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Dietary breadth and resource use of Franois' langur in a seasonal and disturbed habitat.

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American Journal of Primatology 73:1176–1187 (2011)
RESEARCH ARTICLE
Dietary Breadth and Resource Use of Franc- ois’ Langur
in a Seasonal and Disturbed Habitat
GANG HU1,2
1
Institute of Rare Wildlife, China West Normal University, Nanchong, Sichuan, People’s Republic of China
2
Institute of Wildlife, Southwest Forestry University, Kunming, Yunnan, People’s Republic of China
Previous studies of Trachypithecus species indicated that they were selective feeders that concentrated
on relatively few food species/items. From January to December 2005, I quantified potential food
availability and the food species/items eaten by five groups of Franc- ois’ langur (Trachypithecus
francoisi) in the Mayanghe Nature Reserve (MNR), People’s Republic of China. These langurs fed on
164 species, of which the top ten accounted for 51% of all feeding records. Langurs consumed more
species (91) in the spring than in other seasons (73 summer, 75 autumn, and 67 winter), and only
38 species were consumed in all seasons. Nontree food species, such as bushes and lianas, accounted for
47% of the total feeding records and for a majority (68%) of the feeding records in winter. The annual
diet consisted of leaves (64% of feeding records), fruit and seed (32%), and other nonfoliage items (4%);
the langurs switched from being more folivorous in spring (93%) and summer (79%) to being more
frugivorous in autumn (53%) and winter (56%). There was no correlation between the proportion of
feeding records and the food availability in the most frequently consumed species, indicating that these
langurs were selective feeders; there were significant correlations between consumption and abundance
in both the entire set of 112 food species and the set of 86 infrequently consumed species, indicating that
foods that are more available are eaten more frequently. It appeared that in the seasonal and disturbed
habitat, feeding decisions and diet composition of the langur may be driven more by food availability,
and less by animal’s selectivity, than at other sites. The results indicate that Franc- ois’ langur copes
with habitat alterations by broaden its dietary breadth; this has implications for the adaptive
significance of dietary breadth, and has implications for future conservation strategies for species which
exist in degraded habitats. Am. J. Primatol. 73:1176–1187, 2011.
r 2011 Wiley Periodicals, Inc.
Key words: dietary breadth; dietary variability; food availability; Franc-ois’s langur (Trachypithecus francoisi); seasonal and disturbed habitat
INTRODUCTION
Colobines have traditionally been labeled as
‘‘leaf-eaters’’ because of certain morphological and
physiological features (sharp molars, enlarged salivary glands, and multichambered stomach) which
seem to be adaptations for leaf eating [Kay & Davies,
1994], a generalization which does injustice to the
considerable dietary variation documented among
them [Bennett & Davies, 1994; Fashing, 2007;
Kirkpatrick, 2007; Oates, 1994]. Even within the
Asian langurs considerable variation exists: Trachypithecus tend to be more folivorous and Presbytis
more frugivorous, while the proportion of leaves in
the diet of Semnopithecus varies greatly from site to
site [Bennett & Davies, 1994; Kirkpatrick, 2007].
Theoretically, more frugivorous langurs would be
expected to have broader diets than more folivorous
species, because fruit is more ephemeral than
ubiquitous leaves, and generally less available; for
example, in Kuala Lompat, West Malaysia, frugivorous Presbytis melalophos has a more diverse diet
r 2011 Wiley Periodicals, Inc.
than sympatric Trachypithecus obscurus [Benett,
1983]. In addition, langur species living on less
common plant species seem to have more diverse
diets than those which rely on common species; for
instance, T. vetulus in Polonnaruwa, Sri Lanka,
exploited only 28 species, of which three common
Contract grant sponsors: Wenner-Gren Foundation, the Australian National University, the Columbus Zoo, Conservation
International, Pittsburgh Zoo; Primate Conservation Inc.;
Contract grant number: G]443 & 797; Contract grant sponsor:
Nature Science Fund Committee of China; Contract grant
number: 30860051; Contract grant sponsor: National Forestry
Bureau of China; Contract grant number: 2130211; Contract
grant sponsor: Southwest Forestry University; Contract grant
number: 110851.
Correspondence to: Gang Hu, Institute of Rare Wildlife, China
West Normal University, Nanchong, Sichuan, 637009, People’s
Republic of China. E-mail: ganghu126@126.com
Received 2 January 2011; revised 28 June 2011; revision
accepted 17 July 2011
DOI 10.1002/ajp.20985
Published online 24 August 2011 in Wiley Online Library (wiley
onlinelibrary.com).
Foraging of Franc- ois’ Langur at Mayanghe / 1177
species accounted for 70% of its annual intake
[Hladik, 1977], and T. johnii in Kakachi, in the
Western Ghats of India, had a much broader diet of
115 species of which the two commonest trees
contributed only 5% of its annual diet [Oates et al.,
1980]. Thus, particularly for widespread species,
intraspecific dietary variation, enabling them to
survive in diverse habitats, would be expected, and
if marked dietary variation exists between populations, categorizing a species based on a single study
may be inadequate.
Besides the academic implications for the understanding of feeding competition, social behavior, and
structure [Chapman & Rothman, 2009; Koenig et al.,
1998; Snaith & Chapman, 2007; Zhao, 1999], studies
of dietary variation also have specific implications for
conservation. Species that display high dietary
variability might be able to cope better with habitat
alterations than species with a focused diet. Documenting dietary variation can help to identify
which food species are most and least essential, and
to evaluate which species/populations are likely to be
more or less vulnerable to anthropogenic or environmental change [Harris & Chapman, 2007].
Franc- ois’ langur, Trachypithecus francoisi, is
widespread, ranging from the Red River in northern
Vietnam to south central China, about 211300 to
291080 N [Bleisch & Zhang, 2004; Fooden, 1996;
Groves, 2001]. Wild populations remain in fragmented limestone forest habitats scattered within its
range, with great variations in forest type (evergreen
to semideciduous), temperature (7–28 to 18–321C),
annual rainfall (950–3,000 mm), and human disturbance (severely fragmented to intact habitat)
[Hu, 2007], suggesting potential variation in diet.
Previous studies on the feeding ecology of
Franc- ois’ langur and other Trachypithecus species
at more southerly sites have indicated that they are
selective feeders that concentrate their diet on
relatively few food species/items. For example,
Franc- ois’ langurs in Fusui (221240 5100 –360 2000 N,
1071230 410 4300 E), southern China, consumed only
37 species out of a possible 105 species over the
course of a year [Cai, 2004]; the top ten food species
accounted for 90% of feeding time and the langurs
showed extreme folivory, with 94% of feeding time
devoted to leaf-eating [Huang et al., 2008].
In this study, I investigated the dietary strategy
of Franc- ois’ langur in Mayanghe Nature Reserve
(MNR), an area in the northernmost part of its
range, with great seasonality and human disturbance, although it is the largest remaining population of this species (about 43% of the total
population) [Hu, 2011]. I quantified food species
and items consumed by the langurs in MNR, along
with food availability, aiming to understand factors
influencing the diet at this more seasonal and
disturbed site and how the diet differs from that
recorded at other sites.
METHODS
Study Site
I conducted fieldwork from January to December
2005
at
MNR,
China
(281370 3000 –540 2000 N,
0
00
0
00
10813 58 –19 45 E; Fig. 1), about 310 km2. MNR is
in the subtropical wet climatic zone with a long
frostless period and distinct seasonality. Annual
temperature averages 17.21C, with mean temperatures of 17.71C in spring (March to May), 281C in
summer (June to August), 18.31C in autumn (September to November), and 6.91C in winter (December
to February). Annual rainfall is 952 mm, with
approximately 78% falling in spring and summer
[Hu, 2007]. Topography in MNR is characterized by
Karst mountains with steep valleys and gentle limestone platforms ranging from 420 to 1,067 m above
sea level [Wang et al., 1994]. The natural vegetation
is mid-subtropical evergreen broad-leaved forest
[Yang, 1994], but primary forest remains untouched
only in the core protected area, while in other areas it
has been extensively fragmented by cultivation. The
main study area was ca. 800 ha and included sections
of undisturbed forest, buffer zone regions, and areas
that were outside the reserve including settlements,
highways, cultivated land, and forest patches. Most
limestone platforms and gentle slopes have been
cultivated and forest remains in patches in the buffer
zones and nonreserve area but remains intact on
steep slopes [Hu, 2007].
Data Collection
Plant species composition and food abundance
I set up 12 plots (10 100 m each), six in
relatively intact forest and six in fragmented forest
patches. I recorded all trees and woody lianas
Z1.5 cm in diameter at breast height (DBH) within
each plot. I chose long linear plots because these are
more appropriate for surveying heterogeneous habitats [Ganzhorn, 2003; Krebs, 1999]. I set the lower
limit at 1.5 cm DBH because, in a preliminary study
in 2003, langurs were seen feeding on plants of this
size or larger. I recorded species identity, height, and
DBH for all stems in these plots (I took the diameter
at approximately 1 m from the ground as DBH for
creeping liana species). Following Snaith and Chapman
[2008], I used basal area as an index of the leaf
biomass of an individual tree and summed the
cumulative leaf biomass for each species in the area.
Feeding data for Franc- ois’ langur
I observed five langur groups, with an average
group size of 11 individuals (range 8–19). I followed the
groups from 6:30 until approximately 19:30 for an of
average 20 days per month (ranging 1526), with the
start and end times varying seasonally with the amount
of light. Normally, I observed the langurs at a distance
varying from 10 to 100 m with the naked eye or through
Am. J. Primatol.
1178 / Hu
Fig. 1. Location of MNR and the main study area (Location of MNR is the red point in the small map in the upper left corner). MNR,
Mayanghe Nature Reserve. [Color figures can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
binoculars. I collected systematic feeding and behavioral data via scan sampling at 10-min intervals [Altmann,
1974], and added additional species to the list of food
plants from ad libitum observations. I scanned and
recorded all individuals in sight within the first 2 min,
and was careful not to sample an individual more than
once per scan. During feeding bouts, I recorded both
species and item consumed (e.g. Lindera communis,
young leaves). Scan data were not collected continuously when it is in the field, but only when visibility
allowed and when I was not conducting other types of
data collection. The total sample size was 4,553 scans,
with 7,529 feeding records (average 1.65 records per
scan sample); this is roughly equivalent to 759
observation hours.
Am. J. Primatol.
Data Analysis
I defined major food species as those which
comprised 41% of the total feeding records, andtopspecies as the set of species, in descending order of
contribution to the diet, which collectively account
for the first 50% of the total feeding records. I used
the Shannon–Weaver Diversity Index to examine
seasonal variation in dietary diversity, calculated as
H0 5 SPi ln Pi, where Pi is the proportion of feeding
records of the ith species. I used stem density to
measure the degree of dominance of plant taxa. I
used the proportion of basal area of a species as index
of its relative availability, given the relationship
between basal area and food availability [Chapman
Foraging of Franc- ois’ Langur at Mayanghe / 1179
et al., 1995] and, since I calculated cumulative basal
area, both species and individual differences in food
availability (leaf biomass) were taken into account. I
used selection indices to measure the degree of
selectivity for a species by using the proportion of
the feeding record of certain species divided by the
proportion of the plots’ total basal area represented
by that species. A value o1 means that the species is
consumed less than expected based on its basal area,
whereas a value 41 means that it is consumed more
than expected.
I summarized the percentage contribution of
different foods/species to the full set of feeding
records made on a given day (daily records ranging
33–238), and then pooled daily data into a monthly
and an annual data set. I logarithmically transformed summarized feeding data (in proportions)
and used the Pearson Correlation Coefficient to test
whether foods were generally consumed in proportion to their abundance.
This research adhered to the American Society
of Primatologists principles for the ethical treatment
of nonhuman primates. The research complied with
protocols approved by the appropriate wildlife conservation committee of China, and adhered to the
legal requirements of China.
RESULTS
Plant Species and Overall Diet
I recorded 175 woody species (53 families, 110
genera) in the main study area. I recorded 4,157
individual plants belonging to 144 species (50
families, 98 genera), including 79 tree species, 15
bushes, and 50 woody liana species on the plots. The
ten most common families overall accounted for 39%
of total genera, 45% of species, and 68% of individuals (Table I). The 15 most common species overall
accounted for only 47% of sampled individuals, and
about 60% of basal area in the plots (Table II),
indicating the low-dominant nature of the habitat at
MNR. Nontree species such as bushes/lianas were
common: in fact, the five most common species were
bushes and lianas (Table II).
I identified 164 food species (55 families, 108
genera) consumed by the langurs, including 83 trees,
18 bushes, 51 lianas, 9 herbs, 1 crop plant (corn), 1
fern, and 1 bamboo. In 4,553 systematic scan
samples, I collected 7,529 feeding records for identified food species (129 species, including 68 trees, 14
bushes, 39 lianas, 6 herbs, 1 crop, and 1 bamboo) and
feeding items. I recorded another 35 food species in
ad libitum observations. The 26 major food species
accounted for 79% of the total feeding records. The
top species (collectively accounting for 450% of
feeding records) accounted for 51% of feeding records
(Table III), and the other 49% came from a much
broader range of species, 119 in total. The annual
dietary diversity index was 3.76.
Foliage, including young leaves and mature
leaves, made up the majority (63.9%) of the feeding
records. Fruit (25.7%) and seed (6.5%) contributed
32.2%, whereas other nonfoliage items, including
flower buds, flowers, herb roots, and bamboo shoots,
contributed only 3.9% of the diet (Table IV).
Dietary Seasonality
The langurs fed on 91 plant species in spring, 73
in summer, 75 in autumn, and 67 in winter
(Table V); the corresponding dietary diversity indices
were 3.73, 3.51, 3.44, and 3.02, respectively. The
number of top species over the year showed a similar
pattern: ten in spring, eight in summer and autumn,
and five in winter.
Of the 129 species, only 38 were eaten in all the
four seasons, and these accounted for 83% of the
total feeding records. Ninety-one additional species
were consumed in particular seasons only (17 species
in three seasons, 29 species in two seasons, and
45 species in one season).
The diet also showed seasonal change in feeding
items: the langurs switched their diet from more
folivorous in spring (93%) and summer (79%) to
TABLE I. List of the Ten Most Common Plant Families in the Main Study Area at Mayanghe Nature Reserve as
Determined by Transect Sampling
Family
Rosaceae
Verbenaceae
Oleaceae
Ulmaceae
Rutaceae
Papilionaceae
Caprifoliaceae
Cornaceae
Euphorbiaceae
Rhamnaceae
Total
No of genera
% of genera
No of species
% of species
No of individual
% of individuals
9
3
2
3
5
5
2
1
5
3
38
9.2
3.1
2.0
3.1
5.1
5.1
2.0
1.0
5.1
3.1
38.8
16
4
6
6
7
8
4
2
8
3
64
11.1
2.8
4.2
4.2
4.9
5.6
2.8
1.4
5.6
2.1
44.4
711
442
261
242
222
218
209
163
157
146
2,271
17.1
10.6
6.3
5.8
5.3
5.2
5.0
3.9
3.8
3.5
66.7
Am. J. Primatol.
Am. J. Primatol.
Rosaceae
Verbenaceae
Rosaceae
Caprifoliaceae
Verbenaceae
Cornaceae
Ulmaceae
Oleaceae
Oleaceae
Rutaceae
Rhamnaceae
Rosaceae
Lauraceae
Rubiaceae
Rutaceae
Family
260
222
178
176
169
159
147
109
96
92
82
78
70
66
63
1,967
Individuals
6.3
5.3
4.3
4.2
4.1
3.8
3.5
2.6
2.3
2.2
2.0
1.9
1.7
1.6
1.5
47.3
Individuals
proportion
4
1
23
14
29
15
2
12
16
27
5
54
9
18
1.9
46.9
FC
ranking
4.6
13.0
1.1
2.4
0.8
2.4
8.0
2.5
2.2
0.9
3.8
0.2
3.2
Feeding
contribution
0.7
1.3
0.2
0.8
0.8
32.8
18.2
1.2
1.6
0.6
0.2
0.1
0.7
0.1
0.2
59.6
BA
proportion
26
13
49
23
20
1
2
15
11
29
48
69
24
52
54
BA
ranking
11.3
6.5
9.8
5.2
3.1
1.0
0.1
0.4
2.0
1.4
1.6
16.9
1.9
4.3
S-index
8
22
13
27
37
65
104
82
48
61
57
5
52
32
S-index
ranking
Note: Tree; bush; liana.
Callicarpa bodinieri
Ulmus castaneifolia
Pittosporum trigonocarpum
Pyracantha fortuneane
Sageretia rugosa
Millettia speciosa
Pistacia chinensis
Celtis bungeana
Lindera communis
Orencnide frutescens
Total
Species
Verbenaceae
Ulmaceae
Pittosporaceae
Rosaceae
Rhamnaceae
Papilionaceae
Anacardiaceae
Ulmaceae
Lauraceae
Urticaceae
Family
13.0
8.0
4.9
4.7
3.8
3.6
3.5
3.5
3.2
3.0
51.0
Feeding contribution (%)
103
290
142
7
132
34
56
76
49
36
925
Spring
123
159
119
3
66
73
87
82
78
31
821
Summer
196
105
40
63
53
70
53
53
28
67
728
Autumn
Seasonal feeding records
553
50
71
270
32
95
69
49
84
93
1,366
Winter
1.3
18.2
0.3
0.7
0.2
0.4
2.4
0.2
0.7
0.4
24.8
BA
proportion
TABLE III. List of the Ten Most Frequently Consumed Species in the Main Study Area at Mayanghe Nature Reserve
13
2
39
26
48
35
5
58
24
37
BA
ranking
9.8
0.4
14.5
6.5
16.9
9.6
1.5
23.1
4.3
8.6
S-index
13
82
7
22
5
14
59
4
32
15
S-index
ranking
Note: Tree; bush; liana. Individuals refer to the total sampled individuals of certain species; Individuals proportion refer to stem density of certain species in sampling plots; FC ranking refers to the
ranking in feeding contribution; BA proportion refers to the basal area proportion of certain species in sampled plots.
Pyracantha fortuneane
Callicarpa bodinieri
Rose cymosa
Viburnum chinshanense
Vitex negundo var. heterophylla
Cornus wilsoniana Ulmus castaneifolia
Ligustrum delavayanum
Ligustrum sinense
Zanthoxylum simulens
Sageretia rugosa
Rubus parkeri
Lindera communis
Paederia scandens
Zanthoxylum echinocarpus Species
TABLE II. Sampled Individuals, Stem Density, Feeding Contribution, Basal Area Proportion and Corresponding Ranking of the 15 Most Common
Plant Species in the Main Study Area at Mayanghe Nature Reserve
1180 / Hu
Foraging of Franc- ois’ Langur at Mayanghe / 1181
TABLE IV. Annual and Seasonal Diet of Franc- ois’ Langur at Mayanghe Nature Reserve
Young Leaves
Spring
Summer
Autumn
Winter
Annual
Mature leaves
Buds
Flowers
Fruits
Seeds
Roots/Shoots
N
%
N
%
N
%
N
%
N
%
N
%
N
%
Total
N
1,755
1,097
194
217
3,263
83.3
63.7
13.0
12.3
43.3
202
259
426
664
1,551
9.6
15.0
28.5
30.1
20.6
25
60
66
31
182
1.2
3.5
4.4
1.4
2.4
13
12
2
55
82
0.6
0.7
0.1
2.5
1.1
97
263
623
951
1,934
4.6
15.3
41.7
43.1
25.7
16
30
167
275
488
0.8
1.7
11.2
12.5
6.5
0
0
17
12
29
0
0
1.1
0.5
0.4
2,108
1,721
1,495
2,205
7,529
TABLE V. Seasonality of Plant Food Categories for Franc- ois’ Langurs at Mayanghe Nature Reserve
Food categories and number of species
Spring
Summer
Autumn
Winter
Annual
Tree
Bush
Liana
Herb
58
42
33
35
68
9
10
12
9
14
22
18
24
22
39
2
2
5
1
6
Crop
Contribution (% of total feeding record)
Bam
Subtotal
Tree
Bush
Liana
Herb
1
91
73
75
67
129
69.9
59.2
51.9
31.8
52.7
14.4
23.0
24.3
43.1
26.7
15.4
15.8
22.3
24.6
19.5
0.3
0.4
1.2
0.5
0.6
1
1
1
Crop
Bam
Subtotal
0.4
100
100
100
100
100
1.6
0.4
0.1
Bamboo.
more frugivorous in autumn (53%) and winter (56%)
(Table IV).
Importance of Bushes and Lianas
Langurs at MNR depended heavily on nontree
resources, such as bushes and lianas, and about 47%
of the total feeding records came from nontree
species (Table V). Similarly, trees and nontree
species make up almost the same proportion in
both species number and feeding contribution in the
categories of both top ten food species (6 vs. 4 in
species; 26 vs. 25% in feeding records) and the 26
major food species (13 vs. 13 in species; 40 vs. 39%,
respectively). In the winter, nontree species accounted for 68% of the feeding records (Table V).
Moreover, six of the ten most selected species over
the year (with a selection index 410) were bushes
and lianas, though their contribution to overall basal
area was only about 0.6% (Table VI).
Food Choice by the Langurs
Fourteen of the 15 most common species were
eaten by the langurs, of which 11 species were year
round dietary items, including five of the ten most
frequently consumed species on an annual basis:
Callicarpa bodinier, Ulmus castaneifolia, Sageretia
rugosa, Pyracantha fortuneane, and Lindera communis
(Table III). The 15 most common species overall
accounted for only 47% of feeding records, matching
well with their stem density in sampling plots, 47%
(Table II), while the remaining 53% of feeding
records came from 115 other less common species.
The langurs spent a large amount of time
feeding from some species that were less common.
For example, Ficus stenophylla, Sycopsis laurifolia,
and Celtis julianae were ranked the first, third, and
fourth in selection, respectively, though they were
very rare in the habitat, with low basal area
proportion rankings of 124th, 99th, and 58th,
respectively (Table VI). Moreover, all the ten most
selected species (with S-index 410) were less
common, and they overall accounted for 18 % of
feeding records but occupied only 1% of the
total basal area (Table VI). This indicates that these
foods were not consumed proportionally to their
abundance.
To further examine food selection vs. availability, I combined the food species into several categories: including the top species (collectively
accounting for 450% of feeding records), major food
species (each accounting for 41% of feeding records),
infrequently used species (each accounting for o1%
of feeding records), and all 112 species, and tested
the correlations between the number of feeding
records and abundance (proportion of overall basal
area). Because nine woody food species were not
found in transects, and herbs, crop and bamboo were
not recorded in transect sampling, I limited my
analysis to the 112 species for which I had abundance
information. I used the 86 infrequently used species
to confirm whether the consumption of these lessused foods depended on their availability or on
individual selection.
The proportion of feeding records accounted for
by a species was not correlated with its abundance
Am. J. Primatol.
40
79
21
8
5
19
3
18
33
0.013
0.003
0.050
0.150
0.223
0.094
0.342
0.171
0.065
1.1
124
136
99
58
48
78
39
54
88
either for the ten top food species (r 5 0.352, twotailed, P 5 0.318) or the 26 major food species
(r 5 0.166, two-tailed, P 5 0.418). Nine of the ten
top species (Table III), and 23 of the 26 major species,
had S-index 41, indicating that these species were
consumed more than expected based on their
abundance. The correlation was significant, however,
for the 86 infrequently consumed species (r 5 0.226,
two-tailed, P 5 0.036), and for the entire set of 112
food species (r 5 0.301, two-tailed, P 5 0.001). Thus,
for a broader range of dietary constituents, food
consumption reflected relative abundance. Although
langurs consumed large amounts of some foods (e.g.
the top ten species), it was generally the abundance
of a species that predicted the degree to which it was
consumed.This presumption was supported by examining the consumption of some top food species.
For example, the high feeding ranking (second) of
Ulmus castaneifolia was most likely due to its high
abundance (ranked second in basal area ranking),
rather than simply due to the langur’s selectivity
(ranked 82nd in S-index, Table III). Similarly, the
high consumption of Pistacia chinensis was also
attributed to its high abundance (ranked fifth in
basal area ranking), though the S-index was slightly
more than one (Table III).
37
53
53
74
40
15
14
286
14
49
32
16
71
44
11
238
0.5
0.1
1.2
3.5
3.8
1.4
4.9
1.9
0.7
18.0
1
142
50
12
435
21
14
6
39
82
66
17
119
37
14
394
DISCUSSION
Note: Tree; bush; liana.
Ficus stenophylla
Parthenocissus laetivirens
Sycopsis laurifolia
Celtis bungeana
Sageretia rugosa
Acanthopanax trifoliatus
Pittosporum trigonocarpum
Zanthoxylum echinocarpus
Dalbergia hancei
Total
Moraceae
Vitaceae
Hamamelidaceae
Ulmaceae
Rhamnaceae
Araliaceae
Pittosporaceae
Rutaceae
Papilionaceae
38.1
31.0
24.3
23.1
16.9
15.1
14.5
11.3
10.4
2
76
132
Basal area
ranking
Basal
area %
Feeding
ranking
Feeding
record %
Family
S-index
Spring
Summer
Autumn
Winter
Am. J. Primatol.
Species
Seasonal feeding record
TABLE VI. The Feeding Contribution, Basal Area Proportion, and Corresponding Ranking of the Ten Most Selected (S-index 410) Plant Food
Species of Franc-ois’ Langur at Mayanghe Nature Reserve (as Determined by Systematic Sampling Record and Transect Record)
1182 / Hu
Several previous studies on feeding ecology in
Trachypithecus spp in more southerly sites have
documented that they concentrated on relatively few
food species (Table VII). On the contrary, Franc- ois’
langur at MNR had a much broader diet than that of
congeners in southern sites.
The assumption that frugivorous langurs generally have a more diverse diet than folivorous
species is theoretically reasonable, and has gained
support from comparisons of sympatric species and
of multiple populations. For example, more frugivorous Semnopithecus entellus has a broader diet than
more folivorous Trachypithecus vetulus (43 vs. 28) in
Polonnaruwa, Sri Lanka, [Hladik, 1977], and a group
of T. francoisi in Nonggang was more frugivorous
and had a much more diverse diet than a folivorous
group in Fusui [Huang et al., 2008; Zhou et al.,
2006]; some cases, however, seem quite the contrary,
e.g. T. pileatus at Madhupur, Bangladesh fed on 35
species and fruits and seeds made up 32% of feeding
records [Stanford, 1991], while T. leucocephalus at
Fusui exploited 50 species but fruits and seeds
accounted for only 9% [Li et al., 2003]. Kool [1993]
also reported that a group of T. auratus with a more
folivorous diet had a broader diet than a group
that had a more frugivorous diet (Table VII). If
secondary compounds are relatively important in
feeding selection, folivores might be forced to have
broader diets than frugivores; as feeding on more
species may prevent high intake levels of any single,
Pangandaran,
Indonesia
T. auratus
22.1
7–28
1,022
18–25
Evergreen
Semi-deciduous
1,168
22
Evergreen
13
1,168
12
12
12
12
12
12
18
13
12
952
1,350
2,280
19.3–27.3
Deciduous
1,452
4,557
3,084
24.4–31.2
22.535
Temperaturea
Evergreen
Secondary
Evergreen
Forest type
982
759
168
–
379
784
–
726
646
1,381
7,529
–
–
3,668
20,460
1,963
2,009
3,029
42
50
164
37
36
90
35
88
66
94
53
9
32
31
32
27
88
29–34
25
37
67
67
49
115
Leaves
154
164
175
105
140
78–116
Woody
plant
Fruits speciesc
Dietary contents
(%)
85
62
51
90
73
62
71
85
61
65
FC of
top ten
species
(%)d
Huang [2002]
Li et al., [2003]
This study
Huang et al.
[2008]
Cai [2004]
Zhou et al.
[2006]
Kool [1993]
Aggimarangsee
[2004]
Stanford [1991]
Oates et al.
[1980]
Kool [1993]
References
c
b
Mean annual temperature; temperature refer to mean annual temperature or range.
The number of consumed species.
The number of woody plant species in the habitat (the DBH standard for woody plant species survey is 41.5 cm in Fusui and Mayanghe, but not sure the particular standard employed in Pangandaran, and
Madhupur).
d
Feeding contribution of the top ten food species.
a
Khao Lommuak,
Thailand
T. pileatus
Madhupur,
Bangladesh
T. francoisi
Longgang,
People’s
Republic of
China
Fusui, People’s
Republic of
China
Fusui, People’s
Republic of
China
Mayanghe,
People’s
Republic of
China
T. leucocephalus Fusui, People’s
Republic of
China
Fusui, People’s
Republic of
China
T. obscurus
Kakachi, Indian
Study sites
T. johnii
Species
Annual Field Sample
rainfall period time Feeding Dietary
(mm) (month) (hr) records breadthb
TABLE VII. Comparison of Forest Type, Seasonality, Sampling Time, Feeding Records, and Dietary Breadth Across Trachypithecus spp. Sites
Foraging of Franc- ois’ Langur at Mayanghe / 1183
Am. J. Primatol.
1184 / Hu
species-specific, toxic compounds [Freeland &
Janzen, 1974; Marsh et al., 2006].
Langur species whose available foods are more
rare have higher dietary diversity than species that
feed heavily on very common species. For example,
T. johnii in Kakachi had a diverse diet of 115 species,
of which the two commonest trees contributed only
5% of the annual diet [Oates et al., 1980]. T. francoisi
at Nonggang fed on 90 species, and the two most
dominant trees contributed about 19% of feeding
records [Zhou et al., 2006]. Similarly, in Kool’s [1993]
study groups, the one feeding heavily on dominant
species had a less diverse diet than the other which
depended very little on dominant plants (21%, 49
species vs. 6%, 88 species). Franc- ois’ langurs at MNR
are an exception to this pattern, as they fed on 14 of
the 15 most common plants but still exploited as
many as 164 species (Table VII).
The much broader diet and exploitation of
common species at MNR may be related to the great
fluctuation of availability of palatable and/or reliable
food resources, or food nutritional components and/
or secondary compounds in that seasonal and
disturbed habitat. Generally, in less seasonal habitats, young leaves form an important part of the diet
of both African and Asian colobines [Stanford, 1991];
thus, langurs in such habitats could concentrate
their diet on favored items from a few food species.
For example, in Fusui (221240 5100 –360 2000 N),
T. francoisi and T. leucocephalus consumed only
37–50 food species and both had extremely folivorous
diets (88–94%) of which the majority was young
leaves and this pattern was maintained all the year
round [Huang et al., 2008; Li et al., 2003]. Moreover,
the availability of food resources may be more
reliable in less seasonal sites: even if the favored
foliage parts are generally scarce in certain sites,
langurs could subsist on other low quality but
reliably available resources. For instance, the capped
langurs exploited only 35 species and fed heavily on
mature leaves (42%) in the moist deciduous forest at
Madhupur where young leaves were generally scarce
[Stanford, 1991].
Compared with all other Trachypithecus study
sites, MNR is more northerly and experiences more
severe climatic fluctuations and lower annual rainfall (Table VII). It may be the case that marked
seasonality leads to great fluctuation in the availability of favored foods, and thus forced the langurs
to switch their diet among seasons and to feed more
on low quality but more reliable food resources
(Table IV). Availability of both young and mature
leaves showed significant monthly changes at MNR
[Hu, 2007]. Although there were significantly positive correlations between the availability and consumption of these two feeding items, significantly
negative correlation existed between mature leaf
eating and young leaf availability [Hu, 2007],
suggesting that mature leaves were the staple food
Am. J. Primatol.
especially in seasons when preferred foods are less
available. In addition, the situation was severely
aggravated by human disturbance, in the form of
cultivation, goat grazing, and firewood collection,
which lead to loss of some important resources,
especially nontree food species such as Callicarpa
bodinieri and Pyracantha fortuneane [Hu, 2007,
2009].
Furthermore, nontree species accounted for
nearly half the annual diet, and for the majority
(68%) in winter (Table V), some food trees are
deciduous (i.e., Ulmus castaneifolia). By contrast,
tree species constituted the majority (80–94%) of the
diet for Franc- ois langurs in less seasonal sites
[Huang et al., 2008; Zhou et al., 2006] and capped
langurs [Stanford, 1991]. At MNR, food parts of some
nontree species were seasonally available, and some
were eaten in winter even if available all year round
(e.g., Conyza canadensis), thus leading to a broader
diet overall for the langurs inhabiting that seasonal
and disturbed habitat.
The positive correlation across food species
between the frequency of consumption and food
availability for two sets of foods indicates that food
choice was influenced strongly by abundance: more
common foods were eaten more often. Even though
the most-consumed foods were selected out of
proportion to their relative abundance, other species
were not.
Generally, Franc- ois’ langurs at MNR had broader monthly diets than their congeners in Fusui and
Nonggang, with exceptions in February and March
(Table VIII). The lower number of food species (21)
in February may be due to the limited feeding
records in that month (449 records), which would be
reflected also in July: 321 records yielded 28 food
species. Langurs at Nonggang consumed more
species in March than did the langurs in MNR (47
vs. 36): this may be because at Nonggang March is
included in the dry season, during which the langurs
exploited more species [Zhou et al., 2006], while the
first half month of March at MNR was still effectively
in winter though I combined it into the spring
category (into which the majority of the months fell)
in my study. On the contrary, langurs at MNR
consumed more species in spring and maintained a
high proportion of young leaves in the diet
(Table IV).
In food-limited habitats, the feeding strategies of
primates may be influenced by nutrients, and
Ganzhorn [1995] documented that the nutritional
quality of some foods can increase with moderate
disturbance. In addition, van Schaik et al. [2005]
reported that more seasonal habitats might provide
food with higher protein levels, which can support
higher population densities of folivores. In MNR,
however, Li et al. [2009, 2010] and Cai et al. [2011]
reported that the protein content of major foods in
that autumn and winter were 4.2% (range 2.7–7.2%)
Huang et al. [2008]
Cai [2004]
Zhou et al. [2006]
This study
1.83
2.25
3.56
3.76
37
36
90
164
15
10
29
47
16
11
25
43
13
13
18
46
Note: Food diversity H’ based on 129 food species obtained in systematic sampling.
5
7
17
54
6
9
10
51
10
10
–
28
8
8
11
51
7
8
16
60
10
10
19
72
11
11
47
36
–
–
34
21
15
16
21
29
Fusui
Fusui
Nonggang
Mayanghe
January February March April May June July August September October November December Breath Diversity (H’) Resources
Site
Annual dietary
Monthly dietary breath
TABLE VIII. Comparison of Monthly Dietary Breath (Number of Species) of Trachypithecus Francoisi Across Sites: Fusui, Nonggang, and Mayanghe
Foraging of Franc- ois’ Langur at Mayanghe / 1185
and 5.4% (2.9–12%) respectively, which is much
lower than in Kakachi and Pangaandaran, 12.6 and
12.2%, respectively [Kool, 1993; Oates et al., 1980].
There was no significant difference in content of
protein and acid detergent fiber (ADF) between
frequently and infrequently consumed species, and
no significant correlation between the feeding
records of food species/items and the corresponding
contents of ADF, protein, and the ratio of protein to
ADF [Cai et al., 2011; Li et al., 2010]. These results
suggest that the food choice of the langurs at MNR is
not influenced by nutritional content, though the
ratio has been found to correlate well with dietary
selection in some other colobines [McKey et al., 1981;
Waterman & Kool, 1994].
Secondary compounds are likely to play a role in
feeding decision at MNR, considering that high levels
of secondary compounds would certainly constitute
an incentive to spread out feeding time across as
many species as possible. Further phytochemical
studies are needed to test this hypothesis.
Available data suggest that it is food availability,
rather than selection of the most desirable foods,
that plays the key role in foraging patterns in this
habitat. The results also indicate that the langurs are
able to survive well in moderately disturbed habitats
by broadening their diet and using more readily
available common species and nontree species. The
restoration of cultivated land in the vicinity (e.g.
planting species with a high S-index value) could
offer a great opportunity for the conservation of this
species.
To sum up, findings from this study have specific
implications for the adaptive significance of dietary
breadth in seasonal and disturbed habitats, and this
could be well useful in planning future conservation
strategies.
ACKNOWLEDGMENTS
I thank Prof. Colin Groves and Prof. Colin
Chapman for their generous assistance in this study.
Special thanks also to Prof. Craig Stanford, Dr. Craig
Kirkpatrick, and Dr. Ruliang Pan who helped
considerably in the preparation of the study. I am
grateful to Prof. Daixing Wang for plant identification. Research in MNR would not have been possible
without the field assistants Bin Wang and Zhijun
Xiao, who regularly followed the target langur
groups ever since preinvestigation in 2003 and
assisted greatly in field data collection. I especially
thank Prof. Colin Groves, Prof. Colin Chapman,
Prof. Marina Cords, and the anonymous reviewers
for their valuable comments on an early draft of this
manuscript.
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