5. DISCUSSION

Distress in laboratory animals is usually unnecessary (Institute for Laboratory Animal Research, 1992, p 85).
The literature makes it clear that the distress resulting from involuntary permanent confinement in a standard barren cage can be alleviated by providing the imprisoned primate with:

5.1. Compatible Companionship

Group-housing would be the most species-appropriate refinement alternative to single-housing. Safe procedures of transferring single-caged individuals to compatible group-housing arrangements have been documented for pig-tailed macaques, long-tailed macaques, and chimpanzees. There is good reason to believe that other species, such as baboons, stump-tailed macaques, squirrel monkeys, capuchin monkeys and common marmosets can also be transferred from single-housing to compatible group-housing arrangements if basic ethological principles are applied. Attempts with rhesus macaques have so far been discouraging. This species, as probably all other non-human primates species, can readily be transferred from single- to social-housing conditions by carefully pairing adult individuals with same-sex [to avoid uncontrolled breeding] companions or with naturally weaned infant companions. Compatible pair-housing has the advantage over group-housing that individual subjects are readily accessible and that it does not interfere with common research protocols.

There is a professional consensus that
a compatible conspecific probably provides more appropriate stimulation to a captive primate than any other potential environmental enrichment factor (International Primatological Society, 1993, p 11).

National and international regulations and guidelines have incorporated this assumption in their stipulations and recommendations:

  1. Any primate housed alone will probably suffer [emphasis added] from social deprivation, the stress from which may distort processes, both physiological and behavioural (Canadian Council on Animal Care, 1984, p 165).
  2. Social interaction is paramount for well-being. Social deprivation in all its forms must be avoided. Isolation can only be justified for short [emphasis added] periods during the experimental procedure or during essential veterinary treatment (National Health and Medical Research Council, 1997, p 3 & 5).
  3. Primates are very social animals. Physical contact, such as grooming, and non-contact communication through visual, auditory, and olfactory signals are vital elements of their lives. Providing animals with a satisfactory social interaction helps to buffer against the effects of stress, reduce behavioral abnormalities, increase opportunities for exercise and helps to develop physical and social competence (Primate Research Institute, 2003, Chapter IV).
  4. Pair or group housing must be considered the norm [emphasis added]. For experimental animals, where housing in groups is not possible, keeping them in compatible pairs is a viable alternative social arrangement. Single caging should only be allowed where there is an approved protocol justification on veterinary or welfare [emphasis added] grounds (International Primatological Society, 2007, p 11).
  5. Primates should be socially housed as compatible pairs or groups. They should not be singly housed unless there is exceptional [emphasis added] scientific or veterinary justification (Medical Research Council, 2004, p 6-8).
  6. The remarkable sociality of the primate order in general is the most relevant characteristic for their humane [emphasis added] housing (United Stated Department of Agriculture, 1999, p 17).
  7. The environmental enhancement plan must [emphasis added] include specific provisions to address the social needs of nonhuman primates. (United States Department of Agriculture, 1995, §3.81(a)).
  8. Single housing should only occur if there is justification on veterinary or welfare [emphasis added]. Single housing on experimental grounds should be determined in consultation with the animal technician and with the competent person charged with advisory duties in relation to the well-being of the animals (Council of Europe, 2006, p 14).

Despite the significant importance of housing primates in a social setting rather than alone, social caging has yet to become implemented as a standard refinement practice:

Two independent surveys of primate facilities located in the United States revealed that the percentage of indoor caged macaques housed socially did not increase over a time period of nine years (Table 2). Both, in 1994 and in 2003 only about one third of the animals lived with one or several partners, while two thirds were living alone (Baker et al. 2007).
 Table 2. Percentage of indoor caged macaques housed in US facilities with one or several companions in a 1994-survey (Reinhardt, 1994) and in a 2003-survey (Baker et al., 2007)

Some primatologists have taken the side of the traditional single-caging practice, probably because any changes to the traditional housing practices could invalidate the precious historic database (Dean, 1999) and upgrading the standard caging system would require extra funds (Crockett, 1993; Crockett and Bowden, 1994).

The following arguments have been brought forth against the transfer of single-caged primates - especially rhesus macaques - to social-housing arrangements:

  1. The rhesus monkey is extremely nervous and energetic and is difficult to house. Unquestionably [emphasis added], animals involved in experiments should be housed in individual cages (Gisler et al., 1960, p 760).
  2. Any [emphasis added] plan to increase social interaction also increases the risk of injury and death. Unless they have grown up in the same social group, primates are not likely to tolerate each other when placed together as adults. Besides the risk of trauma, there are other disadvantages to allowing increased social interaction. Contact between animals may lead to greater transmission of infectious diseases (Line, 1987, p 858).
  3. 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 [emphasis added] (Coe, 1991, p 79).
  4. When adult rhesus monkeys are first paired there are always [emphasis added] injuries incurred (Rosenberg and Kesel, 1994, p. 470).
  5. The possible behavioral advantages of pair housing may be offset by the increased potential of contagious diseases, for wounding, and for undernourishment in the less dominant partner (Novak and Suomi, 1988, p 769).
  6. Pairing is not uniformly beneficial, however. The animals usually form dominance relationships, and the subordinate partner may be subject to behavioral depression or distress (Line et al., 1989, p 105).
  7. Social pairing is [emphasis added] associated with high health risks to monkeys (Morgan et al., 1998, p 168).
  8. Long-term housing with the same partner may sometimes lead to boredom, as expressed by a decline in social interaction and an increase in general passivity (Novak and Suomi, 1988, p 770).

The reviewed published data make it quite clear that nonhuman primates - including rhesus monkeys - can readily be transferred from single- to pair-housing and some species to group-housing settings if basic ethological principles are applied to minimize the risk of injurious aggression related to the establishment of dominance-subordinance relationships.

Published data also indicate that the health risks tend to decrease rather than increase when single-caged animals are transferred to compatible pair-housing arrangements. There is not one published record demonstrating that subordinate partners of compatible pairs suffer from undernourishment; this is probably due to the fact that food sharing is one criteria of partner compatibility. There is also no published case showing that long-term pair-housing with the same partner leads to boredom, with the two companions showing a decline in their motivation to interact with each other.

Being separated from each other during post-operative recovery, food-intake, metabolic and neurophysiological studies is likely to distress paired companions. The published literature offers practical guidance on how partner separation can be avoided during common research protocols without jeopardizing the safety of the animals and the scientific integrity of the study.

The transfer to compatible social-housing provides previously single-caged primates not only with a living environment that can cure them from the behavioral pathology of self-injurious biting and help them cope with potentially distressing situations, but it also enhances their general well-being by allowing them to be what they truly are: social rather than solitary animals. Living with one or several conspecifics makes it possible for the caged primate to actively express his or her biologically inherent need to engage in social behaviors.

5.2. Foraging Opportunities

The reviewed literature offers numerous options making it possible for caged primates to get more involved in food searching, food retrieving, and food processing activities, thereby allowing them, at least partially, to satisfy their biological urge to forage. The most practical, least expensive, yet effective way of feeding enrichment is the presentation of the daily food ration in such a way that the animals can work for it.

The importance of foraging opportunities for the well-being of caged nonhuman primates is underscored and clearly addressed by some professional guidelines and legal rules, while others do acknowledge foraging behavior but fail to recommend that it should be actively encouraged in captive animals.

5.3. Access to the Vertical Dimension

There is a professional and regulatory consensus that caged nonhuman primates need to have access to high structures in order to feel relatively safe:

  1. Under natural conditions, many primates spend much of their lives above ground and escape upward to avoid terrestrial threats. Therefore, these animals might perceive the presence of humans above them as particularly threatening (National Research Council, 1998, p 118).
  2. The vertical dimension of the cage is of importance and cages where the monkey is able to perch above [emphasis added] human eye level are recommended (International Primatological Society, 1993, p 11).
  3. Cages should be designed and constructed so that the space [is] enough to allow for an appropriate rest structure (Primate Research Institute, 2003, Chapter VI). Perches and three-dimensional structures should be arranged to make as much use of the available space as is possible (Primate Research Institute, 2003, Chapter IV).
  4. The volume and height of the cage are particularly important for macaques and marmosets, which flee upwards when alarmed. Their cages should be floor-to-ceiling high whenever possible, allowing the animals to move up to heights where they feel secure. Double-tiered cages should not be used since they restrict the amount of vertical space available to the animals (Medical Research Council, 2004, p 7). A two-tiered system is not recommended as these cages are usually too small. The lower tiers do not allow primates to engage in their vertical flight response, are often darker, and animals in the lower cages tend to receive less attention from attending personnel (International Primatological Society, 2007, p 12).
  5. The flight reaction of non-human primates from terrestrial predators is vertical, rather than horizontal; even the least arboreal species seek refuge in trees or on cliff faces. As a result, enclosure height should be adequate to allow the animal to perch at a sufficiently high level for it to feel secure. The minimum enclosure height for caged marmosets and tamarins is 1.5 m; the minimum enclosure height for caged squirrel monkeys, macaques, vervets and baboons is 1.8 m [emphasis added]. It is essential that the animals should be able to utilize as much of the volume as possible because, being arboreal, they occupy a three-dimensional space. To make this possible, perches and climbing structures should be provided (Council of Europe, 2006, p 42,52,54).

Access to the vertical dimension addresses the caged monkey's biological urge to retreat to and rest in the relatively safe arboreal dimension of the living quarters. Animal welfare regulations downplay the importance of elevated resting surfaces, such as perches, when they merely list these as optional examples of environmental enrichments (United States Department of Agriculture, 1995, §3.81(b)).
A high perch does not really "enrich" the environment of a caged primate but it is a necessity for the animal and, hence, should be a mandatory standard furniture of every cage in which nonhuman primates are kept. The reviewed literature attests that high perches can easily be installed both in standard and squeeze-back cages and that the animals do make consistent use of them.

5.4. Positive Reinforcement Training

It is obvious that a monkey or ape is distressed when he or she is removed from the familiar home cage, forcefully restrained and then subjected to a life threatening procedure such as injection or venipuncture. It is also obvious that a monkey or ape is less distressed or not distressed at all when he or she has been trained to cooperate, rather than resist during handling procedures. Professional guidelines and regulatory stipulations take this circumstance into consideration:

  1. Procedures that reduce reliance on forced restraint are less stressful for animals and staff, safer for both, and generally more efficient (National Research Council, 1998, p 46).
  2. Restraint procedures should only be invoked after all other less stressful procedures have been rejected as alternatives (Canadian Council on Animal Care, 1993, p 92).
  3. Physical stress, such as physical or chair restraint, most definitely affects the behavior and psychology of laboratory animals. All possible measures to reduce their incidence should be taken. Animals should be trained to be as cooperative as possible to the procedures to facilitate the rapid completion of work and to alleviate stress in both the animals and people in charge (Primate Research Institute, 2003, Chapter IV).
  4. Primates of many species can be quickly trained using positive reinforcement techniques to cooperate with a wide range of scientific, veterinary and husbandry procedures. Such training is advocated whenever possible as a less stressful alternative to traditional methods using physical restraint. Techniques that reduce or eliminate adverse effects not only benefit animal welfare but can also enhance the quality of scientific research, since suffering in animals can result in physiological changes which are, at least, likely to increase variability in experimental data and, at worst, may even invalidate the research. Restraint procedures should be used only when less stressful alternatives are not feasible (International Primatological Society, 2007, p 22).
  5. The least distressing method of handling is to train the animal to cooperate in routine procedures. Advantage should be taken of the animal's ability to learn (Home Office, 1989, p 18).
  6. Primates dislike being handled and are stressed by it; training animals to cooperate should be encouraged, as this will reduce the stress otherwise caused by handling. Training the animals is a most important aspect of husbandry, particularly in long-term studies. Training can often be employed to encourage the animals to accept minor interventions, such as blood sampling (Council of Europe, 2006, p 48).

Despite these common-sense recommendations and the published fact that primates can readily be trained to cooperate during common handling procedures, there is resistance to implement positive reinforcement training as a standard refinement practice in biomedical research institutions. The reason for this inertia of tradition is probably related to misconceptions that have been published in text books and scientific articles:

  1. All [emphasis added] monkeys are dangerous (Ackerley and Stones, 1969, p 207).
  2. Rhesus monkeys in the laboratory have well-earned reputations for their aggressive response and near-intractable disposition (Bernstein et al., 1974, p 212).
  3. Old World primates are [emphasis added] aggressive and unpredictable (IACUC Certification Coordinator, 2008, Web site).
  4. Nonhuman primates are [emphasis added] difficult and dangerous to handle (Henrickson, 1976, p 62).
  5. One of the major drawbacks to the use of nonhuman primates is that they can be difficult and even dangerous to handle. Restraint is therefore necessary [emphasis added] and desirable to protect both the investigator and the animal (Robbins et al., 1986, p 68).
  6. Primates can injure personnel severely if adequate restraint is not used. The risk of herpes virus B infection and other zoonoses transmitted by bite or scratch is minimized by appropriate restraint which may be physical or chemical or a combination of the two (Whitney et al., 1973, p 50).
  7. Adult male rhesus monkeys are [emphasis added] aggressive animals and very difficult to handle. Hence experimental manipulations necessarily involve the use of restraint procedures, either chemical or physical (Wickings and Nieschlag, 1980, p 287).
  8. Nonhuman primates, no matter how small, can be a danger to handlers. Restraint is necessary [emphasis added] to allow sample collection, drug administration or physical examination (Panneton et al., 2001, p 92).

The reviewed literature suggests that these rather sweeping statements, albeit made by scientists, are based on beliefs rather than facts. That they are taken at face value by other scientists is regrettable as it promotes one of the most important extraneous variables, namely restraint stress. It is an irony that nonhuman primates are forcefully restrained in order to protect the handling personnel, yet despite rigorous observance of all precautions, bites and scratches are frequent (Valerio et al., 1969, p 45; cf. Zakaria et al., 1996; Sotir et al., 1997) because the animals are pushed into situations in which they have no other option but defend themselves. When they have been trained to cooperate, they work with rather than against the handling personnel. Under these conditions handling procedures with primates are safe because the animals no longer have any reason to bite or scratch in self-defense.

The published reports on successful training protocols for injection, blood collection, semen collection, saliva collection, blood pressure measurement, oral drug administration, topical drug administration and weighing are encouraging. Their systematic application in the species for which they were originally developed, and their adaptation to other species will make the handling procedures with nonhuman primates more "humane" and the research data collected scientifically more valid.

 

6. CONCLUSIONS

The traditional housing and handling practices of caged primates expose the animals to unnecessary distress, which is not only an ethical concern - distress is a sign of impai red well-being - but also a scientific concern - distress is an uncontrolled variable that increases statistical variance.

It is documented in professional and scientific journals that housing and handling practices of caged nonhuman primates can be refined, without undue labor and expenses, in such a way that distress responses are minimized or avoided if basic ethological principles are applied to:

  1. address the animals' need to be with and interact with at least one compatible conspecific;
  2. structure their living quarters in species-appropriate ways;
  3. address their biologically strong motivation to forage;
  4. train them to cooperate during procedures.

With a little bit of good will and earnest concern for animal welfare and scientific methodology, the systematic implementation of Refinement for caged nonhuman primates is a practical option.

It must be remembered that the goal of Refinement is to decrease the incidence or severity of inhumane practices (Russell and Burch, 1992). The National Research Council (1985, p1) of the United States:

Is it humane and does it promote animal welfare when animals, who are known to have strong social needs, are kept alone in single-cages on a permanent basis?

Is it humane and does it promote animal welfare when animals, who show a biological vertical flight response, are permanently kept in cages without a high resting surface?

Is it humane and does it promote animal welfare when animals, who are highly motivated to engage in foraging behavior, receive their daily food ration in such a way that no effort is required to search, retrieve and process the food?

Is it humane and does it promote animal welfare when intelligent animals, who could readily learn how to cooperate, are forcefully restrained during common procedures?

 

REFERENCES


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