(Colobinae)
Class: Mammalia
Order: Primates
Family: Cercopithecidae
Subfamily: Colobinae
Thumbnail description
Medium-sized, essentially arboreal mammals with forward-facing, quite large eyes, relatively large brains and a quadrupedal pattern of locomotion involving grasping hands and feet
Size
Average body weights range from 9 lb 13 oz (4.45 kg) to 33 lb 5 oz (15.1 kg)
Number of genera, species
10 genera; 59 species
Habitat
Essentially forest-living, but occur in a range of forest types extending from relatively open dry forest to dense evergreen tropical rainforest
Conservation status
Critically Endangered: 4 species; Endangered: 14 species; Vulnerable: 7 species; Near Threatened: 6 species; Data Deficient: 5 species
Distribution
Asia and Southeast Asia, and Africa south of the Sahara
Evolution and systematics
Higher primates (suborder Anthropoidea) include the broad-nosed monkeys of the New World (infraorder Platyrrhini) and the narrow-nosed monkeys and apes of the Old World (infraorder Catarrhini). Old World monkeys and apes, which are widely distributed in Africa, Asia, and Southeast Asia, are uniformly characterized by a dental formula of I2/2 C1/1 P2/2 M3/3. They hence differ from all New World monkeys by reduction in the number of premolars from 3 to 2 in each tooth row. All Old World monkeys and apes have trichromatic color vision comparable to that of humans. Old World monkeys (superfamily Cercopithecoidea) differ from apes (superfamily Hominoidea) in possessing in both upper and lower jaws four-cusped molars with their cusps linked in pairs to form transverse cutting ridges (bilophodonty). Moreover, all Old World monkeys possess prominent hardened sitting pads (ischial callosities) on the buttocks, which are supported by broad, roughened bony flanges (ischial tuberosities) on the pelvis. Apart from gibbons, such a development is lacking in apes. Old World monkeys (family Cercopithecidae) are divided into two main groups, leaf-monkeys (subfamily Colobinae) and cheek-pouched monkeys (subfamily Cercopithecinae). Defining features of these two subfamilies reflect feeding habits. Whereas all cercopithecine monkeys are characterized by possession of cheek pouches for temporary storage of food, all leaf-monkeys have a complex stomach. The complex stomach, which is unique among primates, is subdivided into 4 distinct compartments (cardiac pouch, gastric sac, gastric tube and pyloric chamber). The complex stomach represents an adaptation for housing symbiotic bacteria to permit digestion of plant cell walls in a typically leaf-rich diet. Available evidence indicates that colobine monkeys have somewhat lower basal metabolic rates than cercopithecine monkeys, and this may be connected with their leaf-eating specialization. Leaf-monkeys also differ consistently and obviously from cheek-pouched monkeys in skull morphology: the distance between the eye sockets (interorbital distance) is large in colobines and small in cercopithecines.
Although there seems to be a fairly clear distinction between leaf-monkeys living in Asia and Southeast Asia and those living in sub-Saharan Africa, this is not recognized in any formal subdivision (e.g., as tribes) in current classifications.
Numerous Old World monkeys show some form of sexual dimorphism, in which males and females differ in features not directly related to reproduction. Males and females of a species can differ markedly in general appearance, in overall body size and/or in the size of the canine teeth, although these features can vary somewhat independently. As a general rule, sexual dimorphism is less pronounced in leaf-monkeys than in cheek-pouched monkeys. Nevertheless, there are some quite striking examples of dimorphism in leaf-monkeys as well. The most outstanding example of sexual dimorphism in all three aspects is provided by the proboscis monkey (Nasalis larvatus), in which males weigh more than twice as much as females, have significantly bigger canine teeth and exhibit more extreme development of the prominent nose that characterizes this species.
Although morphological evidence is equivocal, chromosomal and molecular evidence indicates that the African and Asian groups of leaf-monkeys are both monophyletic, each being derived from a separate common ancestor after the leaf-monkeys diverged from the cheek-pouched monkeys. The African leaf-monkeys, which can be referred to collectively as colobus monkeys, include 15 species belonging to 3 genera (Colobus, Piliocolobus, and Procolobus). All of these monkeys were originally included in the single genus Colobus, but it is now recognized that their diversity merits separation at the generic level. Nevertheless, the Asian leaf-monkeys are undoubtedly more diverse both numerically and morphologically, and the 44 species are allocated to 7 different genera. Some of the Asian leaf-monkeys are generally labeled langurs and can be allocated to 3 genera (Presbytis, Semnopithecus, and Trachypithecus). The remaining Asian leaf-monkeys all show some kind of special modification of the nose and can be collectively labeled "odd-nosed leaf-monkeys." They can be allocated to four different genera: Nasalis, Pygathrix, Rhinopithecus and Simias.
The early fossil history of the Old World monkeys is poorly known. Early Miocene deposits of Africa, dated at about 20 million years ago (mya), have yielded Prohylobates and Victoriapithecus, both possessing bilophodont molar teeth. These early fossil forms were originally known exclusively from isolated teeth and jaw fragments. This is still the case for Prohylobates, but a fairly complete skull and parts of the postcranial skeleton are known for Victoriapithecus. As a result, it is known that this genus was characterized by possession of ischial tuberosities on the pelvis and by a short interorbital distance. It is unclear whether Victoriapithecus is specifically related to modern cheek-pouched monkeys, as might be suggested by the small interorbital distance, but there is certainly no trace as yet of an early relative of leaf-monkeys. It is not until the late Miocene and the Pliocene (less than 10 mya) that Old World monkeys become relatively well documented in the fossil record. By that stage, it is certainly possible to distinguish between colobines (relatives of leaf-monkeys) and cercopithecines (relatives of cheek-pouched monkeys). Skulls of colobine monkeys are comparatively common in Pliocene and Pleistocene deposits of northern and sub-Saharan Africa (e.g., Libypithecus, Paracolobus, and Cercopithecoides). In southern Europe the late Miocene leaf monkey Mesopithecus is documented by several skulls and almost all elements of the skeleton, and the Pliocene genus Dolichopithecus is also well documented. Furthermore, partial jaws and isolated teeth from late Miocene deposits in Pakistan have been allocated to the modern genus Presbytis as the species Presbytis sivalensis.
Physical characteristics
In the head, the eyes are always directed directly forwards and the snout is typically relatively short. As is the rule for higher primates, a rhinarium (a naked, moist area of skin around the nostrils that is present in most mammals) is always completely absent. The nostrils are relatively close-set and typically downward-pointing (with the notable exception of the Mentawai Islands snub-nosed leaf-monkey Simias concolor), and in some species the nose is prominently developed. Cheek pouches are never present. As in all other Old World monkeys and apes, the dental formula is I2/2 C1/1 P2/2 M3/3. The canine teeth are typically large, stabbing teeth (although generally less prominent than in cheek-pouched monkeys), and the rear edges of the upper canines are honed against the leading edges of the anterior premolars in the lower jaw. In both upper and lower jaws, all molar teeth are bilophodont. Colobine monkeys typically walk and run quadrupedally in the trees and, in some cases, on the ground. In the trees, they are typically agile climbers. In contrast to cheek-pouched monkeys, the legs are typically somewhat longer than the arms. In the hand, the thumb is generally reduced, and in the colobus monkeys it is virtually vestigial. Fine manipulative actions of the hand are thus largely precluded. Well-developed hardened sitting pads (ischial callosities) are present on the buttocks, and these are supported by broad, roughened bony flanges (ischial tuberosities) on the pelvis. Reflecting the predominance of arboreal habits, the tail is usually relatively long, although it is reduced to a short appendage in some species, for example in the snub-nosed leaf-monkey.
In many species, coloration of the body fur is relatively inconspicuous or even cryptic, generally being darker dorsally and paler ventrally. In several species, infants have a distinctive coloration. The face is usually virtually naked, although there is occasionally tufts of hair on the cheeks and/or chin. Body size ranges from the olive colobus (Procolobus verus), with a head and body length a 19.0 in (48.0 cm) for males and 18.5 in (46.5 cm) for females, and a tail length of 22.5 in (56.0 cm) for males and 23 in (57.5 cm) for females, to the proboscis monkey (Nasalis larvatus), with a head and body length of 30 in (74.5 cm) for males and 25 in (62.0 cm) for females, and a tail length of 26.5 in (66.5 cm) for males and 23 in (57.5 cm) for females. Body mass ranges from 10 lb 6 oz (4.7 kg) for males and 9 lb 4 oz (4.2 kg) for females in the olive colobus (Procolobus verus) to 45 lb (20.4 kg) for males and 21 lb 10 oz (9.8 kg) for females in the proboscis monkey (Nasalis larvatus).
Distribution
In contrast to cheek-pouched monkeys of the subfamily Cercopithecinae, the leaf-monkeys predominantly occur in Southeast Asia, where they are very widely distributed. The only colobine monkeys to occur in Africa are the colobus monkeys (genera Colobus, Piliocolobus, and Procolobus), although they are quite widely distributed south of the Sahara. The remaining seven genera (Nasalis, Presbytis, Pygathrix, Rhinopithecus, Semnopithecus, Simias, and Trachypithecus) are restricted to Asia and Southeast Asia.
Habitat
Leaf-monkeys are essentially forest-living, but they occur in a wide range of forest types, including relatively open dry forest, bamboo jungle, gallery forest, swamp forest, mangrove forest, and dense evergreen tropical rainforest.
Behavior
All members of the subfamily Colobinae are diurnal and most species are arboreal in habits. In all cases, locomotion is typically quadrupedal, although suspensory behavior is also quite common during arboreal feeding. Gregarious social groups that move around and feed as relatively cohesive units are formed by all species, but these vary from multi-male troops through one-male troops to a few rare cases of monogamy. In some species that exhibit one-male groups, surplus males form bachelor male groups. Moreover, there are certain species in which individual groups temporarily combine to form larger bands. In most species, females tend to stay in their natal groups, whereas males migrate at round the time of sexual maturity. However, there are exceptions. For example, in guerezas (genus Colobus), males migrate between groups, whereas in red colobus (genus Piliocolobus) it is the females that migrate.
Feeding ecology and diet
As is indicated by their name, leaf-monkeys feed predominantly on relatively low-energy leaves and other plant parts, although many species show a preference for relatively nutritious young leaves. The bilophodont teeth that characterize all Old World monkeys probably represent an adaptation for mastication of resistant material such as leaves, so it seems likely that the common Old World ancestor of both cheek-pouched monkeys (subfamily Cercopithecinae) and leaf-monkeys (subfamily Colobinae) was at least to some extent folivorous. However, uniquely among primates, colobine monkeys also possess a complex, four-chambered stomach that permits them to digest plant cell wall material with the aid of symbiotic bacteria. Despite this fundamental adaptation for digestion of resistant plant parts, there is considerable variation in diet among colobine monkeys, and some of them have become specialized for feeding on seeds rather than leaves (e.g., Colobus satanas).
Reproductive biology
Generally polygynous. Single births are typical, although twins are born very occasionally, and two teats (mammae) are consistently present in the chest region. All species have a menstrual cycle lasting approximately a month and marked by externally visible menstrual bleeding. In contrast to cheek-pouched monkeys, females generally lack a conspicous sex skin in the genital region that changes in coloration and size over the course of the ovarian cycle. The only exceptions are the olive colobus monkey (Procolobus verus), in which females have a moderately developed sex swelling, and some species of red colobus (Procolobus preussi), in which the sex swelling is enormous. Subadult red and olive colobus males also have a "perineal organ," which mimics the female's sexual swelling. Placentation is of a highly invasive hemochorial type. The gestation period is even longer than in cheek-pouched monkeys, varying between 195 days and 212 days for few species for which data are available.
Conservation status
Four species are Critically Endangered (Piliocolobus rufomitratus, Rhinopithecus avunculus, Trachypithecus delacouri, and Trachypithecus poliocephalus), 14 are Endangered (Nasalis larvatus, Presbytis comata, Piliocolobus badius, Piliocolobus kirkii, Piliocolobus pennantii, Pygathrix nemaeus, Pygathrix nigripes, Rhinopithecus bieti, Rhinopithecus brelichi, Simias concolor, Trachypithecus auratus, Trachypithecus geei, Trachypithecus pileatus, and Trachypithecus vetulus), seven are Vulnerable (Colobus satanas, Colobus vellerosus, Presbytis potenziani, Piliocolobus gordonorum, Rhinopithecus roxellana, Trachypithecus francoisi, and Trachypithecus johnii), and six are Near Threatened (Colobus polykomos, Presbytis femoralis, Presbytis melalophos, Presbytis thomasi, Procolobus verus and Semnopithecus entellus). Five species are listed as Data Deficient (Presbytis fredericae, Presbytis frontata, Presbytis hosei, Trachypithecus laotum, and Trachypithecus villosus).
Significance to humans
Leaf-monkeys are commonly hunted for food (bushmeat) in Asia, Southeast Asia, and Africa, although they are sometimes protected by local taboos in parts of Southeast Asia, as is the case with the northern plains gray langur (Semnopithecus entellus) in India. Despite the fact that they are just as closely related to humans as the cheek-pouched monkeys (subfamily Cercopithecinae), monkeys in the subfamily Colobinae have rarely been used in biomedical research because they are relatively difficult to maintain in captivity.
Species accounts
Mantled guerezaWestern red colobus
Olive colobus
Banded leaf-monkey
Northern plains gray langur
Silvery leaf-monkey
Proboscis monkey
Red-shanked douc langur
Golden snub-nosed monkey
Mentawai Island langur
Resources
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[Article by: Robert D. Martin, PhD]
