addition, diet composition varied seasonally. The monkeys consumed significantly more fruit and fewer young leaves in the fruit‐rich season than in the fruit‐lean season. Fruit consumption was positively correlated with fruit availability, indicating that fruit is a preferred food for Assamese macaques. Of seventy‐eight food species, only nine contributed >0.5% of the annual diet, and together these nine foods accounted for 90.7% of the annual diet. Our results suggest that bamboo consumption represents a key factor in the Assamese macaque’s dietary adaptation to limestone habitat. Am. J. Primatol. 77:171–185, 2015. © 2014 Wiley Periodicals, Inc. Key words: Assamese macaque; Macaca assamensis; dietary adaptations; limestone forests INTRODUCTION more fruit and fewer leaves than those of the Murree Typical diet varies widely among primate species Hills in northwest Pakistan (34% vs. 9% of total diet [Bicca‐Marques, 2003; Campbell et al., 2007; Chap- for fruits, 9% vs. 84% for leaves) [Feeroz, 2011; man et al., 2002, 2006; Chapman & Chapman, 1999; Feeroz, 2012; Harris & Chapman, 2007; Lindburg, Contract grant sponsor: National Natural Science Foundation of 1977; Olupot, 1998; Strier, 1991; Tutin, 1999]. While China; contract grant numbers: 31172122, 31301893, 31360093, macaques in general are regarded as frugivores 31372145; contract grant sponsor: Guangxi Natural Science fi Foundation; contract grant number: 2012 GXNSFBA053045; [Tsuji et al., 2013], interspeci c differences are still contract grant sponsor: Guangxi Key Laboratory of Rare and considerable. For instance, macaques living in the Endangered Animal Ecology, Guangxi Normal University; tropics tend to consume more fruit and fewer leaves contract grant number: 1301z009. than temperate‐living macaques [Hanya, 2004; Tsuji Conflict of interest: None. et al., 2013]. Fruit accounted for approximately 80% ÃCorrespondence to: Guangzhi Ma, College of Life Science, of diet of Sulawesi Tonkean macaques (Macaca South China Normal University, 55# West Zhongshandadao, Guangzhou, Guangdong, China. E‐mail: [email protected] tonkeana) [Riley, 2007], in contrast with only 4.3% ÃÃCorrespondence to: Qihai Zhou, Guangxi Key Laboratory of for Barbary macaques (M. sylvanus) in Algeria Rare and Endangered Animal Ecology, Guangxi Normal Univer- sity, 15# Yu Cai Road, Guiling, Guangxi, China. [Hanya et al., 2011]. Even within species, different E‐mail: [email protected] populations may display widely divergent diets, especially in species with large geographic distribu- Received 28 March 2014; revision accepted 9 July 2014 tions. Rhesus monkeys (M. mulatta) living in the DOI: 10.1002/ajp.22320 northeast of the Moulavi Bazar Forest Range of the Published online 17 September 2014 in Wiley Online Library Sylhet Forest Division, Bangladesh consumed much (wileyonlinelibrary.com). © 2014 Wiley Periodicals, Inc. 172 / Huang et al. Goldstein & Richard, 1989]. Variation in fruit Rogers, 2006; Zhou et al., 2006]. However, there is consumption most likely reflects a difference in fruit little seasonal change in fruit abundance in Assamese availability [Tsuji et al., 2013], since fruit is a macaque habitat in northeastern Thailand [Heesen preferred food for primates [Richard, 1985]. Thus, a et al., 2013]. The lean period for fruit appears to last correlation between the greater abundance of fruit in longer in limestone hills than in tropical forests, the tropics than in temperate habitats and the where fruit is more or less available throughout the increased fruit consumption of tropical macaques year [Ting et al., 2008]. The low plant biomass of may be expected [Hanya et al., 2013]. limestone forests undoubtedly contributes to this Seasonal dietary variation among macaques has difference [Ji & Tang, 2008]. Therefore, in contrast to also been observed [Tsuji et al., 2013]. Macaques tropical macaques, we predicted that Assamese inhabiting forests where fruit only appears at certain macaques in limestone forests would rely more times of the year have evolved flexible feeding heavily on leaves and other vegetative plant parts strategies in response to this seasonal scarcity [Hanya than Assamese macaques in more productive habitat. et al., 2011; Hill, 1997; Richter et al., 2013; Su & Protein‐rich young leaves can also be a preferred Lee, 2001]. Japanese monkeys (M. fuscata) consume food for primates [Richard, 1985], but young leaves large amounts of fruit when available but rely on are also periodically scarce in limestone forests mature leaves when fruit is scarce [Hanya, 2004; [Li & Rogers, 2006; Zhou et al., 2006]. Primates in Hanya et al., 2011; Tsuji et al., 2006]. this habitat may adjust their diets accordingly, Quantitative information on the dietary habits of increasing consumption of mature leaves in large Assamese macaques reflects the trends described quantities only when fruit and young leaves above. These monkeys are primarily frugivorous in become largely unavailable [e.g. Trachypithecus tropical forests [Heesen et al., 2013; Schülke francoisi, Huang et al., 2010; Zhou et al., 2006]. et al., 2011] but folivorous in temperate forests at Although mature leaves re abundant, they also higher latitudes [Ahsan, 1994; Srivastava, 1999]. In have higher cellulose content, restricting nutrient the low‐altitude tropical forests of Northern Thailand, absorption [Richard, 1985]. Mature leaves usually Assamese macaques relied heavily on fruit (42–59% of serve as fallback foods for primates [Hemingway total diet) and animal matter (22–24%), only supple- and Bynum, 2005; Lambert, 1998; Marshall and menting their diets with leaves (13–21%) [Heesen Wrangham, 2007], and therefore, we expected that et al., 2013; Schülke et al., 2011]. In contrast, they Assamese macaques in limestone forests would use consumed more leaves (46–52%) than fruits (11–23%) mature leaves as a fallback food in the lean season, in the temperate forests of Bangladesh and India, when both fruit and young leaves were scarce. which also occur at higher altitude [Ahsan, 1994; Zhou et al. [2011] reported a preliminary study of Srivastava, 1999]. This variation most likely reflects the diet of Assamese macaques in limestone forests. differences in food availability, as well as the However, they collected only 1259 feeding records macaques’ behavioral flexibility in foraging, an from two groups over a 10‐month period. Their important factor in this species’ biology. results did not allow full documentation of seasonal Assamese macaques are distributed from central variation in food availability and diet. As Hanya Nepal east through the Himalayas to southern- [2004] suggested, to determine species‐specific feed- most China and north and central Southeast Asia ing characteristics, dietary composition should be [Fooden, 1982]. They occupy a range of habitats that investigated quantitatively for 1 year at least for includes monsoon evergreen broadleaf forests, decid- as many populations as possible. In this paper, we uous broadleaf forests, mixed broadleaf and conifer present quantitative data on the diet and food forests, and conifer forests [Zhang, 1997]. In Guangxi availability of Assamese macaques for 12 consecutive Province, southwest China, Assamese macaques are months in limestone forests at Nonggang National restricted to limestone forests [Jiang et al., 1993; Nature Reserve. We first summarize data on dietary Wada et al., 2010]. In this habitat, soil is predomi- composition and seasonal changes in the diet, then nantly distributed in the valleys and basins of the analyze the relationship between food choice and rocky hills, and water is nearly absent on the rock floristic composition. Finally, we compare our results surface [Chen, 1988; Hu, 1988]. There is a lower plant with the predictions described above and explore how biomass on the hills with bare stone faces than the
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