Primates

Primates

DIETARY HABITS

SOCIAL SYSTEMS AND BEHAVIOR

BIBLIOGRAPHY

No simple set of diagnostic characteristics defines “primates.” Rather, members of the order Primates share, to varying degrees, several suites of features that reflect a generally arboreal lifestyle. These attributes include:

1. Pentadactyl, prehensile hands and/or feet with nails (rather than claws) on the digits, of which the thumb and/or big toe are opposable.
2. Pronounced sensory emphasis on vision, notably through development of binocular and stereoscopic vision, as well as expansion of the visual cortex.
3. A generalized postcranial anatomy tending toward orthrograde (upright) posture.
4. A trend toward enlargement of the cerebral cortex, especially in monkeys and apes.

Primate taxonomy is debated, but 200 to 350 species are recognized. The majority are distributed in tropical and subtropical regions (roughly between the Tropics of Cancer and Capricorn) and throughout sub-Saharan Africa, south and southeast Asia, and South and Central America, although a few forms, such as the Japanese macaque, inhabit decidedly temperate habitats. Primates are chiefly rain forest and tropical forest dwellers, although many other biomes are ecologically relevant for certain groups, including savanna, woodland scrub, evergreen temperate forest, desert, and high-altitude eflinwood meadow.

Six major groups of primates are usefully distinguished:

1. Lemuriformes: the small nocturnal and larger diurnal lemurs of Madagascar.
2. Lorisiformes: the nocturnal, small-bodied lorises and bushbabies of Africa, south Asia, and island southeast Asia.
3. Tarsiiformes: the small, nocturnal tarsiers of Sumatra, Borneo, Sulawesi, and the Philippines.
4. Playtrrhini: the small- to large-bodied monkeys of Central and South America.
5. Cercopithecoidea: the medium- to large-bodied monkeys of Africa and Asia.
6. Hominoidea: the large apes of Africa and Asia, as well as humans.

The Lemuriformes and Lorisiformes form a coherent suborder, the Strepsirhini, unified by various traits, notably retention of the “rhinarium” (the naked, “wet” mammalian nose), increased reliance on olfaction, and greater seasonality of sexual behavior (“estrus”). Many strepsirhines are nocturnal. The second suborder, the Haplorhini, comprises the primates of the remaining three taxa, which exhibit predominantly diurnal habits (with the exception of tarsiers and one monkey species), enhanced vision and visual communication, and comparatively more continuous (less seasonal) sexual activity and reproduction.

DIETARY HABITS

Diversity and omnivory generally typify primate feeding strategies, rather than marked dietary specialization such as the bovid emphasis on grass. The three principal primate foods are fruits, leaves, and insects, but their relative dietary proportions vary considerably across species. Frugivory is most widely distributed: Most primates eat some fruit, and species strongly committed to frugivory are found in virtually every family. Figs (Moraceae, Ficus species) are an often a crucial keystone fruit source for forest primates. Because of metabolic implications of body size, folivory is more common among larger primates (greater than or equal to 13.5 pounds), such as the Old World “leaf monkeys” (Colobinae), neotropical woolly spider monkeys, and mountain gorillas. Conversely, insects are generally consumed in higher proportions by small primates (less than or equal to 3.5 pounds), such as the nocturnal strepsirhines, tarsiers, and neotropical marmosets, tamarins, and squirrel monkeys. Thus, with increasing body size, primate diets typically grade from insectivory, to insectivory-frugivory, frugivory, frugivoryfolivory, and finally to folivory.

Some less common foods are nevertheless important for certain primates or in specific seasons. For example, marmosets, tamarins, and some strepsirhines rely heavily on exudates (gum), particularly seasonally. Underground storage organs (e.g., rhizomes, tubers, corms) are paramount in baboon foraging. These parts are modified stems or leaves in which the plant stores starch, minerals, and water (the potato being a well-known example utilized by humans). Nectar (for some lemurs and neotropical monkeys), grass (for gelada baboons), and seeds (for saki monkeys) are other examples. Carnivory (predation) occurs at significant rates only among baboons (Papio species), neotropical capuchin monkeys (Cebus species), and most notably chimpanzees (Pan troglodytes ), the latter of which prey heavily upon red colobus monkeys. In contrast to the more individualistic and “opportunistic” prey capture of Papio and Cebus, chimpanzee “hunting” is performed simultaneously by multiple adult males. Researchers debate, however, whether male chimpanzees act independently of one another or coordinate their actions cooperatively through an organized division of labor (different hunting “roles”) and the use of foresight and mental attribution.

The omnivorous, “generalist” feeding inclination of primates has not precluded some adaptive specializations in dentition, physiology, and behavior. One noteworthy example is the gastrointestinal tract of Colobine monkeys: In a manner directly analogous to ruminants, it contains a large, multichambered stomach with variable chemical environments facilitating fermentation by symbiotic, cellulolytic bacteria. Thus, these monkeys are able to metabolize and subsist on otherwise difficult-to-digest, mature foliage.

SOCIAL SYSTEMS AND BEHAVIOR

Perhaps the most striking features of primate biology are the diversity and complexity of social systems. Many nocturnal strepsirhines—as well as the orangutan—live in “dispersed” societies in which adult males and females inhabit individually separate home ranges wherein daily activities are independently pursued. These home ranges may partly overlap and, in some species, differ in size between the sexes. Thus, a single polygynous male may occupy and defend from other males (territoriality) a large home range encompassing several females’ individual ranges. The original characterization of this arrangement as a “solitary” or “asocial” existence was understandable but inaccurate. Not only do “solitary” individuals interact at meaningful rates through indirect olfactory and vocal modalities, they may even aggregate regularly, for example, during feeding in orangutans, or at sleeping sites in some nocturnal strepsirhines. Recent mitochondrial DNA evidence from nocturnal lemurs reveals that such sleeping aggregations comprise related females, thereby suggesting a “hidden” matrilineal dimension of as yet unclear significance in these dispersed social systems.

In contrast, the diurnal lemurs and all monkeys are highly gregarious, living in permanent social groups. With few exceptions, primate societies are generally closed (interaction—particularly affiliatively—between individuals of separate groups is rare) and age-graded (immatures of multiple ages/generations are present). The size and composition of groups vary greatly, as do the nature and patterning of constituent social relationships. This variation is expressed not only between species but also often across populations of the same species.

As with mammals generally, female primates often remain in their natal area and social unit for most if not all of their lives, whereas males disperse to other groups around the age of sexual maturity. The resulting female-bonded societies are thus based on “core” affiliative networks of related females—matrilines—to which males associate in variable numbers and time periods.

For example, in some species (leaf monkeys and guenons) only one adult male lives in a group of several (typically three to ten) adult females and their offspring. Group membership is likely to confer polygynous reproductive advantages to males, although in at least some species, females copulate with other males in the population, which either live alone or in all-male “bachelor” units.

A “multimale” variant of this social system generally emerges with relatively larger female group sizes (e.g., ten to fifty). In such cases, three to fifteen adult (nonnatal) males typically reside with the females and their offspring. This social structure predominates in many of the Old World monkeys—notably the baboons and macaques—in addition to neotropical forms such as capuchin and squirrel monkeys. Relationships among females are highly differentiated, most often manifested as relatively rigid, linear dominance hierarchies organized around kinship (matrilineal relatedness). Several field and laboratory studies suggest a substantive cognitive dimension to nonhuman primate understanding of both “status” and “matrilineal kinship.” Females invest heavily in activities that maintain their status, such as grooming and coalitionary support. Males similarly maintain dominance relationships that are, however, much more dynamic and unrelated to kinship.

In 10 to 15 percent of species—most notably the gibbons (Hylobatidae) and species of small neotropical monkeys—the group comprises one adult of each sex accompanied by several immature individuals of various ages. This social system was originally designated “monogamy” or the “nuclear family,” but the term “social monogamy” is now preferred, particularly in light of avian research. Individuals in over 90 percent of bird species live and breed in heterosexual pairs, but genetic data have revealed that in many species extra-pair paternity may be significantly high (e.g., 40 to 50%). Although not all extra-pair sexual behavior results in fertilization, it is clear that one can no longer assume that sexual or reproductive monogamy results invariably from the monogamous social arrangement of birds. Correspondingly, “extra-pair” copulations, pair-bond termination (“divorce”), and “non-nuclear” families do occur among socially monogamous primates, but the generality and significance of these phenomena remains less clear than is the case for birds.

A polyandrous mating system is found in some marmosets and tamarins that live in groups comprising one adult female, two adult males, and youngsters of various ages. Males, as well as young adult offspring of either sex, are primarily responsible for care of the breeding female’s (fraternal) twin offspring. The reproduction of adult daughter “caretakers” may, in fact, be behaviorally or physiologically suppressed by the dominant female.

Great ape societies are characterized by comparatively attenuated female relationships. As noted, female orangutans pursue largely separate lives. Although gorillas live in unimale, multifemale groups, dispersal of females (as well as males) at sexual maturity constrains the formation of matrilineal relationships; female gorillas instead direct more social attention to the resident male. Individual female chimpanzees occupy separate home ranges, interact infrequently, and have weak dominance relationships. Females disperse at sexual maturity, whereas males remain in their natal community. Thus, the kinship element of chimpanzee society is patrilineal in nature, based on relationships among related males that collectively maintain a territory encompassing the individual home ranges of numerous “solitary” females. These males and females may join and leave temporary foraging parties that vary greatly in size and composition, dynamically undergoing “fusion” and “fission” with other foraging parties and individuals of the community over days, if not hours. Cooperation in competition is a hallmark of male social life. Hunting is one such context, as is vying for dominance and the sometimes violent territorial aggression directed against neighboring communities of related males. Although the patrilineal structure and “fusion-fission” system of social foraging also characterizes bonobos (as well as neotropical spider monkeys), bonobos are noteworthy for the much more amicable nature of their social relationships and apparent female dominance over males.

Negotiating complex relationships involving status, kinship, and affiliation over their relatively long lives is believed to have been an important impetus in the evolution of social cognition in monkeys and, especially, apes.

SEE ALSO Alpha-male; Anthropology; Anthropology, Biological; Kinship; Kinship Selection; Social Status

BIBLIOGRAPHY

Bergman, T. J., J. C. Beehner, D. L. Cheney, and R. M. Seyfarth. 2003. Hierarchical Classification by Rank and Kinship in Baboons. Science 302: 1234–1236.

Cheney, D. L., and R. M. Seyfarth. 1990. How Monkeys See the World: Inside the Mind of Another Species. Chicago: University of Chicago Press.

Dixson, Alan F. 1998. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings. Oxford: Oxford University Press.

Fleagle, John G. 1999. Primate Adaptation and Evolution. 2nd ed. San Diego, CA: Academic Press.

Kappeler, Peter M., and Michael E. Pereira, eds. 2003. Primate Life Histories and Socioecology. Chicago: University of Chicago Press.

Kappeler, Peter M., and Carel P. van Schaik. 2002. Evolution of Primate Social Systems. International Journal of Primatology 23 (4): 707–740.

Martin, Robert D. 1990. Primate Origins and Evolution: A Phylogenetic Reconstruction. Princeton, NJ: Princeton University Press.

Ryne A. Palombit