Seed-eating by red leaf monkeys (Presbytis rubicunda) in dipterocarp forest of northern borneo

Data are presented on the feeding behavior ofPresbytis rubicunda at Sepilok, north Borneo. Emphasis is given to describing the fruit-eating behavior of this small colobine monkey, which specializes in eating seeds from large, dull-colored, and fleshless fruits. The seed predation is conspicuously different from the seed dispersal effected by sympatric monogastric primates and is characteristic of colobine frugivory at other forest sites. Most seed-eating occurred during the period of maximum fruit production and fewer small-seeded, animal-dispersed fruits were eaten at other times.     

A comparison of the floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old World

A comparative floristic survey of lowland tropical rain forest at Kuala Lompat, Krau Game Reserve, West Malaysia and at Sepilok Virgin Jungle Reserve, Sabah, East Malaysia, revealed significant differences in the composition of canopy species, notably in the relative paucity of Dipterocarpaceae and abundance of Leguminosae at Kuala Lompat. A further comparison with data from other sites in Malesia indicated that Kuala Lompat was rather atypical, representing an extreme example of the relatively legume rich and dipterocarp poor forests of West Malaysia. Conversely, the predominance of dipterocarps and lack of legumes at Sepilok was similar to other sites in Borneo. Young and mature leaves were collected from a representative sample of the canopy flora of the two study sites; the levels of nitrogen, fibre, total phenolics and condensed tannins, and degree of digestibility by cellulase and pepsin, were measured. Levels of fibre, nitrogen and phenolics differed significantly between the two floras; foliage from Kuala Lompat being, on the whole, richer in nitrogen but lower in phenolics and fibre. As a consequence of the lower levels of fibre, and less certainly of phenolics, the Kuala Lompat foliage was comparatively more digestible. Possible reasons for the differences in foliar biochemistry between the two sites are discussed. Differences in rainfall and in soil quality are regarded as potential evolutionary causes. A further comparison of the chemical profiles with data for other forests in India and Africa indicate that Sepilok is a site in which trees invest heavily in quantitative defences such as fibre and phenolics whereas trees at Kuala Lompat place a lower emphasis on the production of these. Finally, attention is drawn to the use of foliar chemical profiles in predicting the carrying capacity for colobine monkeys at each of the five Old World forests where data are available. It was found that the ratio of nitrogen to fibre correlated well with the biomass of colobines at the five sites.     

Phylogenetic relationships of leaf monkeys (Presbytis; Colobinae) based on cytochrome b and 12S rRNA genes

Little is known about the classification and phylogenetic relationships of the leaf monkeys (Presbytis). We analyzed mitochondrial DNA sequences of cytochrome b (Cyt b) and 12S rRNA to determine the phylogenetic relationships of the genus Presbytis. Gene fragments of 388 and 371 bp of Cyt b and 12S rRNA, respectively, were sequenced from samples of Presbytis melalophos (subspecies femoralis, siamensis, robinsoni, and chrysomelas), P. rubicunda and P. hosei. The genus Trachypithecus (Cercopithecidae) was used as an outgroup. The Cyt b NJ and MP phylogeny trees showed P. m. chrysomelas to be the most primitive, followed by P. hosei, whereas 12S rRNA tree topology only indicated that these two species have close relationships with the other members of the genus. In our analysis, chrysomelas, previously classified as a subspecies of P. melalophos, was not included in either the P. m. femoralis clade or the P. m. siamensis clade. Whether or not there should be a separation at the species level remains to be clarified. The tree topologies also showed that P. m. siamensis is paraphyletic with P. m. robinsoni, and P. m. femoralis with P. rubicunda, in two different clades. Cyt b and 12S rRNA are good gene candidates for the study of phylogenetic relationships at the species level. However, the systematic relationships of some subspecies in this genus remain unclear.     

Locomotor behavior and muscular anatomy of sympatric Malaysian leaf-monkeys (Presbytis obscura and Presbytis melalophos).

Sympatric Malaysian leaf-monkeys, Presbytis obscura and Presbytis melalophos show quantitative differences in their use of different locomotor patterns during daily activities. P. obscura primarily moves quadrupedally along large boughs; P. melalophos relies more on leaping between smaller supports. P. melalophos also uses forelimb suspension more than does P. obscura. Comparison of the muscular anatomy of the shoulder, arm, trunk, hip and thigh show numerous statistically significant differences between the two species in relative mass of individual muscles and in details of muscular origin and insertion. In almost all instances these differences accord with the types of differences in muscular anatomy predictable from either biomechanical analyses of locomotor behavior or comparative anatomical studies of other mammalian species.     

Group composition,home range,and diet of the maroon leaf monkey (Presbytis rubicunda) at Tanjung Puting Reserve,Central Kalimantan,Indonesia

Maroon leaf monkeys (Presbytis rubicunda) were studied at the Orangutan Research Conservation Project study area at the Tanjung Puting Reserve in Central Indonesian Borneo for approximately 15 months in 1974, 1975, and 1977. Over 250 observation hr involving 300 encounters with the monkeys were logged. Troop size ranged from three to eight individuals in the nine troops surveyed with only one adult male being present in each troop. Home range size varied from 0.33 km² to 0.99 km² and correlated with troop size. Forty-six different food types were observed eaten by the maroon leaf monkeys; of these foods, 52% consisted of fruits, 36% of leaves, and 12% of flowers.     

Craniodental mechanics and diet in Asian colobines: Morphological evidence of mature seed predation and sclerocarpy

Folivory has been accepted as the general dietary pattern for colobines. However, recent ecological studies have revealed that extensive seed eating is found in some colobine species. The ripeness of foraged seeds is also reported to differ between seed eaters. As seeds are generally stress‐limited and may pose greater mechanical demands, seed‐eating species are predicted to exhibit morphological features adaptive for seed predation. In addition, species that feeds on seeds from unripe fruits with hard pericarp is predicted to exhibit increased leverage for anterior dentition. To test these hypotheses, we compared the craniodental morphology of seed‐eating Asian colobines (Presbytis rubicunda and Trachypithecus phayrei) with those of species that rarely exploit seeds (Presbytis comata, Trachypithecus obscurus, and Semnopithecus vetulus). The results show that the seed‐eating colobines possess a masticatory system with enhanced leverage at postcanine bite points. The sclerocarpic forager P. rubicunda also exhibits markedly greater masticatory leverage at anterior dental bite points, while the mature‐seed‐eating T. phayrei shows no such advantage for canine and incisor use. These observations suggest that P. rubicunda is well adapted to husking the resistant pericarps of unripe fruits, using the anterior dentition and to gain access to the immature seeds, whereas such sclerocarpic feeding behavior may be less important for T. phayrei. Our findings indicate that the distinctive craniodental variations of colobines may be linked to mature and/or immature seed eating and suggest the significance of seed predation for the evolution of colobine monkeys. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Predation by the grey leaf monkey (Presbytis hosei) on the contents of a Bird's nest at Mt. Kinabalu Park,Sabah

An adult male grey leaf monkey (Presbytis hosei) was observed in Mt. Kinabalu Park, Sabah, Malaysia, raiding the nest of a grey-throated babbler (Stachyris nigriceps). The monkey removed from the nest and ate at least two eggs and perhaps one young hatchling. This incident appears to be the first reported case of anyPresbytis spp. consuming animal prey.     

Trapping, care, and laboratory management of the silvered leaf monkey (Presbytis cristatus)

The silvered leaf monkey (Presbytis cristatus) from South Kalimantan ( Borneo ), Indonesia is a natural host for a variety of filarial nematodes including Brugia malayi and Wuchereria kalimantani . Experimental studies show that it is host for W. bancrofti, a filarial nematode causing elephantiasis in man. Presbytis cristatus is a gregarious primate of primary and secondary forests, roaming in troops of 20-30 members. Primarily a fruit and leaf eater under natural conditions, this monkey can adapt to a laboratory diet of commercial monkey chow supplemented with fruits and vegetables. Troops, led by an alpha male, immediately respond to protect their young during stressful or dangerous situations. Infants are born singly and are bright orange. Transition to the adult grey and black coloration begins three to five months after birth. Silvered leaf monkeys can be readily trapped. Initially they are aggressive and will attack but become tractable several days after capture. Reaching upward is an important feeding behavior of the silvered leaf monkey and they will not feed from the floor of the cage. In the laboratory they are nonaggressive and lend themselves to various procedures such as blood drawing and examination. Silvered leaf monkeys travel well in commercial animal transport cages. In the United Stages they are not an endangered species and can be readily imported. In Indonesia they are not protected by law and can be exported.     

Studies on the chemoprophylaxis of subperiodic Brugia malayi infection in the leaf monkey (Presbytis melalophos) with diethylcarbamazine citrate

The chemoprophylactic use of diethylcarbamazine citrate at total oral doses of 15--180 mg/kg body weight was tested against subperiodic Brugia malayi infection in the leaf monkey (Presbytis melalophos). A total dose of 45 mg/kg body weight given over 9 days killed all developing infective larvae. Similarly, a total dose of 35 mg/kg body weight given over 7 days killed all fourth stage larvae. The minimum effective dose that prevents infection would be 5 mg/kg body weight daily for 7 days every month.     

Fallback Foods of Red Leaf Monkeys (Presbytis rubicunda) in Danum Valley, Borneo

Animals in Southeast Asia must cope with long periods of fruit scarcity of unpredictable duration between irregular mast fruiting events. Long-term data are necessary to examine the effect of mast fruiting on diet, and particularly on the selection of fallback foods during periods of fruit scarcity. No such data is available for colobine monkeys, which may consume substantial amounts of fruits and seeds when available. We studied the diet of red leaf monkeys (Presbytis rubicunda, Colobinae) in Danum Valley, Sabah, northern Borneo, using 25 mo of behavioral observation, phenology and vegetation surveys, and chemical analysis to compare leaves eaten with nonfood leaves. The monkeys spent 46% of their feeding time on young leaves, 38% on seeds, 12% on whole fruits, 2.0% on flowers, 1.0% on bark, and 1.2% on pith. They spent more time feeding on seeds and whole fruit when fruit availability was high and fed on young leaves of Spatholobus macropterus (liana, Leguminosae) as fallback foods. This species was by far the most important food, constituting 27.9% of the total feeding time, and the feeding time on this species negatively correlated with fruit availability. Consumed leaves contained more protein than nonconsumed leaves, and variation in time spent feeding on different leaves was explained by their abundance. These results suggest that red leaf monkeys show essentially the same response to the supra-annual increase in fruit availability as sympatric monogastric primates, increasing their seed and whole-fruit consumption. However, they depended more on young leaves, in particular Spatholobus macropterus, as fallback foods during fruit-scarce periods than did gibbons or orangutans. Their selection of fallback food appeared to be due to both nutrition and abundance.     

The feeding ecology and activity budget of proboscis monkeys

A group of proboscis monkeys (Nasalis larvatus) consisting of an alpha‐male, six adult females, and several immatures was observed from May 2005–2006. We collected over 1,968 hr of focal data on the adult male and 1,539 hr of focal data on the six females in a forest along the Menanggul River, Sabah, Malaysia. Availability and seasonal changes in plant species consumed by the focal monkeys were determined by vegetation surveys carried out across an area of 2.15 ha along 200–500 m trails in riverine forest. A total of 188 plant species were consumed by the focal monkeys. The activity budget of members of our study group was 76.5% resting, 19.5% feeding, and 3.5% moving. Young leaves (65.9%) and fruits (25.9%) accounted for the majority of feeding time. Over 90% of fruit feeding involved the consumption of unripe fruits and in the majority of case both the fruit flesh and seeds were eaten. Although fruit eating was rare in some months, during other times of the year time fruit feeding exceeded the time devoted to young leaves. We found that monthly fruit availability was positively related to monthly fruit eating and feeding activity, and seasonal fluctuations in dietary diversity were significantly affected by fruit eating. These results suggest that fruit availability and fruit‐eating behaviors are key factors that influence the activity budget of proboscis monkeys. Earlier assumptions that colobine monkeys are obligate folivores do not apply well to proboscis monkeys and certain other colobines. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of Asian colobines. Am. J. Primatol. 71:478–492, 2009. © 2009 Wiley‐Liss, Inc.     

贵州麻阳河地区黑叶猴的食性观察

１９９５￣１９９７年对黑叶猴进行野处食性观察,结果表明：（１）对农作物的取食时间是影响其取食植物种类多少的主要因子;（２）其取食部位季节性明显;（３）各季节取食时间长短与了食农作物时间呈负相关;（４）各季节食物交叉性不强。     

Biosocial functions of grooming behavior among the common Indian langur monkey (Presbytis entellus).

An intensive study of the Indian langur monkey (Presbytis entellus) reveals an interplay between biological and social processes. This study which involved captive animals and over 1,500 observation hours suggests that grooming behavior alone cannot be used to measure status differences between the sexes, nor as a means to understand how pathogens carried by ecto-parasites are controlled. It is shown that the type of grooming exhibited in an interactional setting and the region of the body presented by one animal to another for grooming is often determined by the immediate social events and by the nature of the relationship existing between the participants. For these Colobine langur monkeys grooming behavior not only facilitates integration but it also enables an animal to manipulate a tense situation into a peaceful one. Without reference to many of the other patterns of behavior which only relatively, not absolutely differentiate age and sex classes, grooming behavior cannot be entirely understood.     

Feeding and ranging patterns of forest hanuman langurs (Presbytis entellus)

The feeding and ranging patterns of a troop of hanuman langurs (Presbytis entellus, Colobinae) were studied in Kanha Tiger Reserve, central Indian Highlands for 1850 hr (1981–1982), in a mosaic of moist deciduous forest and anthropogenic meadow. The location, size, and species of each tree within the 74.5-ha troop annual range was known and the phenology of all tree species was sampled. According to scan sampling, the troop spent 25.7% of the daytime feeding, with range use concentrated on an island of dry deciduous forest. Whereas adjacent troops occupied only the periphery of the focal troop's range, all-male bands occupied its center, especially during takeover and infanticidal attacks. The troop consumed items from 60 of the 67 species of trees and woody climbers available; mature leaves (34.9% of feeding time), fruits (24.4%), leaf buds (10.6%), flowers and flower buds (9.5%), young leaves (3.6%), insects (3.0%), and gum (1%). The monthly utilization of fruit, open leaf buds, and flower buds is correlated significantly with their abundance, and the troop spent significantly more time feeding and less time moving when consuming mature leaves. Comparison of tree dispersion and langur ranging patterns suggests that the distribution of the most important food trees is a major influence on their range use.     

Diets of two sympatric colobines in Zaire: More evidence on seed-eating in forests on poor soils

Recent studies have shown that the so- called folivorous African colobines eat a significant amount of seeds. There is disagreement as to whether seed-eating is due to the poor quality of tree foliage, due in turn to poor soils, or to the fact that seeds are a normal part of colobine diets. To test these hypotheses, we studied feeding of red colobus monkeys, Colobus badius tholloni,and black-and-white colobus monkeys, Colobus angolensis angolensis,in a tropical rain forest of Central Zaire (Salonga National Park). We conducted studies on soil properties, vegetation composition, and the availability and chemical contents of food plants simultaneously. Soils were very acid, with a high percentage of sand, very low cation exchange capacity, and very low exchangeable bases. The forest was dominated by legumes (45.6% of trees), among which the Caesalpinioideae were the best represented (85%). C. badiusfed mostly on leaves (61%) and seeds (33%), legumes making up 65% of their diet. C. angolensisfed mostly on seeds (50%) and leaves (27%); 39% of their diet came from legumes. The two species tended to select items richer in crude protein or lipids or both. Total phenolics and condensed tannins were abundant in the foliage and seeds but were poor predictors of colobine choice of food. Intersite comparisons show that colobines in Zaire ate a higher proportion of seeds than all other related species so far studied in Africa and that the Salonga forest had among the poorest soils and harbored the highest percentage of Caesalpinioideae. Our results confirm that seed- eating is more common among colobines living in areas where soils are poor. They strongly suggest that this link is mediated through forest composition, especially the abundance of legumes, and that the development of seed- eating results both from the high availability of nutrient-rich seeds and from the poor quality of mature tree foliage.     

Patterns of reproduction and mortality in two captive colonies of hanuman langur monkeys (Presbytis entellus)

Longitudinal reproductive and mortality data collected from two colonies of Hanuman langur monkeys (Presbytis entellus) in California (University of California, Berkeley; San Diego Zoo) are presented. Approximately 10 years of data from each facility reveal that langur monkey females reach reproductive maturity between 3 and 5 years and have median birth intervals, following the birth of a live infant that survives beyond 9 months, of approximately 15.5 months. Births are not seasonal at either facility and pregnancy failure rates at UCB are approximately 30%. Mortality of subadults was highest during the neonatal period (<30 days), and probability of Sarvivorship at 5 years is between .41 and .50. Observed differences and similarities in patterns of reproduction and mortality between the two colonies and field populations are discussed.     

Taxonomy and distribution ofPresbytis melalophos group in Sumatera,Indonesia

Taxonomy of thePresbytis melalophos group in Sumatera has been based solely on the distinction in the pelage coloration and has been a subject of controversy. In the present study, extensive field observations were undertaken. Three species, i. e.P. melalophos, P. thomasi, andP. femoralis, are recognized in Sumatera based on the cranial morphology, pelage coloration, and vocalization. Subspecies of each species are revised, a new classification is proposed, and a new subspecies,Presbytis melalophos bicolor, is described. A detailed distribution map of species and subspecies is presented. No sympatry occurs between the species. Finally, a cladistic analysis is presented for the three species, based on the cranial characters; the branching sequence is first between theP. melalophos clade and theP. femoralis- P. thomasi clade and second between theP. femoralis clade and theP. thomasi clade.     

Wuchereria bancrofti: effect of single and multiple larval inoculations on infection dynamics and development of clinical manifestations in non-human primate Presbytis entellus

We earlier reported the successful experimental transmission of Wuchereria bancrofti from humans to the Indian leaf monkey (Presbytis entellus) [Misra, S., Tyagi, K., Chatterjee, R.K., 1997. Experimental transmission of nocturnally periodic Wuchereria bancrofti to Indian leaf monkey (Presbytis entellus). Experimental Parasitology 86,155-157.; Dube, A., Murthy, P.K., Puri, S.K., Misra-Bhattacharya, S., 2004. Presbytis entellus: a primate model for parasitic disease research. Trends in Parasitology 20(8), 358-360.] using a small number of animals. The present study, involving 27 langur monkeys, found the development of pathological manifestations ranging from filarial fever, lymphangitis, lymphadenitis, hydrocoele, and limb edema to minor histopathological changes in tissues after single, double, triple, or multiple inoculations of infective larvae of W. bancrofti recovered from Culex quinquefasciatus fed on human microfilaraemic blood. Thirty-eight percent of the infected langurs developed detectable microfilaraemia in their blood. Single or double larval exposure resulted in better worm establishment than multiple exposures with small numbers of larvae. All of the langurs receiving a single large inoculum and 85.71% of those receiving two inoculations harbored adult parasites. Worm establishment decreased with increasing number of larval inoculations. In all, 60% of infected langurs developed classical gross-pathological symptoms of lymphatic filariasis. Of these, 29.16% developed thickening of the lymphatics, 25% suffered from periodic rise in rectal temperature, and 16.66% developed scrotal swelling with presence of microfilariae in the hydrocoele fluid. Only one out of 25 langurs (4%) developed acute limb edema. It appeared that a single inoculum of a large number of infective larvae was able to induce maximum pathology. Fifty-six percent of the infected langurs acquired a peculiar sitting posture, retracting both the hind limbs, usually after 4-5 months of larval inoculation and eventually resulting in reduced mobility. Oral administration of diethylcarbamazine (citrate) at 12mg/kg for 12 consecutive days to one langur caused 80% suppression in microfilaraemia on day 8, killing all the adult parasites. Of the two immunosuppressed (cortisone- or prednisolone-treated) male rhesus monkeys included in the study, neither developed any of the above lymphatic symptoms or parasites after receiving larval inoculations on two or three occasions; however, a rise in rectal temperature in one of the animals was noticed. The present study thus reveals that the Indian leaf monkey, P. entellus, may serve as an ideal non-human primate model of human bancroftian filariasis for carrying out longitudinal studies on pathology, host-parasite interactions, and preclinical evaluation of candidate anti-filarial drugs or vaccines.     

Western Purple-faced Langurs (Semnopithecus vetulus nestor) Feed on Ripe and Ripening Fruits in Human-modified Environments in Sri Lanka

Although most colobines feed mainly on leaves and a few feed heavily on seeds, colobine digestive adaptations for folivory are thought to preclude the high use of ripe fleshy fruits. In this long-term study of Semnopithecus vetulus nestor, the endemic western purple-faced langur of Sri Lanka, I investigated the feeding ecology and dietary flexibility for fruit feeding in 2 free-ranging groups (PT1 and R1) living in human-modified environments with abundant cultivated fruit, at Panadura and Piliyandala, for 19 mo and 13 mo respectively, using scan-sampling, vegetation enumeration, and phenological studies. In contrast to folivorous forest-living colobines, including other subspecies of Semnopithecus vetulus, my focal groups used more fruit (>50%) than foliage (PT1: 36%; R1: 34%). Both groups used many plant species (PT1 115; R1 59), but selected their food species, fruits over leaves, and young leaves over mature leaves. Fruit use was independent of young leaf availability. Notably, 78.4% and 83.4% of fruits consumed by PT1 and R1 were fleshy and human-edible, most of which were ripening or ripe (PT1: 72.4%; R1: 94.8%). The main fruit for both groups was Artocarpus heterophyllus (Moraceae; jakfruit), a cultivar with fleshy fruit. These findings differ from previous understanding of colobine diets. I suggest that environmental factors, such as the abundance and nature of available fruits, and the absence of arboreal-primate fruit competitors, could influence the use of ripe fleshy fruits by colobines strongly, highlighting the need to review the dietary and digestive flexibility of this group in changed and changing natural environments to formulate effective conservation action.     

Food selection by the South Indian leaf-monkey,Presbytis johnii,in relation to leaf chemistry

Summary The leaf-monkey Presbytis johnii has been found to exhibit considerable selectivity in its dietary utilization of mature foliage in a rain-forest habitat. To investigate the basis of this selectivity and to examine the hypothesis that the observed selection is related to the digestibility and toxicity of the available foliage, chemical analyses have been made on 16 of the most important tree species in the monkey's habitat. It has been found that the most heavily used items, which form a staple part of the diet of P. johnii, are characterized by a low fibre content and a very low condensed tannin content. However, neither class of compound is an absolute feeding deterrent as minor, but still significant, mature leaf food items contain considerable amounts of both. It is suggested that the feeding deterrents in these minor items, which may be ingested to supply specific dietary requirements, can perhaps be tolerated because of their dilution in the gut by the dietary staples. An examination of the pepsin/cellulase digestibility of available mature foliage showed that the staple food items tended to be highly digestible. Little correlation has been found between alkaloid content and food selection and it is suggested that the colobine forestomach microflora has the ability to detoxify at least some alkaloids. Additional data on mature leaf petioles and young leaves suggest that the high ratio of cell-sap to cell-wall in these items, and their related high digestibility, explain the high relative abundance of these items in the P. johnii diet.