Cercopithecines are primates that make up one of the two major groups of Old World monkeys. All Old World monkeys are members of a single primate family, Cercopithecidae, and so are referred to collectively as “cercopithecids.” The family consists of two distinct subfamilies, Colobinae (“colobines”) and Cercopithecinae (“cercopithecines”), which separated about 14 million years ago.
About 73 species of cercopithecines are currently recognized. They range in size from dwarf guenons (females 745-820 g, males 1255-1280 g) to baboons, the largest monkeys (anubis baboon females 14.5-15.0 kg, males 22-28 kg). The cercopithecine group includes several species that are common in zoos, laboratories, and field studies, such as various species of macaques (including rhesus monkeys), baboons, drills and mandrills, guenons, and mangabeys. Currently, cerco-pithecines are the subjects of about two thirds of all non-in vitro research publications on nonhuman primates. The behavior, social relationships, group structure, ecology, and demography of various freeranging cercopithecines have been the focus of many studies. As a result, we have, for the best-studied species, a large and rapidly expanding body of information about the lives of these animals in nature.
Distribution, Habitats, and Diets
Other than macaque monkeys, all species of wild cercopithecines are restricted to Africa, with one exception: a small population of hamadryas baboons along the southern edge of the Arabian Peninsula. Conversely, macaques are represented in Africa only by Barbary macaques, in the Atlas Mountain region, but in Eurasia by a series of about 15 species extending eastward across southern Asia to various islands of the south Pacific and north as far as the islands of Japan. The distributions of individual species of cercopithecines range in size from part of one peninsula of one Pacific island (Heck’s macaque) to large portions of Africa (anubis baboons) and Asia (rhesus).
The habitats of various cercopithecine species differ widely: swamp forest, many other types of forest and open woodland, alpine meadows and bamboo thickets, savannah grassland, even Ethiopian rocky desert, and the Japanese island of Hokkaido, which is covered by snow in winter. A few species are primarily arboreal (for example, dwarf guenons) or terrestrial (patas monkeys, hamadryas, geladas), but most species are both, in varying proportions.
The two subfamilies of Old World monkeys are distinguished by various dental and skeletal features, but of particular ecological and behavioral significance are two distinguishing features of the animals’ soft tissues: cheek pouches, found only in cercopithecines, versus a stomach with at least three enlarged fermentation chambers, found only in colobines. The cheek pouches of cercopithecines are used for short-term storage of relatively small but locally concentrated foods that can be harvested faster than they can be orally processed, thus reducing exposure to competition and predation. Later, at their leisure, the monkeys bring the foods back into the oral cavity for processing before swallowing them. Monkeys of this subfamily are sometimes referred to as “cheek-pouched monkeys.”
Few cercopithecine primates are obligate food specialists. Most species can be characterized as eclectic omnivores, in that their foraging is very selective yet their diet is highly diverse. They feed selectively on a great variety of plant and animal foods that are available in their habitat, eating this part of a plant but not that, feeding on the fruit of one species but not that of a similar, closely related species, feeding on fruit that is fully ripe and ignoring fruit that is semi-ripe, removing acacia seeds from their pods, then the naked seeds from its seed coats, and so on. Baboons represent the extreme development of such highly selective omnivory. Their mastery of this mode of life has enabled them to become the most widespread and abundant primates on the African continent. Selection for traits that lead to such success are still present: among yearling baboons, differences in dietary intake of proteins and energy are accurate predictors of survivorship and lifetime reproductive success.
Most cercopithecine populations are partitioned into discrete, relatively closed and permanent social groups. Among the various groups within a local population, age and sex composition varies. Sizes of cercopithecine groups range from two individuals, in monogamous pairs of DeBrazzas monkeys, to 845 animals (mean 620) in hordes of mandrills. At any given time, group composition results from the population’s history of seven processes: births and deaths, emigrations and immigrations across group boundaries, group fissions and fusions, and maturation. The first four of these processes can, under some conditions, result in populations having equal distributions of males and females among groups, and these sex distributions are consistent with observed distributions in several species of wild primates, including baboons. Such purely demographic models can indicate how the distribution of individuals among groups of a local population can remain largely unchanged over time and why group composition varies nonetheless. But they do not clarify the adaptive significance of species differences in group compositions. At present, the primary determinants of mammalian grouping patterns are considered to be ecological factors, particularly access to essential resources, such as food and mates, and reduction in exposure to hazards, such as predators.
For female cercopithecines, the characteristic numbers in groups of each species are thought to be determined largely by the spatial and temporal distributions of food and predation. For example, the smallest groupings (less than five adult females) are found among arboreal fruit and leaf specialists, such as mona monkeys and greater spot-nosed monkeys, which feed in trees on fruits and shoots; group size may be limited by the numbers of individuals that can feed together in one tree. Conversely, large groups with many females occur in species that may be particularly susceptible to predation, such as terrestrial species that range into treeless areas. In addition, large groups may have other advantages for females, including better conditions for child rearing, buffers against group extinction resulting from stochastic effects, and a larger pool of socially transmitted information.
In turn, the distributions of adult males among groups apparently are determined by the distributions of females: Males go where females are. Cercopithecine species with few females per group (average of six at most) always include just one adult male; species whose groups average more than 10 females never do. Overall, the number of males per group increases linearly with the number of females.
The dynamics underlying the distribution of adult males among the groups of a local population were revealed in a long-term study of group processes in the yellow baboons of Amboseli, Kenya. First, males that were reproductively less successful had shorter tenure in groups than males that were more successful. Second, the availability of cycling females and an individual male’s own mating success were powerful predictors of male dispersal patterns. Males, whether natal or immigrants, were much more likely to emigrate in months when the number of males exceeded the number of cycling females, and they virtually never emigrated when cycling females were in excess. Similarly, the proportion of new immigrants in a group was approximately 4 times greater in months when cycling females were in excess. However, for a variety of reasons, such as the risks of dispersal, these intergroup migrations did not result in a perfect balance between the numbers of males and the numbers of cycling females. In several species of seasonally breeding guenons, males commonly move into groups at the time of year that females are receptive.
Several species of large, terrestrial cercopithecine primates live in small, one-male groups that merge into larger aggregations at various times. Such repeated fission and fusion of groups occurs daily in hamadryas baboons and geladas and has been reported to occur in pigtail macaques, drills, and mandrills. Among nonhuman primates, the hamadryas baboons of Ethiopia are the extreme example of multilevel, fission/ fusion societies. Their basic social and reproductive groups are one-male units, each containing a single adult male, several females, and their offspring. (A few such female groupings, often termed “harems” in the literature, contain a second adult male who mates with the unit females only by stealth.) Two or three one-male units that are strongly associated constitute the next-higher unit, clans, within which each one-male unit remains intact. Social interactions are more common within clans than between. Mature males of a clan often bear a strong physical resemblance to each other and so are thought to be genetically related.
At the next-higher level of social organization, several hamadryas clans and some single males form bands. Band membership and clan membership are stable over many years. Bands are autonomous foraging units, but clans sometimes separate temporarily from their band as they feed on the sparse vegetation of their semidesert habitat. At night, members of a clan sleep on the same sleeping bluff. Several bands may congregate at one bluff, forming large herds (troops) of variable-band composition and sometimes numbering over 200 animals. These various levels of social organization in hamadryas appear to be adaptations to the spatial distribution of essential resources in their rocky desert habitat. Small, dispersed groups most effectively harvest sparse food, and large nightly aggregations provide safety in numbers on their large, dispersed night refuges.
Compared with hamadryas, the fission/fusion groupings of geladas show interesting similarities and differences, but again, probably representing adaptations to an extreme environment. For example, their daily fission/fusion cycle is the opposite of that of hamadryas: One-male, multifemale units of geladas in the Simien Mountains of Ethiopia sleep separately on the abundant cliff ledges during the night, then each morning coalesce into herds of hundreds of animals that feed on the lush alpine meadows.
Maternal Kinships and Social Relations
Selected aspects of cercopithecine kinship and social relationship—topics of particular interest to many anthropologists—are briefly discussed below. The patterns that are discussed here are based primarily on the most extensively studied cercopithecines, namely, yellow baboons, rhesus monkeys, Japanese macaques, and vervets. These primates are among the 25 species (out of 46 cercopithecines for which information on social structure is available) that live and breed in multimale-multifemale groups. Multimale bisexual groups are rare among mammals, and so there has been considerable speculation about why these 25 species—primarily macaques, baboons, and mangabeys—should be different. These multimale-multifemale groups are matrilocal: With rare exceptions, all females remain for their entire lives in the social group in which they were born. However, many males leave their natal group about the time that they reach physical maturity. Thus, each of these groups consists of clusters of matrilines (adult females and their descendants) and several adult males, most of whom have immigrated from other groups.
In these primates, adult females are the stable core of a group, not only because of their lifetime tenure in it but also because among them there is a “linear” (transitive and connected) dominance hierarchy that, with few exceptions, remains stable for many years, often for females’ lifetimes. (Among baboon females, the primary exceptions are old females, some of whom drop in rank relative to their daughters.) Furthermore, each adult female ranks above all females of other matrilines that her mother dominates and above all female descendants of those females, again with few exceptions. In that sense, the female lineages themselves can be rank ordered.
In these species of baboons, vervets, and macaques, young females form strong, lifelong social bonds with their mother and other female relatives, and the resulting coalitions may contribute to stabilizing the dominance hierarchy. By contrast, maternal dominance has no discernable effect on rank acquisition among males, perhaps because in these species, the mother is not dominant over any of the other adult males. A few cases of adult females being dominant to adult males have been reported, but in those groups, the relation of a son’s rank to his mother’s is currently unknown. Males tend to rise quickly in rank as they approach physical maturity, reach their highest rank in the next few years (about 2 years in yellow baboons), and then decline more slowly but steadily with age thereafter.
The pattern of strong matrilineal kinship effects described above has been found in provisioned Japanese and rhesus macaques, wild savannah baboons, and vervet monkeys but does not typify macaques of several other species studied in captivity (bonnet, Barbary, Tonkean,
and stump-tailed macaques), in which females show little or no kin bias in affiliative interactions. Furthermore, in captivity, bonnet macaque females may come to outrank not only their mothers but also females dominant to their mothers. These species differences appear to be related to the extent to which the agonistic behavior of a macaque species can be described as “despotic” (rhesus and Japanese macaques), intermediate (long-tailed macaques), or “egalitarian” (Tonkean, bonnet, Barbary, and stump-tailed macaques), in that in the more despotic forms, kinship profoundly influenced social and dominance relations, whereas at the other extreme, affiliative interactions among nonkin were much more frequent, and little severe aggression was observed in egalitarian species.
In some species or populations of cercopithecines, a curious pattern of dominance relationships has been observed between sisters. Each new daughter of the matriarch takes on, as she approaches maturity, a dominance rank immediately below that of her mother but above that of her older sisters. Thus, sisters typically rank in reverse order of their ages. This pattern of “youngest ascendant” may result from the mother’s agonistic support and defense of her infants against any others that the mother dominates.
Since 1958, when this pattern of “youngest ascendant” among sisters was first described in Japanese macaques by Masao Kawai and Shunzo Kawamura, it has also been observed in groups of wild baboons and vervets and in provisioned rhesus monkeys but, curiously, not in unprovisioned wild Japanese macaques.
Even in species in which the “youngest ascendancy” pattern predominates, exceptions have been observed. Several processes have been suggested as promoting these exceptions, including relative physical strengths of the individual females and availability of potential allies, as determined by demographic variables such as interbirth intervals, infant mortality, and competition for clumped food sources.
The tendency for matrilines within a group to be closely related to each other is augmented by two processes. First, when a group of baboons or macaques fissions into two or more new groups, they sometimes do so along kinship lines: Females of each matriline tend to go into the same new group. Second, in some groups, high-ranking females tend to produce a preponderance of daughters (who remain in the group), whereas low-ranking females tend to produce a preponderance of sons, many of whom will eventually leave their natal group. This rank-related sex bias or simply higher reproductive success among high-ranking females, combined with the tendency of daughters to rank just below their mother, results in a “pushdown” system, in which low-ranking matriarchs do not produce as many female descendants, whereas an increasing proportion of the middle ranks come to be occupied by older daughters of high-ranking matriarchs as the lineages of their mother and their higher-ranking younger sisters continue to grow. In such groups, all females probably are related to one another to some degree.
Kinship relations are one of the most important factors influencing behavior and social relationships in female cercopithecine primates. They affect not only dominance relationships and access to resources but also patterns of affiliative behavior, such as spatial proximity, subgroup clustering, social grooming, alliance formation, conflict intervention, reconciliation, and cofeeding. However, females may also form affiliative relationships with supposedly unrelated females. For such cases in particular, rank proximity (closeness in dominance ranks) has been proposed as an alternative basis for attraction among females. Because rank proximity and kinship relatedness are positively correlated, this hypothesis has been difficult to test until recently, when appropriate statistical methods, based on matrix permutations, have been developed. By means of these methods, rank prox-imity has been shown to affect affiliative behavior independent of the effects of maternal kinship. An alternative and possibly correlated factor is a tendency of females to associate with their paternal siblings, discussed below.
Paternal Kinships and Social Relations
Savannah baboons, vervets, rhesus, and Japanese macaques are all polygynandrous: Males potentially mate with more than one female and females with more than one male, even during a single reproductive cycle. Thus, although the mother of each infant can be identified in the field unambiguously on behavioral grounds, the father cannot, and so until recently, only maternal kinship relationships could be positively identified in field studies. However, development of noninvasive methods for genetic analysis of free-ranging animals using hair or feces has made possible the identification of fathers.
In 1979, Jeanne Altmann pointed out the potential importance of paternal sibships in nonhuman primates. A subsequent series of studies of yellow baboons in Amboseli, Kenya, carried out by Susan Alberts, Altmann, and their colleagues have shown, first, that consortships between siblings involve less sexual but more affiliative behavior than those between nonsibs; second, that adult female paternal sisters are at least as affiliative as maternal sisters; and most recently, that baboon fathers preferentially support their own young, even though an infant’s father may not have been the only male to mate with the mother during the fertile part of the cycle in which she became pregnant. Similarly, rhesus females that are paternal sibs and are close in age maintain stronger affiliations with each other than with nonkin.
Thus, these monkeys appear to have an ability to recognize not only their maternal kin but also their paternal kin, that is, to react differentially to them. Beyond that, several experiments, carried out both on group-living captive animals and in the wild, strongly suggest that cercopithecines can also recognize kinship relationships among other individuals in their group. For example, when the distress call of a juvenile vervet monkey was played back, the mother of the infant looked toward the loud speaker, as expected, but the other adult females looked toward the mother. After a group-living, captive, long-tailed macaque was conditioned to respond when shown photographs of a mother and her offspring, she correctly matched photos from her group of mothers and their infants. In agonistic encounters, captive bonnet macaque males consistently recruited support from males that outranked their opponent. In playback experiments, wild chacma baboons responded more strongly to call sequences mimicking dominance rank reversals between matrilineal families than within. In several species (Japanese and pigtail macaques, vervets), monkeys that have recently been threatened will frequently “redirect” aggression by threatening a third party, often specifically targeting a close matrilineal relative of their recent opponent.
The mechanisms for kin recognition by cercopithecines have not yet been identified, but suspects include social familiarity and spatial proximity during development (ultimately based on the mother-infant bond) and phenotype matching, including distinctive odors controlled by genes of the major histocompatability complex. From the standpoint of Hamiltonian kin selection, the essential issue is the result: kin-biased behavior.
Research on paternal kinship is adding a new and unexpected perspective to kinship effects on primate social systems and will lead to réévaluation of the proximate mechanisms whereby social relationships develop.
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