Social enhancement for caged rhesus macaques


Animate enrichment provides compatible companionship
for the expression of non-injurious social behavior



Photos 11 & 12: Housing nonhuman primates in groups would be the ideal way of social enhancement (photo 11), but there can be serious problems associated it.
Overt aggressive conflicts are rather common in groups kept in research laboratories (photo 12). Referring to rhesus macaques, Rolland [1991] makes the following observation: "By far the most common physical problem that I treat as a clinical veterinarian is trauma sustained by macaques in group-housing situations. This occurs even when no changes have been made within a previously compatible group [e.g., Reinhardt et al., 1987a; Judge et al., 1994]. The incidence of traumatic injuries is increased when new groups are formed [e.g., Bernstein & Gordon, 1977; Line et al., 1990a; Reinhardt, 1991a; Clarke & Blanchard, 1994; Westergaard et al., 1999] or when animals have to be removed and reintroduced into a group [e.g., Southwick, 1967; Bernstein et al., 1974] for medical reasons, as inevitably occurs. Trauma may range from superficial abrasions to multiple wounds and lacerations, sometimes leading to life-threatening loss of blood and shock." During an eight-month period, "there were 57 injuries requiring removal from group housing and treatment in the clinic in our group-housed, timed mating colony of about 120 females." Mortality caused by fighting may occur at a rate of 10 or even more deaths per 100 group members per year [Kaplan et al., 1980; Kessler et al., 1985].



Photo 13: Are rhesus macaques really so aggressive?
Probably not, because the species thrives in groups under natural living conditions [Southwick et al., 1965; Lindberg, 1971].
It is us who create the problem, by forcing the animals to live in a confined, inadequately structured environment which is bound to provoke conflicts. Moreover, personnel often is lacking the time, the administrative authority - to guarantee optimal group stability - and the knowledge to manage group-housed animals in accordance with ethological principles.

Photo 14*: Housing rhesus in pairs is a relatively safe alternative to group-housing.

"To enhance the life-style of a primate, one of the most effective, but often over-looked improvements is pair housing" [Rosenberg & Kesel, 1994].

"Little risk and no extra financial burdens are involved in enriching the barren environment of singly caged rhesus monkeys by carefully socializing them with each other or with surplus infants from breeding troops" [Reinhardt, 1987].


Photo 15: Adults - both females and males - are normally inhibited to show overt aggression against young animals who are not older than 18 months. This makes it possibly to introduce naturally weaned, surplus infants to individually caged adults without undue risk [Reinhardt et al., 1987b; cf. Redican & Mitchell, 1973].
Here, 12-year old George protectively holding his 13-month old companion Billy shortly after pair formation [Reinhardt, 1991b].

In a study with 13 adult male/infant pairs, partners were compatible in 92% of cases throughout a one-year follow-up period [Reinhardt, 1994a].

Partners devote much of their time grooming each other and playing with each other [Reinhardt & Dodsworth, 1989].




Photos 16 & 17: Adult rhesus males have a particularly bad reputation for being unpredictably vicious [Wickings & Nieschlag, 1980]. The idea of pairing them with infants originated from the observation that males of breeding troops never injure infants but rather don't hesitate to cradle them (photo 16: 13-year old male with infant) and carry them around (photo 17: 5-year old male with infant) in a remarkably gentle manner [cf. Capitanio & Taub, 1992].



Photo 18: Gina, an adult female rhesus huddling with her companion Gregg shortly after pair formation [Reinhardt, 1987].

In a study with 65 adult female/infant pairs, partners were compatible in 94% of cases throughout a one-year follow-up period [Reinhardt, 1994a].



Photos 19 & 20*: Pair-housing and active research
(photo 19: remote infusion-and-blood-collection-study requiring the tethering of the adult partner;
photo 20: young partner with headcap implant for neureophysiological studies)
do not exclude each other [Reinhardt et al., 1989a; Reinhardt, 1991b].



Photo 21*: The presence of the compatible partner in a "companion cage" has a reassuring, protective effect under stress [Bovard, 1959; Mason, 1960; Coe et al., 1982; Gonzalez et al., 1982; Miller et al. 1986; Reinhardt et al., 1989a; Coelho et al., 1991; Cohen et al., 1992; Gust et al., 1994].
This is particularly valuable in the laboratory setting, where the animals are often subjected to disturbing husbandry and frightening experimental procedures – such as chair
 restraint in this photo – which may trigger fear and stress reactions, thereby introducing  uncontrolled variables into research data [Line et al., 1991a; Reinhardt, 1992a; cf. Brockway et al., 1993].

Adult-infant pair compatibility is long-lasting



Photos 22 & 23: Ulla with her infant companion Uta on the day of pair formation (photo 22), and three years later when Uta is five months pregnant (photo 23). Sharing food (photo 23) is a reliable sign of partner compatibility.





Photos 24 & 25: Bruce with his infant companion Bill a few days after pair formation (photo 24), and three years later when Bill is four years old (photo 25).


 Photo 26: Pair formation protocol for previously single-caged adult rhesus macaques

While individually caged adults readily accept juveniles as companions, adult conspecifics are likely to trigger overt aggression [Southwick et al., 1974; Line, 1987]. This xenophobic response is often used as a warning against pair formation. Coe [1991] for example, makes the following prediction: "Especially when new pairs are formed and dominance relationships are being established, there is a strong likelihood that the veterinarian will be kept quite busy suturing wounds." Rosenberg & Kesel [1994] make a similar assertion cautioning that "when adult rhesus monkeys are first paired ... there are always injuries incurred."

It would contradict basic ethological principles to put two strange rhesus in a cage and wait for the predictable, possibly injurious fight over dominance [e.g., Maxim, 1976].
Why not allow two strangers to first establish their dominance-subordination relationship without risk of injuring each other during a non-contact familiarization period? They will not have to fight 'again' over dominance but rather can engage in affiliative social interaction when being transferred to a new home cage [Reinhardt, 1988].



Photos 27 & 28: Two adult male rhesus macaques in a double cage with grated partition (photo 27) allowing non-contact familiarization. Partners can see but not touch each other (photo 28). In most cases they will establish a clear-cut dominance-subordination relationship without injuring each other within 24 hours [Reinhardt, 1989a,1994a].


How do you know that two animals
have established a dominance-subordination relationship?




Photos 29 & 30: (1) Looking away (photo 29) and grinning (photo 30) are shown in an unidirectional manner by the subordinate partner.




Photos 31 & 32: (2) grimacing (photo 31) and moving out of the way (photo 32) are shown in an unidirectional manner by the subordinate partner.




Photos 33 & 34: (3) Staring (photo 33) and threatening (photo 34) are not reliable signs for an established dominance-subordination relationship. These gestures often occur in a
bidirectional manner and may serve as a mere bluff.



Photos 35* & 36: Once two potential partners have established their dominance-subordination relationship during the familiarization period (photo 35), they can be introduced in a different double cage [to avoid potential territorial antagonism: Reinhardt et al. 1987; Niemeyer et al., 1998] where everything is strange except the familiar partner (photo 36: Donna and Cathy hugging each other shortly after introduction).

  Photo 37*: Peter and Moon engage in allogrooming shortly after pair formation [Reinhardt, 1989a].
They have no reason to fight because they were given the opportunity to establish their dominance-subordination relationship in a harmless manner prior to introduction.

In a study with 154 females and 40 males, pair formation after pre-establishment of rank relations was accompanied by fighting in 'only' 2 (2.6%) of the 77 female pairs and in none (0%) of the 20 male pairs [Reinhardt, 1994a].




Photos 38* & 39*: This pair formation technique has been applied with similar success in stump-tailed (Macaca arctoides; photo 38, Reinhardt, 1994b),
long-tailed (M. fascicularis; Asvestas, 1989; Lynch, 1998; photo 39 by Richard Lynch, AstraZenaca)
and pig-tailed macaques (M. nemestrina; Byrum & St. Claire, 1998).


How do you know that two partners are compatible?

(1) There is no serious wounding,
(2) none of them monopolizes food,
(3) none of them shows signs of depression,
(4) the dominance-subordination relationship between the two is unequivocal.

(5) Affiliative interactions are not reliable indicators that two animals are compatible.

Photo 40*: Two rhesus males who were reared in partial social isolation; they show their compatibility by sharing two apples [Reinhardt, 1990a].

  Photo 41: In a study with 77 female and 20 male pairs, partners were compatible throughout a one-year follow-up period in 88% of the female pairs
and in 80% of the male pairs [Reinhardt, 1994a].

Overall, 'only' 11% (13/97) of the 97 monkey pairs were incompatible.
This figure is amazingly low when considering the fact the divorce rate in humans is about 50%.
Obviously, monkeys possess certain social skills which most humans are lacking.
Of the 194 animals tested, a total of 3 (1.5%) incurred serious, but not life-threatening injuries
in the course of the one-year study period [Reinhardt, 1994a].




Photos 42 & 43: Pair compatibility has been ascertained in many cases over long periods of time [Reinhardt, 1994a,c]. Here, the two males Moon and Peter of photo 37 sharing favored food treats six years after pair formation. Male pairs are kept in male-only areas to avoid possible sexual competition triggered by the presence of females in the same room [cf. Coe, 1991].




Photos 44 & 45: Compatible companions need social space for "social adjustments" [USDA, 1999] and the option of visual seclusion to buffer potential social tension arising from the extreme constraints of permanent cage confinement [cf. NRC, 1998].
At a minimum, pair-housed animals should be allocated at least twice the cage space that is legally required for single- housing [Reinhardt & Reinhardt, 2000a; cf. USDA, 1991].
Double cages can be created by removing the dividing panels of twin modules (e.g., photos 42 & 43), or by interconnecting two adjacent cages with a short tunnel (photos 44 & 45; cf. Bellinger et al., 1992; Baskerville, 1999).

Photo 46*: A cage divider with a passage hole close to the back (not front!) wall diminishes the risk of squabbles over food, because the two animals can retrieve food at the front of the cage without seeing – and possibly begrudging – one another. The privacy panel also reduces the subordinate partner's needs for space by making it possible to quickly get out of the dominant's sight. This avoids antagonism while fostering affili- ation [Reinhardt & Reinhardt, 1991; cf. Maninger et al., 1998; Westergaard et al., 1999].



Photos 47 & 48: Standard double cage with squeeze back, privacy panel, two feeders and two perches for pair-housed macaques [Reinhardt et al., 1991a].
Double cages are arranged horizontally - rather than vertically - to avoid that partners compete over access to the preferred vertical dimension [Reinhardt, 1992b; O'Neill-Wagner, 1994; Watson & Shively, 1996], i.e., upper section of the cage [own unpublished observations; cf. Salzen, 1989].


Photos 49* & 50*: Individually caged monkeys are paired to provide them a species-appropriate environment for the active expression of their need for social contact and social interaction. "Representing an every-changing, yet predictable stimulus, a compatible companion does not lose its boredom-reducing value over time" [Reinhardt & Dodsworth, 1989]. Here 27-year old Sissa grooming her 36-year old companion Senila 15% of the time (photo 49), while Senila spends 32% of the time grooming Sissa (photo 50) more than one year after pair formation [Reinhardt & Hurwitz, 1993; photos by Robert Dodsworth, Wisconsin Regional Primate Reseach Center].
Isosexually pair-housed rhesus macaques spent approximately 20% of the time - females more, males less [Reinhardt, 1990b; cf. stump-tailed macaques: Bernstein, 1980; long-tailed macaques: Crockett et al., 1994] - interacting and contacting each other in non-injurious species-typical manners [Ranheim & Reinhardt, 1989;
Eaton et al., 1994]. This is comparable with the situation of animals living in a natural setting [Teas et al., 1980; Chopra et al., 1992] and suggests that pair-housing offers the animals adequate conditions to meet their basic social needs.




Photos 51 & 52: Subordinate and dominant partners of compatible cage companions do not differ from each other and from single-caged subjects in terms of body weight gains – as compatibility implies that partners share food –, immune responses, serum cortisol concentration [cf. in squirrel monkeys: Coe et al., 1982; Gonzalez et al., 1982], and reproduction [Eaton et al., 1994; cf. Reinhardt et al., 1990,1991b; Reinhardt & Hurwitz, 1993; Schapiro et al., 1993]. There is, however, a conspicuous tendency for pair-housed animals to requiring veterinary treatments - in particular for diarrhea-related problems [Schapiro & Bushong, 1994] - less often than single-housed individuals [Reinhardt, 1990a]. Also, pair-housed companions engage in behavioral disorders less frequently than single-housed subjects [Goosen, 1988; Reinhardt et al., 1988; Eaton et al., 1994]. In a study of seven individually caged rhesus macaques, transfer to compatible pair-housing arrangements effectively cured the animals from the behavioral pathology of self-biting [Reinhardt, 1999a]. A similar finding has also been reported in five long-tailed macaques [Line et al., 1990b], substantiating the assumption that "prolonged individual housing is probably an influential factor" for "self-directed biting' [NRC, 1998].




Photos 53* & 54: Housing rhesus macaques in pairs rather than singly does not interfere with common husbandry procedures such as capture [Reinhardt, 1992c].




Photos 55* & 56*: Housing rhesus macaques in pairs (photo 55: female pair; photo 56: male pair) does interfere with common handling procedures such as injection or blood collection [Reinhardt et al., 1989b].

  Photo 57*: Housing rhesus macaques in pairs does not interfere with experimental manipulations such as headcap implantation [Reinhardt, 1991c].

If one partner has to be chair-restrained, the companion comes along to buffer fear and stress reactions (cf. photo 21).




Photos 58* & 59: Housing rhesus macaques in pairs rather than singly does not interfere with time-mated breeding programs [Reinhardt et al., 1989b]. Max and Ray, for example (photo 58), are compatible cage companions since more than 10 years regardless of the fact that Ray (left) has been used as breeder since all these years while Max was assigned to various physiological projects.

Raising offspring does not affect the compatibility of female pairs [Reinhardt & Dodsworth, 1989;
Reinhardt, 1994c]. Here time-mated Beta (left) holding her baby while sharing apples with her cage companion Little (photo 59); Beta and Little are living together as a pair since three years.




Photo 60 & 61: During controlled food-intake studies partners are separated with a grated cage dividing panel or grooming-contact bars [Crockett et al., 1997; Crockett, 1998, Figure 2]
– allowing continuous non-contact communication (photo 60) –
during the day and reunited during the night (photo 61).

"An important, and often neglected, source of social enrichment, especially when animals must be isolated from conspecifics, is attention from caretakers and technicians" [Reese, 1991].

"It is not an overstatement to say the right technician instills qualities in the animals that make them better and more reliable research subjects. Stress [and fear], on the other hand, leads to profound physiological and behavioral changes that increase the variability of the data and decrease the reliability of the results. ... The caretaker or technician is at the pinnacle of a cascading series of environmental and social influences that determine the well-being of the animals. He [or she] must strive to develop a social bond with all animals. ... The bond with the caregiver conveys to an animal a quiet sense of assurance upon which coping strategies can be developed" [Wolfle, 1996].


Photo 62: A positive human-animal relationship not only might enhance the
psychological well-being of the animals [NRC, 1998] - and of the human! -
but will also facilitate routine and experimental procedures.




Photos 63 & 64: Rhesus macaques often show fear and defense responses – reflected in significant changes in 'normal' physiology [Malinow et al., 1974; Line et al., 1989a] – when personnel is around (photo 63) and tries to remove them from their cages (photo 64). It is not uncommon that monkeys 'freak out' when somebody enters their room and approaches a cage [cf. Arluke & Sanders, 1996]. Such reactions are the result of repeated, negative experiences with people [cf. T-W-Fiennes, 1972] and can, therefore, readily be overcome through consistently positive, species-adjusted manners and interactions.

"The performance of an animal during an experiment depends very much on its confidence in man, something which has to be developed. ... It is therefore recommended that frequent contact should be maintained so that the animals become familiar with human presence and activity. Where appropriate, time should be set aside for talking, handling and grooming. The staff should be sympathetic, gentle and firm when associating with the animals" [European Economic Community 1986; cf. Home Office, 1989].

"Interactions between human and nonhuman primates can be made less stressful by ... familiarity with handlers and researchers through positive interactions outside [emphasis added by authors] the handling context. ... Most monkeys respond appropriately to consistent considerate treatment but can be quite dangerous when teased, tricked, or bullied. ... Well-trained and motivated caregivers can provide an enormous difference in reducing the stress of the animals" [NRC, 1998].


  Photo 65: A positive human-animal relationship is the basic condition for successful positive reinforcement training programs. "If handled with sympathy and understanding they [laboratory primates] can become more than research tools
- even co-operative partners in experimentation" [T-W-Fiennes, 1972].




Photos 66* & 67: Training rhesus macaques to cooperate during common procedures – such as injection (photo 65) followed by positive reinforcement (photo 66) – in the familiar home cage is a very valuable and effective option of social enhancement, providing mental stimulation not only for the animal subject but also for the human handler [Reinhardt, 1992a]. The interaction between animal and personnel is now based on trust, rather than fear [Reinhardt & Dodsworth, 1989].

Successful training for injection has also been reported for baboons (Papio sp.; Levison, 1964), mandrills (Mandrillus leucophaeus; Priest, 1991a,b), chimpanzees (Pan troglodytes; Byrd, 1977), orangutans (Pongo pygmaeus; Berman & Greenblatt, 1989), and Gorillas (Gorilla gorilla; Lynn, 1997; Quisenberry, 1997; Brown, 1998).


Photos 68 & 69: Even though "rhesus monkeys in the laboratory have well-earned reputations for their aggressive response
and near-intractable disposition" [Bernstein et al., 1974],
positive reinforcement techniques can safely be used to train them for
the most common research-related procedure, namely blood collection
- from the saphenous vein (photo 67) or from the femoral vein (photo 68) –
in the familiar home cage rather than in hallways or in treatment rooms.


Several different investigators have reported of rhesus macaques who have been trained to present a limb for blood collection [Elvidge et al., 1976; Bernstein et al., 1977; Walker et al., 1982; Vertein & Reinhardt, 1989; Reinhardt, 1991d; Phillippi-Falkenstein & Clarke, 1992; Eaton et al., 1994]. Some of the reports include a step-by-step description of the actual training protocol [Vertein & Reinhardt, 1989; Reinhardt, 1991d; Phillippi-Falkenstein & Clarke, 1992].

Animals who have been trained to cooperate during blood collection – here two females –
do not show behavioral fear reactions and significant changes in hematological parameters [Verlangieri et al., 1985; Reinhardt, 1991c] and stress-sensitive hormones – e.g., cortisol, testosterone, growth hormone, prolactin – that typically occur during the traditional blood collection procedures, where the subject is forcefully restrained or anesthetized [Elvidge et al., 1976; Puri et al., 1981; Eidara et al., 1991; Fuller et al., 1984; Herndon et al., 1984; Reinhardt et al., 1991c; Reinhardt, 1992a]. "Procedures that reduce reliance on forced restraint ... are less stressful for animals and staff, safer for both, and generally more efficient" [NRC, 1998].
"The least distressing method of handling is to train the animal to co-operate in routine procedures. Advantage should be taken of the animal's ability to learn" [Home Office, 1989].

Successful training for blood collection has also been reported for long-tailed macaques (M. fascicularis; Hein et al., 1989), stump-tailed macaques (M. arctoides; Reinhardt & Cowley, 1992), Celebes macaques (M. nigra; Iliff, 1997), vervet monkeys (Cercopithecus aethips; Wall et al., 1985; Suleman et al., 1988), baboons (Papio anubis; Suleman et al., 1988), mandrills (Mandrillus leucophaeus; Priest, 1991a,b), chimpanzees (Pan troglodytes; T-W-Fiennes, 1972; McGinnis & Kraemer, 1979;
April, 1994; Laule et al., 1996), and orangutans (Pongo pygmaeus; Moore & Suedmeyer, 1997).



Photos 70* & 71*: There is no need to forcefully restrain rhesus macaques during blood collection to guarantee the safety of the handling personnel.

In fact "despite rigorous observance of all precautions, bites and scratches are frequent" [Valerio et al., 1969; cf. Zakaria et al., 1996], obviously because the fearfully resisting monkey will do everything to defend herself or himself in self-defense. At the same time, "it is only common sense ... that an animal will not respond normally if it is stressed" [Schwindaman, 1991] while data are being collected.

"The stress involved in venipuncture lies primarily in the physical restraint necessary to obtain the sample" [NRC, 1998]. Yet, it is uncommon to find descriptions of the blood collection protocol in scientific publications [Reinhardt, 1999b]. This suggests that many investigators do not recognize that the manner of collecting blood can introduce uncontrolled stress variables into research data, leading to increased data variability and, therefore, unnecessaily increasing the number of experimental animals needed to obtain statistically acceptable results [cf. Fox, 1986; Home Office, 1989; Brockway et al. 1993; Schnell & Gerber, 1997; Ödbrink & Rehbinder, 1999].


Photos 72*-74*: Practical evidence questions the conventional wisdom that "adult male rhesus monkeys are aggressive animals and very difficult to handle" and, therefore, that "experimental manipulations necessarily involve the use of restraint procedures, either chemical or physical" [Wickings & Nieschlag, 1980].
Here an adult rhesus male who has been trained with a simple positive reinforcement technique to actively cooperate during blood collection in his familiar home cage [Reinhardt, 1991d, 1996].

This procedure is absolutely safe for the handling person, because the male has
no reason to aggressively defend himself (photos 72 & 73).

Cooperation is always reinforced with a favored food reward (photo 74).

Photo 75*: Training rhesus macaques – here another adult male – to cooperate during in-home-cage venipuncture increases the validity of research data collected because it helps to avoid undue excitation and associated alteration in basal physiology of the research subject.
With the refined blood collection technique the experimental monkey can easily be handled by
one person, whereas conventional techniques usually require two or three people to control
the resisting animal (cf. photo 68 & 69; Reinhardt, 1996).


Once trained, a monkey will cooperate with any person who is experienced in working with rhesus macaques [Reinhardt, 1991d, 1992a].
It has been argued that "monkeys can be trained to offer their arms or legs for blood collection with positive reinforcement, but this requires a considerable amount of time and dedicated staff" [Hrapkiewicz et al., 1998]. It is true that dedicated staff is needed to establish and foster a trustful relationship with the animals in order to create a safe work environment for the training.
The time investment for the actual training, however, does not have to be "considerable".

In a study with 10 pair-housed and 5 single-housed adult rhesus males an average of 13 three-minute training sessions were necessary to ensure that individuals voluntarily present a leg and display no resistance during in-home-cage blood collection [Reinhardt, 1991d].
Total cumulative time spent with a male ranged from 16 to 74 minutes,
with a mean of 40 minutes (pair-housed males 39 min; single-housed males 44 min).
This report clearly describes the steps of the training procedure.



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