Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu Tibet adaptations to a marginal environment.код для вставкиСкачать
American Journal of Primatology 69:1141–1158 (2007) RESEARCH ARTICLE Diet and Feeding Behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: Adaptations to a Marginal Environment ZUO-FU XIANG1– 3, SHENG HUO2, WEN XIAO2, RUI-CHANG QUAN2, 4 AND CYRIL C. GRUETER 1 Central South University of Forestry and Technology, Changsha, Hunan, PR China 2 Kunming Institute of Zoology, Chinese Academy of Sciences (CAS), Kunming, Yunnan, PR China 3 Graduate University of CAS, Beijing, PR China 4 Anthropologisches Institut und Museum, Universität Zürich-Irchel, Zürich, Switzerland The diet and feeding ecology of a wild subpopulation of black-and-white snub-nosed monkeys (Rhinopithecus bieti) were studied at Xiaochangdu in Honglaxueshan Nature Reserve, Tibet. This region is climatologically harsher than any other inhabited by non-human primates. Black-andwhite snub-nosed monkeys fed on 48 parts of 25 plant species, at least three species of lichens and seven species of invertebrates. The number of food items exploited varied markedly among seasons, with dietary diversity being greatest in spring and summer. In winter, black-andwhite snub-nosed monkeys had to subsist on fallback foods such as dried grass and bark. Ubiquitous lichens formed a major dietary constituent throughout the year, contributing about 75% of feeding records. Even though lichens act as a staple, our findings signify that the monkeys at Xiaochangdu prefer feeding on foliage, which is higher in protein content than the former. We provide evidence that black-and-white snub-nosed monkeys are able to cope with an array of food items other than lichens and hence can be regarded as feeding generalists. We discuss the results with reference to previous studies on other subpopulations living in habitats that are floristically more diverse and offer more plant food items than the marginal habitat at Xiaochangdu. Am. J. Primatol. 69:1141–1158, 2007. c 2007 Wiley-Liss, Inc. Key words: Rhinopithecus bieti; Colobinae; feeding ecology; lichens; diet; Tibet Contract grant sponsor: Chinese Academy of Sciences; Contract grant number: KSCX2-1-03, KSCX2-1-09. Correspondence to: Zuo-Fu Xiang, College of Life Science and Technology, Central South University of Forestry and Technology, 498 Shaoshan Nanlu, Changsha, Hunan, 410004, PR China. E-mail: email@example.com Received 15 April 2006; revised 14 December 2006; revision accepted 18 December 2006 DOI 10.1002/ajp.20412 Published online 1 March 2007 in Wiley InterScience (www.interscience.wiley.com). r 2007 Wiley-Liss, Inc. 1142 / Xiang et al. INTRODUCTION Members of the subfamily Colobinae exhibit several anatomical features that can be regarded as adaptations for ingesting leaves. One notable feature is their molars with high, sharp cusps and long lophs [Kay, 1978]. Another unique trait among primates is the enlarged, sacculate forestomach that permits the breakdown of cellulose by microbial fermentation [Chivers, 1994; Kay & Davies, 1994]. The physiology of the colobine gastrointestinal tract allows them to harvest abundant plant food resources such as mature leaves [Kay & Davies, 1994]. These morphological traits obviously point to folivory. However, a categorization of primate species into folivorous, frugivorous, etc., is usually imprecise, taking into account that a given species often relies on several kinds of food resources, and that its diet varies regionally and seasonally [Hill, 1997]. The dietary repertoire of a species may certainly be constrained by phylogeny, thus making it prone to be either folivoury or frugivoury, but it is widely held that the habitat in which the species lives also has a profound influence on shaping its dietary niche [Hladik & Chivers, 1978]. Colobines inhabit a wide range of habitats, ranging from tropical moist lowland forests to temperate montane regions [Oates et al., 1994]. In line with such differing environments, flexibility and breadth of diet are hallmarks of colobine feeding ecology as well [Bennett & Davies, 1994; Oates, 1994]. They are not merely consumers of young or mature leaves, but some populations actually feed predominantly on fruits or seeds whenever available in phenological cycles [e.g., Bennett, 1983; Oates, 1994; Starin, 1991; Supriatna et al., 1986]. Especially, extreme marginal habitats may promote a rather eclectic dietary strategy that diverges somewhat from the ‘norm’. In addition, strong seasonality, i.e., striking annual variations of both rain and temperature, may illustrate the degree of behavioral plasticity developed in response to such an environment. Among those colobines that are found in such marginal habitats are the black-and-white snub-nosed monkeys (Rhinopithecus bieti), which are endemic to China. Their distribution extends from Zhina (291200 N), Southeast Tibet in the north [Xiang et al., in press], to Mt. Longma (261140 N), Northwest Yunnan in the south, and is delimited by the upper Yangtze River (Jinshajiang) to the east and the upper Mekong River (Lancangjiang) to the west [Long et al., 1994]. Although the diets of many wild colobines are documented [reviewed in Waterman & Kool, 1994], however, studies on selection of food in R. bieti are still not comprehensive enough. One reason for the lack of data is that direct observational studies are hampered by the harsh physical conditions within the species’ natural habitat. The extremely rugged terrain is often inaccessible for researchers, and some of the mountain paths are closed for 3–6 months due to heavy snowfall. The first studies on feeding ecology made known that R. bieti eat emerging bamboo sprouts and young leaves of birch trees as well as conifer leaves (needles) [Li et al., 1982]. Other studies, however, came to the conclusion that conifer needles do not appear to be major food items [Ding & Zhao, 2004; Kirkpatrick, 1996; Long et al., 1994; Yang & Zhao, 2001], and it would be surprising for an animal with forestomach fermentation to ingest conifer needles likely to contain bacteriostatic resins [Brattsten, 1979; Freeland & Janzen, 1974]. On the basis of systematic observations of a group in the high-altitude (ca 4,000 m) conifer forests at Wuyapiya in the northern part of the species’ distribution, Kirkpatrick  estimated the group’s diet to be composed of 75% arboreal lichens, especially Bryoria spp., seasonally varying from 60% in spring to 95% in winter. However, by analyzing scat collected from the same group, Wu Am. J. Primatol. DOI 10.1002/ajp Diet and Feeding Behavior of Rhinopithecus bieti / 1143 and He  estimated the percentage of lichens in the diet to be only about 30–40%. Results on diet composition in R. bieti derived from direct observations and analyses of fecal samples may not coincide well as also happens in other studies. As an example, Ding and Zhao (2004) had no scan record for feeding on bamboo leaves/shoots at all, but bamboo leaves/shoots were found in 43% of all investigated fecal remains. Furthermore, analyses of fecal remains of a group at a more southern location (Lijang) in the deciduous forest (ca. 3,500 m) revealed that the diet was made up primarily of bamboo leaves (59%) and only a little lichen (ca. 5%) [Yang & Zhao, 2001]. One reason for such contradictory findings is the limited or biased view—with the ground usually not clearly visible—when engaging in direct observations using a field scope. Such an observation with a field scope is biased toward observing food items exploited in tree crowns (such as lichens) and against food items exploited on the ground or in the bush (i.e., leaves of angiosperm plant, bamboo leaves/shoot). Owing to limitation of scan sampling with a field scope [Kirkpatrick, 1996], which overestimates lichens, and feces remains analysis which overestimates the low-digestibility items [Kirkpatrick et al., 2001], the diet or food composition, especially of the northern-most distribution, of R. bieti, needs to be reevaluated. We tried to overcome, or at least partially alleviate, the problem of ‘‘differential visibility’’ by way of applying two complementary observational procedures to investigate the monkeys’ dietary composition: (i) SFS: scan with a field scope from a distance (50–1,000 m), (ii) AOB: approach the monkey group and observe with or without binoculars at a relatively close distance (15–50 m). We then integrate (weigh) the results of the two methods—based on the percentage of time that the animals spent in the trees, bushes and on the ground—to better estimate diet composition. Apart from this methodological improvement, other objectives of this paper are to describe the diet of a subpopulation of R. bieti at Xiaochangdu, Tibet, which is among the most unusual habitats for primates due to its high elevation and extremely cold climate (temperatures can drop to as low as 151C in winter). Moreover, we compare the diet and habitat characteristics between the focal subpopulation and two other subpopulations living further south, to evaluate ecological flexibility and adaptability of this species. METHODS Study Site and Animal We conducted our study at Xiaochangdu (291150 N, 981370 E) in Honglaxueshan National Nature Reserve (HNNR), Mangkang County of Southeast Tibet (Fig. 1). HNNR was founded in 1993 to protect black-and-white snub-nosed monkeys and their habitat. It forms the northernmost tip of the geographical distribution of this species. The region lies in the Hengduan Mountains (Trans-Himalayas). The climate at HNNR is strongly seasonal and affected by the southwest monsoon, which brings moist warm air in summer and cold dry air in winter. The study subpopulation, with about 210 individuals, mainly ranged between 3,500 and 4,250 m a.s.l. They have never been seen to take foods from farmers and researchers, directly or indirectly. Small villages, totaling about 60 families, bordered the main range of the monkeys; none of which is above 3,800 m a.s.l. Hunting was limited, though there were summer ranging of livestock and other human activities in the monkeys’ range. Am. J. Primatol. DOI 10.1002/ajp 1144 / Xiang et al. Fig. 1. Study site (Xiaochangdu), Honglaxueshan National Nature Reserve (981200 –981590 E, 281480 –291400 N), and the localities of the monkey groups mentioned in the text. Climate and Vegetation The annual precipitation is 740 mm, and the mean annual temperature is 4.71C (from March 2004 to February 2005). The monthly variation in precipitation and temperature is presented in Fig. 2. The month with the largest amount of precipitation is July (231 mm), and the month with the least precipitation is November (3 mm). The highest monthly mean temperature is 12.51C in August, and the lowest monthly mean temperature is 3.61C in Am. J. Primatol. DOI 10.1002/ajp Diet and Feeding Behavior of Rhinopithecus bieti / 1145 Fig. 2. Monthly precipitation (mm) and monthly lowest, mean and highest temperatures (1C) at Xiaochangdu (data collected at 3,800 m over the period of a year). January. The highest temperature was 26.91C in August; and the lowest temperature was 15.41C in January. The meteorological data were recorded at 3,800 m a.s.l. beside our study camp using the following equipment: HOBO Pro RH/Temp (H08-032-08, 642988), Data Logging Rain Gauge (RG2M, 650817) with a HOBO Event Data Logger (H07-002-04, 658017), all of which are manufactured by Onset Computer Corporation. After a brief reconnaissance of the study area and signs of monkey presence, we were able to identify four habitat types within the assumed home range of the study group. The monkeys did not enter any other habitat types over the course of the study. The four habitat types were: (i) primary conifer forest (PC)—mainly composed of Picea likiangensis and Abies squamata trees, and sporadic bushes of less than 2 m in height, (ii) secondary conifer forest (SC)—mainly composed of P. likiangensis and A. squamata trees and dense bushes. This forest was selectively logged to extract wood for building of houses, (iii) larch forest (LF)— mainly composed of Larix griffithiana and Rhododendron spp. trees and a thick undergrowth of bushes (mostly Rhododendron spp.) usually surpassing 2 m, and (iv) evergreen broadleaf forest (EB)—mainly composed of Quercus aquifolioides trees and low density of bushes rarely growing to more than 2 m in height. Nested quadrate sampling was applied to provide estimates of abundance of plant species in each habitat type within the home range of the study group. Three series of transects were designed along a south-north oriented valley. Each series were five 1,000 m transects in length, parallel to each other and laid out at 100 m elevation intervals from 3,800 to 4,200 m a.s.l. Sampling points were then determined at 250 m intervals along these transects for nested quadrate analysis (sensu Goldsmith et al., 1986). At each sampling point, the number of plant species within quadrates of increasing sizes was counted, and the number of species in quadrates was then plotted against the quadrate size (side length) to develop a species-area curve. Thirty-six sampling points were located within PC, 20 within SC, six within LF, and 13 within EB. The species-area curves for the Am. J. Primatol. DOI 10.1002/ajp 1146 / Xiang et al. four habitat types are shown in Fig. 3. The abundance order of plant species in 50 m 50 m plot among the four habitat types is LF4SC4PC4EB, and were found to differ significantly (ANOVA, F 5 104.6, df 5 3, Po0.001). Phenology and Food Availability Phenological data on vegetative and reproductive plants were gathered monthly during the study period. We established a 50 m 50 m phenological plot within SC at 3,900 m a.s.l. In this plot, we selected three specimens of every species (height42 m) known to be a potential food source. If the species in a lot is less than three specimens, we choose the nearest specimen of this plot. Sixtythree specimens were chosen for phonological monitoring. Of the specimens, 57 are tree species. We identified potential food sources based upon preliminary observations of the monkeys’ feeding behavior, and information received from local field assistants who are familiar with the habitat. There is no significant monthly variation in precipitation, soil type or overall phenology, between 3800 and 4200 m (Z.-F. Xiang, personal observation), the belt that includes 95% of the home range of this study subpopulation [Xiang, 2005]. Therefore, we consider it a representative sample site. One reason for establishing the phenological plot within SC is that most potential food tree species there can grow to be higher than 2 m. This is because in spring and summer many livestock destroy the tagged tree species lower than 2 m. We regard this height as a convenient precondition for estimation of relative food availability. Another reason is because almost allpotential food tree species found in PC, LF and EB can also be found in SC. There are only two kinds of nuts/fruits at our site that the snub-nosed monkeys actually feed on: the first (Rosa omeiensis Rosaceae), is rare and sporadically occurs in PD and SC, and the other, (Q. aquifolioides Fagaceae), is ample and evenly distributed in EB. We also tagged three Q. aquifolioides trees within EB, and three Rosa omeiensis in SC for nut/fruit monitoring. Fig. 3. Species-area (nested quadrat side length) curves for estimating food availability in four habitat types using nested quadrat analysis. Am. J. Primatol. DOI 10.1002/ajp Diet and Feeding Behavior of Rhinopithecus bieti / 1147 Food availability was estimated via the crown density method of Mash (1981). Different plant parts known to be potential food items were assessed on a monthly basis by visual inspection of the designated trees for the presence of buds, mature leaves, young leaves, and flowers. Each plant part was assigned to a relative abundance value ranging from 0 to 3. A value of 0 corresponds to a complete absence of that plant part, a value of 1 was recorded when that part encompassed o25% of the crown, a value of 2 when it encompassed 25–50% of the crown, and a value 3 when it encompassed 450%. As we were interested only in evaluating the relationship between the monkeys’ diet composition and the relative food availability, plant parts that had not been eaten or had not shown a monthly variation (i.e., lichens, barks, etc.) were not included in the calculation of the food availability scores. Since Q. aquifolioides nuts turned out to be a major food item in autumn and winter, we also assessed the abundance of these nuts in three monitored areas, where the monkeys usually ranged, of 1 m2: ‘‘2’’ denotes more than ten nuts present, ‘‘1’’ denotes 1–9 nuts present and ‘‘0’’ denotes absence of nuts on the ground within EB. Behavioral Sampling We collected behavioral data during follows of the Xiaochangdu group from June 2003 to March 2005. Instantaneous scan sampling [Altmann, 1974] at 15-min interval was employed. Data on individual behaviors were collected either with a field scope (Nikon ED II, 25–56X) (SFS) at a distance about 50–1,000 m, which bias to the food items in the tree crown, or by approaching the animals to about 15–50 m and observing them with or without binoculars (AOB), which biases to observations of food items collected from the ground and low-lying bushes. The total scan time was 549.25 h, of which 52 h were AOB (Table I). As there are too many human disturbances (mainly from mushroom collectors) in TABLE I. Observation Time, Feeding Records and Dietary Diversity of Scanning With a Field Scope (SFS) and Approach the Monkey Group and Observe With or Without Binocular (AOB) Scan time (h) Year Month 2003 June July August October November December March April May June January February March Total 2004 2005 Feeding records Dietary diversity SFS AOB Total (h) From SFS From AOB Total From SFS From AOB 31.5 91 30.25 12 44 47 39 30 27.75 25 8 41.75 70 497.25 3.25 6 6.5 0 8 4.25 7.25 0 12 4.75 0 0 0 52 34.75 97 36.75 12 52 51.25 46.25 30 39.75 29.75 8 41.75 70 549.25 583 2,216 752 242 1,354 652 598 893 1,339 351 273 284 2,060 11,597 73 179 164 0 209 133 190 0 292 159 0 0 0 1,399 656 2,395 916 242 1,563 785 788 893 1,631 510 273 284 2,060 12,996 0.8449 0.5330 0.5383 0.3601 0.1981 0.1848 0.4051 0.3697 0.8054 0.9241 0.1925 0.0886 0.4290 — 1.4131 1.1061 1.0020 — 0.9148 0.6705 0.7812 — 1.1060 1.1830 — — — — Am. J. Primatol. DOI 10.1002/ajp 1148 / Xiang et al. September and October [Xiang et al., in press], scan sampling was only conduct for about 12 h in October. The subpopulation was followed for only 3 days in September, and we could not sample (scan) due to heavy fog and human disturbance. Once we spotted an individual processing a food item, we tried to identify both the species and the food category. Given the limitation that most observations were SFS, food samples were gathered: (1) primarily when items were seen being eaten (when buds were eaten in spring, the plant was marked, and a sample was taken later when it flowered or its mature leaves were available), (2) in some cases, immediately after the monkeys had left a feeding site that had been used for at least 1 h, we entered the forest to collect samples of the parts corresponding to the remnants of the parts just eaten. Food categories were classified as: (1) lichens, (2) buds and leaves, (3) flowers and fruits/nuts, (4) invertebrates, (5) bark, root, resin, grass, etc. Voucher specimens were identified by Prof. D.-D. Tao at the Kunming Institute of Botany, the Chinese Academy of Science. Most specimens were identified to species, though in some cases, only the genus or family could be determined. Data Analysis Feeding records for different food categories acquired via the two observational methods were first calculated as proportions of the monthly diet to reduce biases resulting from unequal sample sizes. Monthly proportions were then averaged over a year to obtain an overall estimate of the relative contributions of different items to the diet of R. bieti. Then, based on the percentage of time that spent in different forest layers (trees, bushes and ground), we integrated (weighed) the results of the two methods to get a relatively real diet composition using the following formula: DCR ¼ DCSFS PTT DCAOB PTBG where DCR is the relative real diet composition, DCSFS the diet composition obtained from SFS, DCAOB the diet composition obtained from AOB, PTT the percent time spend in the tree (76.7%), and PTBG the percent time spend in the bush and on the ground (23.3%) [Xiang, 2005]. We calculated the dietary diversity of each month using the Shannon–Wiener index (H0 ) [Krebs, 1999]: X H0 ¼ fPi lnðPi Þg where Pi is the proportion of feeding records of each category in certain months. We used the monthly index of relative food availability (Wi) to describe the annual variation of food availability. Wi ¼ Oi =P where Wi is the food availability index in i month, Oi is the sum scores of food availability of certain categories in i month, and P is the sum of yearly highest score of relative food availability for all tagged tree species of certain categories. An index value ‘‘1’’ indicates high food availability, and value ‘‘0’’ indicates no food availability. We used the spearman rank correlation [Zar, 1999] to investigate relationships between food availability of leaves and fruit and the percentage of feeding records for lichen. The sum scores of food availability of certain categories for all tagged tree species in certain months are used for this analysis. Am. J. Primatol. DOI 10.1002/ajp Diet and Feeding Behavior of Rhinopithecus bieti / 1149 RESULTS Phenology and Food Availability Conifers (with the exception of larch), oaks and rhododendrons at Xiaochangdu were evergreen. Other trees and shrubs were deciduous and showed strong seasonality. A flush of productivity began in mid-May; all deciduous plants came into leaf virtually simultaneously and by mid-October most deciduous plants had lost all their leaves. Generally speaking, buds and leaves were available on the tree from May to September, flowers and fruits/nuts from May to August. Availability of buds, leaves, flowers, and fruits/nuts as food showed clear seasonal variation (Fig. 4). The monkeys can find fallen nuts on the ground until March the following year. Lichens, bark and edible grass (fresh or dried) were available year around. Diet We recorded about 25 species of trees, shrubs and ground plants from 19 genera and 13 families in the diet of R. bieti at Xiaochangdu with two unidentified grass species and one unidentified angiosperm species (Table II). Of these species, 48 parts were exploited in total (not including the lichens). Among the food items that the monkeys consumed throughout the year there were at least three species of arboreal lichens, two species of grasses, at least two kinds of invertebrates in decayed wood and three under stones, and resin from two tree species. Although lichens formed a ubiquitous food resource throughout the year, the snub-nosed monkeys fed on many other food items with conspicuous differences across seasons (Fig. 5). The monkeys included substantially more food items in their diet in spring and autumn compared to other seasons. In general, the diet becomes more diverse from May, and diverse decreases abruptly after September. In spring, the monkeys’ diet constituted buds and young leaves of 16 tree species and the flowers of six tree species. In summer, the monkeys ate young leaves of 15 tree species, flowers of three tree species as well as the unripe nuts of Q. aquifolioides, the fruits of Rosa omeiensis and the invertebrates under small stones or in decayed wood. In autumn, their diet was composed of mature leaves of at least one Fig. 4. Monthly variation of food availability index with 63 tagged specimens in the secondary conifer forest at Xiaochangdu, Tibet (see text). Am. J. Primatol. DOI 10.1002/ajp Berberis ignorata Lonicera acuminata L. szechuanica Carex sp. Bergenia purpurascens Rhododendron cephalanthum R. uravifolium Cotoneaster acutifolius Lyonia villosa Quercus aquifolioides Ribes himalense Irix sp. Picea likiangensis Abies squamata Primula sp. Clematis montana Prunus conaderia Rosa omeiensis Sorbus prattii Salix disphila S. paraplesia Populus notundifolia (Poaceae) (Poaceae) Berberidaceae Caprifoliaceae Am. J. Primatol. DOI 10.1002/ajp 11 Sp Sp Sp Sp W Sp W Sp W Sp Sp Sp Sp Sp Buds 16 Sp Su Sp Su Sp Su Sp Sp Su Sp Su Sp Su Sp Su Sp Su Sp Su Sp Su Sp Su Sp Su Sp Su A Sp Su Sp Su Leaves 6 Sp Su Sp Sp Sp Sp Su Sp Flowers 2 Su A Su A W Fruits 1 Su Roots 6 W W W W W W Barks Season: Sp, Spring (May, Jun); Su, Summer (Jul, Aug, Sep); A, Autumn (Oct, Nov); W, Winter (Dec, Jan, Feb, Mar, Apr); Y, four seasons. Usnea longissima, Usnea florid, and Bryoria spp. on fir tree, evergreen tree, bushes, etc. b a Number of ‘‘species-parts’’ eaten Invertebrate in the decayed wood (at least two species) Invertebrate under barks of Rhododendron uravifolium (at least two species) Invertebrate under the stone on the ground (at least three species) Grass 1 Grass 2 Unidentified plant 1 Salicaceae Primulaceae Ranunculaceae Rosaceae Fagaceae Grossulariaceae Iridaceae Pinaceae Cyperaceae Diapensiaceae Ericaceae Species Family Parts 2 Y Y Resins Su W 4 Y Y Y Sp Su Sp Su Alls 3 Y Y Y Lichenb TABLE II. Directly Observed Food Species and Food Parts in the Diet of Rhinopithecus bieti at Xiaochangdu, Tibet over the Study Perioda 1150 / Xiang et al. Diet and Feeding Behavior of Rhinopithecus bieti / 1151 Fig. 5. Plant parts of different species eaten by Rhinopithecus bieti at Xiaochangdu throughout the year. tree species and two kinds of ripe fruits/nuts. In winter, food availability was low and some sources were depleted. The monkeys’ diet consisted of the bark of six tree species, two species of dried herbs on the ground and the fallen nuts of Q. aquifolioides, as well as at least two kinds of invertebrates found under the bark of Rhododendron uravifolium. Monkeys were seen eating the not yet ripened nuts of Q. aquifolioide in the trees on early August, and they continued to consume fallen nuts till March, found in a layer of accumulated fallen leaves. Contrary to some previous records (see above), we have never observed the snubnosed monkeys eating conifer foliage (needles). Diet Composition and Its Relation to Food Availability A total of 12,996 feeding records were obtained with 1,399 from AOB (Table I). Arboreal lichens were the single most numerous food item in the diet year-round, contributing more than 50% of the feeding records in scans. The diet composition that was obtained from two observation methods are significantly different (cross table test, w2 5 24.09, df 5 4, Po0.001). From SFS, we obtained a diet composition of 82.1% lichens, 12.1% buds and leaves, 1.1% flowers, fruits/ nuts, 0.6% invertebrates, 4.2% resin, bark, herbs. From AOB, we obtained a composition of 50.8, 28.5, 7.1, 6.5, and 7.1%, respectively. We integrated (weighed) the results of the two methods and got a relatively real diet composition of 74.8% lichens, 15.9% buds and leaves, 2.5% flowers and fruits/nuts, 2.0% invertebrates and 4.9% resin, bark, herbs. The monthly variations are displayed in Figure 6. Inter-monthly variation in the contribution of the two primary food items to the snub-nosed monkeys’ diet was considerable: from SFS, we got monthly proportions ranging from 52.5% (May) to 98.2% (Feb) for lichens, and 0% (Dec, Jan, and Feb) to 44.6% (May) for buds and leaves; from AOB, we got monthly proportions ranging from 30.7% (July) to 78.9% (Dec) for lichens, and 0% (March, Dec) to 54.2% (Aug) for buds and leaves. Irrespective of the observational technique applied (i.e., either SFS or AOB), non-lichen food items such as leaves, buds, flowers, and fruits/nuts were more commonly eaten in spring and summer than in autumn and winter. The monthly dietary diversity from two observation methods are shown in Table I. Dietary diversity calculated from AOB is higher than that from SFS (t-test, t 5 4.93, df 5 19, Po0.001). In general, the monkeys displayed the greatest dietary diversity in spring and summer (from May to September). Am. J. Primatol. DOI 10.1002/ajp 1152 / Xiang et al. Fig. 6. Monthly diet composition of Rhinopithecus bieti based on feeding records. (A) Data collected with a field scope (SFS), (B) data collected with or without binoculars (AOB). The correlations between diet composition (both from SFS and AOB) and food availability are shown in Table III. There are significant negative correlations between the percentage of feeding records for lichens in the diet and the percentage of leaves and buds (spearman rank correlation, of SFS: rs 5 0.803, Po0.001; of AOB: rs 5 0.898, Po0.01), as well as between the percentage of feeding records for lichens and the availability of leaves and buds (of SFS: rs 5 0.737, Po0.01; of AOB: rs 5 0.934, Po0.001). There are significant positive correlations between the percentage of feeding records for leaves and buds and the availability of leaves and buds (of SFS: rs 5 0.832, Po0.001; of AOB: rs 5 0.910, Po0.01). These correlations indicate that the snub-nosed monkeys prefer to feed on leaves and buds to lichens whenever they can be obtained. Feeding Behavior The snub-nosed monkeys were selective in their choice of food, consistently selecting specific parts of particular plant species. The monkeys ate the buds, slender leaves and flowers of Prunus conaderia, but feeding on the mature leaves was never observed. They ate the leaves and buds of Sorbus prattii, but the Am. J. Primatol. DOI 10.1002/ajp Diet and Feeding Behavior of Rhinopithecus bieti / 1153 TABLE III. Correlations Between Diet Composition (L, BL and FF) and Food Availability (BLa and FFa) in Rhinopithecus bieti at Xiaochangdua,b,c L L BL FF Bla FFa 0.803 0.045ns 0.737 0.540ns BL 0.898 0.095ns 0.832 0.799 FF ns 0.675 0.442ns BLa FFa 0.934 0.910 0.457ns 0.597ns 0.025ns 0.441ns 0.509ns ns 0.146 0.062ns 0.812 a Spearman rank correlation, ns, no significance; *Po0.05; **Po0.01; ***Po0.001. Diet composition of left lower part is obtained by SFS, right upper is obtained by AOB. c L, Lichens; BL, buds and leaves; FF, flowers and fruits; BLa, buds and leaves availability; FFa, flowers and fruits availability. b flowers and fruits of the same species were neglected. They ate the bark and flowers of Rhododendron uravifolium, but not the buds and leaves. The monkeys were frequently observed winding their way along trunks of P. likiangensis and A. squamata trees. We consider this behavior to be related to looking for exudates (resin) of conifers. This supposition is grounded on at least four times when we actually witnessed an individual consuming such resin. Occasionally, the monkeys consumed the roots of young A. squamata trees, and foraged on invertebrates by uncovering stones or decayed wood. In winter when the ground was covered with snow, they also foraged terrestrially and searched for fallen nuts of Q. aquifolioides that were scattered among fallen leaves. They were observed foraging for invertebrates from under stones in summer and from under the bark of rhododendrons in winter. Also, they were observed feeding the bark of Lonicera rzechuansis. Furthermore, the monkeys were observed digging up and feeding dried grass on the ground when there was heavy snowfall (about 70–80 cm in depth) in the high elevation forest from 18 February to 20 March 2005. In this period, the focal monkeys have to range within a relatively low altitude valley (about 3,500–3,700 m a.s.l.), close to the Mekong River. DISCUSSION The list of food plants exploited by black-and-white snub-nosed monkeys at Xiaochangdu in Tibet is certainly incomplete, mainly because direct observation time of monkey groups was relatively short. For example, as the monkeys were followed for only 3 days in September due to heavy fog and human disturbance, which led to only qualitative data for this month compared to others. Nevertheless, the data obtained via the two observation methods (SFS and AOB), which alleviate the effects of the rugged terrain, do provide a representative picture of the range of food items selected by R. bieti and provide insights into seasonal differences. Our study further demonstrates that overall availability of food such as buds and leaves influences the actual diet composition. Furthermore, possibly confounding effects of social factors constraining diet [Chapman, 1987] were assumed to be of limited importance since there was no apparent food competition with other primates or large mammals for the same resources (Z.-F. Xiang, personal observation). Therefore, considering that the abundance of plant species in each habitat type within the home range of the study group is relatively low (Fig. 3), we are reasonably confident that this short list represents most of the dietary plant species of this study group and is comparable to other subpopulations of this species studied elsewhere. Am. J. Primatol. DOI 10.1002/ajp Am. J. Primatol. DOI 10.1002/ajp Xiaochangdu Tacheng Mt. Longma 13 28 17 No. of plant families ‘‘/’’ 5 not mentioned or not identified. 41.5 42 41.5 Site a Study length (years) 19 42 52 No. of plant genera 25 59 97 No. of plan species 11 15 93 Buds 16 29 38 Leaves 6 / 51 Flowers 2 29 41 Fruits/Seeds Parts eaten 3 9 1 Lichens 13 17 25 Other TABLE IV. Comparison of Diet Composition of Rhinopithecus bieti Among Three Typical Study Sitesa 51 490 249 Total This study Ding and Zhao  Huo  Data source 1154 / Xiang et al. Diet and Feeding Behavior of Rhinopithecus bieti / 1155 TABLE V. Comparison of Habitat Characteristics of Rhinopithecus bieti Among Three Study Sitea Elevation (km) Annual AT (1C) Lowest monthly AT (1C) Highest monthly AT (1C) Annual precipitation (mm) No. of months with snow blanket Vegetation typesb Xiaochangdu Tacheng 3.5–4.25 2.7–3.7 4.7 7.5 3.6 0 12.5 14.9 740 — 5–6 4–5 12 123 Mt. Longma 2.7–3.4 8.8 1.9 14.3 1000–1400 3–4 1234 Site Data source This study Ding and Zhao  Huo  a AT, average temperature. Temperature was recorded at the following elevations: 3,800 m at Xiaochangdu, 2,800 m at Tacheng and 2,900 m at Mt. Longma. b 1, conifer forest; 2, evergreen broadleaf forest (oak forest); 3, mixed conifer-broadleaf forest; 4, deciduous broadleaf forest. Diet Characteristics of the Black-and-White Snub-Nosed Monkey The percentage of feeding records for lichens of the Xiaochangdu subpopulation from SFS amounts to 82.1%, this is a little more than the value obtained by direct observation with a field scope for the Wuyapiya subpopulation studied by Kirkpatrick . Both of these subpopulations live in the northern sector of the geographical distribution of R. bieti. Compared to these two groups, the percentage of lichens in the diet of the Tacheng subpopulation living in the middle sector is low (ca. 60%) [Ding & Zhao, 2004], and the percentage of lichens in the diet of the Jinsichang subpopulation living in the south sector is far lower (ca. 5%) [Yang & Zhao, 2001]. The latter value was not derived from direct observation, but from analyzing fecal contents [Yang & Zhao, 2001]. However, according to empirical results, out of 60% of all lichens feeding recorded, 9% were found in feces per year [Ding & Zhao, 2004]. Five percent of the lichens remain from feces of the Jinsichang subpopulation could suggest that lichens eating accounts for about 30% of the overall diet. If so, then lichens eating in subpopulations listed from north to south, Xiaochangdu, Wuyapiya, Tacheng and Jinsichang, are approximately 82.2, 75, 60 and 30%, respectively. This empirical evidence suggests that the amount of lichens that black-and-white snub-nosed monkeys ingest, decreases as latitude decreases and habitat diversity increases. Dietary Adaptations to An Extreme Habitat Factors such as elevation and habitat composition (in terms of species richness) influence the diet of colobine monkeys [Bennett & Davies, 1994]. Habitats at lower elevations tend to be complex with regard to floristic composition, and they usually contain more food species than those at higher elevations. In the case of R. bieti, there is a remarkable within-species variation in habitat features and diet composition, compared to two other subpopulations of R. bieti living at lower altitudes/latitudes. The diet of the Xiaochangdu subpopulation is the poorest in terms of the number of species exploited and plant parts eaten (Table IV). From north to south, black-and-white snub-nosed monkeys show an overall tendency to feed on more plant species and plant parts and to consume more non-lichens food. Compared to other study areas, the habitat of the Xiaochangdu group is less complex in terms of botanical diversity and more inclement in terms of climate (prolonged snowy season, lower Am. J. Primatol. DOI 10.1002/ajp 1156 / Xiang et al. temperatures) (Table V). A recent study indicates that the monkeys at Gehuaqing also strip the bark from spruce and fir trees to search for invertebrates [C.-C. Grueter, personal communication]; feeding on bark had been observed at Tacheng [Ding & Zhao, 2004] as had also been noted by Kirkpatrick . However, no previous studies, such as those by Kirkpatrick , Ding and Zhao , Yang and Zhao , and Huo , have found evidence of R. bieti incorporating invertebrates and resin in their diet. Feeding on items such as invertebrates, resin and bark seem to be adaptations to an extreme habitat and indicate the species’ behavioral plasticity and dietary flexibility. On the other hand, the observation that shoots and leaves of bamboo are favorite food items at Tacheng [Ding & Zhao, 2004], Jinsichang [Yang & Zhao, 2001] and Mt. Longma [Huo, 2005] was not true for this study subpopulation, because there is no bamboo at Xiaochangdu in the study area. In summary, the results of this study illuminate site-specific variability in dietary strategies of black-and-white snubnosed monkeys. Why Do Black-and-White Snub-Nosed Monkeys Eat Lichens? Considering that lichens are low in protein [Kirkpatrick, 1996], feeding on fruits/nuts, invertebrates and leaves may be a strategy to compensate for the scarcity of protein in the diet in spite of the fact that Colobus monkeys may be able to get protein from intestinal bacteria during the process of proliferation accompanied with fermentation of celluloses [Chivers, 1994; Kay & Davies, 1994]. Among the few other mammals that rely on lichens as a food source are caribou (Rangifer tarandus) and Barbary macaques (Macaca sylvanus). Both caribou [Bergerud, 1972; Servheen et al., 1989] and Barbary macaques [Hladik, 1981; Menard & Vallet, 1987] choose this low-protein item as fallback food during winter. Although reportedly low in protein, lichens’ high-carbohydrate content [Kirkpatrick, 1996] may well make it a good, quick-energy food for primates living in the cold Himalayas. Nevertheless, subsistence on lichens may only be a proximate response to the habitat at Xiaochangdu where environmental conditions are harsher and alternative foods are fewer than in other habitats. The negative correlation between the percentage of feeding records for lichens and the relative availability of buds and leaves (Table III) suggests that the monkeys prefer alternative foods to lichens whenever obtainable. A similar tendency has also been detected at other localities with greater floristic diversity where the study groups included substantial amounts of non-lichen foods in their diet [Ding & Zhao, 2004]. All this indicates feeding on lichens is an adaptive feeding strategy to strong variation in seasonal food availability. This is to say, our results support the previous view that black-and-white snub-nosed monkeys feed on lichens as a fallback food in bad seasons when there are few other food items available in the high-elevation conifer forests [Kirkpatrick, 1996]. Implications for Conservation Given that non-lichens item are relatively high in protein content [Kirkpatrick, 1996], the selection of non-lichens when available may be used partly to balance the diet. One of the non-lichen foods that deserve attention is the nut of Q. aquifolioides, which are plentiful and evenly distributed within EB. It is one of only two kinds of fruit/nut resources that the monkeys use at Xiaochangdu. The monkeys feed upon them both in the tree crowns when they are still unripe (from early August on), and also harvest fallen nuts from a layer of accumulated leaves on the ground in winter. These oak nuts may be an important Am. J. Primatol. DOI 10.1002/ajp Diet and Feeding Behavior of Rhinopithecus bieti / 1157 source of protein for the snub-nosed monkeys, especially for pregnant females in winter. However, locals habitually collect these fallen nuts in late autumn as fodder for domestic pigs. Accordingly, as a means of conservation, we suggest that the bureau of HNNR forbid local people from harvesting these nuts within the monkeys’ home range. In line with other recently completed studies [Ding & Zhao, 2004; Huo, 2005; Yang & Zhao, 2001], we provide evidence that they are capable of coping with an array of food items other than lichens and hence can be regarded as generalists. Considering that conifer forests are the prime targets for economical exploitation in the area, the snub-nosed monkeys’ ecological flexibility possibly implies a higher chance of survival. ACKNOWLEDGMENTS We acknowledge the staff at the administrative bureau of Honglaxueshan National Nature Reserve of Mangkang County in Tibet for their support. Special thanks are given to Professor Q.-K. Zhao for his warm encouragement and valuable suggestion, Professor D.-D. 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