4.1.2.2. Grooming Opportunities

As an alternative to a social partner, Lam et al. (1991) gave three adult male long-tailed macaques a grooming cushion, consisting of a 20 x 20 x 60 cm large piece of synthetic fleece, every other day. The males would typically squat on the cage floor or sit on the perch and gently pluck at, stroke, or part small pieces of fleece with their fingers, just as they would do when grooming another monkey. This behavior was often accompanied by lip smacking. During one-hour observations, the animals spent on average 11 percent of the time grooming the cushion; there was no indication that they got tired of doing so in the course of an 11-day test period (Figure 30). A grooming cushion would probably provide suitable enrichment also for other primate species when individuals have to be caged alone for research- or health-related reasons.

Figure 30 Mean grooming activity of three single-caged male long-tailed macaques who have 60-minute access to a grooming cushion every other day (Lam et al., 1991).

Crockett et al. (1997) housed same-sex pairs of adult long-tailed macaques in double-cage units in which partners were separated by a blind panel for 19 hours daily. During the remaining five hours of the 24-hour day, they were separated by grooming-contact bars, allowing them to reach through with their arms. Of 16 female pairs tested, 100 percent were compatible and partners spent about 43 percent of the time grooming each other. Of 45 male pairs tested, 89 percent were compatible and partners spent about 7 percent of the time grooming each other (Figure 31).

The usefulness of grooming-contact bars or woven wire panels with mesh openings, large enough so that adjacent neighbors can groom each other (Coelho and Carey, 1990), has also been confirmed in adult iso- and heterosexual pairs of baboons (Coelho et al., 1991; Crockett and Heffernan, 1998) and adult heterosexual pairs of pig-tailed macaques (Crockett et al., 2001; Lee et al., 2005). Compared with other species, rhesus macaques do not adjust well to the grooming-contact housing system; paired animals show a relatively low incidence of compatibility, i.e., 16% versus 51% in pig-tailed macaques, 67% in long-tailed macaques and 64% in baboons (Crockett et al., 2006).

Figure 31 Grooming-contact bars restrict paired companions to separate sections of the cage, but allow them at the same time to engage in species-typical grooming behavior. Here two adult male long-tailed macaques (Macaca fascicularis) in grooming-contact cages at the Washington National Primate Research Center. Photo by Carolyn M. Crockett, Washington National Primate Research Center.


4.1.2.3. Foraging Opportunities

Perhaps the easiest way to allow primates to engage in food processing behavior is the daily provision of whole fruits, whole nuts and whole vegetables of the season - such as apples, bananas, oranges, grapes, ears of corn, celery, melons, pumpkins, sugar cane, etc. (Figure 32a-c). The common practice of chopping these supplemental food items deprives the animals of an opportunity to engage in a very important natural behavior. There are no published reports suggesting that the regular feeding of certain whole fruits, whole nuts or whole vegetables has any adverse side effects.

Figure 32a-c Offering caged nonhuman primates whole fruits (a), whole ears of corn (b) and peanuts in their shells (c) allows the animals to engage in species-typical food processing activities.


Numerous gadgets have been described to promote foraging in caged primates, but their actual effectiveness in promoting foraging - which does not include eating, i.e., ingesting food - for an extended period of time has been evaluated in only a few cases.

4.1.2.3.1. Food Puzzles
Murchison (1995) designed a forage feeder for macaques that replaced the freely accessible standard feeder as primary source of the animals' daily biscuit ration. Both feeders were of the same dimension, but the puzzle had four holes, each 3 cm in diameter, while the box had a 5 cm-diameter opening through which the much smaller biscuits could be directly picked up by the animals (Figure 33). During the first hour after distribution of biscuits in the food box or in the food puzzle, 20 adult female pig-tailed macaques spent on average: 1 percent (51 seconds) of the time collecting 44 biscuits from the box, versus 11 percent (400 seconds) of the time retrieving 44 biscuits from the puzzle.

 

Figure 33 Reducing the size of the access hole (right) of the standard feeder (left) is a simple option for promoting skillful food retrieval behavior in nonhuman primates. Reproduced with permission from Murchison, M.A. 1995. Forage feeder box for single animal cages. Laboratory Primate Newsletter 34(1), 1-2.

Reinhardt (1993a) re-mounted the two ordinary food boxes of eight pair-housed male rhesus macaques away from the 7.3 x 4.7 cm large opening right onto the 2.2 x 2.2-cm mesh of the front of the cages (Figure 34a,b). Skillful manipulations with the fingers were now required to maneuver each of the 4.0 x 2.4 x 1.6 cm large biscuits into the right position, break protruding parts off with the teeth or fingers and finally push-pull a biscuit through the mesh. The eight males received their daily ration of 66 biscuits in the early morning. Each pair was observed once when the ration was distributed in the ordinary food boxes, or in the two food puzzles to which the animals had first been habituated for 30 days.

Figure 34a,b Moving the ordinary food box away from the access hole (a) onto the mesh panel of the cage (b) will make it more difficult for the monkey to retrieve the food.

When the standard biscuit ration was placed in the food puzzles instead of the food boxes:

  1. The average percentage of time spent foraging during the first 30 minutes increased significantly.
  2. The average total time spent collecting/retrieving 33 biscuits per animal increased significantly (Figure 35).

 

Figure 35 Average time pair-housed adult male rhesus macaques spend foraging when their daily biscuit ration is placed in the ordinary food box mounted over the access hole (a) versus directly onto the wire mesh panel (b) of the cage (Reinhardt, 1993a).

Working for the retrieval of their daily biscuit ration had no adverse effect on the males' body weight (Reinhardt, 1993b).

Reinhardt (1993c) tested this simple puzzle under the same methodological conditions in five adult single-caged female and seven adult single-caged male stump-tailed macaques (Figure 36a-c). When the 33-biscuit standard ration was placed in the puzzles instead of the food boxes:

  1. The average percentage of time spent foraging during the first 30 minutes increased significantly:
    (a) in females from 1 to 63 percent, and
    (b) in males from 1 to 62 percent.
  2. The average time spent collecting/retrieving all 33 biscuits increased significantly:
    (a) in females from <1 to 31 minutes, and
    (b) in males from <1 to 23 minutes. The males retrieved the biscuits more quickly than the females, probably because they have stronger fingers and, therefore, can break biscuits and push them through the mesh more easily.

 Figure 36a-c Stump-tailed macaque Steve retrieves a biscuit of his daily ration through the wire mesh panel of the cage.

Foraging from the puzzle rather than collecting their daily biscuit ration from the food box did not affect the body weight development of the animals.

Glick-Bauer (1997) distributed the standard diet of an adult male cotton-top tamarin pair in the morning and again in the afternoon, either in an ordinary food dish, or in a 20 x 13 x 11 cm large plastic box with a hinged lid containing six holes 4 cm- diameter holes through which the subjects had to reach for and retrieve food items. During the first hour after food distribution, the two males spent on average:

Reinhardt (1993d) distributed the daily food ration, consisting either of 66 small bar-shaped or 32 large star-shaped biscuits, of eight pair-housed adult male rhesus macaques in their two ordinary food boxes, or on the 22 x 22 mm square mesh ceiling of the cage. The males had been habituated to both feeding options for a 12-day period. In the food box-situation, they had nothing to do but pick up one biscuit after the other; there was no effort involved. In the ceiling puzzle situation, the males had to maneuver each biscuit into the right position so that a part of it was protruding through the mesh, nibble or bite a piece off until the rest of the biscuit could be pushed with the fingers or pulled with the teeth through the mesh (Figure 37a-c). During the first four hours after biscuit distribution, the males spent on average:


Figure 37a-c Distributing the daily biscuit ration on the wire mesh ceiling of the cage, rather than in the standard open food boxes, allows macaques to engage in skillful foraging behavior. This kind of feeding enrichment is effective, yet does not cost anything.

When the biscuits were presented in the open food box, the monkeys quickly took a few in their cheek pouches and threw many of the remaining ones onto the floor of the cage while starting to eat. When the biscuits were placed on the mesh ceiling, the animals ate all the retrieved pieces directly; they never stored them in the cheek pouches nor threw them on the floor.

Bertrand et al. (1999) placed the daily biscuit rations of 12 individually housed rhesus macaques - of unspecified age and gender - for a period of two weeks, either in the ordinary freely accessible food box, in a container/puzzle mounted behind the mesh wall of the ceiling, or behind the mesh wall of the front of the cage. The two puzzles required skillful manipulations to retrieve the biscuits through the mesh. It took the animals on average about:

4.1.2.3.2. Food Dispensers
Bjone et al. (2006) exposed four adult female marmoset pairs twice daily for 20 minutes to a custom-designed feeder filled with standard food. The feeder was designed in such a way that the animals had to swing small discs to the left or right to uncover and retrieve food by reaching through little holes. The marmosets had simultaneous access to their ordinary open food bowls filled with the same food ad libitum. When given a choice between easily accessible food in a bowl and food from the food dispenser, the marmosets predominantly chose to retrieve food from the food dispenser. During six test sessions, they spent on average approximately:

Celli et al. (2003) mounted an open transparent polyethylene bottle, which was daily filled with honey, in front of the cage of three adult chimpanzee female pairs and offered the animals various materials, such as plastic brushes, wires, chopsticks and rubber tubes from which they could chose those suitable for retrieving honey from the bottle, similar to fishing for termites (Goodall, 1964) from termite mounds. During daily one-hour observations [probably right after presentation of the bottle] the animals spent on average:

The chimpanzees engaged in these foraging activities consistently over the 10-day study period.

4.1.2.3.3. Food with or on Substrate
Bryant et al. (1988) released six individually caged adult male long-tailed macaques, one animal at a time, into a playpen on four consecutive days each week for a three-week study period and recorded their behavior 30 minutes prior to and 30 minutes after transfer to the pen. The monkeys were then returned to their home cages where they received their normal food ration. The playpen was almost four times larger than the home cages and was furnished with a nylon ball, a telephone directory and a nylon rope, plus a tray placed below the grid floor of the cage, containing woodchips scattered with sunflower seeds and peanuts. The animals showed little interest in the enrichment items, but spent on average 33 percent (10 minutes) of the 30-minute observations in contact with the foraging tray, searching for and retrieving seeds and peanuts by reaching through the wire mesh of the cage floor. They increased their engagement in foraging in the course of the three-week study (Figure 38).

Figure 38 Mean foraging activity of six single-caged adult male long-tailed macaques who have daily access to a foraging tray placed beneath the mesh floor of the cage (Bryant et al., 1988).

Baumans et al. (2007) quote an animal technician who distributes wood shavings sprinkled with sunflower seeds in the catch pans of rhesus and squirrel monkeys:

Our rhesus and squirrel monkeys search with their fingers through the litter and pull the seeds through the floor grids, eat them or store them in their cheek pouches. Since we change the pans three times a week, rather than dump the bedding, we don't have any drainage problems in the rooms. This feeding enrichment technique doesn't require undue extra work time in our colony of approximately 130 monkeys. I'd say the benefit of being able to provide even a brief period of "natural" foraging behavior for our caged primates is worth the little additional time it takes to put the bedding in the pans and add a handful of seeds.

Spector et al. (1994) furnished the drop pans of 24 single-caged baboons of unspecified age and gender with 29 x 44 x 6 cm large foraging trays. Every other afternoon, a mixture of seeds, dried fruits, pieces of vegetables, alfalfa cubes, feed corn and dog biscuits was added to the tray and then covered with a thin layer of fresh hay. The baboons had to reach through the bars of the cage floor, search for food items and then retrieve them. The animals were not systematically observed, but a review of many hours of video recordings taken during two years indicates that the baboons spent 30 to 120 minutes per day foraging in these trays.

Lam et al. (1991) gave three single-caged adult male long-tailed macaques each a 20 x 20 x 60 cm large synthetic fleece cushion sprinkled with favored tidbits before the regular feeding time on alternate days. The animals would sit on the perch or squat on the cage floor, picking out food crumbles with the fingers or directly licking the fleece. During the first 60 minutes after fleece cushion distribution, the males spent on average 40 percent (24 minutes) of the time foraging in this manner. They did not lose interest in foraging from the cushion over the course of a 12-day study period.

 

Figure 39 Female rhesus macaque Boo picks up tidbits from her foraging board that is attached outside to the front rather than inside to the floor of the cage. Photo by Natasha Down.

Bayne et al. (1992a) designed a 36 x 79 cm large foraging board consisting of Plexiglas covered with artificial turf. The board was secured to the cage floor and occupied approximately one third of it. Particles of flavored food items were sprinkled daily on the turf between the regular morning and afternoon feeding. These small tidbits sift down through the 13 cm long blades of the turf, thereby inducing an animal to engage in skillful manipulations to obtain the food (Figure 39). The board was tested in eight adult single-caged male rhesus macaques. It was replenished with food particles each day, after which the animals were observed for 30 minutes. During 20 sessions distributed over six months, subjects were occupied with foraging for an average of 52 percent of the time. Over the course of the study, the males increased the amount of time spent foraging from the turf board (Figure 40).

Figure 40 Mean foraging activity of eight single-caged adult rhesus macaques who have access to a turf board replenished daily with food particles (Bayne et al., 1992).

Lutz and Farrow (1996) secured 30 x 24 cm large turf boards to the outside of the front panel of the cages of ten adult female long-tailed macaques and sprinkled sunflower seeds on the turf every morning after the animals had received their daily biscuit ration. During three weekly 30-minute observations conducted at random times over a period of eight weeks, the animals spent an average of 11 percent (206 seconds) of the time foraging from the boards. The boards were used by the animals with consistency; there was no indication that they lost interest in them over time.

Fekete et al. (2000) mounted a 15 x 41 cm large turf board inside, on a shelf of the cages of ten pair-housed adult female squirrel monkeys and sprinkled a mixture of nuts, seeds and dried fruits onto the board on 11 consecutive days, right after the normal food was distributed. During the first 20 minutes, the squirrel monkeys spent on average 36 percent (7.3 minutes) of the time foraging from the board and ingesting the food they retrieved.

Chamove and Scott (2005) placed a 29 x 13 x 12.5 cm large forage box filled with a mixture of sawdust and food items into the cages of four female and four male individually housed adult marmosets, several hours before the daily standard food ration was distributed in open bowls. Over a 13-day test period the monkeys spent 13 to 70 percent of the first hour searching for and retrieving food items from this box.

4.1.2.4. Access to the Vertical Dimension

The biologically inherent need of nonhuman primates to access the safe arboreal dimension can be met in the laboratory setting by installing resting surfaces in the animals' primary enclosures, preferentially at a height that allows the animals to retreat above eye level of humans (International Primatological Society, 1993; National Research Council, 1998; European Commission, 2002) who, after all, are natural predators for them (Figure 41).

 
Figure 41 A high perch offers caged primates a species-appropriate resting surface. Note that this male rhesus macaque shows no signs of distress while being approached by personnel; he seems to be free of anxiety or fear.

Commercial built-in perches are often placed at such a low height, i.e., less than 30 cm (e.g., Bryant et al.,1988, Figure 1A; Watson, 2002, Figure 1; Reinhardt, 2003a, Figure 1; Allentown Caging Equipment, 2002), that they no longer serve the intended purpose of providing the occupant(s) access to the vertical dimension, but rather block part of the minimum floor area that is required by the animal(s) to turn around freely without touching the perch and the side walls of the cage (Figure 42).

Figure 42 Commercial built-in perches are often placed much too low, thereby blocking part of the minimum floor area that would be required by an animal - here two individually caged baboons - to turn around freely.

In order to be useful, the resting surface (e.g., a perch or a platform) should reach from the back to the front of the cage so that an animal can:

  1. freely move or sit under it (Figure 43),
  2. retreat on it to the back of the cage during alarming situations,
  3. sit on it in the front of the cage and maintain visual contact with other animals of the room (Figures 41 & 43).

 

Figure 43 In the standard-size cage, the perch should be placed in such a way that an animal can freely turn around under it and sit on it at the front or at the back of the cage.

Clarence et al. (2006) observed four pair-housed adult female rhesus macaques who lived in 280 cm high cages, each equipped with two same-sized platforms, one mounted 200 cm the other 140 cm above the woodchip-covered ground. During 20 half-hour sessions, the animals spent on average:

Reinhardt (1990a) tested 60 pair-housed rhesus macaques who had lived for 18 months in upper-row tier standard double-cage units each furnished with two perches. The perches consisted of gray, 10 cm-diameter polyvinyl chloride (PVC) pipes that were suspended diagonally with a slope of about 15 degrees. The lower end of a pipe was attached with a chain at the front of the cage, approximately 175 cm off the ground, while the upper end rested at the junction of the back and side wall at a height of approximately 185 cm (Reinhardt, 1989b; Reinhardt, 1990b). During one-hour observation sessions, the perches were used on average:

Access to an elevated surface seems to be particularly important in the traditional double-tier caging system for animals who are caged in the bottom rack. Living close to the "unsafe" ground in the shade of the upper row, these animals receive very little light (Figure 44). Access to the vertical dimension exposes them to more light and presumably enhances their feeling of security, as they can rest at a greater distance from the ground.

 
Figure 44 Animals caged in the bottom row live much closer to the ground and in a much darker environment than animals caged in the top row. A properly installed perch enables them to sit at least a little bit higher and at a shorter distance to the light source.


Woodbeck and Reinhardt (1991) compared perch use of 28 adult female rhesus macaques who lived since two years in double-cages located either in the upper row 140 cm above the ground (n=14) or in the lower row 30 cm above the ground (n=14; Figure 44). Each cage was furnished identically with two 10 cm-diameter PVC pipes. During 30-minute test sessions, the monkeys sat on a perch on average:

While perching, the animals were located:

Reinhardt (1989) confirmed these findings in adult rhesus males who had lived for one year alone in upper-row (n=14) or lower-row cages (n=11), each furnished with a diagonally suspended 10 cm-diameter PVC pipe. During two one-hour observations, individuals caged in the bottom row sat on their perch for a significantly longer time than those caged in the top row (Figure 45).

Figure 45 Mean time spent perching by 25 single-caged adult male rhesus macaques, caged either in the bottom row (n=11) or in the top row (n=14) of the cage rack (Reinhardt, 1989b).

While perching, the animals sat in front of the cage 95 percent of the time, and in the middle and back of the cage 5 percent of the time.

Bayne et al. (1992b) observed eight adult rhesus males during eight 30-minute sessions. The animals were kept individually [presumably on the upper row] in cages that were each furnished with three enrichment devices and one galvanized steel perch of unspecified diameter, which was placed approximately 20 cm off the floor of the cage, parallel to the side wall. The males sat on their perches on average 17 percent of the time.

When rhesus macaques are given the choice of sitting in one half of a double-cage on a perch made of PVC or wood, they show no significant preference for either material (Reinhardt, 1990c).

Elevated resting surfaces can readily be installed in standard cages. Schmidt et al. (1989a) and Reinhardt and Pape (1991) developed two different designs for cages with squeeze-back walls (Figure 41). In both instances, the perch (a) runs parallel to the sides of the cage, allowing an animal to sit in the back or in the front of the cage, and (b) allows the squeeze-back mechanism to slide freely from the back to the front of the cage. The diameter of the perch is predetermined by the bar spacing or the wire mesh size of the squeeze-back in the design by Schmidt et al. (1989a) - typically about 2 cm - but not in the design by Reinhardt and Pape (1991) - typically about 10 cm (Figure 46a,b). Kenney et al. (2006) developed a perch that automatically folds flat against the side wall of the cage and can be pulled down by the animal(s) to a horizontal position, providing a ledge on which to sit or stand. The squeeze-back has to be adjusted so that it can be moved over the folded perch.

Figure 46a,b This double-cage is equipped with two perches, one squeeze-back and a privacy panel. Note that the perch in the left half of the cage does not interfere with the operation of the squeeze-back.

While caged macaques make use of and benefit from fixed elevated resting surfaces such as perches and platforms, they show little interest in swings (Dexter and Bayne, 1994). The spatial constraint of the standard cage does not allow for true swinging. When they have the choice, adult rhesus will clearly prefer sitting on a PVC pipe that is mounted onto the back and front walls rather than suspended from the ceiling of the cage (Kopecky and Reinhardt, 1991). It is probably more comfortable for a monkey to rest on a stable rather than unstable raised structure.

4.1.2.5. Environmental Enrichment

Environmental enrichment temporarily enhances well-being if it provides opportunities for the expression of behaviors that have survival value, such as foraging and retreating to the vertical dimension. There is very little evidence that environmental enrichment also helps the confined subject to cope with permanent confinement distress as reflected in serious behavioral pathologies.

It has been claimed repeatedly that self-biting and hair-pulling can be controlled to some extent with environmental enrichment (Bryant et al., 1988; Gilbert and Wrenshall, 1989; Erwin, 1991; Watson, 1992; Watson et al., 1993; Niemeyer et al., 1996; Tustin et al., 1996; Storey et al., 2000; Marshall et al., 2002; Turner and Grantham, 2002; Tully, 2003; Honess et al., 2005), but there is only one report to support this claim with scientific data. Smith et al. (2004) describe the case of an adolescent female chimpanzee who engaged in hair-pulling to the point of creating open lesions. The animal was offered large quantities of shredded paper to add opportunities for non-self-directed activities. Systematic behavioral data were collected for a 10-day period prior to the provision of enrichment, and for a three-month period during which the animal had uninterrupted access to paper. Hair-pulling decreased already on the first day when the animal received shredded paper and it continued to decrease with prolonged exposure. The chimpanzee used the paper in different ways; one of them resembled leaf-pile pulling, a behavior pattern reported in wild chimpanzees.

4.2. Separation from the Companion

Separation from and loss of a companion is a major stressor for human primates (Biondi and Picardi, 1996; Hamiel et al., 1999; Shear and Shair, 2005); there is good reason to believe that the same holds true for nonhuman primates, who like humans develop strong long-lasting bonds among each other (Chance, 1956; Chance, 1961; Chance and Jolly, 1970; Chance, 1975; de Waal and Luttrell, 1986; Fruth and Hohmann, 1998; Casanova and Garcia, 1996; Hemelrijk et al., 1999; Stopka et al., 2001; Silk, 2003; Fujisawa et al., 2004; Hermano-Silva and Lee, 2004; Smuts, 2004; Bonnie and de Waal, 2006; Duffy, 2006; Kapsalis and Johnson, 2006; Silk et al., 2006; Nakamichi and Yamada, 2007; Shibata and Ford, 2007; Watts, 2007).

4.2.1. Signs of Distress and Impaired Well-Being

Being forcefully separated from the companion is an intrinsic stressor that is reflected not only in behavioral, vocal, endocrinological and cardiovascular stress responses (Rasmussen, 1985; Hennessy, 1997; Smith and French, 1997; Watson et al., 1998; Gerber et al., 2002; McMillan et al., 2004), but subjects can be so traumatized that they react by injuriously biting themselves (Maple et al., 1973; Anonymous, 2004).

4.2.2. Alternatives to Partner Separation

4.2.2.1. Post Operative Recovery

In many facilities, protocol demands social deprivation of primates after surgery for several days, because it is commonly believed that the presence of another conspecific would jeopardize the safety and wound healing of the post-surgical subject.

Murray et al. (2002) challenged conventional wisdom and allowed 15 pair-housed female long-tailed macaques to return to their companions on the same day of vascular access port surgery once they had fully recovered from anesthesia. Change in hierarchy status, self-traumatic events, weight loss or diarrhea did not occur in any of these animals, and the incision sites healed without complication. The animals ate and drank normally and readily accepted post-operative oral medication.

Baumans et al. (2007) cite a report on a long-tailed macaque colony in which 95 percent of the animals are pair-housed:

The animals are subjected to a lot of orthopedic procedures. There have never been problems with the re-pairing of the animals after surgery. We partition the pair's cage with a transparent panel, which we remove after the treated companion has fully recovered from anesthetic effects (usually 24 hours). It has never happened that animals who had no surgery showed any negative behavioral reactions toward their temporarily probably weaker cage mates.

In a small study we compared post-op recovery of the animals when:
a) only one partner had surgery resulting in a full length cast on one of the legs,
b) both companions had the surgery, and
c) the animal, who had surgery, was kept alone for a few days.

We found that there was:

4.2.2.2. Food-Intake and Metabolic Studies

Controlled food-intake studies traditionally imply that paired animals are separated.

Reinhardt and Reinhardt (2001) install wire mesh partitions prior to food distribution. In this way, paired partners are separated in their familiar homecages, but maintain visual, olfactory and auditory contact while one or both of them are being tested (Figure 47a-c). After food intake for the day has been recorded, the dividing panel is pulled so that the two animals have full contact with each other during the night until new food is distributed the next morning.

 
Figure 47a-b For food-intake studies, paired rhesus macaques Klaus and Mark are separated in their home cage (a) with a grated cage divider (b) that is removed during the night when food intake is not assessed.

A wire mesh divider is also an option for studies requiring the collection of urine and feces. It allows cage companions to keep uninterrupted contact with each other without interfering with the collection of individual-specific urine and feces samples.

4.2.2.3. Neurophysiological Studies

Paired animals are often separated when they are assigned to neurophysiological studies requiring cranial implants.

It has been repeatedly documented that keeping compatible pairs of rhesus macaques together, after one or both partners have been instrumented with cranial implants, does not jeopardize the safety of the animals and the safety of the implants, and also does not interfere with physiological testing (Figure 48a,b; Reinhardt, et al., 1989; Reinhardt and Dodsworth,1989; Reinhardt and Reinhardt, 2002). Roberts and Platt (2005) confirmed these clinical observations in six cranial-implanted adult male rhesus macaques who lived for several years in compatible pair-housing arrangements without adverse effects on their clinical health and without adverse effects on the implants.

Figure 48a,b Pair-housed rhesus macaques Gina and Sylvia with cranial implants in their home cage (a) and during experimentation, when one partner is chair-restrained, while the other partner provides psychological support in a mobile cage (b).

Paired animals are also regularly separated when one or both of them are assigned to physiological studies requiring remote sample collection via a tether system.

Coelho and Carey (1990) designed a social-tether cage system for baboons that gives tethered cage neighbors tactile contact with each other through grated dividing panels. This system provides an advantage in that:

Socially housed baboons interact with compatible cage neighbors, while individually housed baboons attempt to shake and dismantle their cages. During the four years that the social-tether cage system was used with several hundred baboons, it never happened that neighboring baboons bit the hand or fingers of each other and they never pulled the catheter or attempted to remove or dismantle the jacket of another animal.

Figure 49a,b Tethered rhesus macaques Betty (a) and Chewy (b) with their juvenile companions Lissy and Cute during an experiment requiring remote sample collection. Note that Betty grooms Lissy who has a cranial implant (a).

In some cases, there may actually be no need to separate partners with a wire mesh panel when one of them is tethered: Reinhardt (1991c) and Reinhardt (1997) documented two cases of adult-infant rhesus macaque pairs in which the presence of the young companion did not interfere with the tethering of the adult companion for remote sample collection (Figure 49a,b).

4.3. Social Conflicts

Conflicts among otherwise compatible social partners are unavoidable. In the wild, they are relatively rare and subtle because the animals have the necessary space to get away from each other as dictated by dominance-subordinance relationships (Hall and De Vore, 1965; Southwick et al., 1965; Kummer, 1968; Van Lawick-Goodall, 1968; Chance and Jolly, 1970; Wheatley, 1999).

4.3.1. Signs of Distress

The unnatural spatial restrictions in the research lab setting does not allow nonhuman primates to maintain inter-individual social distances as needed. Overt aggressive conflicts can, therefore, be quite common. Individuals may become the target of repeated overt aggression from their cage companion. This will make them extremely anxious, intimidated and depressed, a situation that finally necessitates the separation of the two animals (Figure 50).

 
Figure 50 Adult rhesus macaque Eve is depressed because she has been repeatedly harassed by her cage mate.

Social distress is also often caused when an animal is transferred to a new housing area in which the residents constantly intimidate the newcomer (Figure 51a,b).

Figure 51a,b Rhesus macaque Kim (a) is intimidated by Bobby (b) who constantly threatens her from across the aisle.

4.3.2. Refinement

4.3.2.1. Breaking Visual Contact

Reinhardt and Reinhardt (1991) designed privacy panels for 30 adult pair-housed female rhesus macaques: A sheet of stainless steel with a passage hole divides the double-cage in such a way that the two partners have the option of accessing one of the two food boxes in a different half of the cage without being seen by each other (Figure 52a,b). With the privacy panels in place:

  1. Dominant partners no longer tried to prevent their subordinate cage mates from getting food.
  2. Companions spent more time grooming and hugging each other.
  3. The incidence of conflicts - expressed in fear-grinning, threatening, pushing and slapping - decreased.

Figure 52a,b With a privacy panel, paired rhesus males Moon and Grey spend most of the time in the same half of the cage (a; Reinhardt and Reinhardt, 1991; Basile et al., 2007), but they can break visual contact, especially when they collect biscuits from the food boxes (b).

As a consequence of these results, privacy panels were installed throughout the colony of more than 600 pair-housed rhesus macaques. Basile et al. (2007) concluded from similar findings that a privacy divider may provide a safe haven and give monkeys the ability to diffuse hostile situations before they escalate.

Ratajeski and McDonald (2005) mention a case study in which a sub-adult female long-tailed macaque pulled large amounts of hair from her caudal area and posterior thigh following relocation to a new housing room. The animal was obviously very intimidated by her new neighbors and spent much of the time clinging to the upper back wall of her cage. To alleviate the distress, a blind was installed so that the newcomer could choose to avoid visual contact with other animals of the room. This had the effect that the female's hair-pulling and clinging behavior ceased [emphasis added].

4.3.2.2. Access to the Vertical Dimension of the Enclosure

Kitchen and Martin (1996) observed five adult female-male pairs of marmosets for 20 hours distributed over 12 days (a) in their standard home cage without furniture, and (b) in their home cage equipped with three perches. Access to the perches resulted in a significant decrease in aggression (Figure 53).

Access to elevated structures is likely to moderate aggression also in other primate species as it has been shown that the provision of high perches significantly decreases aggression among group-housed mangabeys (Neveu and Deputte, 1996) and Japanese macaques (Nakamichi and Asanuma, 1998).

Figure 53 Access to elevated structures helps marmosets diffuse social tensions by allowing cage mates to quickly increase social distance as needed. Photo by Eric F. Savage on Flickr.

4.3.2.3. Careful Re-Introduction after Separation

Overt aggression among compatible cage mates is often unintentionally provoked when they are re-united after one of them has been separated for research-related reasons; the two animals don't recognize each other instantaneously and, therefore, treat each other as strangers and start fighting.

Empirical evidence indicates that this risk can be avoided by giving temporarily separated partners the chance to recognize each other first and then re-unite them. This can be accomplished by partitioning the pair's home cage with a transparent panel, and then introduce the partner who had been away into the empty section of the cage. The two companions will quickly recognize each other and treat each other accordingly when the dividing panel is removed (Reinhardt, 1992a; Jackson, 2001).

4.4. Enforced Restraint


Table of Contents