Old World Monkeys

Colobines are leaf-eating specialists with high-cusped molars and multi-chambered stomachs housing mutualistic microbes that digest cellulose and detoxify plant defensive compounds. Leaves are a major component of many species' diets, up to 92% in a population of Ugandan red colobus (Piliocolobus tephrosceles; Snaith and Chapman 2008). The proportion of seeds and fruits in the diet can increase seasonally, however, reaching 87% seeds in the maroon leaf monkey (Presbytis rubicunda; Davies 1991). The winter diet of some mountain-dwelling snub-nosed monkeys is almost exclusively lichen (Kirkpatrick 2010). Colobines are discriminating leaf-eaters, often preferring certain species and younger leaves with fewer structural and chemical defenses. Many African colobines select leaves high in protein and/or low in fiber (Fashing 2010). A growing appreciation of variability and selectivity in colobine diets has led researchers to recognize that these monkeys compete for food more than had been previously thought (Snaith & Chapman 2007).

Home ranges of most colobines are small (<1 km²), reflecting the relative abundance of the leaves they eat. Even those with larger ranges typically travel <1 km/day. The enormous home ranges of Nepal gray langurs (Semnopithecus schistaceus) and snub-nosed monkeys (>10 km²) likely reflect their relatively unproductive montane habitat (Kirkpatrick 2010). Range sizes of many colobines vary seasonally, tracking the proportion of different dietary components.

West African olive and red colobus often associate with Diana monkeys (Cercopithecus diana), a cercopithecine. A likely benefit to both colobus and Diana monkeys is mutual predator detection: red colobus, traveling higher in the canopy, are better positioned to detect shared aerial predators, while Diana monkeys sound the alarm (recognized by colobus) for arboreal and terrestrial predators (Fashing 2010). One of the most dangerous species to both is a fellow primate: at some sites over 90% of chimpanzees' mammalian diet is red colobus, who may suffer major long-term decline as a result (Lwanga et al. 2011).

The more leaves consumed, the more time gut microbes need to process them. Colobine field researchers, therefore, excel at watching their stationary subjects digest. One of the largest colobines, the proboscis monkey, spends up to 75% of daylight hours resting (Figure 3; Matsuda et al. 2009).

Colobine groups are typically moderate-sized (10–20), containing multiple adult females and 1–2 adult males. Multi-male groups of some Asian colobines are best described as traveling assemblages of one-male units. Snub-nosed monkeys are a striking extreme — 20 one-male units can form bands of over 300 individuals (Kirkpatrick 2010). Other multi-male groups may be only temporary, occurring during male take-overs or when a son has matured. The African red colobus is an exception to this pattern, living permanently in larger multi-male groups of 25–50 (Fashing 2010).

Colobines exhibit various patterns of sex-biased dispersal (Fashing 2010, Kirkpatrick 2010). Male-biased dispersal characterizes Asian colobines and African black-and-white colobus, although females may also transfer groups; in some species, dispersing males join all-male groups. In contrast, females are generally the ones to disperse in African red and olive colobus. A notable exception is the endangered Zanzibar red colobus (Piliocolobus kirkii) living at high densities in human gardens, where philopatric females may obtain food more successfully when supported by female kin (Siex 2003).

The prevalence of one-male units in Asian colobines suggests strong male-male competition for resident status. Indeed, interactions between units can be aggressive, and species with the most frequently associating units are the most sexually dimorphic (Grueter and van Schaik 2009). The folivorous diet of colobines rarely leads to aggressive food competition between females, and between-group encounters involve mainly males, who appear to be defending mates. Unlike Asian colobine males, however, male guerezas (Colobus guereza; Figure 4) and ursine colobus (C. vellerosus) appear to defend food resources, perhaps as indirect mate defense. Indeed, female ursine colobus seem to evaluate males based on how well they fight (Teichroeb et al. 2009).

Infanticide, a dramatic expression of male-male competition, has been reported in several colobines but is apparently absent in some populations and species. Killing another male's offspring can be an adaptive reproductive strategy if the infanticidal male is not the father and if females become sexually receptive sooner than they would have otherwise and then mate with the infanticidal male. Strong support for this sexual-selection explanation comes from gray langurs and ursine colobus (C. vellerosus; Fashing 2010). In Thomas's langur (Presbytis thomasi), infanticide by extra-group males may induce females without infants to transfer with the infanticidal males to smaller groups (Wich and Sterck 2010).

Cercopithecine diets are typically more diverse than those of leaf-loving colobines (Cords in press). Baboons and macaques are famous for their dietary flexibility, and in general cercopithecines can be characterized as opportunistic yet selective. As temperate habitats are generally less species-rich than tropical ones, diets in northern latitudes and high elevations are correspondingly less diverse, including primarily leaves and seeds, than those of equatorial and lowland species. Tropical guenons and mangabeys eat the most fruit, whereas geladas eat grass almost exclusively. All cercopithecines have cheek pouches that serve to transport fruits, seeds, and sometimes leaves away from the watchful eyes of predators and competitors alike.

Cercopithecines generally travel farther than colobines, as their foods are more scattered. They also spend less time resting and more time socializing, with grooming a major form of social exchange. Many of the forest-dwelling species form mixed-species groups, which may function in predator defense. These associations are especially common among guenons and mangabeys, less so among sympatric macaques and colobines in the same forest.

Group size and composition are highly variable across and within cercopithecine species (Cords in press). Typical groups include 10–100 individuals, but temporary associations of geladas can surpass 1200 individuals, and mandrill ‘hordes,' which are persistent social units, average 620 members (Swedell 2010).

The groups of many papionins contain multiple males, but some, such as hamadryas baboons (Papio hamadryas), geladas, and, possibly, drills (Mandrillus leucophaeus) and guinea baboons (P. papio), have smaller one-male groups as basal social units. These units are nested into a hierarchical system of bands and troops. Less frequently, single- and multi-male mangabey groups merge into ‘supergroups.' Such sub-grouping may be a way to maintain flexibility in face of changing ecological conditions and to negotiate shared resources such as watering holes and sleeping cliffs. Mandrills show a different type of social flexibility — unique among primates, their massive hordes lack adult males outside of the breeding season (Abernethy et al. 2002).

In contrast to most papionins, almost all guenon groups include just one adult male for most of the year. During breeding seasons, however, resident males may be overwhelmed by an influx of mate-seeking bachelors. Non-resident cercopithecine males are generally solitary; only in geladas, Japanese macaques, and some guenons do there exist all-male groups similar to those of Asian colobines (Cords in press).

Almost all cercopithecine females remain in their natal groups for life; hamadryas baboons are the sole exception. Females form the stable social core, and kin-directed spatial proximity, grooming, and coalitionary support are common (Figure 5; Cords in press). Stable matriline-based hierarchies often develop as a result, but dominance style varies by species. ‘Despotic' species, such as rhesus and Japanese macaques, baboons, and vervets, exhibit strict and steep female dominance relations, with strong kin biases and little reconciliation. In contrast, three Sulawesi macaques (M. nigra, M. tonkeana, M. maurus) exemplify a more symmetrical ‘egalitarian' dominance style (Thierry 2010). Members of the Cercopithecini tribe, however, do not always conform to the traditional cercopithecine pattern: female patas monkeys, though philopatric, only occasionally form stable, matrilineally based hierarchies, and there is only limited evidence in blue monkeys that female rank correlates with any proxy of biological fitness (Foerster et al. 2011). Neither do female blue monkeys form frequent coalitions; they may instead simply minimize contests over food by avoiding each other while feeding.

Relations between male cercopithecines are typically antagonistic. Grooming is rare, though the males of some species form coalitions to improve competitive success. Rather than being kin-biased — males, being the dispersing sex, are not closely related to each other — the decision to participate in coalitions seems to depend instead on reciprocity or mutual advantage in conjunction with differential bargaining positions.

Females typically mate with more than one male, at times seeking extra-group partners, and may engage in sexual activity even when they cannot conceive. Such behavior may confuse paternity, thus forestalling infanticide, which does occur in many cercopithecines. Copulation calls, sexual swellings, and color changes signaling ovulation may incite mate guarding, male-male fighting, and/or sperm competition. Females of many species show preferences for individual males, and not necessarily the highest-ranking ones. In multi-male groups, the degree to which females can exercise mate choice depends on factors such as breeding synchrony, degree of sexual dimorphism, and habitat (i.e., the feasibility of hidden rendezvous). In one-male guenon groups, influxes of extra-group males make it particularly difficult for resident males to monopolize breeding.