American Journal of Primatology 77:171–185 (2015)

RESEARCH ARTICLE Dietary Adaptations of Assamese (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 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 , 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 ’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 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% Correspondence 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% Correspondence 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 , 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 Assamese macaque has adjusted its dietary on hills still covered with soil [Liang et al., 1988]. strategy to living in limestone habitat. Moreover, the limestone forests of southwestern Guangxi province are characterized by seasonally fl variable rainfall, which may in uence fruiting METHODS phenology [Zhou et al., 2006]. Fruit production correlates strongly with rainfall in limestone forests, Study Site and Study Subjects resulting in a period of low fruit abundance from The study population inhabits the Nonggang October to March, thus causing resident primates to National Nature Reserve, southwest Guangxi experience dramatic fluctuations in availability [Li & Province, China (22°2902500N, 106°5303300E, Fig. 1).

Am. J. Primatol. Dietary Adaptations of Assamese Macaques / 173

Fig. 1. Location and the surrounding area of the study site in Nonggang Nature Reserve, Guangxi, Southwest China.

This reserve consists of limestone hills ranging in core area of the macaques’ home range, where more altitude from 400 to 600 m a.s.l., covered by than 80% of daily activity occurred (unpublished limestone seasonal rainforests [Guangxi Forestry data), and covered approximately 2% of the mac- Department, 1993]. The main study site is located aques’ annual home range. We could not set up plots on the edge of the reserve (Fig. 1), which is partly on bare cliffs because they were inaccessible. Within surrounded by small‐scale agricultural plots. Graz- each plot, we recorded and identified both trees and ing pressure from livestock (cattle) is high at this woody lianas with diameter at breast height (DBH) location. 3 cm. We recorded a total of 1,836 trees and woody We collected data on climate, including minimum lianas. For unidentified plant species, we collected temperature (Tmin), maximum temperature (Tmax), specimens and took auxiliary photos for later and rainfall. The lowest mean monthly minimum identification with the help of botanists from Guangxi temperature was 6.1°C in January 2013, whereas the Institute of Botany, Chinese Academy of Sciences. highest mean monthly maximum temperature was To evaluate the dominance of each species within 31.3°C in June 2013 (Fig. 2). During the study period, a plot, we calculated the relative density (RD), total rainfall was 1055 mm. relative frequency (RF), and relative coverage (RC) We followed one group of Assamese macaques for each species as follows: RD ¼ number of individu- composed of 14 individuals (two adult males, six als of species i/total number of individuals in all plots; adult females, and six juveniles) at the beginning of RF ¼ number of plots with species i/total number of the study period, increasing to 16 individuals with plots; and RC ¼ sum of basal areas of species i/sum of the birth of two infants. We could not reliably identify basal areas of all species. Then we expressed the individuals by age class. Individuals could be app- Dominance (D) by summing RD, RF, and RC [Burton roached to 40 m before fleeing. et al., 2005]. Based on previous studies of Assamese macaques [Zhou et al., 2011] and our own 3‐month pilot study, Food Availability Assessment we selected 20 plant food species for phenology To investigate vegetation composition, we sam- monitoring. We randomly selected and tagged 10 pled from 24 plots (20 m 20 m) within the main individuals of each species in the main study area, study site: 4 in the valley basin, 18 on the hillsides, and monitored a total of 200 trees. At the end of each and 2 on the hilltops. These plots were located in the month, we visually inspected all tagged trees for the

Am. J. Primatol. 174 / Huang et al.

Fig. 2. Daily average temperatures (maximum and minimum) and rainfall at the study site according to month.

presence of young leaves, flowers, and fruit, scoring August 2013 after 3 months of habituation from their abundance (% of crown cover) with a 5‐point June to August 2012. During each full‐day follow, we scale: 0 ¼ absent, 1 ¼ 0.1–25%, 2 ¼ 25.1–50%, began behavioral observation after locating the 3 ¼ 50.1–75%, and 4 ¼ 75.1–100%. We separately macaques near their sleeping sites at dawn and calculated monthly food availability index (FAI) for ended at nightfall, without losing contact with main food items (young leaves, flowers, and fruits) monkeys for more than 30 min. During each par- by integrating the density, basal area, and pheno- tial‐day follow, we began data collection whenever logy scoreP of plant species with the formula as we located the macaques, and ended when they ¼ n FAI i¼1 DiBiPi, where Di is the density of the disappeared for over 30 min or entered a sleeping tree species i (number of stem/ha), Bi is the average site. Most of the partial‐day follows occurred basal area of tree species i (m2/ha), and Pi is the mean when macaques moved to the hilltops for resting phenology score of particular food item in the crown of at noon. We used instantaneous scan sampling species i in a given month [Albert et al., 2013]. [Altmann, 1974], with scans starting every 15 min Based on Zhou et al. [2011], we expected the and lasting 5 min. To avoid sampling bias toward young, infolded leaves of a small shrubby bamboo, certain individuals, we scanned the group from left to Bonia saxatilis, to be the most important food right or in a clockwise sweep, and collected behavioral for Assamese macaques in limestone habitats. To records on as many different individuals as possible. assess the distribution and abundance of this plant, During the study period, we obtained a total of 17,186 we set up a 5 m 5 m sub‐plot in the center of individual records from 3,616 scans (Table I), with an each 20 m 20 m plot, and recorded the numbers of average of 4.8 individuals per scan. More than 80% of individuals of this bamboo. We also opportunistically the scans came from the 66 full‐day follows and the tagged 10 bamboo clumps to assess the relative rest from 58 partial‐day follows. availability of young leaves at the end of each month. During each scan, we recorded the predominant Following a method modified from Franklin [2005]. behavior of each individual after observing it for 5 sec. We visually estimated the abundance of young We categorized behavior as follows: resting, moving, bamboo leaves as the percentage of terminal branch- feeding, grooming, playing, and other (behavior not lets with young leaves in each clump, which we scored encompassed by any of the five previous classes). We on a 5‐point scale as described above. We expressed defined feeding as manually or orally manipulating a the monthly availability indices of young bamboo food item. When an individual fed, we noted the plant leaves as the percentage of the maximum possible species and parts eaten, including young leaves, phenology score of all bamboo clumps monitored. mature leaves, flowers, fruit, seeds, bark, petioles, stems, or unknown. We also recorded plant species eaten by the monkeys via ad libitum sampling Behavioral Data Collection [Altmann, 1974]; we used these records in a food H.Z.H collected behavioral data with assistance species list, but not when assessing contributions to from field guides between September 2012 and the monthly diet.

Am. J. Primatol. Dietary Adaptations of Assamese Macaques / 175

TABLE I. Diet Characteristics of Assamese Macaques in Limestone Forests of Nonggang

Dietary compositiona Food Observation Young Mature Number of diversity days per Total Feeding Month leavesb leaves Flowers Fruits Othersc food species index month scans records

Sep‐12 59 (58.9) 0.4 0 40.6 0 19 1.3 8 176 461 Oct 71.4 (69.1) 3.9 0 24.5 0.2 18 1.1 9 220 465 Nov 94.5 (94.1) 2.4 0.3 1.7 1.1 19 0.4 12 336 798 Dec 94.8 (93.1) 2.5 0 1.7 0.9 16 0.4 11 327 579 Jan‐13 81.8 (80.3) 10 0 1 7.2 26 1.0 14 427 687 Feb 97.5 (92.1) 0 0 2.5 0 7 0.4 6 210 297 Mar 85.6 (66.8) 0.2 6.3 4.8 3.1 34 1.6 13 412 568 Apr 69.8 (60.7) 2.5 7.7 19.5 0.6 21 1.6 14 385 486 May 63.9 (60.3) 0 1.8 33 1.3 17 1.4 8 234 328 Jun 49.6 (48.8) 0 0 50.4 0 13 1.3 9 301 457 Jul 69.7 (64.2) 0 0 29.5 0.8 16 1.4 12 313 356 Aug 68.1 (65.9) 0 0 31.9 0 12 1.2 8 275 381 Annual Mean 75.5 (71.2) 1.8 1.3 20.1 1.3 18.2 1.1 10.3 301.3 488.6 SD 15.3 (15.1) 2.9 2.7 17.4 2.1 6.9 0.5 2.7 81.4 148.8 Fruit‐lean 90.9 (85.3) 3 1.3 2.3 2.5 20.4 0.8 11.2 342 585.8 season meand SD 6.8 (11.7) 4.1 2.8 1.5 2.9 10.2 0.6 3.1 86.3 186.4 Fruit‐rich 64.5 (61.1) 1 1.4 32.8 0.4 16.6 1.3 9.7 272 419.1 season meand SD 7.9 (6.5) 1.6 2.9 10.2 0.5 3.2 0.2 2.4 69.1 62.6 aPercentage of feeding time (see text for details). bNumber in bracket represent % of feeding time spent on young leaves of the bamboo (Bonia saxatilis). cIncluding stems, petioles, barks, seeds, invertebrates, unknown parts, and other items. dFruit‐lean season included months between November 2012 and March 2013, while fruit‐rich season included the rest months of study period.

Data Analysis <20% of data collection days. When we examined the Following Hanya and Bernard [2012] and Shaffer proportion of the diet on monthly and annual scales, ‐ [2013], we expressed diet composition as the percentage we did not detect a difference for full day versus ‐ ‐ > of time spent feeding on various items/species. We partial day data (T test, P 0.9 for all variables), fi first divided the number of individuals devoted to suggesting no signi cant bias introduced by observa- feeding on particular items/species for each scan tion conditions. We used the Shannon–Weaver Diversity Index, by the total number of individuals recorded in that n 0 P scan, then divided this value by the proportion of H ¼ Pi ln Pi (where Pi is the percentage of individuals engaged in feeding activity to determine i¼1 the percentage of feeding time spent on given items/ feeding records of the plant species i) to express species for that scan. We averaged the data for dietary breadth. We also assessed food selection on an each hour to correct for potential bias introduced by annual basis with a selectivity index (S‐index), which uneven scan records across the day before we we calculated as the percentage of feeding time for averaged these percentages within each month to a particular species in the diet divided by its relative determine monthly percentages of feeding time basal area in the habitat. A value >1 indicates spent on given items/species. We expressed seasonal preference for this species [Hu, 2011; Mekonnen and annual dietary composition as the average et al., 2010]. proportion across the relevant months. It is possible We tested all variables with a one‐sample that the amount of bamboo in the diet is an over- Kolmogorov‐Smirnov Test to examine normality. estimate because of the way we located the monkeys FAIs and monthly percentages of food item and on partial observation days. During partial‐day species in feeding time were not transformed since all observations, we located macaques primarily by their of them were normally distributed. (P > 0.05 for all calls and the sound of their movements. We detected variables). We therefore employed T‐tests to compare them most easily when they were in the bamboo the seasonal variation for all variables, and Spear- clumps where the sound was most loud, probably man rank correlations for relationships between leading to overestimate bamboo feeding records. them. All tests were 2‐tailed, with significance levels However, partial observation days only account for of 0.05.

Am. J. Primatol. 176 / Huang et al.

This research adhered to the American Society Overall Diet and Importance of Bonia of Primatologists’ principles for the ethical treat- saxatilis ment of nonhuman primates. All data collection During the study period, we identified 78 food and analysis complied with protocols approved by plant species, of which 72 were recorded in scans and the appropriate wildlife conservation committees of 6 ad libitum. In addition, Assamese macaques fed on China and adhered to the legal requirements of fungus and invertebrates. Of plant species, trees China. were the most common type consumed (65% of food species), followed by vines (23%), bushes (8%), herbs RESULTS (3%), and epiphytes (1%). Assamese macaques were primarily folivorous, Seasonal Changes in Resource Availability spending 75.5% of their time feeding consuming Phenology changed significantly between young leaves, and an additional 1.8% on mature months (Fig. 3). Young leaves were abundant during leaves (Table I). Fruit and flowers contributed to the transitional period between the fruit‐lean season 20.1% and 1.3% of time spent feeding, respectively. and the fruit‐rich season, with peaks in March and Other items (including petioles, stems, bark, seeds, May 2013. Similarly, flowers were mainly available invertebrates, and unknown items) accounted for a in February and March 2013. To more easily discuss negligible 1.3% of the annual diet in total. results based on fruit abundance, we defined a fruit‐ Bonia saxatilis, a shrubby bamboo, is the most lean season from November 2012 to March 2013 with important food for Assamese macaques at Nonggang. <500 monthly fruit FAI, and a fruit‐rich season in the This bamboo is densely distributed in the upper half remainder of the study period with >500 monthly of the limestone hills’ middle vertical zone, with a fruit FAI. Based on the average monthly FAI values, density of 21,814 individuals/ha on average in the fruit availability was significantly higher in the fruit‐ habitat. Young bamboo leaves were available in large rich season than in the fruit‐lean season (t ¼ 6.438, quantities throughout the year, with a peak between df ¼ 10, P < 0.001), peaking in June 2013. The March and May (Fig. 3). Monthly availability index availability of young leaves and flowers did not differ for bamboo young leaves did not vary according to significantly according to seasons (t ¼ 0.057, df ¼ 10, season (t ¼ 0.31, df ¼ 10, P ¼ 0.763). These bamboos P ¼ 0.955 for young leaves; t ¼1.063, df ¼ 10, contributed to 71.2% of the annual diet, and their P ¼ 0.334 for flowers). Furthermore, there was a young leaves accounted for 92.4% of all leaf consump- significant positive correlation between monthly tion and 94.5% of young leaf consumption. Moreover, fruit availability and rainfall (rs ¼ 0.762, N ¼ 12, Assamese macaques consumed this item year‐round; P ¼ 0.004). it represented between 48.8% and 94.1% of the

Fig. 3. Food Availability Index (FAI) for young leaves, flowers, fruits, and bamboo young leaves in the study site between September 2012 and August 2013.

Am. J. Primatol. Dietary Adaptations of Assamese Macaques / 177

monthly diet (Table I). The macaques consumed young leaves) in large quantities. In contrast, the more young bamboo leaves in the fruit‐lean season fruit of Caryota ochlandra and the mature leaves of than the fruit‐rich season (t ¼4.597, df ¼ 10, Trachelospermum brevistylum were consumed in P ¼ 0.001). The consumption of this item increased large quantities only during the fruit‐lean season. as fruit consumption decreased (rs ¼0.888, N ¼ 12, The number of food species consumed, as well as P < 0.001), and as food diversity decreased (rs ¼ dietary diversity, differed by month. The number of 0.727, N ¼ 12, P ¼ 0.007). We tested the relation- monthly food species varied from 7 to 34 (mean SD: ship between the monthly consumption of this item 18.2 6.9, N ¼ 12), and monthly diversity index and the availability index for bamboo young leaves, ranged from 0.4 to 1.6 (1.1 0.5, N ¼ 12) (Table I). and found no significant correlation (rs ¼0.307, However, we found that the fruit‐rich and fruit‐lean N ¼ 12, P ¼ 0.332). season did not differ significantly in the monthly number of food species consumed, or food species diversity (t ¼0.81, df ¼ 10, P ¼ 0.458 for species Seasonal Variations in Diet number, and t ¼ 2.158, df ¼ 10, P ¼ 0.09 for diversity). There was significant seasonal variation in which types of foods Assamese macaques consumed most frequently (Table I). They ate significantly more fruit Forest Composition and Food Choice and fewer young leaves in the fruit‐rich season than In vegetation plots, we recorded a total of 111 in the fruit‐lean season (t ¼ 6.502, df ¼ 10, P < 0.001 plant species from 84 genera belonging to 44 families. for fruits; and t ¼6.052, df ¼ 10, P < 0.001 for young The dominance value of the 10 most important tree leaves). Across months, fruit and leaf (sum of young species ranged from 0.39 to 0.99 (Table II). The 10 leaves and mature leaves) consumption correlated most dominant families were Euphorbiaceae, Mor- negatively (rs ¼0.930, N ¼ 12, P < 0.001). Monthly aceae, Ebenaceae, Tiliaceae, Poaceae, Meliaceae, fruit consumption positively correlated with avail- Sterculiaceae, Verbenaceae, Rubiaceae, and Sapin- ability (rs ¼ 0.804, N ¼ 12, P ¼ 0.002). However, daceae, respectively, which accounted for 74.3% of the the consumption of flowers and mature leaves did total stems (range: 2.5–16.5%). not show significant seasonal variation (t ¼ 0.019, Of 78 food species, only nine appeared to be staple df ¼ 10, P ¼ 0.985 for flowers; t ¼1.236, df ¼ 10, food species that each accounted for greater than P ¼ 0.245 for mature leaves). Other items including 0.5% of the annual diet (Table III). Together, these petioles, stems, bark, and seeds were ingested only in nine staple foods contributed 90.7% of the annual the fruit‐lean season, although differences between diet. For each month, the top three food species seasons were not statistically significant as these accounted on average for 88.9% of that month’s diet foods were rarely consumed (t ¼1.579, df ¼ 10, (Table IV). Of the staple foods, four plant species were P ¼ 0.187). Consumption of most plant species varied preferentially selected (with a >1S‐index; Table III). by season with the exception of Bonia saxatilis. All of them together contributed to 82.9% of fruit During the fruit‐rich season, when food was more feeding time, of which Streblus indicus accounted for available, the monkey consumed the fruit of Can- the most, followed by Sinosideroxylon pedunculatum thium dicoccum, Ficus microcarpa, Iodes vitiginea, var. pubifolium, Caryota ochlandra, Canthium di- Sinosideroxylon pedunculatum var. pubifolium (in- coccum, Ficus microcarpa, Iodes vitiginea, and cluding flowers), and Streblus indicus (including Trachelospermum brevistylum.

TABLE II. Dominance of 10 the Most Common Tree Species in the Vegetation Plotsa

Density Mean Relative Relative Relative % of stems Species Family (individuals/ha) DBH(cm) density frequency coverage Dominance for family

Diospyros siderophylla Ebenaceae 187.5 8.5 0.1 0.79 0.1 0.99 12.1 Streblus indicus Moraceae 102.1 8.0 0.05 0.54 0.03 0.63 15.5 Vitex kwangsiensis Verbenaceae 66.7 13.3 0.03 0.5 0.06 0.60 3.5 Excentrodendron Tiliaceae 56.3 10.7 0.03 0.46 0.04 0.53 7.3 tonkinense Ficus hispida Moraceae 69.8 13.3 0.04 0.38 0.06 0.47 Diospyros eriantha Ebenaceae 31.3 5.5 0.02 0.42 0.01 0.44 Pterospermum Sterculiaceae 40.6 7.4 0.02 0.38 0.01 0.41 3.9 heterophyllum Maclura tricuspidata Moraceae 35.4 6.0 0.02 0.38 0.01 0.40 Cleistanthus saichikii Euphorbiaceae 100.0 5.3 0.05 0.33 0.01 0.40 Cleistanthus petelotii Euphorbiaceae 21.9 7.0 0.01 0.38 0.01 0.39 16.5 aRanked by dominance.

Am. J. Primatol. 178 / Huang et al.

TABLE III. Contribution of Staple Food Species Consumed by Assamese Macaques in Limestone Forests of Nongganga

Plant Parts Total month % of fruits % of annual Species Family typeb eatenc used feeding time feeding time S‐indexd

Bonia saxatilis Poaceae B YL 12 71.2 — Streblus indicus Moraceae T YL,MF,FR 12 38.7 7.8 2.4 Sinosideroxylon Sapotaceae T YL,FL,FR 7 13.5 4.1 3.8 pedunculatum var. pubifolium Canthium dicoccum Rubiaceae T YL,FL,FR 5 11.8 4 4.1 Trachelospermum brevistylum Apocynaceae V YL,MF,FR 6 0.1 1 — Ficus microcarpa Moraceae T IF,MF,FR 8 4.8 0.8 0.4 Caryota ochlandra Arecaceae T FR 5 12.4 0.7 2.1 Indosasa angustata Poaceae T IF 4 0.6 0.1 Iodes vitiginea Icacinaceae V FR 2 1.6 0.5 — aStaple food species include those with 0.5% in annual diet. bPlant type: T,tree; B,bush; V,vine. cParts eaten: YL,young leaves; ML,mature leaves; FL,flowers; FR,fruits. dS‐index: proportion in annual diet (%)/relative basal area of trees in plots (%); the index was not available when its relative basal area was not measured because its DBH was less than 3 cm.

Of the staple foods, only one species (Streblus Zhou et al. [2011], who found that Assamese indicus) belonged to the 10 most common trees in macaques in limestone forests were highly folivorous vegetation plots (Tables II and III), indicating that (leaves comprising 77.4% of the diet), and that fruit these foods were not consumed in proportion to their accounted for only 17.4% of the diet in a preliminary abundance. Moreover, there was no significant study (Table V). The dietary profile of Assamese relationship between the consumption of tree species macaques in limestone forests is similar to that of found in the vegetation plots and their relative congeners in temperate forests at higher latitudes density (rs ¼ 0.298, N ¼ 40, P ¼ 0.062), nor was there [Ahsan, 1994; Srivastava, 1999], but different from one between the consumption of tree species and those in tropical forests [Heesen et al., 2013; Schülke their relative biomass (multiplying relative density et al., 2011] (Table V). Surprisingly, the high and relative basal area; rs ¼ 0.289, N ¼ 40, P ¼ 0.071). proportion of leaves in the diet was mostly accounted for by the consumption of the young leaves of a single bamboo species (Bonia saxatilis). Young leaves from DISCUSSION this species were the most important food resource for As predicted, Assamese macaques in limestone Assamese macaques in limestone forests, contribut- forests of Nonggang relied more heavily on leaves ing the bulk of the diet [this study, Zhou et al., 2011]. than fruits. Leaves accounted for bulk of the annual The bamboo‐rich diet of Assamese macaques diet, whereas fruit constituted only a quarter of the could, at least partly, be explained by the availability annual diet. This finding is consistent with that of of Bonia saxatilis in limestone forests. This bamboo is

TABLE IV. Monthly top 3 food Species Used by Assamese Macaques in Limestone Forests of Nonggang (monthly % of feeding time)

Species 12‐Sep Oct Nov Dec 13‐Jan Feb Mar Apr May Jun Jul Aug

Bonia saxatilis 58.9 69.1 94.1 93.1 80.3 92.1 66.8 60.7 60.3 48.8 64.2 65.9 Cansjera rheedi 2.8 Canthium dicoccum 32.4 12.7 Caryota ochlandra 3.9 Memecylon scutellatum 1.2 1.2 Pueraria montana var. lobata 1.8 Radermachera sinica 2.3 Sabia sp. 4.5 Sapium rotundifolium 4.2 Sinosideroxylon 19.1 5.7 5.6 16.6 pedunculatum var. pubifolium Streblus indicus 13.6 17.5 12.6 18.8 11.7 7 8.5 Trachelospermum brevistylum 1 1.6 5.6

Am. J. Primatol. TABLE V. Comparison of Dietary Composition (%) of Macaque Species

Dietary composition (%)

Annual Other precipitation Young Mature vegetative Species Habitat (mm) Fruits Seeds leaves leaves Leavesa Flowersb partsc Othersd References

M. Forest in No data 22.9 45.7 31.4 Ahsan [1994] assamensis Bangladesh Forest in No data 11 32 20 52 37 2 Srivastava Northeast India [1999] Dry evergreen 1444 42.4 21.2 36.4 g Schülke forest, et al. [2011] Northeastern Thailand Limestone seasonal 1372 17.4 74.1 3.3 77.4 2.7 2.5 Zhou rainforest, et al. [2011] Southwest China Dry evergreen 1444 59.1 12.8 28.1 h Heesen forest, et al. [2013] Northeastern Thailand Limestone seasonal 1055 20.1 0.1 75.5 1.8 77.3 1.3 0.8 0.5 This study rainforest, Southwest China M. cyclopis Secondary 237– 53.8 14.92 7.32 14.2 9.76 Su and Lee Macaques Assamese of Adaptations Dietary broadleaf 583/month [2001] evergreen forest, Taiwan Island, China M. Degraded lowland 1300 70 9 1 13 7 Sussman fascicularis forest, Western [1981] Mauritius Riverine secondary 2376 59.2–87 3.7–18.4 1.3–3.3 0–18.4 2.7–6 Wheatley forest, Indonesia [1982] Freshwater peat 2878.8 66.7 17.2 8.9 7.3 Yeager [1996] swamp forest, Indonesia M. fuscata Warm temperate 100– 30.2 13.2 6.6 28.5 35.1 5.6 1.2 14.9 Hill [1997] broad‐leaved 400/month forest, Yakushima, m .Primatol. J. Am. Japan Warm temperate 2600 31.6 19.5 4 22.4 26.4 5.9 3 13.7 Agetsuma and broad‐leaved Nakagawa

forest, [1998] 179 / Yakushima, Japan m .Primatol. J. Am. / 180 TABLE V. Continued

Dietary composition (%) al. et Huang

Annual Other precipitation Young Mature vegetative Species Habitat (mm) Fruits Seeds leaves leaves Leavesa Flowersb partsc Othersd References

Mixed forest of 1500 10.2 43.6 14.5 2.8 17.3 3.3 20.1 5.7 Agetsuma and deciduous trees Nakagawa and coniferous [1998] trees, Kinkazan, Japan Coniferous forest, 4986 13 4 3 38 41 15 4 22 Hanya [2004] Yakushima, Japan M. leonina Semi‐evergreen 2000 86.5 1.9 4.7 2.6 4.3 Feeroz [1998, forest, 2011]; Bangladesh Hasan et al. [2007] M. mulatta Moist Himalayan 1757 8.5 84.4e 3.7 2.2 1.1i Goldstein and temperate forest, Richard Northwest [1989] Pakistan Evergreen and 1926 6.2 1.4 16.7 24.3 41 2.2 49.1 Zhou et al. deciduous [2009] broadleaved forest, Southwest China Semi‐evergreen 2000 34.1 6.3 8.8 4.1 46.7j Feeroz [2011]; forest, Hasan et al. Bangladesh [2007] M. munzala Western Arunachal No data 11.4 22.4 17 39.4 3.3 37.7 8.4 Mendiratta Pradesh, et al. [2009] Northeastern India M. nigra Tropical lowland 1550–2400 65.4 2.5f 31.5 O’Brien and rainforest, Kinnaird Sulawesi, [1997] Indonesia M. Tropical broadleaf No data 74.6 7 4.1 1.9 12.6 Cited from nemestrina evergreen forest, Richter Lima Belas, et al. [2013] Westren Malaysia M. Tropical lowland 2388 85.1 3.5 11.4 Kohlhaas nigrescens rainforest, [1993] Sulawesi, Indonesia TABLE V. Continued

Dietary composition (%)

Annual Other precipitation Young Mature vegetative Species Habitat (mm) Fruits Seeds leaves leaves Leavesa Flowersb partsc Othersd References

M. radiata Dry evergreen 1400 41 5.1 7.8 17.8 25.6 8.7 0.5 19.9 Krishnamani forest, Southern [1994] India M. siberu Tropical lowland 3601 75.7 4.4 0.2 2.8 17 Richter et al. rainforest, [2013] Siberut Island, Indonesia M. silenus Evergreen 5000 59.5 2 38.6 Singh et al. rainforest, India [2000, 2002] M. sinica Tropical dry 1671 70 30k Dittus evergreen forest, [1977a, b] Sri Lanka M. sylvanus Coniferous/ No data 4.3 26 48 Hanya et al. evergreen [2011] broadleaved forest, Algeria M. thibetana Mixed evergreen‐ 1578 29.5 43 5.1 22.4 Zhao et al. deciduous broad‐ [1991]; leaf forest, Deng and Macaques Assamese of Adaptations Dietary South‐West Zhao [1991] China M. tonkeana Tropical lowland 3113 78.1–85.8 1.6–4.2 0–1.3 2.9–4.2 0.8 2.1–3.1 6.3–16 Riley [2007] and montane forest, Sulawesi, Indonesia

aYoung leaves þ mature leaves. bInclude flowers buds. cInclude stems, barks, shoots, roots, herb, and lichen. dInclude , fungi, unknown items, and others. eInclude leaves, stems, and other vegetative parts. fInclude unripe seeds, leaf, flowers, pith, terminal shoots, herbs, grass seeds, and fungus. gInclude flowers. hInclude flowers and bark. iSap/Resin. jInclude crops. kInclude 1–2% animal matter, the remainder was of leaf shoots, leaves, flowers, seeds, petioles, mushrooms, fungi, herbs, grasses, roots, tubers, the pith of succulent twig growths, and resin. m .Primatol. J. Am. 181 / 182 / Huang et al.

superabundant and endemic to limestone hills [Liang of which a type of bamboo (Arundinaria alpina) et al., 1988]. Their young leaves are plentiful accounted for 76.7% of the diet, while the top 5 food throughout the year, and their availability is invari- species contributed to an overwhelming 94.3% of the ant between seasons. Thus, they may provide a long‐ diet [Mekonnen et al., 2010]. Although Assamese term staple food resource for Assamese macaques in macaques in limestone forests consume many more limestone habitats. Hu [2011] documented that using plant species, they show a similar dietary specializa- more readily available common plant species as tion on bamboo. The top three food species accounted foods is an effective strategy for François’ langurs to for most of the average monthly diets, of which Bonia survive well in seasonal and disturbed limestone saxatilis contributed more than half (Table IV). In all habitat. In addition, Bonia saxatilis occurs in dense cases, the bamboo was the top‐ranked food for clumps in the mid‐upper vertical zone of the Assamese macaques in the limestone forests of limestone hills, covering most of the areas where Nonggang, which would influence several aspects of trees are sparse. Assamese macaques spent succes- their feeding ecology. sive days staying on the same hill, then moved on to Compared with other Asian macaques, Assamese another hill which they again occupied for multiple macaques in limestone forests at Nonggang rely on days (unpublished data). This reduction of time spent leaves more heavily than other Asian macaques, foraging is indicative of an energy‐conserving strate- except for rhesus macaques residing in a degraded gy. However, one problem for primates that consume habitat of northwestern Pakistan (mostly herb, large quantities of bamboo is the cyanide content Table V). The proportion of leaves in the diet of [Mekonnen et al., 2010; Tan, 1999; Twinomugisha our study group is much higher than the mean value et al., 2006]. To decrease cyanide intake, these for Asian macaques [25.1%, Tsuji et al., 2013]. primates tend to select young bamboo leaves, which The leaf consumption of these macaques is even appear to be lower in cyanide than mature leaves higher than the mean value (52%) reported for 24 [Ballhorn et al., 2009; Tan, 1999; Twinomugisha et al., colobine species, which are fore stomach‐fermenting 2006; Mekonnen et al., 2010]. Assamese macaques primates and traditionally regarded as folivorous show the same preference for young bamboo leaves, [Kirkpatrick, 1999]. The high percentage of leaves in but nevertheless consume a great deal of this plant the diet of our study group may be related to the fact material. However, it remains unclear how macaques that Nonggang has the lowest annual rainfall of all of cope with the potential toxin. Further field studies, in the macaque sites we compared (Table V), since conjunction with biochemical analysis of bamboo, will rainfall is one of the important factors determining improve our understanding of the food selection of fruit production [Tsuji et al., 2013], which in turn Assamese macaques in limestone forests. affects fruit availability [Ting et al., 2008]. Tsuji et al. Other primates known to depend heavily on [2013] analyzed regional variation in the diets of bamboo include the bamboo lemurs endemic to the Asian macaques, and concluded that macaques rain forests of Madagascar (e.g. Hapalemur aureus, decrease the time spent eating fruits in favor of H. griseus, H. simus), the Bale monkeys ( eating leaves as mean annual rainfall decreases. In djamdjamensis) in the Odobullu forests of Ethiopia, addition, fruit phenology in limestone forests shows and the golden monkeys (Cercopithecus mitis kandti) marked seasonal change in accordance with monthly at Mgahinga forests of Uganda. These species have rainfall, and little fruit is available in drier months an unusual degree of dietary specialization and [this study, Li & Rogers, 2006; Zhou et al., 2006]. display a species‐poor diet (Table VI). For example, These factors could force Assamese macaques to rely the Bale monkeys eat only 11 different plant species, more on leaves and less on fruit.

TABLE VI. Comparison of Diet Composition for Bamboo‐Based Primates

Bamboos in Total numbers of Species Habitat diet (%) food species References

Hapalemur aureus Submontane rain forest, Madagascar 78 21 Tan [1999] H. griseus Submontane rain forest, Madagascar 72 24 Tan [1999] H. simus Submontane rain forest, Madagascar 95 7 Tan [1999] Chlorocebus djamdjamensis Bamboo forest, Ethiopia 76.7 11 Mekonnen et al. [2010] Cercopithecus mitis kandti Bamboo forest, Uganda 52.4 16 Twinomugisha et al. [2006] Macaca assamensis Limestone seasonal rainforest, 48.7 69 Zhou Southwest China et al. [2011] Limestone seasonal rainforest, 71.2 78 This study Southwest China

Am. J. Primatol. Dietary Adaptations of Assamese Macaques / 183

Young leaves were the primary fiber‐rich food They were folivorous and used the superabundant consumed by Assamese macaques in limestone young leaves of Bonia saxatilis as a fallback food in forests [this study; Zhou et al., 2011]. This pattern response to fruit scarcity in the fruit‐lean season, differs from other macaque species, whose fiber‐rich which differs from other monkeys, including popula- foods are mostly mature leaves (Table V). For tions of Assamese macaques in other forests. It example, Japanese macaques in coniferous forest could be a distinctive dietary adaptation to limestone ate a much greater amount of mature leaves (38% forests. of the annual feeding time) compared to young leaves (5%); the latter was also seasonally limited [Hanya, 2004]. Primates should prefer young leaves ACKNOWLEDGMENTS to mature leaves because they are richer in protein and poorer in fiber and secondary compounds We are very grateful to the Guangxi Forestry [Richard, 1985]. Similar patterns occur in other Bureau and Nonggang National Nature Reserve for folivorous primates, including colobines (young permitting us to conduct research in the study site. leaves accounting for 69% of the total fibrous foods) We would like to express our sincere gratitude to [Kirkpatrick, 1999], and other primate species [e.g. Prof. Ruyong Sun and Prof. Haisheng Jiang (both Alouatta palliata, 87%, Estrada et al., 1999; Propi- from South China Normal University) for their thecus diadema, 65%‐73%, Hemmingway, 1998]. support and suggestions. We acknowledge Mr. Similar to other macaque species [Hemingway & Hengshan Huang, Mr. Tianying Nong, Mr. Kechu fi Bynum, 2005], fruit is still the preferred food for Zhang, and Mr. Lin Ning for their assist in the eld. Assamese macaques in limestone forests, even We thank Dr. Weibin Xu and Dr. Yusong Huang for fi though it represents only a small proportion of the botanical identi cation. We also thank two anony- diet. This preference is evidenced by the correlation mous reviewers and Prof. Marina Cords for their between fruit consumption and availability. Fruit valuable comments, and Dr. Ali Krzton (from Texas preference is also reflected in the higher S‐index of A&M University, USA) for her help in language important fruiting tree species (Table III). Macaques editing. have an enlarged caecum and colon as their primary fermentation chamber, which enhances their ability to digest large amounts of fiber‐rich foods while still REFERENCES retaining the capacity to eat fruit [Lambert, 1998; Agetsuma N, Nakagawa N. 1998. Effects of habitat differences Hanya, 2004]. When fruit became scarce in the fruit‐ on feeding behaviors of Japanese monkeys: comparison lean season, Assamese macaques at Nonggang between Yakushima and Kinkazan. Primates 39:275–289. significantly increase the consumption of young Ahsan MF. 1994. Feeding ecology of the primates of Bangladesh. In: Thierry B, Anderson RJ, Roeder JJ, leaves. This indicates that young leaves are impor- Herrenschmidt N, editors. Current primatology. Vol 1. tant fallback foods for Assamese macaques in Ecology and evolution. Strasbourg: University of Louis limestone forests in response to the seasonal scarcity Pasteur. p 79–86. of fruit. This conclusion is in contrast to our Albert A, Hambuckers A, Culot L, Savini T, Huynen M‐C. 2013. prediction that Assamese macaques in limestone Frugivory and seed dispersal by northern pigtailed mac- aques (Macaca leonina), in Thailand. International Journal forests would use mature leaves as a fallback food in of Primatology 34:170–193. the lean season. This foraging strategy differs from Altmann J. 1974. Observational study of behavior. Sampling other Macaca species [e.g.,M. fuscata, Hanya, 2004; methods. Behaviour 49:227–262. M. siberu, Richter et al., 2013; M. cyclopis,Su& Ballhorn DJ, Kautz S, Rakotoarivelo FP. 2009. Quantitative variability of cyanogenesis in Cathariostachys madagascar- Lee, 2001; M. fascicularis, Yeager, 1996], as well as iensis—the main food plant of bamboo lemurs in Southeast- other sympatric primates [e.g. Trachypithecus fran- ern Madagascar. American Journal of Primatology 71: coisi, Huang et al., 2010; Zhou et al., 2006]. In these 305–315. populations, mature leaves are the main fallback Bicca‐Marques JC. 2003. How do howler monkeys cope with foods. Despite the seasonal shortage of young leaves habitat fragmentation? In: Marsh LK, editor. Primates in fragments: Ecology in conservation. New York: Kluwer in limestone forests [this study, Li & Rogers, 2006; Academic/Plenum. p 283–303. Zhou et al., 2006], Assamese macaques depend Burton ML, Samuelson LJ, Pan S. 2005. Riparian woody plant heavily on young leaves almost year‐round. This is diversity and forest structure along an urban‐rural gradient. mostly accounted for by macaques’ feeding on the Urban Ecosystems 8:93–106. Campbell C, Fuentes A, MacKinnon K, Panger M, Bearder S. young leaves of Bonia saxatilis. This item contributed 2007. Primates in Perspective. Oxford: Oxford University to the bulk of monthly diets, especially in the fruit‐ Press. lean season (Table I). Thus, the bamboo‐dominated Chapman CA, Chapman LJ. 1999. Implications of small scale diet could be a key factor in the difference between variation in ecological conditions for the diet and density of – these macaques and others’ fallback foods. red colobus monkeys. Primates 40:215 232. Chapman CA, Chapman LJ, Gillespie TR. 2002. Scale issues in In summary, Assamese macaques appear to have the study of primate foraging: red colobus of Kibale National adapted to limestone habitats by consuming young National Park. American Journal of Physical Anthropology bamboo leaves as a staple while still preferring fruits. 117:349–363.

Am. J. Primatol. 184 / Huang et al.

Chapman CA, Wasserman MD, Gillespie TR. 2006. Behavioral Hemingway CA, Bynum N. 2005. The influence of seasonality patterns of colobus in logged and unlogged forests. In: on primate diet and ranging. In: Brockman DK, van Schaik Newton‐Fisher NE, Notman H, Reynolds V, Paterson JD, CP, editors. Seasonality in primates: Studies of living editors. Primates of Western Uganda. New York: Springer. and extinct human and non‐human primates. Cambridge: p 373–390. Cambridge University Press. Chen P. 1988. A report on the soil investigation of the Hill DA. 1997. Seasonal variation in the feeding behavior and Nonggang Natural Reserve. Guihaia Suppl 1:52–73 diet of Japanese macaques (Macaca fuscata yakui)in (in Chinese). lowland forest of Yakushima. American Journal of Prima- Deng Z, Zhao Q. 1991. Early mother‐infant relationships of tology 43:305–322. Macaca thibetana at Mt. Emei China. Primates 32:197–205. Hu CG. 1988. Report on the investigation of hydrogeology Dittus WPJ. 1977a. The socioecological basis for the conserva- from Longgang Natural Reserve. Guihaia Suppl 1:17–32 tion of the Toque monkey (Macaca sinica) of Sri lanka (in Chinese). (Ceylon). In: Monaco HSHPRI, Bourne GH, editors. Primate Hu G. 2011. Dietary breadth and resource use of Francois’ conservation. New York: Academic Press. p 237–265. Langur in a seasonal and disturbed habitat. American Dittus WPJ. 1977b. The ecology of a semi‐evergreen forest Journal of Primatology 73:1176–1187. community in Sri Lanka. Biotropica 9:268–286. Huang ZH, Huang CM, Zhou QH, Wei H, Meng YJ. 2010. Estrada A, Juan‐Solano S, Martínez TO, Coates‐Estrada R. Diet and the seasonal changes of the François’ langur 1999. Feeding and general activity patterns of a howler (Trachypithecus francoisi). Acta Ecologica Sinica 30:5501– monkey (Alouatta palliata) troop in a forest fragment at Los 5508 (in Chinese). Tuxtlas, Mexico. American Journal of Primatology 48: Ji JF, Tang JW. 2008. Biomass and its allocation pattern of 167–183. monsoon rain forest over limestone in Xishuangbanna of Feeroz MM. 1998. Food and feeding behaviour of the pig‐tailed Southwest China. Chinese Journal of Ecology 27:167–177 macaque (Macaca nemestrina leonine) in semi‐evergreen (in Chinese). forest in Bangladesh. Primate Eye 65. Jiang XL, Wang YX, Ma SL. 1993. Taxonomic revision Feeroz MM. 2011. Resource partitioning among the sympatric of Macaca assamensis. Zoological Research 14:110–117 primate species of West Bhanugach forest reserve of (in Chinese). Bangladesh. Proceedings of the International Conference Kirkpatrick RC. 1999. Colobine diet and social organization. In: on Biodiversity—Present State, Problems and Prospects of Dolhinow P, Fuentes A, editors. The nonhuman primates. its Conservation 33–43. Mountain View, CA: Mayfield Publishing. p 93–105. Feeroz MM. 2012. Niche separation between sympatric pig‐ Kohlhaas AK. 1993. Behavior and ecology of Macaca nigres- tailed macaque (Macaca leonina) and rhesus macaque cens: behavior and social responses to the environment (M. mulatta) in Bangladesh. Journal of Primatology 1:106. and fruit availability [Dissertation]. Boulder: University Fooden J. 1982. and evolution of the sinica group of of Colorado. Available from: University Microfilms Inter- macaques: 3. Species and subspecies accounts of Macaca national, Ann Arbor, MI. assamensis. Fieldiana Zoology (New Series) 10:1–152. Krishnamani R. 1994. Diet composition of the Franklin DC. 2005. Vegetative phenology and growth of a (Macaca radiate) in a tropical dry evergreen forest of facultatively deciduous bamboo in a monsoonal climate. Southern India. Tropical Biodiversity 2:285–302. Biotropica 37:343–350. Lambert J. 1998. Primate digestion: interactions among Goldstein SJ, Richard AF. 1989. Ecology of rhesus macaques anatomy, physiology, and feeding ecology. Evolution An- (Macaca mulatta) in Northwest Pakistan. International thropology 7:8–20. Journal of Primatology 10:531–567. Li ZY, Rogers ME. 2006. Food items consumed by white‐headed Guangxi Forestry Department. 1993. Nature reserves in langurs in Fusui, China. International Journal of Primatol- Guangxi. Beijing: China Forestry Publishing House (in ogy 27:1551–1567. Chinese). Liang ZF, Liang JY, Liu LF, Mo XL. 1988. A report on Hanya G. 2004. Diet of a Japanese macaque troop in the vegetation in Nonggang Nature Reserve. Guihaia Suppl coniferous forest of Yakushima. International Journal of 1:83–184 (in Chinese). Primatology 25:55–71. Lindburg D.G., 1977. Feeding behavior and diet of rhesus Hanya G, Bernard H. 2012. Fallback foods of red leaf monkeys macaques (Macaca mulatta) in a Siwalik forest in Norther (Presbytis rubicunda) in Danum Valley, Borneo. Interna- India. In: Clutton‐Brock TH, editor. Primate ecology: Studies tional Journal of Primatology 33:322–337. of feeding and raging behaivour in lemurs, monkeys, and Hanya G, Ménard N, Qarro M., et al. 2011. Dietary adaptations apes. London: Academic Press. p 223–249. of temperate primates: comparisons of Japanese and Marshall AJ, Wrangham RW, 2007. Evolutionary consequen- Barbary macaques. Primates 52:187–198. ces of fallback foods. International Journal of Primatology Hanya G, Tsuji Y, Grueter CC. 2013. Fruiting and flushing 28:1219–1235. phenology in Asian tropical and temperate forests implica- Mekonnen A, Bekele A, Fashing PJ, Hemson G., 2010. tions for primate ecology. Primate 54:101–110. Diet, activity patterns, and ranging ecology of the Bale Harris TR, Chapman CA. 2007. Variation in diet and ranging of monkey (Chlorocebus djamdjamensis) in Odobullu Forest, black and white colobus monkeys in Kibale National Park, Ethiopia. International Journal of Primatology 31:339– Uganda. Primates 48:208–221. 362. Hasan MK, Feeroz MM, Islam MA, Kabir MM, Begum S. 2007. Mendiratta U, Kumar A, Mishra C, Sinha A. 2009. Winter Substrate use by the western hoolock gibbon (Hoolock ecology of the Arunachal macaque Macaca munzala in hoolock) in a semievergreen forest of Bangladesh. Zoos’ Pangchen Valley, Western Arunachal Pradesh, Northeast- Print Journal 22:2702–2705. ern India. American Journal of Primatology 71:939–947. Heesen M, Rogahn S, Ostner J, Schülke O. 2013. Food O’Brien TG, Kinnaird MF. 1997. Behavior, diet, and movement abundance affects energy intake and reproduction in of the Sulawesi crested black macaque (Macaca nigra). frugivorous female Assamese macaques. Behavioral Ecology International Journal of Primatology 18:321–351. and Sociobiology 67:1053–1066. Olupot W. 1998. Long‐term variation in mangabey (Cercocebus Hemmingway CA. 1998. Selectivity and variability in the diet albigena johnstoni Lydekker) feeding in Kibale National of Milne‐Edwards’ sifakas Propithecus diadema edwardsi: Park, Uganda. African Journal of Ecology 36:96–101. implications for folivory and seed‐eating. International Richard AF. 1985. Primates in nature. New York: W.H. Journal Primatology 19:355–377. Freeman.

Am. J. Primatol. Dietary Adaptations of Assamese Macaques / 185

Richter C, Taufiq A, Hodges K, Ostner J, Schülke O. 2013. Tsuji Y, Fujita S, Sugiura H, Saito C, Takatsuki S. 2006. Long‐ Ecology of an endemic primate species (Macaca siberu)on term variation in fruiting and the food habits of wild Siberut Island, Indonesia. SpringerPlus 2:137. Japanese macaques on Kinkazan Island, Northern Japan. Riley EP. 2007. Flexibility in diet and activity patterns of American Journal of Primatology 68:1068–1080. Macaca tonkeana in response to anthropogenic habitat Tsuji Y, Hanya G, Grueter CC. 2013. Feeding strategies of alteration. International Journal of Primatology 28:107– primates in temperate and alpine forest, comparison of 133. Asian macaques and colobines. Primate 54:201–215. Schülke O, Pesek D, Whitman BJ, Ostner J. 2011. Ecology of Tutin CEG. 1999. Fragmented living: behavioural ecology of Assamese macaques (Macaca assamensis) at Phu Khieo primates in a forest fragment in the Lopé Reserve, Gabon. Wildlife Sanctuary, Thailand. Journal of Wildlife in Primates 40:249–265. Thailand 18:1–15. Twinomugisha D, Chapman CA, Lawes MJ, O’Driscoll Wor- Shaffer CA. 2013. Feeding ecology of northern bearded sakis man C, Danish LM. 2006. How does the golden monkey of the (Chiropotes sagulatus) in Guyana. American Journal of Virungas cope in a fruit‐scarce environment? In: Newton‐ Primatology 75:568–580. Fisher NE, Notman H, Paterson JD, Reynolds V, editors. Singh MR, Singh ME, Kumar MA., et al. 2002. Distribution, Primates of Western Uganda. New York: Springer. p 45–60. population structure, and conservation of lion‐tailed mac- Wada K, Hamada Y, Li YP., et al. 2010. Distribution pattern aques (Macaca silenus) in the Anaimalai Hills, Western of macaques in Guangxi. Mammalian Science 50:21–29 Ghats, India. American Journal of Primatology 57:91– (in Japanese). 102. Wheatley BP. 1982. Energetics of foraging in Macaca fascicu- Singh MR, Singh ME, Kumar MA., et al. 2000. Niche laris and Pongo pygmaeus and a selective advantage of large separation in sympatric lion‐tailed macaques (Macaca body size in the orang‐utan. Primates 23:348–363. silenus) and Nilgiri langur (Presbytis johnii) in an Indian Yeager CP. 1996. Feeding ecology of the long‐tailed macaque in tropical rain forest. Primate Report 58:83–95. Ialimantan Tengah, Indonesia. International Journal of Srivastava A. 1999. Primates of Northeast India. Bikaner: Primatology 17:51–62. Megadiversity Press. p 1–208. Zhang YZ. 1997. Distribution of mammalian species in China. Strier KB. 1991. Diet in one group of woolly spider monkeys, or Beijing: China Forestry Publishing House (in Chinese). muriquis (Brachyteles arachnoides). American Journal of Zhao Q, Deng Z, Xu J. 1991. Natural foods and their ecological Primatology 23:113–126. implications for Macaca thibetana at Mount Emei, China. Su HH, Lee LL. 2001. Food habits of formosan rock macaques Folia Primatologica 57:1–15. (Macaca cyclopis) in Jentse, Northeastern Taiwan, assessed Zhou QH, Wei FW, Li M, Huang CM, Luo B. 2006. Diet and food by fecal analysis and behavioral observation. International choice of Trachypithecus francoisi in the Nonggang Nature Journal of Primatology 22:359–377. Reserve, China. International Journal of Primatology 27: Sussman RW. 1981. Behavior and ecology of Macaca fascicu- 1441–1460. laris in Mauritius. Primates 22:192–205. Zhou QH, Tang HX, Wei CQ, Huang CM. 2009. Diet and Tan CL. 1999. Group composition, home range size, and diet of seasonal changes in rhesus macaques (Macaca mulatta)at three sympatric bamboo lemur species (Genus Hapalemur) Seven‐star Park, Guilin. Acta Theriologica Sinica 29:419– in Ranomafana National Park, Madagascar. International 426 (in Chinese). Journal of Primatology 20:547–566. Zhou QH, Wei H, Huang ZH, Huang CM. 2011. Diet of Ting S, Hartley S, Burns KC. 2008. Global patterns in fruiting the Assamese macaque Macaca assamensis in limestone seasons. Global Ecology and Biogeography 17:648–657. habitats of Nonggang, China. Current Zoology 57:18–25.

Am. J. Primatol.