PRIMATE DEMOGRAPHY

Primate demography is the study of population processes in species most closely related to humans. Primates include the prosimians (lemurs, lorises, galagos, etc.) and the anthropoids (monkeys and apes). Prosimians differ from the rest of the primate order in their largely nocturnal habits, reliance on smell rather than vision, and because they generally live in smaller groups. For these reasons and for human relevance this article is focused on the anthropoid primates. Knowledge of primate demography provides the context for understanding how human demography is constrained by general mammalian and ancestral primate patterns of birth, death, and movement. Some of these patterns are specific to primates and some reflect broader mammalian patterns. Primate demography provides a backdrop against which uniquely human characteristics may be discerned. Human lineage probably diverged from that of the other great apes some five to six million years ago. Humans and chimpanzees, however, still share many life history traits such as male philopatry (females leave their natal home range at maturity while males remain) and prolonged post-weaning dependency of young on their mother. Humans differ from chimpanzees in that humans have longer prereproductive periods than would be expected for a mammal of similar body size, delayed reproductive maturity for body size, relatively short interbirth intervals, and have probably always had a sizeable proportion of individuals with long post-reproductive life spans. While quantitative demographic information on wild primate populations is limited, there is a useful literature on primate life history that relates to demographic processes.

Life history traits are suites of co-evolved traits affecting reproduction, growth and development, patterns of social organization, and mortality. Just as the sources of mortality and physiological constraints on reproduction strongly influence life history, life history also affects birth and death rates and patterns of movement.

Although primates are mammals and share many demographic patterns arising from the constraints of mammalian reproduction (e.g., lactation leads to primarily maternal care of infants in most mammals, larger species tend to live longer and reproduce more slowly, etc.), their demography differs in many ways. The origin of primates in the tropical forests, their frugivorous (fruit eating) diets, evolution of larger brains, and complex social groupings, resulted in divergence from mammalian norms. Primates live longer than expected for mammals of similar body size and have low reproductive rates due to delayed maturity, singleton births, and prolonged dependency of young. Primates exemplify what Harvey and Promislow termed the "slowed down" life histories that are unusual for mammals and thus require special explanation. Primates as a group have larger brains than expected in a mammal of their body size. Within the order, positive selection for brain size is indicated by the fact that brain size increased faster than body size–a relationship that is not observed in most orders of mammals.

Social Organization

With a few exceptions (some prosimians, orangutans) primates live in long-term social groups that are kin-based. Polygyny is the most common mating system, but monogamy (a single male mates with a single female), polyandry (one female mates with multiple males) and polygynandry (multiple females mate with multiple males) are also represented within the order. In most Old World monkeys, males disperse while females remain in their natal groups. Apes show the full range of sex-differential dispersal: Both sexes leave natal home ranges among the monogamous lesser apes (gibbons), the solitary orangutans, and the polygynous gorillas; while female chimpanzees most often disperse. Dispersal patterns are even more varied among New World monkeys with long-lived Cebus (capuchin monkeys) demonstrating many of the life history traits–including female emigration–more common among Old World monkeys. Essentially all primate groups are dominance structured. Group size, composition, and social status are often related to both reproductive success and mortality. In 2001, Carey and Judge proposed that reduced levels of mortality and fertility are related through increased intergenerational transfers.

Fertility

Birth of singleton young is the ancestral primate norm. Singleton births of slow growing young take place at annual or longer intervals that correlate with body size. Young are most commonly carried in the mouth (prosimians), cling ventrally, or ride on the back of the mother. Primate fertility increases with age to a peak after the first reproduction and subsequently shows senescent decline. However, as in the vast majority of mammals, true menopause is absent in nonhuman primates studied to date.

Several small bodied groups of prosimians and New World monkeys have secondarily evolved litter sizes of two to three young that are produced at less than annual intervals. In the small New World marmosets and tamarins, group members, other than the mother, most frequently carry the multiple infants and juveniles, thus facilitating the ability of the females to produce two litters per year, which is a substantially higher reproductive rate than observed in larger primate species.

Most of the fertility data for New World monkeys come from captive marmosets and tamarins (Callithricidae). As noted, the members of these groups are small bodied and unusual in terms of litter size (greater than 1), early reproduction (beginning at approximately 1 year of age), short interbirth intervals (less than one year), and also in the predominance of allomaternal care (care by group members other than the mother). These traits are not characteristic of most of the New World monkeys and, thus, the demography of New World monkeys is ripe for additional research.

The models for Old World monkeys are based on several species of macaques. These monkeys begin to reproduce at the age of two years and produce one offspring every one to two years. In most species, female offspring remain in a natal troop of dominance ranked matrilines (a grouping of related female lineages) and male offspring disperse at adolescence. In contrast, apes have longer immature periods after controlling for body size, which is related to the four to five year length of their interbirth intervals. Unlike other apes, human interbirth intervals are not long given their body size. Hawkes, O'Connell, and their colleagues related this to the prevalence of allomaternal care, mainly by older female relatives, especially grandmothers. Gage estimated total fertility for all three groups of nonhuman anthropoid primates at approximately six–similar to that of contemporary populations of humans in developing countries prior to the fertility transition.

Sugiyama's 1994 study of demographic patterns in a wild female population of common chimpanzees in Bossou suggested similarities in reproductive parameters to those of humans in some hunter-gatherer populations. Age at first birth varied between 12 and 14 years and fertility increased to peak at an average of 0.33 per year at 20 to 23 years of age. Mothers over 40 years of age produced very few infants, none of whom survived. The mean interbirth interval after a surviving offspring was 5.1 years. Gage suggests that the earlier age, compared to humans, of first reproduction and the similar agerelated decline in fertility mean that chimpanzees have longer reproductive life spans than do humans and that this is probably related to different patterns of immature mortality.

Mortality

Primates demonstrate many aspects of the mammalian pattern of high neonatal mortality, followed by a mortality decline to a pre-reproductive lifetime minimum, after which mortality rises at an increasing rate into old age. Human mortality departs from that of non-human primate patterns in the relatively low immature mortality achieved as a result of lower infant mortality and a more rapid decline in age-specific mortality of human juveniles relative to infants. Mortality increases at sexual maturity and there is evidence, especially in low mortality populations, of an early-adulthood mortality hump both among non-human primate and human males, often attributed to accidents. In Bossou, Guinea, 73 percent of chimpanzee infants survived to age four, 71 percent survived from age four to age eight, and 22 percent survived from age eight to age 12. The last of these values suggests unusually high mortality that may be conflated by female outmigration. But this is not entirely an artifact of measurement: In all natural populations, outmigration from the natal home range is associated with an increase in age-specific mortality in early adulthood.

While models suggest that life expectancy is quite low among wild chimpanzees and that life expectancy at sexual maturity is only an additional 15 years on average (with approximately 35 years of age as the outside age limit), these models are based on increasing mortality rates with age. There is evidence, however, that mortality rates of non-human primates as well as of humans level off, rather than continuing to increase, in very old age; indeed, there are numerous chimpanzees in the wild that are estimated to be well past 45 years of age. Clearly there is much yet to be learned about the mortality scenarios of older primates in natural populations.

New World monkeys generally have the shortest lives and the earliest reproduction, with the important exception of the genus Cebus. Old World monkeys both live, and delay maturity, longer than New World monkeys. The apes, all of which are Old World, exceed Old World monkeys in life span and in age at maturity; the longest lived and latest maturing primate after controlling for body size is the human. The survivorship curves become increasingly rectangular (i.e., exhibit prolonged survivorship followed by rapid decline at old age) over the same phylogenetic gradient. This picture is undoubtedly over-simplified if for no other reason than the paucity of data and the limited New World taxa for which demographic data are available.

Migration

Male emigration from natal groups, similar to that in most mammals, is temporally associated with increases in mortality. This mortality may be due to risks associated with poorer knowledge of resource distribution in new areas, with greater vulnerability to predators, and with intraspecific competition, particularly male–male competition in polygynous species. Research regarding sex-specific mortality associated with emigration in male versus female philopatric species is needed. Even in semi-captive groups of female philopatric species, young adult males are more likely to disappear from censuses than are other age classes or females. Unlike most mammals, female rather than male chimpanzees emigrate at puberty or early adulthood; interestingly, high-status female chimpanzees do not necessarily leave their natal ranges. Demographic research on New World species will be enlightening since females, or both sexes, emigrate in many of these groups. The common human practice of female outmarriage (the practice of women moving further from their natal family than men at marriage) often results in females leaving their natal communities at sexual maturity; however, sex differentials at young adult ages among humans still exhibit excess male mortality. Sources of mortality risks in young adulthood may include ecological (resource levels, predation risks) and social (e.g., male–male competition for mates) factors.

See also: Animal Ecology; Evolutionary Demography.

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Debra S. Judge