Dietary breadth and resource use of Franois' langur in a seasonal and disturbed habitat.код для вставкиСкачать
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: email@example.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 , 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  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  Li et al.,  This study Huang et al.  Cai  Zhou et al.  Kool  Aggimarangsee  Stanford  Oates et al.  Kool  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  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  documented that the nutritional quality of some foods can increase with moderate disturbance. In addition, van Schaik et al.  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.  reported that the protein content of major foods in that autumn and winter were 4.2% (range 2.7–7.2%) Huang et al.  Cai  Zhou et al.  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. 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