General Care and Psychological Well-Being
The amount and type of care required to promote the psychological well-being of nonhuman primates in captivity depend on a great number of variables, including individual animal characteristics, species, opportunities for natural social interaction, degree of confinement, purpose or goal of confinement, and projected length of confinement. All those variables will affect decisions regarding type of housing, degree of human contact, types and delivery of food, and health care. Each circumstance presents a challenge to animal care technicians, researchers, and veterinary medical staff to provide a level of care necessary both to meet the needs of the animals and to make the animals available for the intended purpose.
This chapter presents information that is applicable to any primate-care program. Chapter 4 considers the special needs of primates used for particular research purposes. Detailed information on the husbandry, nutrition, and medical care of nonhuman primates has already been published elsewhere (Bennett and others 1995; NRC 1978, 1996). The present chapter focuses on aspects of care especially pertinent to psychological well-being.
It is important to recognize the great diversity, not only among major taxa but among species within a single genus, and to acknowledge that diversity in designing animal care programs. Once the species characteristics have been identified, consideration should be given to individual differences in temperament, developmental history, sex, and age and to the fact that behavioral competence of many nonhuman primate adults depends on early experience. Pertinent aspects of those issues are discussed in the chapters that cover specific taxa.
Nonhuman primates in captivity have been maintained in varied housing conditions. Animals have been housed for many years in research facilities in individual cages that can be easily sanitized and placed in climate-controlled rooms. Indoor-outdoor runs have been used as primary housing, usually with the indoor portion engineered to protect the animals from environmental extremes (NRC 1996). Heavy-wire units originally built to store corn and often referred to as corn cribs and corrals with areas of 0.1–3.0 hectares (0.2–7.4 acres) have been used as outdoor housing. Some corrals contain structures to protect the animals from the elements; others are connected to structures that provide shelter and are used to capture the animals. Nonhuman primates have also been maintained on islands, some with areas of over 175 hectares (430 acres). Each form of housing has advantages and disadvantages.
The acceptable temperature range for primates adapted to the outdoors varies greatly. Some species, such as savanna baboons, when properly acclimated can tolerate temperatures from near freezing to over 39°C (102.2°F), whereas other species, such as pygmy marmosets, can survive only in relatively narrow temperature ranges. Regardless, primates housed outdoors should be protected from environmental extremes in ways that are appropriate to their species, age, disease status, and acclimatization. Indoor-housing temperature fluctuations should be kept within the range of 18–29°C (64–84°F) (NRC 1996; see Chapters 5–9 for species-specific information).
Efforts to provide cage size recommendations according to animal size have been frustrated by the enormous diversity of nonhuman primate lifestyles and locomotor activities. No single factor, such as body weight or size, is sufficient to specify cage designs for captive primates. A matrix of factors should be considered, including species-typical behavior, postures, locomotor activity, age of the animals, required duration of caging, and number and sex of animals to be housed in each cage. However, housing should allow the animals to exist in a state of physical and psychological well-being.
Cages should be designed to permit normal postures and locomotor activity. When not stressful (e.g., with breeding pairs of marmosets), walls should be as open as possible—e.g., consisting of mesh, glass or clear plastic, or bars—because the ability to monitor their environment visually is very important to some primates. A nest box or shelter with opaque walls will allow an animal to "hide" when it wants to be out of direct view. Cage design should minimize discomfort and risk of injury to the animals. For example, some species have anatomical features, such as long tails, that might require a taller cage than other species of the same body weight. An animal maintained for an extended period might require a larger cage so that it can partake of its normal locomotor activity. Smaller quarters might be justified case by case for quarantine, veterinary, or experimental requirements.
Individual Housing. There are both advantages and disadvantages to individual caging. The physical health of a primate might be best protected when it is maintained in a cage that can be completely sanitized. Proper sanitation has virtually eliminated many endemic diseases, such as shigellosis and salmonellosis. Individual caging also minimizes wounding due to fighting. However, some animals that previously exhibited normal behavior in social settings develop atypical patterns of activity, including self-wounding, when kept in individual cages for an extended period (Bryant and others 1988), although this period has not been defined. Similarly, some physiological measures appear to be altered in individually housed primates (Coelho and others 1991; Gonzalez and others 1982; Mendoza and Mason 1994; Mendoza and others 1991; Saltzman and others 1991; Shively and others 1989). Reinhardt and others (1991) found no differences in cortisol levels with single vs. social housing.
The ability to see, hear, and smell other primates and even touch them to a limited degree by reaching through the cage walls does not preclude the development of abnormal patterns. Extensive tactile contact with conspecifics, at times of the animals' choosing, seems to contribute substantially to psychological well-being. Other factors associated with single caging—such as reduced mobility, restricted visual field, inability to get out of sight of a nearby animal, low environmental diversity, and minimal control over or predictability of a given environment—also might influence an animal's psychological well-being. Variation by species, age, and sex and even between individual animals of the same age-sex classification in the same environment has also been reported (Suomi and Novak 1991).
Most primates are social creatures and should not be housed in a room alone except for short periods. Whenever possible, social species should be socially housed. Even in individual cages, however, nonhuman primates interact with one another, so cages should be arranged to ensure that animals within visual range are compatible. Primates that continually threaten each other should be moved out of direct visual contact. Some individual primates also appear to experience stress if they are housed close to the animal-room door or a window that exposes them to human traffic. Such animals can be moved to the back of the room away from doors and windows. Husbandry practices can also be a source of stress and should be conducted in a smooth, predictable manner that minimizes disruption and decreases extraneous noise. Cages should be cleaned in a manner that does not wet the animals (NRC 1996, pp. 42–43).
Where social opportunities are limited, environmental enrichment can take on increased importance. Environmental enrichment programs attempt to increase environmental diversity by providing manipulable objects (Bayne 1989, 1991; Brent and Belik 1997; Cardinal and Kent 1998; Line and Morgan 1991); social stimulation through interaction with known humans (Bayne and others 1993a; Wolfle 1985, 1987) through the use of mirrors (Collinge 1989; Eglash and Snowdon 1983; O'Neill-Wagner and others 1997; Platt and Thompson 1985) or
video monitors (Brent and others 1989; Rumbaugh and others 1989); increased visual stimulation (Fritz and others 1997; Reinhardt 1997c) and auditory stimulation (Morgan and others 1998); and additional foraging opportunities (Bayne and others 1992b; Murchison 1994; Reinhardt 1994a). But not all stimuli elicit interest on the part of all species or ages of animals (Line and others 1991), and some stimuli might evoke negative reactions in some species or individuals; e.g., mirrors elicit aggressive behavior in some animals, such as chimpanzees (Lambeth and Bloomsmith 1992). Furthermore, some primates rapidly habituate to many kinds of stimulation. To complicate matters, rapid habituation to manipulable objects has been noted in individually housed rhesus monkeys, whereas socially housed animals continued to manipulate objects for months after initial exposure (Novak and others 1993). Thus, environmental enrichment, although of greater importance to singly caged animals, might be more difficult to achieve in these circumstances.
Aggression directed toward the physical environment or toward the aggressor's own body is greater in small single cages than in enriched cages or social settings (Bryant and others 1988; Chamove and others 1984; Line and others 1990b; Reinhardt 1990b.) Such aggression is apparently rare in free-ranging animals, although the use of branches and other objects in aggressive displays occurs in some species of free-ranging New World and Old World monkeys and in apes. In captivity, these forms of aggression are more common in some species than others. They might be examples of what has been called redirection, which is characterized by the direction of an act toward a different target from the one that elicited it. In a singly caged animal, of course, the eliciting stimulus is generally out of reach.
Chronic self-injurious behavior that causes tissue damage is particularly troubling. Although this behavior has long been labeled "self-directed aggression," the association between aggression and self-directed biting is probably not absolute (Novak and others, in press). We therefore prefer to call it self-injurious behavior or self-directed biting. It has been most frequently reported among adult male macaque monkeys housed individually (Bayne and others 1995; Chamove and others 1984; Gilbert and Wrenshall 1989; Line and others 1990b); if it is a firmly established pattern, it is resistant to treatment. Although the causes of severe self-directed biting are poorly understood (Pond and Rush 1983), prolonged individual housing is probably an influential contributing factor. The handling of self-directed biting is an example of how the overall program or plan for the psychological well-being of an institution's nonhuman primates relates to the procedures adopted for intervention in a specific situation. As in the institution's occupational health and safety, veterinary care, and sanitation programs, there need to be standard operating procedures (SOPs) for each aspect of the program. When single housing is required and an animal exhibits self-directed biting, the SOP should detail the steps to be taken. These steps need to be based on current scientific information but accommodate flexibility in adapta-
tion to an individual animal, housing situation, and possible antecedent conditions that are at the root of the behavior. Alleviation of self-injurious behavior is frequently achieved through enrichment of the environment (Chamove and others 1984; see also the other discussions and references on this topic throughout this report) or introduction of the animal to compatible cagemates or social groups (Bernstein 1991; Line and others 1990b; Vermeer 1997; Williams and Abee 1988). If well-being cannot be achieved, euthanasia is a compassionate final option (AVMA 1993, AWIC 1990).
Group Housing. Group housing generally promotes behavioral health; primates typically exhibit a broad range of species-typical behavior when housed with other primates. But group housing increases risks of disease transmission, aggression, wounding, and food deprivation because of competition.
Various steps can be taken to minimize the risks. Food and water should be available from several locations to prevent individual animals from dominating a single source (Bloomsmith and others 1994; Maki and others 1989) and the food and water should be available in quantities sufficient to ensure that all animals receive an adequate ration. Also, shade, ancillary heat sources, and shelter should be provided so that some animals do not prohibit others from gaining access to critical resources. Likewise, environmental enrichment techniques should not incite aggressive competition over a device intended to enhance well-being (Maki and others 1989).
Disease transmission can be minimized by keeping social groups intact and introducing new animals only when necessary. (Some introductions of new animals are required in almost every colony for genetic diversity and replacement; it is critical that such introductions be handled carefully.) (See Chapter 2, "Social Companionship.") Equipment, such as transport cages, should either be dedicated to particular groups or be sanitized after use with a particular group of animals.
The risk of serious injuries caused by aggression to other animals is considerably greater in socially housed animals than in those living alone (Erwin 1979; Rolland 1991). No matter how carefully animals are selected for group living and no matter how well they have gotten along in the past, sudden outbreaks of aggression can occur and result in serious injuries (Ehardt and Bernstein 1986). Such spontaneous occurrences might be an important source of scientific information about the causes and consequences of social aggression. In any case, the facility staff has the obligation to monitor these events closely and to intervene in order to prevent serious injury to the participants. Decisions as to when and how to intervene require a considerable knowledge of the species, the particular social group, and effective techniques for dealing with serious aggression. Premature separation (e.g., before the social structure and dominance hierarchy are established) can invite renewed aggression when an animal is reintroduced.
Close observation of animals will often detect the onset of social instability long before aggression leads to injuries. For example, chasing, threatening, and
avoidance can increase before the first physical attack. Changes in established feeding orders and social relationships can also serve as warning signs. Excessive time hiding in physical structures—such as visual blinds, tunnels, barrels, and boxes—can also indicate that active intervention is required.
Social instability might be an indication that the environment lacks stimulation needed for species-specific behaviors and that enrichment is needed. Enriching the environment with perches (Bayne and others 1989, 1992a; Crockett and Bowden 1994; Shimoji and others 1993), visual breaks and hiding areas (if none exist), and foraging tasks (Bayne and others 1991; Boccia 1989; Chamove and Anderson 1979) might be successful in reducing hostility.
If combative behaviors continue after environmental complexity has been assessed and changed, various other techniques for restoring social stability should be considered. In some species, stability can be restored by removing the victim (Vermeer 1997); in other species, a new victim replaces the old. Likewise, removing an aggressor might restore harmony in one case and increase social instability in another. A victim that is removed and treated can be safely returned to some groups but not all. In some species, the longer the victim has been away, the riskier is the return. Clearly, no simple formula describes the most effective procedure for all species.
When animals repeatedly initiate biting attacks or when biting presents a potential for serious injury to personnel or other animals, dental modification should be considered. In many species, severe puncture and slashing injuries can be caused by elongated canine teeth. Extraction of canines is not advisable; these teeth are deeply rooted, and extraction places the animal at risk of structural damage to the maxillary sinuses, dental malocclusions, and periodontal disease. A better procedure is to blunt the canines (Carter and Houghton 1987; Coman and others, in press). In considering this procedure, it is well to remember that in Old World monkeys, the trailing edges of the upper canines are honed on the lower first bicuspid or premolar. Only when the canines are reduced so that they no longer project beyond the occlusal surface do they lose their potential to inflict slash and puncture injuries. The procedure is not without risk and might expose the tooth pulp chamber and result in an abscess. When required, a pulpectomy should be performed by a qualified professional and the tooth filled with dental amalgam or acrylic (Carter and Houghton 1987). That procedure, of course, does not preclude inflicting serious crushing injuries.
Aggression can be minimized by keeping social groups intact, but this is not always possible. If animals used in research protocols, or sick or injured animals, require removal for treatment, efforts should be made eventually to reintroduce them to their social group. Reintroductions often become riskier with the passage of time, although they are generally easier when an entire group is separated into single cages than when only one or two animals have been removed. All reintroductions, however, should be monitored continuously for the first hour and periodically thereafter. Introductions or reintroductions generally involve housing
unfamiliar animals nearby for a few days and observing them for the presence of combative behavior. Many descriptions of this procedure are available (for chimpanzees, Fritz 1986, 1989, 1994; for macaques, Coe 1991, Bernstein 1969, Bernstein and others 1974a, b, Crockett and others 1997, Reinhardt 1988, 1989a, 1991a; for capuchins, Cooper and others 1997; and for squirrel monkeys, Vermeer 1997).
Group housing can pose a problem in gaining access to individual subjects for testing or biomedical sampling. At least three solutions have been used: training of individual animals to enter small transfer cages, movement of animals to smaller gang cages and then to transfer cages, and the inclusion of tunnels within group enclosures so that animals can be herded into the tunnels and then moved one at a time into transfer cages (Clarke and others 1988; Knowles and others 1995; Phillippi-Falkenstein and Clarke 1992; Reinhardt 1992a; see also "Restraint and Training" later in this chapter). Those techniques are superior to techniques that require personnel to enter group pens with nets and gloves to capture specific animals. The latter procedures are stressful and dangerous to technician and animal alike. Although the limited use of nets is recommended in Chapter 6 for some small New World monkeys, we do not recommend it in general or especially for macaques, for which training to enter a transfer cage is much preferred, because it reduces the risk to personnel of exposure to bites, Circopithecine herpesvirus, and other zoonoses.
Before a social group is established, the social organization of the species under free-ranging conditions should be examined. For example, young male rhesus monkeys form associations, so pair housing of males might be successful (Reinhardt 1989a, 1994b, 1995). Adults of other species are often intolerant of members of their own sex (Coe and Rosenblum 1984; Crockett and others 1994), especially in the presence of adults of the other sex; for example, because of the natural social affiliations of squirrel monkeys, females are more readily housed together than males (see Saltzman and others 1991). Knowledge of natural sex or age-class affinities can aid in the planning of social units.
Several key elements of the housing area for social units should be addressed in either cage design or SOPs. Provision of refuges might be beneficial to prevent fighting in some species. Provision should be made for easy removal of individual animals if fighting occurs and for ready access to animals for protocol purposes or husbandry routines. The safety of facility personnel should also be a driving force behind SOPs or enclosure design for routine husbandry procedures. For example, the use of a shift or transfer cage or run might be necessary when staff enter an enclosure to perform routine tasks. Flexibility in converting social to individual housing of animals might be desirable to control feeding and to treat or examine an individual animal. The ability to partition a larger cage for short periods greatly facilitates cleaning and maintenance.
Although social housing of primates can enhance reproductive capability and development of species-typical behavior, some animals cannot be success-
fully paired or incorporated into social groups (see also Coe 1991). It might therefore be more humane to house some animals alone; these animals could find a solitary life less stressful. The forced pairing or grouping of every primate is not recommended.
Sanitation must be provided, but the procedures used to accomplish good sanitation depend on cage type and species. Sanitation, as used in this report, indicates the maintenance of conditions conducive to health and involves bedding changes, cleaning, and disinfection. Cleaning removes excessive amounts of dirt and debris, and disinfection reduces or eliminates unacceptable concentrations of microorganisms (NRC 1996, p. 42). Portable cages can be taken to a mechanical cage-washer, but built-in cages require hand washing with either brushes or high-pressure sprayers. Corrals might require spot cleaning of feces if heavily populated; otherwise, the sun should desiccate the waste products sufficiently. Wooden structures, such as perches and tree limbs, introduced into a cage need to be replaced as they become worn. Primates have a tendency to lick cage surfaces; therefore, a clean-water rinse should be used to ensure that no trace of detergents or disinfectants remains on these surfaces. Enrichment devices should be sanitized or replaced as appropriate (Bayne and others 1993a; NRC 1996).
When primates are housed outdoors, vermin control in the area is essential. Wild rodents can transmit diseases, and wild animals have been known to attack primates. The ground inside corrals should be graded to permit rainwater runoff and steps should be taken to prevent the formation of stagnant pools of water, such as placing gravel or concrete under waterers. Continuously running streams of water might provide not only drinking water but enrichment, inasmuch as some species enjoy playing in water.
Cage cleaners should always be mindful of the important role of pheromonal communication, especially for callitrichids and prosimians (Epple 1986; Epple and others 1993). Complete sanitizing of a cage can be undesirable for species in which chemical communication is important. At the very least, a few perches or a nest box should be left with odors intact when cages are cleaned. These items should be cleaned at times other than when the entire cage is to be cleaned. Because of the strong role of scents in the lives of many nonhuman primates, one should not be overconcerned about the elimination of odors in a primate room but regular cleaning of surfaces contaminated with urine and feces should be maintained.
The daily observation of all primates in a colony is an important part of a program to provide animal well-being. Caregivers should note deviations from
physical and behavioral norms for an animal, in addition to evidence of illness or injury. Lethargy in a normally active animal might be the only readily notable indication of a life-threatening condition. Unless a special diet has been prescribed to control excessive weight, caregivers should be certain that at least some food remains each day. Old food should be removed when new food is provided. It is especially important that caregivers ensure daily that all watering systems are functioning. If any animal shows less interest than usual in eating when fresh food is provided, that should be noted. A special effort should be made to check each animal in a social group, although this might not always be possible in some situations, such as in island colonies. The minimal requirements for daily care include the provision of food that is adequate in nutritional value and presented in a form that is easily consumed, the availability of potable water at all times during normal housing, and cleaning of cages in a manner and with a frequency that ensure control of disease (NRC 1996).
A balanced diet is essential to maintain the physical health of primates. The dietary requirements of a few species of primates have been defined (Knapka and others 1995; NRC 1978) and several commercial manufacturers produce dry biscuits or moist products that meet these requirements. Some primates require a diet relatively high in protein, although excessive protein might lead to kidney problems in some night monkeys (Aotus). Diets can be purchased with different percentages of protein (15–25%) as appropriate to the colony. No diet can be considered appropriate for all primates. However, vitamin C is an essential component of the primate diet. Vitamin C added to commercial feed loses potency rather quickly, depending on storage conditions. If feed is refrigerated, the vitamin will be preserved longer, but commercial feed generally should be used within 90 days of milling. Supplementation with fruits that contain vitamin C provides food variety. Primates also require vitamin D in their diets, especially when housed indoors, and New World primates require vitamin D3 supplementation (Bennett and others 1995). Because primates have diverse requirements for nutritional well-being, it might be difficult to form a balanced diet with only unprocessed natural foods. Most primates are omnivorous and cannot exist on a diet consisting only of grains, fruits, and vegetables.
All primates require regular access to water. Open watering pans or bowls can be used, but they are readily contaminated with feces, urine, and debris. If water is piped to primates housed outside, care should be taken to prevent freezing or excessive heating by the sun. Whereas most primates rapidly learn to use automatic watering devices, new animals need to learn how to use them.
Feeding can be used to provide positive behavioral stimulation as a means of enhancing primate well-being (Bayne and others 1992b; Fajzi and others 1989; NIH 1991). Variations in feeding strategies are particularly appealing because
foraging under natural conditions accounts for a substantial portion of the diurnal activity budget (Herbers 1981; Malik and Southwick 1988; Marriott 1988; Milton 1980; Strier 1987). Several foraging devices are available commercially, and many are individually designed and constructed ''in house"; these products offer a substantial range of price, ease of integration into husbandry procedures, sanitizability, and durability. Food can also be dropped into a substrate that partially obscures it from view. Feeding can present an opportunity for positive interaction between animals and caregivers (Bayne and others 1993a); however, hand feeding poses a potential hazard to personnel and therefore should be used selectively.
Earlier it was stated that routine practices minimize distress because they are predictable. But novel foods and feeding routines can be used for enrichment. They should be carefully monitored to ensure that animals are not so disturbed that they fail to consume their normal dietary intake. Novel foods, such as treats, can immediately be recognized as pleasant and need not be considered a potential source of stress.
Restraint and Training
Restraint of animals for examination and treatment might be unavoidable, but most primates resist handling. Restraint should be as brief as possible and carefully tailored to the species, training, and experience of the animals. Insufficient restraint can result in injury to handlers, and undue force can result in injury to an animal. Injuries due to excessive force are of particular concern in the handling of small animals such as squirrel monkeys and marmosets.
To reduce the stress of physical or chemical restraint, many primates can be trained for routine procedures (Reinhardt 1997d). Rhesus monkeys have been trained to enter transport cages to present a limb for injection or venipuncture (Bunyak and others 1982; Heath 1989; Reinhardt 1991b, 1997a) to cooperate in the use of vascular access ports (McCully and Godwin 1992), and to present their perineum for examination and swabbing (Bunyak and others 1982). Even singly housed savanna baboons (Turkkan and others 1989), chimpanzees (Bloomsmith and others 1994; Byrd 1977; Laule and others 1992, 1996), and group-housed monkeys (Goodwin 1997; Knowles and others 1995; Phillippi-Falkenstein and Clarke 1992; Reinhardt 1990a; Williams and Bernstein 1995) have been trained to assist with clinical procedures, such as blood collection and injections, and to move into holding pens. Such training eliminates the need to anesthetize an animal for a procedure that lasts only a few seconds, reduces the time required to obtain a sample, reduces the use of pharmacological restraint agents, and, more important, gives the animal a degree of control in the situation.
Several basic principles are common to all training procedures. First, the appropriate response needs to be apparent to the subject. For example, if an animal is required to enter a compartment from the home cage, it should have
seen and inspected the door. Experienced technicians wait until an animal visually fixates on the escape door before encouraging it to leave its home cage. Second, training should proceed in steps with attainable goals established. Once begun, it should continue until an animal has accomplished the goal for that session.
In avoidance training, an animal is encouraged to escape from or avoid something that it considers undesirable. The animal should be allowed to "escape" the threat of a net, gloved hand, or cage squeeze no matter how easily it might be caught at the time. The threat of noxious stimuli is more effective than the actual use of such stimuli. Escape from threat of restraint by a gloved hand or net is more effective than escape from restraint. The animal should be able to control the perceived threat of noxious stimuli by using an effective means of escape. Avoidance-training procedures should discontinue the aversive stimulus immediately. For example, if a squeeze-back cage is used to immobilize an animal's arm or leg for examination, the squeeze back should be released as soon as the limb is obtained; maintaining the squeeze while one examines the limb is counterproductive, in that no connection is established between presenting the limb and having restraint removed. Similarly, if resistance is rewarded by the technician's giving up, it will become even harder to overcome later the "reward" of the first experience. For example, an animal can learn that racing around a cage aimlessly can lead to withdrawal of the technician, net, or hand. Training should continue until the session's goal is achieved.
That principle also applies to positive reinforcement. If a favorite food is to be offered when an animal enters a new cage, giving the same food to a resisting animal rewards resistance rather than compliance. With patience, many animals can be trained to comply with laboratory requirements through the use of positive reinforcement alone. Reinforcement should be prompt. When an animal has complied with the desired activity, positive reinforcement (for example, food reward) should follow immediately. There should be no delay while notes are written or other activities performed.
Third, the procedure should be routine. When animals are to be handled or restrained, technicians and researchers should wear distinctive clothing, such as a different-colored laboratory coat or clothing other than what is worn for routine feeding and watering, behavioral observation, research, or any other daily activity. Although the animals might still recognize the individuals participating in the activity, the distinctive clothes separate this somewhat invasive situation from all other daily routines. Quiet, deliberate movements result in more effective cooperation than noisy, abrupt activity. Use of a routine can reduce overall stress. For example, capture of animals in a fixed order will allow animals to learn when their turn is coming and produce less stress than a varying order of capture and handling.
Fourth, animals should be allowed some latitude in performance. Each primate is an individual and can respond to a given situation idiosyncratically.
No matter how inefficient or awkward an animal's response might be, it should be accepted if it leads to the desired goal. It is futile to attempt to train all animals to a common standard. (For additional information on training of nonhuman primates to assist with routine procedures see Laule and others 1992, 1996.)
The committee does not advocate mating as a necessary component of psychological well-being, but it does recognize that many facilities breed primates. To promote the well-being of these animals, housing strategies should be based on naturally occurring mating systems. Mating patterns vary among the primates, and we summarize here what is known about the variations.
- Solitary species. Many nocturnal prosimians and orangutans (Pongo pygmaeus) lead largely solitary lives and engage in little physical contact with conspecifics other than maternal associations. Adults, however, often maintain overlapping home ranges and regularly exchange information with long-distance signals, including vocalizations and scent-markings. The term semisocial might be appropriate in classifying these species. Chemical signals are particularly important in prosimian communication (Charles-Dominique 1974). Two patterns of mating have been described in the orangutan: forced copulation and consort relationships. We recommend that a captive female be given access to the male's quarters through a door too small for the male to pass through if she refuses to join him or withdraws from him.
- Monogamous pairs. A single male and a single female typically bond in some species, such as indris, mongoose lemurs, night monkeys, titis, gibbons, and siamangs. Most of the callitrichid monkeys also appear to be monogamous under captive conditions, but their social system in the wild is more flexible than that of the aforementioned species (see Chapter 6).
- One-male groups. A single mature male lives with several adult females in several species of forest guenons, many colobine monkeys, the patas monkey, and gelada and hamadryas baboons. Their societies vary in structure; under captive conditions, multiple one-male units of gelada and hamadryas can coexist in large enclosures (see Chapter 8). Aggressive takeover of a one-male unit by a new male is sometimes associated with infant deaths. In the Hanuman langur, for example, a successful challenger might kill young infants in the group; this has been observed in chimpanzees (Alford and others 1986). Obviously, that type of male reproductive strategy has to be taken into account in the captive husbandry of species that pursue it. It is probably unwise to replace a resident langur, chimpanzee, loris, or galago male with a new male while small infants are in the group.
- Multimale groups. Multiple males and females living in a single group without permanent associations between particular males and females is representative of all major taxa—e.g., the ring-tailed and black lemurs, the ruffed
- lemur, most New World monkeys (cebids), many Old World monkeys, and the African apes—and has been used as a captive breeding strategy in some cases (Conlee and others 1996). But the details of the social organization of multimale groups vary widely. For example, in many groups, males disperse (e.g., rhesus monkeys); in others, the females transfer to other groups (e.g., chimpanzees); in some cases, both sexes disperse.
- Hand rearing. As a general rule, primates are good parents; however, as with other animals, including humans, some primates either reject their infants or encounter conditions that prevent proper infant care. Fostering or hand rearing is then possible, but providing for an infant's physical needs is far easier than providing for its social needs (Fritz and Fritz 1982, 1985). Substantial efforts will be require to provide the level of social stimulation necessary for the development of social skills in hand-reared animals. Frequent periods of interaction between young animals of similar age facilitate normal development, but continuous housing of hand-reared infants together is undesirable because it prolongs infantile behavior (Mason 1991) and might make the animals more susceptible to disease through alterations of the immune system (Gust and others 1992). Although some animals can be successfully placed with foster mothers of their own or closely-related species, many rejected infants are raised by humans. It is seldom possible under these circumstances to produce an infant with the same frequency and intensity of social contact and stimulation as provided by the natural mother and group, but every effort should be made to maximize the time that such infants are held, carried, and allowed to engage in social interactions. Inanimate surrogates and occasional contact with others will not ensure normal social development. (For additional reading on hand rearing, see Fritz and Howell 1993a; Fritz and others 1992a; Maki and others 1993; Meder 1985; O'Neill and others 1991; Reisen 1971.)
Appropriately trained and observant personnel are essential to maintaining primates in captivity. The caregivers should be knowledgeable not only about general husbandry procedures but also about the specific behavioral characteristics of the primate species for which they are responsible. Because of their contact with the animals in their care, they are often in the best position to note signs of illness, injury, or distress. Human interactions with primates can al have a profound impact on both physical and behavioral well-being (Baker 1997; Bayne and others 1993a; Miller and others 1986). For example, personnel can engage in activity that communicates negative messages to the animals, such as macaques and baboons, which can interpret a direct stare as a threat. Conversely, personnel can communicate messages that reduce animal stress, such as lip-smacking at chimpanzees or macaques.
For an enhancement program to succeed, those responsible for implementing
and monitoring it should have knowledge of and experience with nonhuman primate behavior. They should attempt to predict and prevent harm to the animals caused by social partners, or even toys, on the basis of their knowledge of their animals. They should be alert to subtle changes in behavior, noting improvements due to enrichment or declines due to illness or other stressors. Periodic training of staff to acquaint them with advances in the field is essential.
Personnel should be aware of safety precautions needed to prevent physical injuries and disease transmission between themselves and the animals. Some enrichment techniques and devices that necessitate daily setup can place a caregiver at increased risk and are inappropriate with many animals. Good judgment in these cases requires individual knowledge of the animals, and caregivers should be encouraged to interact in positive and nonthreatening ways with their animals. Personnel practices that result in frequent exposure of primates to unfamiliar caregivers can also be stressful to animals and should be avoided.
Nonhuman primates and their caregivers must be protected from exposure to hazardous agents. Appropriate protective clothing is required to prevent transmission of disease to humans and to animals, particularly when infectious agents are involved (Bennett and others 1995; CDC-NIH 1993; NRC 1997a). Whereas protective clothing does not preclude forming individual relationships between animals and personnel, the use of a standard uniform, with minimal individual variation, hinders individual identification. It is sometimes advantageous to wear attire peculiar to individual caregivers or procedures (e.g., cleaning and feeding versus handling), rather than a standard uniform. It might convey useful cues to the animals and avoid undue alarm over a potential capture every time a person enters the room. Where possible, staff should avoid barriers that hinder the development of individual relationships between nonhuman primates and the people that care for them. The committee believes that the use of masks, face shields, gloves, and special uniforms should be based on specific needs to protect against identified hazards (NRC 1997a). The intense sociality of many primates is often expressed in forming social relationships with humans (Bayne and others 1993a; Hummer and others 1969; Wolfle 1985); these relationships not only might enhance the psychological well-being of the animals but also will facilitate many routine and even unusual procedures (see "Restraint and Training" earlier in this chapter). A familiar caregiver can often encourage an escaped animal to return to its usual housing or induce an animal to accept medicated food.
Interactions between humans and nonhuman primates can be made less stressful by adherence to routine schedules and procedures, familiarity with handlers and researchers through positive interactions outside the handling context, and the use of training procedures to elicit cooperation and thus minimize force or restraint (Chambers and others 1992; Phillippi-Falkenstein and Clarke 1992; Reinhardt 1990a, 1991b, 1992a, b; Reinhardt and Cowley 1992; Vertein and
Reinhardt 1989). Procedures that reduce reliance on forced restraint and that reduce invasiveness are less stressful for animals and staff, safer for both, and generally more efficient. Using cooperative methods of data collection can lead to higher-quality results. Therefore, training animals and staff to cooperate in routine procedures can be a valuable element of a well-being program.
Veterinary care should be the responsibility of a veterinarian who has training or experience in primate medicine. The veterinarian should be responsible for medical care and should have a leadership role, with investigators and other personnel, in establishing policies and procedures with respect to husbandry, animal well-being, hazard containment, nutrition, handling, occupational health, safety, and enrichment (CDC/NIH 1993; NRC 1996). The physical and, to a large degree, behavioral well-being of primates depends on a well-considered and comprehensive program of animal care and use.
An effective preventive-medicine program is the foundation on which a healthy, successful primate colony is built. Many factors contribute to a preventive-medicine program, including husbandry procedures, facility design, quarantine and isolation procedures, and clinical care. Primates usually do not show obvious signs of disease until they are seriously ill. In clinical terms, that means that animals identified as ill are often critically ill by the time they are discovered. Therefore, prevention of disease, rather than treatment, should be the primary focus of the veterinary care program.
Quarantine is a time when emphasis is placed on identification and treatment of disease. It is also a time of stabilization, permitting animals to adjust to changes in their physical and social environment, e.g., relocation from a native environment to sudden confinement or less-dramatic changes, as from one captive environment to another. Stresses associated with such moves are usually associated with various modes and distances of transportation, unfamiliar caregiver personnel, new surroundings and caging, different types and availability of food and water, and frequently repeated testing and sampling procedures.
Much of that is unavoidable, but it is helpful to give animals as much continuity with the familiar as is possible, including sensory contact with familiar conspecifics (Coe and others 1982; Coelho and others 1991; Gust and others 1994). Incoming animals that have previously lived together as a social group should be quarantined together as space permits. Infants should be kept with their mothers. Young juveniles will also likely benefit if kept in pairs or trios after arrival. The problems of medical treatment and control of disease should be balanced against the stress of separation and arousal. Such stresses can have profound consequences, especially in younger animals, and can lead not only to behavioral depression, but to changes in endocrine, physiological, immunologi-
cal, and cognitive responses, which can exacerbate disease (Coe 1993; Gluck 1979; Goosen 1988; Gordon and others 1992; Laudenslager and others 1990).
The rigorous quarantine requirements for primates newly imported into the United States, as regulated by the Centers for Disease Control and Prevention (CDC), might limit but do not preclude attempts to provide enrichment. The relevant federal policies include foreign quarantine regulations (42 CFR Part 71.53), ebola-related filovirus infection and interim guidelines for handling nonhuman primates during transit and quarantine (CDC 1990), nonhuman primate importation (CDC 1991), and tuberculosis in imported nonhuman primates (CDC 1993). Although the purpose of the CDC-imposed quarantine is to try to detect and prevent the introduction of diseased animals that could present a threat to humans or other nonhuman primates, quarantine is also a time of stabilization and routine disease monitoring. Programs for enriched, single-cage housing or various social groupings can be initiated during quarantine and continued after the quarantine and stabilization period.
Removal of an animal from its usual housing for treatment of an illness or injury can also prove stressful. Whereas such hospitalization is not as great a change as experienced by newly arrived quarantined animals, suggestions concerning maintaining ties in quarantined animals will still apply. Very young animals might need to be removed with their mothers or some familiar companion to reduce the stress of isolation, even if the second animal requires no treatment. Whenever possible, consideration should be given to ensuring that noninfectious animals under treatment can maintain at least some sensory contact with their usual companions.