Primates

(Primates)

Class Mammalia

Order Primates

Number of families 14

Number of genera, species 62 genera; 350 species

Introduction

The order name "Primates" (literally: "those of first rank") was introduced by Linnaeus in 1758 for a group that included man along with several non-human primates known at that time. Interestingly, Linnaeus also included bats in his order Primates, but this was soon abandoned by other taxonomists. The number of living primate species recognized in standard classifications has been steadily climbing and has reached at least 350. It is highly likely that additional species will be recognized, notably because of contributions from molecular studies and the discovery of further previously unrecognized "cryptic species" among the incompletely studied night-active (nocturnal) primates. The total number of extant primate species is therefore likely to settle at about 400. The living primates fall quite clearly into six "natural groups," based on a combination of geographical distribution and key characteristics: (1) lemurs (infraorder Lemuriformes), (2) lorises and bushbabies (infra-order Lorisiformes), (3) tarsiers (infraorder Tarsiiformes), (4) New World monkeys (infraorder Platyrrhini), (5) Old World monkeys (superfamily Cercopithecoidea), (6) apes and humans (superfamily Hominoidea). The last two groups—Old World monkeys, apes, and humans—are relatively close together, so they are given the status of superfamilies within the single infraorder Catarrhini. The first three groups of living primates (lemurs, lorises, and tarsiers) have all retained numerous primitive features, and these "lower primates" have therefore commonly been allocated to the suborder Prosimii (literally: "before the monkeys"). The remaining three groups (monkeys, apes, and humans) all share a set of advanced characters, and these "higher primates" have been allocated to the suborder Anthropoidea.

Evolution and systematics

The known fossil record of undoubted primates dates back to the beginning of the Eocene epoch, some 55 million years ago (mya). A group of fossil mammals from the preceding Paleocene epoch (55–65 mya), containing many North American and European representatives and allocated to the infraorder Plesiadapiformes (e.g., Ignacius, Palaechthon, Plesiadapis, Purgatorius), is commonly included in the order Primates. However, some authors have questioned the proposed link between Plesiadapiformes and Primates and the principal similarities involve the molar teeth. It is, in any case, generally agreed that the Plesiadapiformes branched away before the origin of modern primates. They are hence no more than a sister group and have accordingly been given the label "archaic primates." Modern primates and their direct fossil relatives ("primates of modern aspect" or Euprimates) can only be traced back to the basal Eocene. Close to 500 fossil primates of modern aspect have been recognized, and this total will surely increase. Surprisingly, the earliest representatives, from the Eocene epoch, have been discovered primarily in North America and Europe, where numerous species have been documented. This is unexpected, because primates today are very largely confined to the southern continents (South America, Africa, and Asia). Most of the Eocene primates that have been found are of course relatively primitive and hence most closely resemble modern prosimians. Indeed, it is possible to find both lemur-like species (infraorder Adapiformes) and tarsier-like species (infraorder Omomyiformes). Representatives of both of these groups are found in Europe and North America (e.g., European Adapis and American Notharctus among Adapiformes and European Necrolemur and American Tetonius for Omomyiformes).

For a long time, the earliest known direct fossil relatives of higher primates dated back only to the beginning of the Oligocene, about 35 mya. These early Oligocene anthropoids are all derived from a single fossil site in Egypt, the Fayum, and include a dozen genera belonging to two distinct groups with different dental formulae (e.g., Aegyptopithecus versus Apidium). A few enigmatic Eocene forms with some monkey-like features had been reported from Asia (e.g., Amphipithecus and Pondaungia from Myanmar [formerly Burma]), but the remains were so fragmentary that their affinities were uncertain. Recovery of more complete specimens revealed that these Asian forms are, indeed, related to higher primates, and the discovery of monkey-like Siamopithecus from Eocene deposits in Thailand has provided additional confirmation. Thus, the earliest known relatives of higher primates come from Asia. Fissure fillings from the Chinese middle Eocene site of Shanghuang have also yielded several fossils that have expanded our understanding of early primate evolution. In addition to adapiforms and omomyiforms, the Shanghuang deposits contain a possible early anthropoid (Eosimias) and an apparent direct relative of modern tarsiers (Tarsius eocaenus).

Overall, an impressive range of early fossil primates of modern aspect is known from the Eocene and early Oligocene, primarily from the northern continents. However, there is a period of 6 million years during the middle of the Oligocene epoch (26–32 mya) from which not a single fossil primate species has been recovered. A few primate fossils have been discovered in late Oligocene deposits, and from the Miocene upwards (i.e., over the last 25 million years) the primate fossil record is again relatively good. Miocene deposits have yielded direct relative of modern lorises and bushbabies, of New World monkeys, of Old World monkeys, and of apes (hominoids). Nevertheless, there are still some marked gaps in the fossil record. For instance, no single fossil lemur has ever been discovered on Madagascar, although a score of subfossil lemur species (predominantly large-bodied forms) dating back just a few thousand years have been discovered.

The order Primates is one of a score of major groups that radiated from the ancestral stock of placental mammals that existed at some time during the Cretaceous. One key question therefore concerns the relationship between primates and other mammals. Primates of modern aspect undoubtedly constitute a monophyletic group. In other words, they are all derived from a single, distinct common ancestor. Various attempts have been made to link this monophyletic group of primates to other orders of mammals. For some time, the tree shrews (now allocated to the separate order Scandentia) were actually included in the order Primates, but it eventually emerged that the similarities between tree shrews and primates are attributable to retention of primitive mammalian features and convergent adaptations for arboreal life. There has also been much support for recognition of a superorder Archonta containing primates, tree shrews, colugos (Dermoptera), and bats (Chiroptera). (In the original proposal, Archonta also included elephant shrews, but they were subsequently quietly dropped.) One problem with recognition of the Archonta is that it perpetuates the disputed link between primates and tree shrews by other means. Furthermore, it continues the practice of suggesting links on the basis of likely retention of primitive mammalian features and convergent adaptations for arboreal life. A quite different suggestion, based on certain features of the visual system, is that primates are the sister group of fruit bats (Megachiroptera). Among other things, this "flying primate hypothesis" has the corollary that the bats are not monophyletic and that flight evolved twice, once in ancestral fruit bats and once in the ancestor of the remaining bats (Microchiroptera). Comprehensive analyses of relationships between mammalian orders using large molecular data sets have now fairly clearly ruled out any connection between tree shrews and primates or between bats and primates. Indeed, several molecular studies have indicated that tree shrews may have some link to rabbits, while a whole host of morphological and molecular evidence resoundingly indicates that the bats form a monophyletic group. Hence, the "flying primate hypothesis" has been largely discredited and there is little support for recognition of a superorder Archonta. On the other hand, there are indications from the molecular data that there might be some kind of link between colugos and primates.

Because the earliest known undoubted fossil primates are only 55 million years old, it has been widely accepted that the common ancestor of primates of modern aspect dates back only to the Paleocene, some 60–65 mya, thus post-dating the demise of the dinosaurs at the end of the Cretaceous. However, comprehensive phylogenetic trees for placental mammals based on molecular evidence suggest that many orders, including the Primates, began to diverge during the Cretaceous, about 90–100 mya. Furthermore, a statistical analysis that takes into account the numerous gaps in the primate fossil record indicates that these gaps have led to marked underestimation of the age of the last common ancestor of primates of modern aspect. Calculations suggest that ancestral primates existed at least 82 mya.

Relationships within the order Primates are now relatively well established, at least as far as the living representative are concerned. Numerous sources of evidence, including morphology, chromosomes, and molecular data, all point to a basic divergence between one lineage leading to lemurs and the loris group and another leading to tarsiers and higher primates. Modern lemurs, lorises, and bushbabies have retained the rhinarium (a hairless area of moist skin surrounding the nostrils) and are referred to as strepsirrhines. They uniformly exhibit a non-invasive (epitheliochorial) type of placentation. Furthermore, they are generally characterized by the development of a toothcomb in the lower jaw, in which the bilaterally flattened crowns of the lower incisors and canines have become almost horizontal. This distinctive dental specialization can be traced back over 40 million years. By contrast, modern tarsiers and higher primates have completely lost the rhinarium and are accordingly labeled haplorhines. They uniformly exhibit a highly invasive (hemochorial) type of placentation, and this in fact provided the first evidence of a link between tarsiers and higher primates. Haplorhine primates lack any dental development resembling the toothcomb of strepsirrhine primates. On the other hand, they all have a virtually complete bony wall (postorbital plate) behind the orbit, whereas strepsirrhine primates merely have a bony strut (postorbital bar) around the outer margin of the orbit. The relationships between Eocene primates and modern primates are uncertain. Although the Adapiformes resemble modern lemurs in many respects, this is mainly because both possess relatively primitive primate features. Significantly, the Adapiformes lack any dental development that can be linked to the distinctive toothcomb of modern strepsirrhines. Hence, it seems likely that the Adapiformes may be a sister group of the strepsirrhines or perhaps just a side-branch from the ancestral primate stock. Similarly, the relationship between Omomyiformes and modern tarsiers is tenuous. Although both groups show an intriguing similarity in possessing relatively large molar teeth and a bell-shaped upper dental arcade, the Omomyiformes merely have a postorbital bar and lack a postorbital plate. Thus, there is probably no more than a sister-group relationship between Omomyiformes and tarsiers. From the late Eocene through the lower Oligocene, there is increasing evidence of the development of higher primate characteristics in certain lineages. Deepening of the lower jaw (mandible) and the presence of a postorbital plate are identifiable in the late Eocene, and by the lower Oligocene there are fossil forms with spatulate (rather than peg-like) incisors and medial fusion of the right and left halves of the mandible. All of these are advanced features of the higher primates. From the beginning of the Miocene onwards, it is possible to identify representatives of all three natural groups of higher primates on the basis of defining characteristics.

For many years, it was customary to classify the primates into two suborders: Prosimii and Anthropoidea. This reflected a classical, grade-based approach to classification in which the most primitive surviving forms are allocated to a basic group along with all early fossil forms. The suborder Prosimii hence included the fossil Adapiformes and the Omomyiformes along with the extant lemurs, lorises, and tarsiers, while the suborder Anthropoidea included the extant monkeys, apes, and humans along with any fossil forms showing

certain advanced features that characterize this subgroup of primates. However, many authors now favor a cladistic type of classification in which the main subdivisions are designed to reflect directly the main divergences within the reconstructed phylogenetic tree. This has led to the widespread adoption of an alternative classification in which lemurs and lorises are allocated to the suborder Strepsirrhini and tarsiers and higher primates to the suborder Haplorhini. This approach is not followed here for entirely practical reasons. In the first place, if a classification directly matches an inferred phylogenetic tree, it must logically be changed every time the tree is changed. This is a prescription for classificatory instability. Secondly, most primate fossils (particularly the earlier representatives) are known only from isolated molar teeth and there is no known way of reliably distinguishing all strepsirrhines from all haplorhines on the basis of molar features alone. In any event, almost all primate classifications in general use have a primary subdivision into two suborders. The consensus view is that these contain a total of at least 14 families with extant representatives. Reflecting the diversity of the lemurs of Madagascar, five of these families belong to that group alone: Cheirogaleidae (dwarf and mouse lemurs); Lemuridae (true and gentle lemurs); Lepilemuridae (sportive

lemurs); Indriidae (indri group); and Daubentoniidae (ayeaye). The loris group can be divided into two families: Loridae (lorises); Galagonidae (bushbabies). There are only five species of modern tarsiers, and these are all allocated to the single family Tarsiidae. The New World monkeys have classically been divided into two families: Cebidae (true New World monkeys) and Callitrichidae (marmosets, tamarins and Goeldi's monkey). The Old World monkeys are all morphologically very similar and they are generally placed in the single family Cercopithecidae. However, some authors regard the leaf-monkeys as sufficiently different to place them in a separate family Colobidae. Finally, the hominoids have been traditionally divided into three families: Hylobatidae (lesser apes, or gibbons), Pongidae (great apes), and Hominidae (modern humans and their fossil relatives).

Physical characteristics

Living primates cover a very large range of body sizes, extending from 1 oz (30 g) for the pygmy mouse lemur (Micro-cebus berthae) to about 375 lb (170 kg) for a full-grown adult male gorilla. There is accordingly a more than 5,000-fold difference between the smallest and largest living primates. As a rule, fossil primates fall at the lower end of this size range, although some of the recently extinct subfossil lemurs of Madagascar were comparable in size to an adult female gorilla (175 lb [80 kg]). The earliest known fossil primates from the Eocene and Oligocene were generally quite small. Some of them were apparently even smaller than the pygmy mouse lemur, while the biggest probably did not exceed 22 lb (10 kg). Among living primates, it is notable that nocturnal species are generally markedly smaller than diurnal species. The average body weight for nocturnal primates is about 1 lb (500 g), whereas the average body weight for diurnal primates is approximately 11 lb (5 kg), representing a ten-fold difference.

The hands and feet of primates are typically adapted for grasping rather than grappling while moving around. A widely divergent big toe (hallux) provides the basis for a powerful grasping action of the foot in all primates except humans, while the hand usually exhibits at least some grasping capacity. In most primates, the digits (fingers and toes) typically bear flat nails rather than narrow claws, and in all cases the hallux bears a nail. On the ventral surfaces of the hands and feet there are tactile pads with skin ridges (dermatoglyphs) that serve an anti-slip function on twigs and branches. These skin ridges, in combination with special tactile sense organs (Meissner's corpuscles), also permit enhanced tactile sensitivity. Patterns of movement (locomotor sequences) are typically hindlimb-dominated. The location of the body's center of gravity is typically closer to the hindlimbs, with the result that the typical walking gait shows a diagonal sequence (forefoot precedes hindfoot on each side). In the foot, there is usually at least some degree of relative elongation of the distal segment of the heel bone (calcaneus). Primates also tend to have longer limbs, in relation to overall body size, than other mammals, and this results in increased stride length. The visual sense is greatly emphasized in primates. The eyes are relatively large and in the eye sockets (orbits) there is at least a bony strut (postorbital bar) on the outer margin. A large degree of binocular overlap is ensured by pronounced forward rotation of the eyes and orbits. The proportions of nerve fibers passing from the retina of each eye to the two sides of the brain are approximately balanced and they are organized in a very unusual way such that the opposite half of the visual field is represented in each half of the brain. The ventral floor of the bony capsule protecting the middle ear (auditory bulla) is formed predominantly by the petrosal bone, which is unusual among mammals. Partly because of the increased emphasis on vision, the primate brain is typically enlarged at least to some extent, relative to body size, in comparison to other living mammals. The brain of living primates always possesses between the frontal and the parietal lobes a true Sylvian sulcus (joining the rhinal sulcus) and a complex calcarine sulcus on the inside of the occipital lobe. Primates are unique among living mammals in that the brain constitutes a significantly larger proportion of body weight at all stages of fetal development. The dental formula exhibits a maximum of two incisors, one canine, three premolars and three molars on each side of upper and lower jaws, differing from ancestral mammals in the loss of one incisor and one premolar from each toothrow. In association with the reduction in the number of incisors, the premaxilla bone at the front of the upper jaw is very short, and the incisors are arranged more transversely than longitudinally. The cheek teeth are typically relatively unspecialized, although the cusps are generally low and rounded, while in the lower molars the heels (talonids) are raised and enlarged.

Distribution

Modern primates are very largely confined to tropical and subtropical regions of the world, hence occurring predominantly in the southern continents. The smaller-bodied prosimian primates are even more restricted in their distribution, while a few of the larger-bodied higher primates (notably macaques) can occur quite far north in regions where snow is found in winter (Barbary, rhesus, and Japanese macaques). The lemurs are confined to Madagascar and are the only primates to occur on that island. The lorises and bushbabies are an Afro-Asian group. However, whereas the lorises occur in both Africa and Asia, the bushbabies occur only in Africa. The tarsiers are restricted to various islands in Southeast Asia. The New World monkeys occur in South and Central America and are the only primates to be found in the Neotropical region. The Old World monkeys, like the lorises, are an Afro-Asian group with a very wide distribution. However, the guenons and their relatives primarily occur in Africa, with only the macaques as an essentially Asian offshoot, while the leaf-monkeys are primarily Asiatic and represented in Africa only by the colobus monkeys. Finally,

the hominoids are also an essentially Afro-Asian group, although humans began to expand outside that range about two million years ago. The gibbons and the orangutan are found only in Southeast Asia, while chimpanzees and gorillas are confined to Africa.

In the distant past, during the Eocene epoch, primates occurred at very high latitudes in North America and Europe, in regions where they subsequently left no trace. One plausible explanation for this is that a marked increase in ambient temperatures at higher latitudes that marked the transition from the Paleocene to the Eocene led to a northward expansion of tropical and subtropical forests, thus expanding the potential geographical range of habitats available to primates. At the end of the Eocene, temperatures at higher latitudes declined markedly and this doubtless explains why primates virtually disappeared from the northern continents at that time, with only a few species surviving for a while into the Oligocene. In fact, it seems likely that primates also occurred widely in the southern continents during the Eocene, at least in Africa and Asia, but for various reasons we have very few fossils from those regions. The most likely interpretation for

the current geographical distribution of primates is that they have always been present in the south and that their range expanded temporarily into the north during the Eocene when temperatures where higher, only to contract again at the end of the Eocene when temperatures declined. In the Old World, primates also occurred somewhat further to the north during the Miocene, as fossil apes and monkeys from that epoch have been documented for the circum-Mediterranean region, for southern Europe and as far north as Hungary and Czechoslovakia.

Habitat

Primates are typically tree-living (arboreal) inhabitants of tropical and subtropical forest ecosystems. Their grasping hands and feet represent adaptations for grasping twigs and branches while moving around in the trees. Ancestral primates, which were probably small-bodied creatures, were seemingly adapted for movement in the fine branches of trees and bushes, where they fed on a mixture of fruits and arthropods. The enlarged, forward-facing eyes of primates probably developed for visually oriented leaping among fine branches while seeking both fruits and animal prey.

Although they are generally restricted to tropical and subtropical forests, primates nevertheless occupy a remarkably wide range of habitats, ranging from evergreen tropical rain-forest with year-round rainfall to quite dry scrub forest with strictly seasonal rainfall. Primates are also characteristic inhabitants of gallery forests along the banks of rivers running through otherwise relatively dry areas. Madagascar is a good example of the variety of habitats. Lemurs inhabit the evergreen rainforests extending along the eastern coast; the deciduous forests found on the northwestern and western coasts; the semi-arid, cactus-like forests in the southwestern and southern regions; and in the cooler forests on the central plateau. A general rule for primates is that the number of species living in any one area (sympatric species) tends to increase as the total annual rainfall increases. For example, the maximum number of sympatric lemur species in Madagascar is found in the eastern rainforest, while the minimum is found in the dry forests of the south and southwest.

Most primates are entirely arboreal in habits, living virtually all of the time in trees and rarely descending to the ground. The prosimian primates are almost exclusively typically arboreal. The only obvious exception to this rule is provided by the ringtailed lemur (Lemur catta), which spends approximately 25% of its time on the ground. The New World monkeys are also almost exclusively typically arboreal. However, even typically arboreal primate species descend to the ground occasionally. For instance, mouse lemurs, some bushbabies, and tarsiers commonly scan the leaf litter on the forest floor from some vantage point low down in the trees and then trap insects with sudden, rapid dashes to the ground. It is only among the Old World monkeys and apes that we find semi-terrestrial or terrestrial species that spend a significant amount of the time moving around and feeding on the ground, as is the case with baboons and gorillas.

Behavior

Primates generally live in well-developed social networks and this can be regarded as a defining characteristic of the order. Although species that are active by night (nocturnal) have commonly been described as solitary, field studies have revealed that there are intimate social links between individuals, maintained by intermittent contacts during the night and by sharing of nests during the daytime. Nevertheless, there is a major distinction between day-active (diurnal) primates and nocturnal species in that the former typically live in obvious cohesive social groups, whereas the latter usually move around and feed alone at night. In sum, while all primates have intricate social systems, as a general rule diurnal species are gregarious whereas in nocturnal species individuals are dispersed. Among nocturnal primates, the only exceptions to solitary behavior are found in a few species that are monogamous (pairliving), such as the avahis (Avahi) in Madagascar and the owl monkeys (Aotus) in the New World. Among diurnal primates, the only representative that is almost solitary like most nocturnal primates is the orangutan (Pongo) of Southeast Asia. Otherwise, the groups of gregarious diurnal primates can be classified into three main categories according to the composition of their groups: monogamous family units, one-male groups and multi-male groups. Monogamous groups typically consist of an adult pair living together with their immature offspring. Clear-cut examples of monogamy are found among lemurs (e.g., avahis, mongoose lemurs, red-bellied lemurs, and indri), among New World monkeys (e.g., owl monkeys, marmosets, tamarins and Goeldi's monkey), in a few Old World monkeys (e.g., Mentawai langur) and in all gibbons. Such groups are necessarily relatively small and may contain between two and a dozen individuals. One-male groups, also known as harem groups, contain a single adult male, several adult females and a variable number of immature individuals. The best-known examples of one-male groups are found among such Old World monkeys as Hamadryas baboons (Papio hamadryas), geladas (Theropithecus), guenons (Cercopithecus species), patas monkeys (Erythrocebus patas), and the majority of leaf-monkeys (e.g., black-and-white colobus and several langur species). Among the apes, gorillas also live in one-male groups. In many species that are characterized by harem groups, the surplus males join together in bachelor groups. Furthermore, in some cases several harem groups and bachelor male groups may move together in large herds that may contain over a hundred individuals, as is the case with Hamadryas baboons and geladas. Multi-male groups contain several adult males along with several adult females and a variable number of immature individuals. Examples of such social groups are widespread among primates and found in various diurnal lemurs like ringtails (Lemur catta) and some sifakas (e.g., Propithecus verreauxi); in most New World monkeys (e.g., capuchins, howler monkeys, spider monkeys, and woolly monkeys); in several Old World monkeys (e.g., plains baboons, vervet monkeys, and red colobus); and in chimpanzees. Various attempts have been made to reconstruct the evolutionary history of primate social systems. One key finding is that, although individuals are typically dispersed, nocturnal primates show social networks that exhibit parallels to the array of monogamous, one-male, and multi-male patterns found among diurnal primates. Reconstruction in comparison with other mammals suggests that the ancestral primates were nocturnal and lived in multi-male social networks similar to those found in most modern nocturnal prosimians.

Because they live in well-defined social networks, primates typically exhibit regular and relatively intense social interactions. One very common form of social interaction is grooming, which is frequently reciprocal. Even in nocturnal primate species that show dispersal of individuals at night, and in orangutans, which are usually dispersed by day, social grooming is a prominent feature of occasional encounters between familiar individuals. In prosimians, social grooming is usually carried out mainly with the teeth, and in lemurs and lorises (strepsirrhines) the tooth-comb is actively used. In higher primates, by contrast, the hands usually play a more intense role in social grooming, particularly in Old World monkeys and apes. Although the visual sense is highly developed in primates, olfactory signals continue to play a role in social interactions, particularly in prosimians and New World monkeys. Nocturnal lemurs and lorises still have relatively large olfactory bulbs in the brain, and marking with urine and/or feces and with secretions from special skin glands (e.g., on the chest) is prominent. For dispersed nocturnal prosimians, olfactory marking may be the primary means of communication between individuals while active. Visual displays are particularly important in diurnal primates, some of which have developed quite striking coloration patterns of the fur (e.g., certain lemurs, Old World monkeys, and gibbons). In fact, ringtailed lemurs show an interesting display pattern that

combines both olfactory and visual elements. During encounters between groups that have been labeled "stink fights," individuals anoint their tails with secretions from marking glands on the arms and then wave their tails in the air while strutting around. Perhaps the greatest diversity of color patterns on the face and elsewhere on the body is found in the African guenons, which often have characteristic head movements that emphasize any species-specific facial markings. Vocalizations are also generally important for social interactions among primates. Nocturnal primates usually have a relatively restricted vocal repertoire, but the calls that they do have are important for maintaining contact between dispersed individuals. Some of the smallest nocturnal primates (e.g., mouse lemurs, dwarf bushbabies) have calls that are in the ultrasonic range. Diurnal primates generally have richer vocal repertoires containing numerous calls in the audible range and their subtlety (e.g., through intergradation between call types) can be quite pronounced, particularly in certain Old World monkeys and chimpanzees. Many species like the lion tamarins and titi monkeys have long calls to maintain contact between neighboring groups.

Although it is often assumed that all primates show territorial behavior, defense of an exclusive territory is in fact comparatively rare among primates. Numerous nocturnal primates show range overlap between adults of both sexes, and diurnal primates that live in gregarious groups often show quite extensive overlap between group ranges. Some nocturnal prosimians, such as sportive lemurs (Lepilemur) in Madagascar and in a minority of diurnal primates, including some lemurs (e.g., certain populations of sifakas, Propithecus, and in the indri), show true territoriality in the sense of behavior shown to defend an exclusive area. There seems to be a general trend for primates that live in monogamous groups to show marked territorial behavior, and it has in fact been suggested that one of the factors promoting monogamy is joint defense of an area containing vital resources. Territorial behavior has been found in a variety of monogamous species, including such nocturnal lemurs as avahis (Avahi), such cathemeral lemurs as the mongoose lemur (Eulemur mongoz), such diurnal lemurs as the indri (Indri), most marmosets and tamarins (Callitrichidae), and all gibbons (Hylobatidae). In fact, the indri, the gibbons, lion tamarins, and titi monkeys show conspicuous, often melodious vocalizations that carry over great distances in the forest and seem to play a part in territoriality. These "great calls" of the monogamous indri and gibbons provide one of the most striking examples of convergent evolution to be found among primates.

Most primate species are either exclusively nocturnal (active at night between dusk and dawn) or clearly diurnal (active by day between dawn and dusk). The majority of prosimian primates are nocturnal in habits, whereas simian primates are typically diurnal. Indeed, the only nocturnal representatives among simian primates are the owl monkeys of South and Central America (Aotus species); all the rest of the monkeys and apes, like humans, are diurnal. Of the three natural groups of prosimian primates, two contain only nocturnal species (loris group; tarsiers) while the third (lemurs) contains mainly nocturnal species but also some diurnal species. Among the lemurs, there is also an unusual pattern known as cathemerality in which there is a combination of nocturnal and diurnal activity. This is found in most or all brown lemurs (Eulemur species) and gentle lemurs (Hapalemur species). It has been found that in such species the proportions of nocturnal and diurnal activity vary over the annual cycle, and it seems that seasonal variation in ambient temperatures plays a part in this. Cathemeral activity has also been reported for some owl monkey populations in South America. Compared to other mammals, all primates have relatively large eyes, but in nocturnal primates the eyes are generally even larger. As a further adaptation to nocturnal life, lemurs and lorises typically possess a special reflecting layer behind the retina of the eye, known as a tapetum lucidum. Unique among mammals, the reflecting properties of this structure are derived from flat crystals of riboflavin. Although they are also nocturnal, both tarsiers and owl monkeys lack a reflecting layer behind the retina and they compensate for this by having even larger eyes than nocturnal lemurs and lorises. This is just one indication that tarsiers and owl monkeys are secondarily nocturnal and have adapted in a different way to night-time activity.

Feeding ecology and diet

Primate species exhibit a wide range of diets, although most of them include at least some fruits in their food intake. If there is a typical dietary category for primates generally, it is surely fruit consumption, as this is found from the smallest to the largest species. Although most primates eat at least some fruits, primates can be classified into three main dietary categories representing at least 50% of food intake: (1) insectivores, feeding mainly on arthropods (e.g., tarsiers); (2) frugivores, feeding mainly on fruits (e.g., most forest-living monkeys); (3) folivores, feeding mainly on leaves (e.g., leaf-monkeys). There is a general trend among primates for the diet to shift progressively from insectivory through frugivory to folivory as body size increases. This is understandable because small-bodied mammals have relatively high-energy requirements per unit body weight and must eat foods with a rich, easily available energy content. Large-bodied mammals have relatively low energy requirements per unit body weight and can consume foods that have a poor energy content and require extensive digestion. As a general rule, insectivorous primates do not exceed 1.5 lb (700 g) in body weight, while folivorous primates tend to be quite large-bodied species. Sportive lemurs (Lepilemur) and avahis (Avahi), which weigh between 1.4 lb (650 g) and 2.2 lb (1 kg), are both exceptions to this rule, but they can cope with their relatively low-energy food intake because they have unusually low metabolic rates. In fact, a fourth dietary category known as gummivory must be recognized for primates whose food intake includes more than 50% of plant exudates (gums). Gums resemble fruits in that they are a major source of carbohydrates, but they resemble leaves in that the carbohydrates are polymerized and require extensive digestion. Many primate species include at least some plant exudates in their diets, but there are just a small number of gum-feeding specialists, such as the fork-crowned

lemur, the needle-clawed bushbaby and some marmoset species.

Most primates forage primarily in trees or bushes for insects, fruits, leaves and/or gums. Regardless of the diet, the visual sense plays a major part in searching for food. Nocturnal primates generally have only a very restricted capacity for distinguishing colors and must rely on other dietary cues, but diurnal primates usually have some form of color vision. Fully developed trichromatic color vision of the kind found in humans occurs in Old World monkeys and apes and a few New World monkeys. Most New World monkeys and all diurnal lemurs have fundamentally dichromatic vision, although in certain New World monkeys there is an unusual polymorphism of the gene coding for a retinal pigment on the X-chromosome, such that some females have a form of trichromatic vision. Prosimian primates generally collect their food primarily with the mouth, but in higher primates the hands play an increased role. As a rule, food items are consumed directly, but in some cases there is some pretreatment of food items. For instance, some capuchin monkeys break nuts by pounding them on branches or tree trunks, while certain chimpanzee populations show nut-cracking involving the use of some kind of hammer and anvil. Chimpanzees have also been reported to use twigs or stems as tools to extract termites from their mounds.

Most primates lack any obvious special foraging adaptations, but there are a few conspicuous exceptions. The tooth-comb in the lower jaw of strepsirrhine primates is, for instance, commonly used in gathering food as well as for grooming. Some lemurs, bushbabies and lorises use the tooth-comb to harvest gum, and many species use it to scoop out the pulp of large fruits. However, the tooth-comb is quite fragile, so it is typically used simply to scrape up plant exudates that seep out following insect damage to tree trunks and branches. In marmosets, by contrast, the lower incisors are elongated to match the canines and all of these stout teeth are used together as a dental tool to gouge holes in tree-trunks to promote the flow of gum. This dental adaptation distinguishes the marmosets from the closely related Goeldi's monkey and tamarins. Undoubtedly the most striking foraging adaptation in primates is found in the aye-aye (Daubentonia) of Madagascar, which has rodent-like incisors in both upper and lower jaws and a very thin middle finger in each hand. The gnawing incisors are used to open up channels occupied by wood-boring larvae in tree trunks, and the thin finger is used as a probe to extract the prey. Experiments have confirmed that the aye-aye can locate larvae in a tree trunk by tapping with the probe-like finger and listening to the echoes. It should also be mentioned that the leaf-monkeys (Colobinae) are unique among primates in that they have a complex stomach to permit efficient digestion of leaves.

Reproductive biology

A number of reproductive features are typical of primates. Male primates are characterized by permanent descent of the testes into a scrotum that is always located behind the root of the penis (postpenial position). Although several other mammal groups exhibit such descent of the testes, primates are un-usual in that it occurs very early in life, usually by the time of birth. Female primates are characterized by the absence of a urogenital sinus, which is a shared canal for the urinary and reproductive systems that is primitively present in mammals. In all female primates, the urethra and the vagina have separate external openings. In all primates, placentation is relatively advanced in that involvement of the yolk sac in the circulation of the placenta has been partially or completely eliminated. Relative to maternal body size, primates typically have long pregnancies (gestation periods), and they produce a small number of well-developed (precocial) neonates that are characteristically born with a covering of fur and with their eyes and ears open. Both fetal and postnatal growth are characteristically slow in relation to maternal size, and lactation periods are also relatively long. Sexual maturity is attained late and life spans are correspondingly long relative to body size. In a nutshell, primates are adapted for slow reproductive turnover and intensive, long-term investment in individual offspring.

Another defining feature of primates is that the non-pregnant cycle of females is typically quite long, usually lasting about a month. (The only striking exception is the squirrel monkey, which has a cycle lasting only nine days or so.) Furthermore, ovulation during the female cycle occurs spontaneously and is not induced by the act of mating as in many other mammals. Lasting bonds between individual males and females are generally typical of primates, and the process of bonding may be quite intense and drawn out. However, the frequency and duration of mating show great variation between species. As a rule, mating is seen relatively rarely in monogamous primate species, whereas in multi-male species mating may be very frequent, often involving several males for any individual female. One conspicuous feature associated with the female cycle and mating that is found in several Old World monkey species and in chimpanzees is the occurrence of sexual swellings, which reach a peak of size and coloration at about the time of ovulation.

It has often been assumed that primate mating systems are directly related to the patterns found in social groups. For instance, with species living in social groups with a single adult male (monogamous or harem groups), it has been widely assumed that that male is the father of all offspring born in the group. However, in most cases such restricted paternity has not yet been confirmed with genetic tests. Furthermore, there are some harem-living species in which incursions by extra-group males are known to occur quite regularly. This has, for example, been reported for patas monkeys and certain guenons. It has also been widely assumed that in multi-male groups of primates often showing a relatively clear hierarchy among males, paternity is related to male rank. In some cases (e.g., long-tailed macaques and plains baboons), this expectation has been confirmed with genetic tests, but in others (e.g., Barbary and Japanese macaques; hanuman langurs) it has been found that paternity is unrelated to rank.

Intensive parental care is also a hallmark of the primates. In most cases, there is a single offspring, although some prosimian species and marmosets and tamarins typically give birth to two or three infants at a time. All primates have frequent suckling bouts, long lactation periods, and intensive physical contact between the infant(s) and the mother, in some cases because they spend much time together in a nest but usually because the mother carries her infant(s) around with her, clinging to her fur. Incidentally, the characteristic grasping foot of the primates also plays an important role in infant clinging during parental carriage. In many monogamous primate species, the father (sometimes along with other group members) also plays a part in infant carriage. This is seen most conspicuously in certain New World monkeys (marmosets, tamarins, Goeldi's monkey, and owl monkeys), but it is also seen in some monogamous lemurs.

Primates show all possible patterns of breeding over the annual cycle, ranging from year-round breeding with only mild fluctuations right through to strict seasonal breeding, with mating and births restricted to tightly constrained periods of the year. In a few cases, as with the Moholi bushbaby (Galago moholi), there are two mating periods and two birth periods during the year. Primate species living in rainforests with year-round rainfall generally show little seasonal restriction in mating and births, although there are some notable exceptions (e.g. squirrel monkeys, Saimiri). By contrast, primates living in forests characterized by a marked dry season tend to show some seasonal restriction of breeding. Unusually, almost all lemurs on Madagascar show strictly seasonal breeding patterns, regardless of whether they live in rainforests or in dry forests. The only two exceptions seem to be the aye-aye and the gentle lemurs.

Conservation

In contrast to certain other mammal groups (e.g., artiodactyls, bats), no known primate species has become extinct as yet, but it is probably only a question of time. Indeed, a score of lemur species documented only by subfossils died out about 2,000 years ago, following the initial human invasion of Madagascar, so this may have been the first major wave of human-induced primate extinction. As a rough approximation, it can be said that one third of extant primate species are subjected to some identifiable degree of threat. Close to 120 primate species (out of a total of 350) have been identified as critically endangered, endangered or vulnerable in the IUCN Red List of Threatened Species. The 19 species identified as critically endangered include species in South America, Africa, Madagascar, and Asia. They are the Sumatran orangutan (Pongo abelii), a gibbon (Hylobates moloch), a macaque (Macaca pagensis), a colobus monkey (Procolobus rufomitratus), a snub-nosed monkey (Rhinopithecus avunculus), two langurs (Trachypithecus delacouri, T. poliocephalus), two woolly spider monkeys (Brachyteles arachnoides, B. hypoxan-thus), a woolly monkey (Oreonax flavicauda), two titi monkeys (Callicebus barbarabrownae, C. coimbrai), a capuchin monkey (Cebus xanthosternos), three lion tamarins (Leontopithecus cais-sara, L. chrysopygus, L. rosalia), two gentle lemurs (Hapalemur aureus, H. simus), and a sifaka (Propithecus tattersalli). Of the remaining 230 primate species, approximately half are probably threatened to some extent by reduction and fragmentation of habitat, while the other half can be provisionally regarded as relatively common.

Because primates are typically inhabitants of tropical and subtropical forests, the primary threat to natural populations comes from large-scale deforestation. Hunting is also a common threat to primates, although this is only a major menace where modern firearms have replaced traditional hunting methods. In tropical regions of South America, Africa, and Asia, large-scale hunting of primates to provide bushmeat has become an increasing problem. Trapping of certain species for biomedical use or for zoos has also posed a threat in the past, although this has been considerably reduced as a result of increasing awareness of conservation issues.

Recognition of the need for effective conservation measures is reflected by targeted programs in natural habitat areas and by breeding programs in captivity. The World Conservation Union (IUCN) plays a vital coordinating role through such programs as its Species Survival Commission (SSC), which has established a Specialist Group for primates. Extensive coordination of captive breeding has promoted the compilation of more than 30 international studbooks for primate species. In the wild, primates are protected to various extents through a network of national parks and reserves that are primarily designed to preserve tropical and subtropical forests, but effective protection remains an elusive goal in many cases.

Significance to humans

The most prominent use of non-human primates has been in biomedical research, where certain species (notably the rhesus monkey, the baboon, and the common marmoset) have become standard laboratory species. An emphasis on development of breeding programs has greatly reduced the impact of such usage on natural populations.

Some primates—notably macaques—are agricultural pests, raiding various crops (e.g., plantations of fruit trees and even stocks of maniok soaking in water) and occasionally causing major losses.

As a rule, primates are not directly dangerous to humans. Despite their reputation as fierce creatures, gorillas generally avoid contact with humans and their famous charges usually occur only when they feel threatened. Primates that are provisioned by humans, notably macaques, may inflict quite serious bites if they feel threatened. Primates can also represent a threat to humans because they harbor such pathogens as the Marburg and Ebola viruses.

Resources

Books

Alterman, Lon, Gerald A. Doyle, and M. Kay Izard, eds. Creatures of the Dark: The Nocturnal Prosimians. New York: Plenum Press, 1995.

Ciochon, Russell L., and A. Brunetto Chiarelli, eds. Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum Press, 1980.

Conroy, Glenn C. Primate Evolution. New York: W. W. Norton, 1990.

Cowlishaw, Guy, and Robin Dunbar. Primate Conservation Biology. Chicago: University of Chicago Press, 2000.

Fleagle, John G. Primate Adaptation and Evolution. New York: Academic Press, 1999.

Fleagle, John G., and Richard F. Kay, eds. Anthropoid Origins. New York: Plenum Press, 1994.

Gautier-Hion, Annie, François Bourliére, and Jean-Pierre Gautier, eds. A Primate Radiation: Evolutionary Biology of the African Guenons. Cambridge: Cambridge University Press, 1988.

Groves, Colin P. The Taxonomy of Primates. Washington, DC: Smithsonian Institution Press, 2001.

Harcourt, Caroline, and Jane Thornback. Lemurs of Madagascar and the Comoros. The IUCN Red Data Book. Gland, Switzerland: IUCN, 1990.

Lee, Phyllis C., Jane Thornback, and Elisabeth L. Bennett. Threatened Primates of Africa: The IUCN Red Data Book. Gland, Switzerland: IUCN, 1988.

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

Mittermeier, Russell A., Ian Tattersall, Willam R. Konstant, Douglas M. Meyers, and Rodney B. Mast. Lemurs of Madagascar. Washington: Conservation International, 1994.

Rowe, Noel. The Pictorial Guide to the Living Primates. East Hampton, New York: Pogonias Press, 1996.

Simons, Elwyn L. Primate Evolution: An Introduction to Man's Place in Nature. New York: Macmillan, 1972.

Smuts, Barbara B., Dorothy Cheney, Robert M. Seyfarth, Richard Wrangham, and Thomas Struhsaker, eds. Primate Societies. Chicago: Chicago University Press, 1987.

Sussman, Robert W. Primate Ecology and Social Structure. Vol. 1. Lorises, Lemurs and Tarsiers. Needham Heights, MA: Pearson Custom Publishing, 1999.

——. Primate Ecology and Social Structure. Vol. 2. New World Monkeys. Needham Heights, MA: Pearson Custom Publishing, 2000.

——. Primate Ecology and Social Structure. Vol. 3, Old World Monkeys and Apes. Needham Heights, MA: Pearson Custom Publishing, in press.

Szalay, Frederick S., and Eric Delson. Evolutionary History of the Primates. New York: Academic Press, 1979.

Tattersall, Ian. The Primates of Madagascar. New York: Columbia University Press, 1982.

Wallis, Janice, ed. Primate Conservation: The Role of Zoological Parks. New York: American Society of Primatologists, 1997.

Wolfheim, Jaclyn H. Primates of the World: Distribution, Abundance, and Conservation. Seattle: University of Washington Press, 1983.

Robert D. Martin, PhD