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Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu Tibet adaptations to a marginal environment.

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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: zorph111@yahoo.com.cn
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 [1996] 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 [1989] 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 [2004]
Huo [2005]
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 [2004]
Huo [2005]
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 [1996]. 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 [1996].
However, no previous studies, such as those by Kirkpatrick [1996], Ding and Zhao
[2004], Yang and Zhao [2001], and Huo [2005], 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. Tao for identifying plant specimens,
Professor Michael Huffman for useful suggestions and editing the English of
the manuscript, and two anonymous reviewers for useful suggestions that
improved the manuscript. Without the help of our field assistants, Mr. Z. Ding,
R. Ci, J. Zhu, Z. Wang, A’Nan and P. Deng, it would have been impossible for us to
complete the fieldwork.
REFERENCES
Altman J. 1974. Observational study of behavior: sampling methods. Behaviour 49:
227–267.
Bennett EL. 1983. The banded langur: ecology
of a colobine in a West Malaysian rainforest, PhD thesis. Cambridge: Cambridge
University.
Bennett LE, Davies AG. 1994. The ecology of
Asian colobines. In: Davies AG, Oates JF,
editors. Colobine monkeys: their ecology,
behaviour, and evolution. Cambridge: Cambridge University Press. p 129–171.
Bergerud A. 1972. Food habits of newfoundland caribou. J Wildlife Manage 36:913–923.
Brattsten LB. 1979. Biochemical defense mechanisms in herbivores against allelochemicals. In: Rosenthal GA, Janzen DJ, editors.
Herbivores: their ineraction with secondary
plant compounds. New York: Academic
Press. p 199–270.
Chapman C. 1987. Flexibility in diets of three
species of Costa Rican primates. Folia
Primatol 49:90–105.
Chivers DJ. 1994. Functional anatomy of the
gastrointestinal tract. In: Davies AG, Oates
JF, editors. Colobine monkeys: their ecology, behaviour, and evolution. Cambridge:
Cambridge University Press. p 205–227.
Ding W, Zhao QK. 2004. Rhinopithecus bieti at
Tacheng, Yunan: diet and daytimes activities. Int J Primatol 25:583–598.
Freeland WJ, Janzen DH. 1974. Strategies
in herbivory by mammals: the role of plant
secondary compounds. Am Nat 108:
268–289.
Goldsmith FB, Harrison CM, Morton AJ.1986.
Description and analysis of vegetation. In:
Moore PD, Chapman SB, editors. Methods in
plant ecology (2nd edition). Oxford: Blackwell Scientific Publications. p 437–524.
Hill DA. 1997. Seasonal variation in the
feeding behavior and diet of Japanese
macaques (Macaca fuscata yahui) in lowland forest of Yakusima. Am J Primatol 43:
305–322.
Hladik CM. 1981. Diet and the evolution of
feeding strategies among forest primates.
In: Harding RSO, Teleki G, editors. Omnivorous primates: gathering and hunting in
human evolution. New York: Columbia
University Press. p 215–254.
Hladik CM, Chivers DJ. 1978. Concluding
discussion: ecological factors and specific
behavioural patterns determining primate
diet. In: Chivers DJ, Herbert J, editors.
Recent advances in primatology. Vol 1:
Behaviour. London: Academic Press.
p 433–444.
Huo S. 2005. Diet and habitat use of Rhinopithecus bieti at Mt Longma, Yunnan, and
phylogeny of the Family Viverridae in
China, Ph.D. Dissertation, Chinese Academy
Am. J. Primatol. DOI 10.1002/ajp
1158 / Xiang et al.
of Sciences. Kunming: Kunming Institute of
Zoology.
Kay RF. 1978. Molar structure and diet in
extant Cercopithecidae. In: Butler PM, Joysey KA, editors. Development, function and
evolution of teeth. New York: Academic
Press. p 309–339.
Kay RNB, Davies AG. 1994. Digestive physiology. In: Davies AG, Oates JF, editors.
Colobine monkeys: their ecology, behaviour,
and evolution. Cambridge: Cambridge University Press. p 229–250.
Krebs CJ. 1999. Ecological methodology. Hartlow, England: Addison Wesley Longman Inc.
Kirkpatrick RC. 1996. Ecology and behavior
of the Yunnan Snub-nosed langur (Rhinopithecus bieti, Colobinae), Ph.D. Diss. Davis:
University of California.
Kirkpatrick RC, Zou RJ, Dierenfeld ES, Zhou
HW. 2001. Digestion of selected foods by
Yunnan snub-nosed monkey Rhinopithecus
bieti (Colobinae). Am J Phys Anthrop 114:
156–162.
Li ZX, Ma SL, Hua CH, Wang YX. 1982. The
distribution and habits of the Yunnan golden monkey, Rhinopithecus bieti. J Hum
Evol 11:633–638.
Long YC, Kirkpatrick RC, Zhong T, Xiao L.
1994. Report on the distribution, population, and ecology of the Yunnan snub-nosed
monkey (Rhinopithecus bieti). Primates 35:
241–250.
Mash CW. 1981. Ranging behaviour and its
relation to diet selection in Tana River red
colobus (Colobus badius rufomitratus).
J Zool (Lond.) 195:473–492.
Menard N, Vallet D. 1987. Diet and food
resources for two Macaca sylvanus troops
living in contrasting habitats in Algeria. Int
J Primatol 8:496.
Oates JF. 1994. The natural history of African
Colobines. In: Davies AG, Oates JF, editors.
Colobine monkeys: their ecology, behaviour,
and evolution. Cambridge: Cambridge University Press. p 75–128.
Oates JF, Davies AG, Delson E. 1994. The
diversity of living colobines. In: Davies AG,
Oates JF, editors. Colobine monkeys:
Am. J. Primatol. DOI 10.1002/ajp
their ecology, behaviour, and evolution.
Cambridge: Cambridge University Press.
p 45–73.
Servheen G, Lyon LJ. 1989. Habitat use by
woodland caribou in the Selkirk Mountains.
J Wildlife Manage 53:230–237.
Starin ED. 1991. Socioecology of the red
colobus monkey in the gambia with particular reference to female-male difference
and transfer pattern, Ph.D thesis. New
York: City Univeristy of New York.
Supriatna J, Manullang BO, Soekara E. 1986.
Group composition, home range, and diet of
the maroon leaf monkey (Presbytis rubicunda) at Tanjung Putting Reserve, Central
Kalimantan, Indonesia. Primates 27:
185–190.
Waterman PG, Kool KM. 1994. Colobine food
selection and plant chemistry. In: Davies
AG, Oates JF, editors. Colobine monkeys:
their ecology, behaviour, and evolution.
Cambridge: Cambridge University Press.
p 251–284.
Wu BQ, He SJ. 1989. A micro-quantitative
analysis of types of residuary diets among
excrements of a group of Rhinopithecus bieti
in snowing season. Zool Res 10(Suppl):
101–109.
Xiang, ZF. 2005. The ecology and behavior of
black-and-white snub-nosed monkeys (Rhinopithecus bieti, Colobinae) at Xiaochangdu
in Honglaxueshan National Nature Reserve, Tibet, China, Ph.D. Dissertation.
Kunming: Chinese Academy of Sciences.
Kunming Institute of Zoology.
Xiang ZF, Wang L, Huo S, Cui LW, Xiao W,
Quan RC, Zhong T. Distribution, status and
conservation strategies of the black-andwhite snub-nosed monkey Rhinopithecus
bieti in Tibet. Oryx. In press.
Yang SJ, Zhao QK. 2001. Bamboo leaf-based
diet of Rhinopithecus bieti at Lijiang, China.
Folia Primatol 72:92–95.
Zar JH. 1999. Biostatistical analysis (4th
edition). Upper Saddle River, NJ: PrenticeHall Inc. Simon & Schuster/A Viacom
Company.
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