Non-human Primates

Last modified on May 23, 2010

Taxonomy     Reproductive characteristics         

Behavior and Psychological Well-Being

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Taxonomy

Information about anatomy, physiology and behavior is included here in separate Web pages about  prosimians, New World monkeys (cebids and callitrichids), and  Old World monkeys (cercopithecines and apes).

1. Suborder Prosimii (strepsirhines): have a naked, moist rhinarium with fixed upper lip, most are nocturnal, have a toilet claw, a toothcomb and a sublingual structure for cleaning it, all have epitheliochorial placentas except Tarsiidae (hemochorial).{4762}

a. Superfamily Lemuroidea

I. Family Lemuridae (lemurs)

II. Family Indriidae (sifakas, indris)

b. Superfamily Lorisoidea

c. Superfamily Daubentonioidea (aye-ayes)

d. Superfamily Tarsioidea (ACLAM slide series calls this a suborder, and Walker's Primates of the World{4048} calls it a family in the suborder Haplorhini)

2. Suborder Anthropoidea

a. Infraorder Platyrrhini (New World monkeys) : some have prehensile or pseudoprehensile tails, no cheek pouches or ischial callosities, require vitamin D3, all have estrous cycles except Cebus, all are arboreal, all are diurnal except Aotus (the only nocturnal simian), all have hemochorial placentas, and a high percentage (80%) of twinning. Marmosets and tamarins have opposable big toes, but not opposable thumbs. They are scent markers, using the circumgenital and sternal glands. Only one adult female in a group reproduces.{4762}

I. Family Callitrichidae

A. Callithrix (marmosets); smaller than tamarins; found in Brazil in secondary disturbed forests or edge habitats. The common marmoset (C. jacchus) is on appendix II of CITES (not endangered). C. jacchus groups can be of any type (males and females), but only the high-ranking pair will breed.

B. Leontopithecus and Saguinus (tamarins); Saguinus are found in Panama, Bolivia and Brazil, in the forest. S. oedipus is on appendix I of CITES (threatened with extinction). They have multimale-multifemale social structure; multiple males copulate with the breeding female (polyandry).

II. Family Callimiconidae

III. Family Cebidae

A. Subfamily Aotinae (owl monkeys)

B. Subfamily Callicebinae (titis)

C. Subfamily Saimiriinae (squirrel monkeys)

D. Subfamily Alouattinae (howler monkeys)

E. Subfamily Pitheciinae (sakis)

F. Subfamily Cebinae (capuchins)

G. Subfamily Atelinae (woolly and spider monkeys)

b. Infraorder Catarrhini (Old World monkeys) : all menstruate, all diurnal, all have hemochorial placentas.{4762}

I. Superfamily Cercopithecoidea

A. Family Cercopithecidae

i. Subfamily Cercopithecinae (macaques, baboons, guenons, patas monkeys, mangabeys)

ii. Subfamily Colobinae (colobus and proboscis monkeys)

II. Superfamily Hominoidea

A. Family Hylobatidae (gibbons, siamangs)

B. Family Pongidae (orangutans, gorillas, chimpanzees)

C. Family Hominidae (me)

The tarsiers appear to have diverged from the other primates about 65-60 million years ago. However, modern tarsiers more resemble the platyrrhines than the lemurs and lorises, so some authors (i.e. Nowak {4048}) place the tarsiers with the platyrrhines and call them the Haplorhines, and call the other prosimians Strepsirhines.

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Reproductive characteristics

Primates are distinguished from lower mammals by the size of the developing fetal brain. Neonates have larger brains than other mammals of comparable body size. Although by adulthood primates still have relatively large brains, there is considerable overlap with lower species. Since the developing primate fetus requires more time to develop this large brain, the rate of fetal body growth is relatively slow, and the maternal energy needs are not as great compared with those of altricial species. Primates are considered to be precocial even though the neonates are relatively helpless.

Prosimians are distinguished by their production of multiple offspring and by their use of nests (particularly in Cheirogaleidae, Galaginae and Varecia variegata). These are relatively primitive traits for primates.

As most primate mothers carry their infants, nursing can be achieved when the infant wants to, rather than when the mother is ready. Consequently, primate milk is lower in fat and protein and higher in carbohydrate.{4048}  

How do taxonomists distinguish a strepsirhine from a haplorhine? According to Nowak{4048}, two important features are used: the type of placentation and the relative size of infants. Strepsirhine primates have diffuse endotheliochorial placentas; this means that the intact uterine epithelium contacts the chorion. Fetal growth rates are lower and neonates are one-third the size of a haplorhine, despite similar gestation periods. Haplorhines have discoid hemochorial placentation, in which maternal blood bathes the chorion directly in discrete areas. Further, prosimians have a duplex uterus like other lower mammals, whereas anthropoids have a simplex uterus.

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Behavior and Psychological Well-Being

Environmental enrichment is "an independent variable that refers to manipulations to improve the environments of captive primates to enhance psychological well-being." Psychological well-being is "an abstract term that is inferred by measuring behavioral and physiological variables in the affected animals to determine whether a manipulation had the desired effect."{3563} PWB plans must provide for behavioral diversity, and must also take into account that some kinds of species-typical behavior are better indicators than others. For example, successful reproduction and rearing of infants is considered to be a good indicator of PWB, probably better than the absence of self-injurious behavior; but not all colonies are involved in reproduction and not all animals are capable of it. Furthermore, if animals in a colony were raised in unnatural situations they may display behaviors that are pathological and cannot be cured. The best PWB plan might not completely rid the animal of abnormal signs if its early rearing experience was negative.

A required, but difficult, activity for lab animal veterinarians is to assess the PWB of the animals in their charge. Some indices for the measurement of PWB are:

As part of the daily care provided to NHPs, all recognizable instances of behavior and physiology that deviate from normal for that species warrant further inquiry. Instances must be noted, as well as the diagnosis and the treatment prescribed and the outcome of the case. The animal care staff is absolutely crucial in the provision of care. If they are not sufficiently trained and their training not kept up to date, they will be unable to alert the veterinary staff to situations that warrant examination. In this way, PWB does not differ from provision of care for physical ailments. Routine daily checks should be used to monitor such things as hair condition, alertness, gait, appetite, body weight, and injury. Adaptation in the animals can be monitored by their responses to temporary routine husbandry events, such as cage changes or cleaning.

Although the PWB plan must be implemented in the form of specific SOPs that address all the major situations encountered in the colony, it is not likely that absolute standards are possible or desirable for the four characteristics listed above. More importantly, the staff must develop the ability to determine if the PWB program actually results in improved well-being of the animals. With NHPs this can be difficult in part because the human observers must be skilled enough to evaluate PWB relative to the species of animal, and not by anthropomorphic standards. A large measure of creativity and a will to be innovative are critical.{3563} 

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Background of PWB plans

In 1985 Congress amended the Animal Welfare Act in response to the public’s request for improving the environment in which laboratory animals, specifically NHPs and dogs, were kept. The USDA developed regulations in 1991 to describe how the law would be enforced. In part these regulations state that "...research facilities must develop, document, and follow an appropriate plan for environmental enhancement adequate to promote the psychological well-being of nonhuman primates..." A committee of experts was convened by the NRC to write a report to help animal care personnel grapple with this requirement.{3563}

One approach that will in all likelihood not work is to change the engineering standards governing animal housing. For example, simply increasing the size of the enclosure does not necessarily improve PWB and in fact may detract from it with some species. A better approach is to use current knowledge of the species to focus on the animals’ response to captivity, and attempt to make the animals’ environment as conducive to their health as possible.{3563}

As a first step, since little is known about some species, efforts must be made to identify and document signs of chronic distress, as manifested in maladaptive or pathological conditions. Therefore, the signs of distress must be defined, as well as the specifics of what constitutes maladaptive or pathological behavior. Much of the documentation will be subjective, and so it is even more important that animal care professionals be well-educated and continue to improve and share their knowledge.{3563}  

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Nonhuman primate groups and natural behavior

The order Primates is very large and contains diverse families of animals and man. Species from each of these families are found in research settings or in zoological parks and breeding operations.

The prosimians are the more primitive of the primates, and include the lemurs, tarsiers, sifakas, indris, aye-ayes, lorises, pottos and bushbabies (also called galagos). Most are nocturnal and have pointed muzzles, a naked rhinarium (moist patch of bare skin around the nose), and claws (rather than nails) on some fingers and toes. They are rare in captivity, but some zoos exhibit the ring-tailed lemur (Lemur catta) and Galago spp. {3563}

All other primates belong to the suborder Anthropoidea: monkeys, apes, and man. One way to group the species is by their geographical origin, i.e. New World vs. Old World primates. The major distinction is that New World primates have 3 premolars, whereas the Old World primates and man have 2. Also, the nasal septum is broader in New World primates.

New World primates are called platyrrhines and include marmosets, tamarins, howler monkeys, spider monkeys, owl monkeys, capuchins, squirrel monkeys, titi monkeys, sakis, and uakaris. Genera found in research laboratories include Callithrix jacchus (common marmoset), Saguinus oedipus (cotton-top tamarin) and Saimiri spp. (squirrel monkey). {3563}

Old World primates are found naturally in Africa and Asia, and include chimpanzees (Pan), macaques (Macaca), baboons (Papio), and vervets or green monkeys (Chlorocebus aethiops).

Normal behaviors in the animals’ natural environment can be used as indicators of PWB in captivity. Some relevant characteristics include the nature of social structure, mating system, group size and composition, range of locomotor patterns, dietary selection, sleeping places, nocturnality vs. diurnality, sedentary vs. mobile activity, reproduction, age at sexual maturity, seasonality, prenatal care, and communication.

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Social structure in NHPs

Most primates live in stable groups, although the size and structure of the group varies among species. There are few similarities in social structure that mirror the taxonomy of NHP groups; for example, such widely diversified species as the tarsiers, a couple of lemur species, and the orangutan exhibit the noyau social system in which individuals are generally solitary and congregate periodically into larger groups in overlapping territories. The orangutan (Pongo pygmaeus) is the only diurnal primate that leads a solitary lifestyle.{4048} 

In contrast, other primates form strong monogamous pairs and live in family groups. Titis (Callicebus), Aotus , indris, diurnal lemurs, De Brazza's monkey (Cercopithecus neglectus), and Hylobates live this way. The pairs are very territorial, with noisy inter-group interactions. Gibbon pairs (Hylobates) engage in a form of territorial vocalization known as "duetting", highly melodious and individualized calling used as an early warning of an intruder.{4048}

De Brazza's monkey (Cercopithecus neglectus) is the only cercopithecine known to be monogamous.  They are seriously endangered in Kenya.{4048}  

As primate groups increase in size, group dynamics become more complex. There are two categories of groups: one-male groups and large bisexual groups. In one-male groups, mating is thought to be restricted to the single male, even if subordinate males are present in the group. Erythrocebus patas, red-tailed monkeys (Cercopithecus ascanius) and the gentle monkey (C. mitis) are one-male group formers, as are squirrel monkeys (Saimiri), howlers (Alouatta), Colobus, and the gorilla. All-male groups of the extras may form up. There is strong competition on the part of the males for the females, with takeovers every few years and infanticide when a new male succeeds. 

Groups composed of both sexes fall into two types: fission-fusion societies such as those of the spider monkeys (Ateles) and chimpanzees (Pan) and harems or one-male subgroups, such as those of hamadryas and gelada baboons and drills. Macaques form large groups composed of many males and females, with rigid matrilineal hierarchy and emigration of young males. In fission-fusion species the community is formed of a group of related males which forage and groom together and patrol a range of unrelated females and their young which are largely independent. Males associate with females only for mating.{4048}  

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PWB plans should have as goals the following:

1.      social companionship;

2.      opportunities to engage in behaviors related to foraging, exploration and other appropriate activities;

3.      housing that permits suitable postural and locomotor expressions;

4.      freedom from unnecessary pain and distress. {3563}

Social companionship enables monkeys to groom, play, huddle together while sleeping, and display normal sexual behavior. Variation in the environment, challenge and control are also present in social situations. However, attempts to pair or group animals are fraught with difficulties and must be done with great care to avoid injuring the animals. The ability to separate animals if they fight must be planned in advance. Even animals that have been housed in groups for a long time may suddenly become aggressive. Close observation may detect the onset of hostility in time to prevent fighting. For example, chasing, threatening, and avoidance usually increase before the first fight starts. Some animals may spend more time than usual hiding. {3563}

Aggression in groups of macaques may be minimized by: (CL Davis 2001)

Restraint must be as brief as possible and used with care. Many primates can be trained to cooperate with routine procedures. Examples include entering transfer boxes, presenting limbs for venipuncture, and presenting the rear end for vaginal swabbing or IM injection. The desired response should be made clear to the animal to ensure success; for example, if one is trying to get an animal to go through a door, wait until the animal visually fixes on the door before encouraging the animal to move. Training should proceed in stages with attainable goals reached at each session. The trainer should move quietly and deliberately, and it helps if one wears distinctive clothing to allow the animals to associate with the person.

Species-typical activities vary tremendously. Along with knowing what the species’ normal habits are, an understanding of the time budget devoted to foraging, eating, sleeping, and activity is needed. The animal’s prior history must be taken into account, particularly if it was hand-reared. The concept of control (synonymous with work) is involved with species-typical activities; for example, hiding food items in wood chips allows animals to decide when to perform foraging. Animals can make use of devices such as manipulable objects, foraging apparatuses, or cage furniture. Texture, shape, and color may help to sustain an animal’s interest. Species that scent-mark (especially callitrichids and prosimians) should be allowed to do so, with sanitation performed in a rotational manner so as to leave some marked furnishings alone when others are changed.{3563}

Housing must provide sufficient space and furnishings and be placed in a manner to support basic locomotor patterns. If it is not stressful for the species, the cage walls should be as open as possible, i.e. made of mesh, bars or clear glass or plastic. Primates that continually threaten each other should be moved out of visual range. A nest box allows animals to seek privacy. An animal room that is pleasing to the animal care staff (i.e. bare walls, tidy floors and minimal odors) are not necessarily conducive to the well-being of the animals who live there. Some species need to chew on wood or other material, while others need to scent-mark their furniture. If these items are replaced when they become excessively worn or dirty they should be provided to the animals. Similarly, some animals may enjoy mirrors, while others (chimps) may find them a threat.{3563}

Chronic self-injurious behavior that causes tissue damage is troubling and requires intervention. It is most frequently reported among adult male macaques housed individually. It may be an example of redirection, characterized by the direction of an act toward a different target from the one that elicited it. In a singly-housed animal the stimulus is probably out of reach, i.e. another male nearby. Guanfacine, an alpha-2A adrenergic agonist drug used to treat children with ADHD, has been successfully used to control severe self-injurious behavior in two rhesus macaques and a baboon. A dose of 0.5mg/kg twice daily orally halted all self-biting without any overt side effects. The mechanism of action is unknown but may be related to strengthened prefrontal cortex inhibitory functions.{4213}

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Suggested Plan for PWB

According to the Committee on Well-Being of Nonhuman Primates, the following should be included in the institutional plan for PWB.

1. Statements of goals
2. Pertinent information on the natural history and behavioral ecology of each species; environmental enrichment, animal records
3. Social interactions, such as pair housing, positive interactions with people
4. Environmental enrichment techniques
5. Special considerations: strategies for unusual situations such as hyperaggressive animals, veterinary care, tethered animals, very old and very young
6. Monitoring: assessment of PWB, such as daily physical health and behavioral monitoring; methods of remediation

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©1999, Janet Becker Rodgers, DVM, MS, DipACLAM, MRCVS

All rights reserved.

Comments? Send an email to janet.rodgers@vet.ox.ac.uk