Comfortable Quarters for Nonhuman Primates in Research Institutions

Viktor Reinhardt

Animal Welfare Institute, PO Box 3650, Washington, DC 20007, USA

In the United States there are approximately 57,000 nonhuman primates kept in laboratories (United States Department of Agriculture, 2000). To safeguard their well-being and their suitability for valid scientific research the following primate-specific characteristics must be taken into consideration in the care and use of these animals.

 
Figure 1. "There is no such thing as a boring animal, rhesus or otherwise; only the conditions under which we keep them can be boring" (Mahoney, 1992, p. 36). Primates have intensive social needs; solitary confinement in a barren cage is a severe punishment for them (Sokol, 1993).

There are simple ways to provide captive primates with housing and handling conditions that address these five characteristics, thereby promoting both the well-being of the animals and the quality of research conducted with them.

Housing primates in groups is the ideal way to account for their social disposition. Conditions for long-term harmonious group-housing, however, are usually not met in research institutions. Aggression-related injury and social distress can often not be avoided when new groups are formed from previously single-housed individuals. The risk remains inherent even in established groups because of the spatial constraints set by confinement and the artificial instability of social relationships resulting from research and managerial stipulations and from health care considerations. It should be emphasized that these risks can be overcome in research facilities committed to exceptionally high animal husbandry standards (Hartner et al., 2001). Housing the animals in pairs offers a practicable alternative to group-housing. Protocols for the safe formation of compatible pairs of previously single-caged adults of the same sex have been documented for numerous species, including chimpanzees (Fritz and Fritz, 1979), baboons (Jerome and Szostak, 1987), squirrel monkeys (Gwinn, 1996), owl monkeys (Weed and Watson, 1998), marmosets (Jackson, 2001; Majolo et al., 2001) rhesus macaques (Reinhardt, 1989a), stump-tailed macaques (Reinhardt, 1994a), long-tailed macaques (Lynch, 1996), and pig-tailed macaques (Byrum and St. Claire, 1998). While adult animals need to be carefully familiarized before being introduced with each other in the same cage, there is little or no danger involved when new pairs are formed by introducing juvenile individuals with strange single-housed adults or by introducing unfamiliar juveniles with each other (Reinhardt, 1994b).

 
Figure 2. Being housed with a compatible companion –– here two male long-tailed macaques engrossed in social grooming –– is a good compromise for addressing the social needs of primates kept in research facilities. Photo by Richard Lynch, AstraZeneca, Wilmington.

Choice studies conducted with capuchin monkeys have demonstrated that the animals "value social companionship as they value food: It is a necessity, not a luxury" (Dettmer and Fragaszy, 2000, p. 303). The social companion is the one environmental enrichment option of which the caged primate never gets bored (cf., de Waal, 1992). Partners of compatible pairs spend about the same amount of time interacting with each other as wild animals do (Line et al., 1990; Reinhardt, 1990a; Brent, 1992a) `even' when they have lived together for several years (Ranheim and Reinhardt, 1989). This suggests that pair-housing is a reasonable option for addressing their social needs (Figure 2). The behavioral disorder of self-injurious biting is resistant to occupational therapy attempts (Preilowski et al., 1988; Kinsey et al., 1997; Novak et al., 1998) but can be cured by transferring the afflicted single-caged individuals to a compatible pair-housing setup (Line et al., 1990; Bushong et al., 1992; Reinhardt, 1999). Transferring single-caged individuals to compatible pair-housing not only improves their behavioral health, but it also decreases their susceptibility to physical health problems (Schapiro and Bushong, 1994), particularly to stress-related diseases (Schapiro et al., 2000). The two partners of a compatible pair do not differ from each other in terms of stress-sensitive parameters (Gonzalez et al., 1982; Reinhardt et al., 1991; Eaton et al., 1994). Rather than being a source of distress, the companion serves as a stress buffer in fear-provoking situations such as experiments requiring chair-restraint or tether-restraint (Mason, 1960; Coe et al., 1982; Coelho et al., 1991; Figure 3).

 

Figure 3. During potentially distressing experimental situations there should always be a compatible companion close by, serving as a psychological support.


The horizontally arranged double cage can provide a suitable primary enclosure for paired primates. It must be furnished with two feeders and two elevated resting sites, one in each half of the cage. A dividing panel with a passage hole close to the back wall of the cage minimizes the risk of squabbles over access to these essential resources and makes it possible for the two animals to sometimes get out of each other's sight. This avoids antagonism while fostering affiliation (Reinhardt and Reinhardt, 1991). The vertically arranged double cage does not offer suitable housing conditions because the dominant partner may monopolize the well-illuminated environment of the upper half thereby forcing the subordinate partner to spend most of the time in the dim environment of the bottom half (own unpublished observation; cf., Williams et al., 1988).

Housing primates in pairs does not interfere with husbandry procedures and common management and research protocols (Reinhardt et al., 1989; Schapiro and Bushong, 1994; Shively, 2001; Figure 4). If an animal has to be kept temporarily alone –– e.g., during intensive postoperative care or during a metabolic study –– the caging arrangement must allow the individual animal to maintain visual contact with at least one compatible conspecific (cf., Mahoney, 1992; Lindburg and Coe, 1995) to minimize the stress resulting from social deprivation (cf., Coelho et al., 1991). "We all realize that one is better off with the ups and downs of a social life than without a social life at all. Would it be any different with nonhuman primates?" (de Waal, 1992, p. 86).

 

Figure 4. Pair-housing does not jeopardize in any way the health status of animals with headcap implants.


While social contact and social interaction with another compatible conspecific is a prerequisite for the psychological and behavioral health of a primate, a trustful relationship with the attending personnel is essential for his/her well-being. Giving the animals names, rather than referring to them as numbered research objects helps to develop such a relationship (cf., Reese EP 1991; Sokol, 1992; de Waal, 1992). The compassionate and respectful attitude "conveys to the animal a quiet sense of assurance on which coping strategies can be developed for dealing with other stressful aspects of the laboratory" (Wolfle, 1987, p. 1221). The macho-type person is out of place in the animal room because s/he triggers distress reactions which will skew scientific findings even before the actual experiment has started. Typically, the animals will panic when such a person comes into their room (own unpublished observation; cf., Arluke and Sanders, 1996).

In order to provide not only a physically but also a psychologically comfortable environment, staff time must be set aside for interacting and communicating with the animals in a positive manner every day (cf., Home Office, 1989). "There should be no sharp demarcation between 'good guys' and 'bad guys.' Nonhuman primates are quick to forget, or perhaps forgive, the momentary fear or resentment they feel towards a human being who has just subjected them to an unpleasant experience if a strong bond of trust already exists with that person" (Mahoney, 1992, p. 35). The investigator, veterinarian or technician who pretends to be too busy to deal with the animals other than during experimental or clinical procedures lacks basic professional qualification.

Indoor enclosures of primates should take maximum advantage of the height of the room, allowing the installation of climbing structures and resting surfaces at different levels. Elevated structures not only increase the usable cage volume but also provide environmental enrichment by stimulating the animals to spend a major portion of their time engaged in species-typical arboreal activities. A perch can readily be installed in any cages, `even' in those that are equipped with a movable back-wall (Reinhardt and Pape, 1991; Watson, 1991). The monkey perch should be made of non-metallic, i.e., 'warm' material, and have a sufficiently large diameter so that the animal(s) can sit on it comfortably (Abee, 1985) or, as in the case of squirrel monkeys and lemurs lie flat on it with limbs dangling on either side for balance (own unpublished observation; McGivern, 1993).

The perch must be placed at a height that the animal(s) are able to sit on and under it in an unrestricted, i.e, not crouched position (Reinhardt and Reinhardt, 1999). Monkeys prefer to look out of their enclosure rather than hide in the back of it (van Wagenen, 1950; Reinhardt, 1989b). Elevated fixtures, therefore, have to be placed in such a way that the animal(s) can sit on them in a look-out position in the front of the cage (Figure 5). An adequate number of elevated sites must be provided for socially housed animals to avoid competition over access (Williams et al., 1988). When this condition is met, access to perches helps the animals to avoid social conflicts and foster affiliative relationships (Neveu and Deputte, 1996.)

 
 Figure 5. The elevated resting surface should be placed in such a way that the animal can sit on it in a look-out position.

Nonhuman primates can get extremely frightened when a person dressed in protective garb approaches them. To minimize the stress, there should be sufficiently high structures which allow the animals to show a vertical flight response and retreat to a quasi safe location above human eye level (cf., International Primatological Society, 1993; Kaumanns and Schönmann, 1997; Wakenshaw, 1999). Mobile structures such as swings and ropes are generally less preferred than fixed structures (Williams et al., 1988; Howell et al., 1997), particularly in cages that provide only the bare minimum space for postural adjustment (Kopecky and Reinhardt, 1991).

 

 

Figure 6. Placing the food on the mesh ceiling of the cage is an inexpensive but very effective way of allowing primates to engage in foraging activities.

Figure 7. The primary feeder can be transferred into a foraging device by remounting it away from the access hole. Dexterity is now required to maneuver the biscuits through the mesh covering the face of the box.


Since primates are biologically programmed to spend the major portion of their time gathering and processing food, feeding enrichment provides optimal environmental stimulation for them. The urge to forage is so strong that they will work for food even when identical food is placed right next to them (Markowitz, 1979; Evans et al., 1989; Reinhardt, 1994c). Distributing the food on the chain-link or mesh ceiling of the enclosure rather than in food boxes, troughs or on the floor is perhaps the simplest way to trigger foraging behavior for standard food and supplemental food, such as fruits, vegetables and bread (Figure 6). Depending on the size of the individual food pieces, macaques increase their foraging time more than 100-fold when their daily standard biscuit ration is placed on the mesh ceiling of their cage rather than in ordinary, freely accessible food boxes (Reinhardt, 1993a). The same effect can be achieved when the food box is remounted a few centimeters away from its access hole (Reinhardt, 1993b). Dexterity is now required to maneuver the biscuits through the mesh covering the face of the box (Figure 7). These two feeding enrichment options use structural elements of the cage, redesigned in such a way that they serve as primary feeders for the daily standard food ration. Therefore, no extra time is needed to clean them and bait them with special treats. The animals only work for food that they actually eat (Murchison, 1994; Reinhardt and Garza-Schmidt, 2000). This avoids the accumulation of spoiled foodstuff, a problem which commonly occurs with ordinary feeders, when the animals hoard food and waste part of it by dropping it on fecal material.

 
Figure 8. In their natural environment marmosets show 'tree-gouging' and 'exudate-feeding'. A simple gum- feeder can support this behavior under laboratory conditions. Photo by Katie Eckert, University of California, San Francisco. 


Marmosets and tamarins are adapted to probe for embedded food in order to extract it. Simulating a natural food-source with an artificial device stocked with gum (McGrew et al., 1986; König et al., 1987; Kelly, 1993) or baited with raisins mixed with corn cob (Molzen and French, 1989) is cheap and easy but allows the animals to engage in extensive foraging activities (Figure 8). Chimpanzees are proficient in using twigs to extract termites from logs and mounds. Simple probefeeder devices filled with sticky foods –– such as applesauce, mashed bananas, jam –– can encourage this mode of foraging in captivity (Murphy, 1976; Goodall, 1979; Nash, 1982; Maki et al., 1989; Gilloux et al., 1992; Perret et al., 1998; Figure 9).

   
Figure 9. In the wild, chimpanzees are proficient in extracting termites from logs and mounds. Probefeeders can promote this behavior in the research laboratory. Photo by Kai Perret, Allwetterzoo Münster, Germany.


Straw, woodchips, woodwool, and argilla espansa are ideal foraging substrates in the form of deep-litter on the solid floor of pens (Chamove and Anderson, 1979; Fragaszy and Adams-Curtis, 1991; Brent, 1992b; Beck, 1995; Brown et al., 1995; Riviello and Misiti, 1995; Baker, 1997) or distributed on trays mounted under the mesh floor of cages (Bryant et al., 1988; Mahoney, 1992). When mixed with seeds, grain, or other small edible items such materials promote intensive foraging behavior (Burt and Plat, 1990; Byrne and Suomi, 1991; Combette and Anderson, 1991; Grief et al., 1992; Poenisch, 1992; Figure 10). The distracting effect of this feeding enrichment technique is so strong that it reduces social antagonism in group-housed animals (Chamove et al., 1982; Boccia, 1989).

 

Figure 10. Woodchips provide an ideal foraging substrate for group-housed primates; here a group of stump-tailed macaques foraging for seeds. Photo by James R. Anderson, University of Sterling.


All captive primates should be fed daily at least one whole, medium-size fruit or vegetable (Figure 11a,b,c). The time required by animal care personnel to cut produce into small pieces can be spent in much more meaningful ways (cf., Smith et al., 1989; Kerridge, 1997). For example, portioning the daily standard food ration in several rather than a single feeding, probably does not take more time than chopping the supplemental produce for the animals, but it increases substantially the amount of time they can engage in foraging activities (cf., Taylor et al., 1997).

 

 

 
 Figure 11a,b,c. Primates deserve fresh fruit or vegetables on a daily basis. It would be a waste of time to chop the produce for the animals; they have the time and they enjoy doing it themselves.


Branch segments of dead deciduous trees –– red oak disintegrates into flakes that are so small that large quantities pass sewage drains without clogging them (Reinhardt, 1992a) –– are perfect toys for primates, stimulating not only processing but also manipulative and play activities (Figure 12). They constantly change their form and texture due to wear and dehydration and, therefore, retain their stimulatory value (Reinhardt, 1989b; Eckert et al., 2000). Commercial toys lack the natural, ever-changing texture of wood; this is probably the reason why the animals quickly lose interest in them (Crockett et al., 1989; Line et al., 1989; Hamilton, 1991; Pruetz and Bloomsmith, 1992; Kessel and Brent, 1998), unless several different toys are offered and substituted regularly with new ones (cf., Paquette and Prescott, 1988; Weick et al., 1991). Access to a variety of manipulable objects seems to be particularly beneficial for capuchins and baboons, who exhibit sustained interest in them and respond with a significant reduction in abnormal behaviors (Brent and Belik, 1997; Boinski et al., 1999).

 

Figure 12. Branch segments are perfect toys for primates. Constantly changing their texture and configuration due to wear, these wooden toys do not lose their stimulatory value over time.


A major contention is the need for proper illumination in the caging arrangement of medium- and small-sized primates. In order to minimize housing expenses, these animals are traditionally kept in two-tier cages, with one row stacked on top of another. This doubles the number of primates that can be accommodated in one room, but involves serious implications for the individual animals. Those relegated to the lower rows are restricted to a terrestrial lifestyle, unable to withdraw in alarming situations and retreat to a safe place above the human predators who periodically capture them and subject them to distressing, or even deadly procedures. Moreover, the sanitation tray, which runs the length of the room beneath the upper tier of cages, reduces significantly the amount of light that can penetrate to the lower-cage tier (Schapiro et al., 2000); "animals in the lower tier are thus relegated to a permanent state of semi-gloom" (Mahoney, 1992; p. 32). The cave-like living quarters of bottom-row caged animals is often so dim that caretakers routinely have to use flashlights to identify and inspect them (Figure 13). It has been noticed in marmosets that the housing environment of lower-row caged animals can be so poor that it results in markedly reduced fertility (Heger et al., 1986). Routinely rotating animals between bottom and top tiers (National Research Council, 1998) offers no solution to this problem. It merely "rotates" the problem by alleviating the situation for lower-row subjects, while aggravating it for the same number of upper-row subjects. At the same time it introduces the additional stress-variable associated with cage transfer (Mitchell and Gomber, 1976; Phoenix and Chambers, 1984; Crockett et al., 1993; Schapiro et al., 1997). Even if techniques can be developed to assure uniform illumination, the bottom tier cage will remain a potential source of distress whenever personnel enters the room (cf., Kaumanns and Schönmann, 1997).

 
 Figure 13. Even though it is the prevailing housing arrangement, the double-tier caging system is unacceptable both for ethical and scientific reasons.

In order to provide ethically and scientifically acceptable caging conditions, nonhuman primates must be housed in single-row cages to assure that (a) all animals receive the same quantity and quality of light, (b) all cages are of sufficient height so that occupants are in a position to retreat above animal care personnel, and (c) all animals in the room can be adequately inspected.

Training nonhuman primates to cooperate during procedures is one of the most significant options of making life a little bit more bearable for laboratory primates. It not only challenges the animals' high degree of intelligence, offers them –– and the caregivers –– some relevant distraction and eliminates data-confounding distress responses, but it also increases personnel safety by no longer giving the animals reason to defend themselves by means of biting or scratching during compulsory immobilization. To be forcefully removed from the familiar cage and subdued during painful husbandry and research procedures must, indeed, be a terribly frightening experience for a monkey or an ape. Research data collected from such an animal are tainted by the subject's stress reactions (review: Reinhardt et al., 1995) and, therefore, have questionable scientific value (Figure 14).

Figure 14. Scientific data collected from a subdued animal are skewed by the subject's fear response.


With gentle firmness, patience and positive reinforcement many primate species can be conditioned to work with –– rather than against –– personnel during common procedures such as transfer to a holding area (Goodwin, 1997; Bloomsmith et al., 1998), capture from the home cage (Reinhardt, 1992b), capture from the group (Reinhardt, 1990b,c; Kessel-Davenport and Gutierrez, 1994; Mendoza, 1999; White et al., 2000), blood collection (McGinnis and Kraemer, 1979; Reinhardt, 1991; Laule et al., 1996; Moore and Suedmeyer, 1997), blood pressure measurement (Smith and Ansevin, 1957; Mitchell et al., 1980; Turkkan, 1990), systemic injection (Spragg, 1940; Levison et al., 1964; Byrd, 1977; Priest, 1991; Reinhardt, 1992c; Figure 15a,b), urine collection (Kelly and Bramblett, 1981; Ziegler et al., 1987; Bond, 1991; Anzenberger and Gossweiler, 1993; Shideler et al., 1994), saliva collection (Bettinger, 1998; Bettinger et al., 1998), topical drug application (Reinhardt and Cowley, 1990; Segerson and Laule, 1995), oral drug application (Turrkan et al., 1989), semen collection (Brown and Loskutoff, 1998), insemination (Desmond et al., 1987), vaginal swabbing (Bunyak et al., 1992; Hernándes-López et al., 1998) and veterinary examination (Brown, 1998). The initial time investment in the training quickly pays off in: (a) a reduction of time required to obtain a sample, administer a drug or capture an animal, (b) a reduction of risks associated with defense aggression, (c) a reduction in the use of pharmacological restraint agents, (d) more reliable research data (Elvidge et al., 1976; Reinhardt, 1992c; Schnell and Gerber, 1997; National Research Council, 1998) and a more satisfactory relationship between handling personnel and research subject (Figure 16a,b,c,d).

 

 

Figure 15a,b. There is no need to forcefully restrain an animal for Ketamin injection, thereby introducing stress as an uncontrolled variable even before the actual experiment has started. Primates are intelligent and can be readily trained to cooperate during such a simple procedure.


Providing primates in research institutions with primate-adequate housing and humane handling conditions is no sentimentalism. On the contrary, it is essential to employ such refined methodology in order to adhere to the very basic principles of good science. A primate who behaves like a primate and who is free of distress, certainly has a greater potential of being a useful research model than one who is a behavioral cripple as a result of understimulation and one who experiences distress during research-related procedures.

 

 

 

Figure 16a,b,c,d. It takes less than a cumulative total of one hour to train adult male rhesus macaques to cooperate – rather than resist – during blood collection in the familiar home cage (Reinhardt, 1991).

 

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Viktor Reinhardt is Laboratory Animal Advisor to the Animal Welfare Institute in Washington, DC. He is a clinical veterinarian and ethologist and did extensive research in reproductive physiology, animal husbandry and ethology in cattle, muskox and bison.

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