Laboratory animal welfare NHPs USDA 1999a

Welfare

Primates

US Dept. of Agriculture (USDA) Animal and Plant Health Inspection Service (APHIS), Animal Care. Final Report on Environmental Enhancement to Promote the Psychological Well-Being of Nonhuman Primates. Riverdale, MD, US: Animal Care: 1999.

A. Background on Evaluation of the Performance-Based Standard for Nonhuman Primates 2
B. Team Methods 3
C. Results of Surveys and Interviews 4

A. Intent and Language of the Animal Welfare Act 7
B. Community Response 7
C. Other Nations and Societies 7
D. Difficulties Inherent in Measuring Psychological Well-being 10
E. Species-Typical Behavior (STB) 11

A. Social Grouping 17
B. Social Needs of Infants 26
C. Structure and Substrate 29
D. Foraging Opportunities 35
E. Manipulanda 41
F. Consideration of Sensory Stimulation 43
G. Consideration of Novelty and Control 47

A. References 53
B. Other Sources 85

APPENDIX A. 9 CFR SECTION 3.81
Environment Enhancement to Promote Psychological Well-Being of Nonhuman Primates 91

This report provides Animal and Plant Health Inspection Service (APHIS) Animal Care employees, the facilities they regulate, and the public with a policy on environment enhancement to promote the psychological well-being of nonhuman primates. The policy is an interpretation of the regulation published in 9 CFR, Part 3, Subpart D, §3.81. This report explains the scientific basis for the policy and how it was developed. It consists of the following:

Reviews background of the project to develop the policy: how it was initiated, the methods used, and the results of surveys and interviews.

Explains the Animal Welfare Act, the language of U.S. regulatory standards, other nations' requirements regarding primates' psychological needs, the difficulties inherent in measuring psychological well-being, and the reason why this policy relies on species-typical noninjurious behavior as the primary indicator of psychological well-being.

Introduces the concept of categories of primate behavioral needs and explains that there are environment enhancement strategies or elements that correspond to each. Gives the critical elements to be addressed in each environment enhancement plan for captive primates.

Reviews the professional literature applicable to meeting the psychological needs of captive primates. Presents the findings for each critical element and additional considerations.

Shows facts about primate species commonly found in U.S. facilities. Includes how they live in the wild and suggests options or strategies for each critical element.

A. Background on Evaluation of the Performance-Based Standard for Nonhuman Primates

Performance-based standards in Animal Care have been controversial since their inclusion in the 1985 Amendments to the Animal Welfare Act.⁽¹⁾ In 1991, when USDA, APHIS adopted Title 9 of the Code of Federal Regulations (CFR), Part 3, Subpart D, "Specifications for the Humane Handling, Care, Treatment, and Transportation of Nonhuman Primates", it included Section §3.81 called, "Environment enhancement to promote psychological well-being of nonhuman primates." (See Appendix A for the text.) After about five years, APHIS conducted an internal evaluation⁽²⁾ of the performance-based standards. It administered a brief mail survey of its Animal Care field employees about their opinions and experiences applying these standards. The survey results indicated a number of concerns regarding the effectiveness of the standards for environment enhancement of nonhuman primates.

Many of the opinions expressed by Animal Care employees in the 1996 survey centered around a lack of clarity and specificity in the standards and a perceived lack of enforceability. Almost half the responding employees felt that the criteria in the regulations were not adequate for facilities to understand how to meet them and for inspectors to judge if a facility was in compliance. About two thirds of the responding employees suggested additional criteria or items that should be in a facility's primate enhancement plan. Twelve employees proposed some specific requirements on social grouping, primary enclosure space, foraging opportunities, novelty, or other environmental features.

The 1996 study report offered some recommendations on how to improve the effectiveness of the standards, including:

As a result of these recommendations, APHIS's Animal Care Management Team assigned a team of Animal Care field employees to develop a model for primate environment enhancement and a policy for inspectors and facilities. Their goal was to retain the performance-based approach, and maintain a balance between the Agency's need for inspection practicality and enforceability and its need for flexibility and results-orientation. It is hoped that the interpretive policy developed as a result of this team's work will assist in the fair application and enforcement of the environment enhancement standard.

APHIS Animal Care's Primate Environment Enhancement Team was formed in March, 1997. It was composed of five Veterinary Medical Officers, an Animal Care Inspector, a Regional Director, a resource specialist from USDA's National Agricultural Library's Animal Welfare Information Center, the coordinator of APHIS Animal Care's Strategic Direction initiative, and an anthropologist from APHIS's Policy and Program Development. They are, alphabetically, Tim Allen, Ruth Bakker, Lisa Bellamy, Charlie Currer, Greg Gaj, Betty Goldentyer, Betsy Lyons, Natalie Roberts, Sylvia Taylor, and Dick Watkins.

From March, 1997 to March 1998, the Enhancement Team embarked on an extensive review of the professional primatology literature, a number of facility primate enhancement plans, and some enforcement case histories. Comments made by employees in the 1996 mail survey were reviewed. A number of respected professionals, knowledgeable about primates, were consulted.

During the early phase of the project, members of the Primate Environment Enhancement Team needed to understand their colleagues' opinions more clearly and in more detail than could be derived from the 1996 employee survey data. To supplement the information collected, the team members contacted 21 other Animal Care field employees who inspect primate facilities. They interviewed them regarding current conditions at the facilities they inspect that house primates. They asked what the problems are and what should be required of facilities to improve the care of primates. These in-depth interviews revealed that certain inadequate environment enhancement conditions and practices persist at regulated facilities although the 1985 amendments to the Animal Welfare Act were intended to minimize these conditions or practices. The inspectors echoed many sentiments expressed in the 1996 mail survey and called for guidance that would provide more structure and specificity and clarify the minimum quantity and quality of enrichment that will be enforceable.

In a series of conference calls and meetings, the Primate Environment Enhancement Team developed a conceptual model and a policy. Members also drafted this discussion and the supplementary materials shown in the appendices that are intended to aid inspectors and regulated parties. The Enhancement Team members circulated the draft materials for comment and revision to colleagues at the Animal Care Employees National Work Conference in Riverdale, Maryland in March, 1998, and to the Supervisory Animal Care Specialists and Animal Care Staff in August, 1998. The team tested the application of the proposed policy by visiting four facilities, and as a result, made several modifications to the policy.

In preparation for the document's release to the public for comment, it was reviewed by several members of USDA management and federal partners. Modifications were made to ensure the policy's enforceability and consistency with other policies and the report's readability and proper form. A decision was made to call the new document a "policy" rather than "guidelines", as it had been referred to up to this point. The accompanying Federal Register documents were developed.

The Team would like to acknowledge and thank many people who have contributed to the development of this document so far. Researchers, librarians, and consultants have provided copies of publications. Facilities, associations, and animal interest groups have provided background information and expressed their opinions. APHIS Animal Care inspectors and Supervisory Animal Care Specialists have reviewed earlier drafts and provided feedback. They facilitated the field visits. Other staff members in Headquarters have facilitated the clearance of the policy, assisted with production, distribution, and communications. USDA's National Agricultural Library has provided editorial advice. In particular we would like to thank: Janet Baer, Kate Baker, Mollie Bloomsmith, Sue Boinski, Linda Brent, Cobie Brinkman, Allegra Bukojemsky, John Cant, Douglas Cohn, Debra Forthman, Nelson L. Garnett, Marisa Garza Schmidt, Larry Jacobsen, Michael D. Kreger, Jean A. Larson, Barbara Lester, Trevor Poole, Viktor Reinhardt, David Seelig, and Lucy Lerner Wormser. While these individuals were very helpful in providing their input, they are in no way responsible for the text of this document or the policy, in whole or in part.

Below is a summary of issues raised in both the mail survey and telephone interviews of APHIS Animal Care employees.

1. Minimum Criteria Need Clarification

The standards in 9 CFR §3.81 emphasize the presence of a physical document called an "environment enhancement plan for primates" at each facility, but the standards contain few solid criteria on which an inspector can judge the content of the plan as "in compliance" or "out of compliance". The regulations state that the plan must address social grouping, enrichment of the physical environment, special considerations, and restraint devices, but what is required in order to address these in a minimally compliant manner is unclear. Some inspectors said they had the impression that the only legally necessary condition for compliance was the existence of the document itself, regardless of its contents. A few commented that once the facility's attending veterinarian approved a plan, it was problematic to enforce additional requirements, even if that plan was very poor.

A few inspectors expressed the concern that without adequately specified criteria and only a notion of an abstract endpoint to achieve (psychological well-being, which can not be directly or unequivocally measured), facilities are free to try, or NOT try, anything--including a very behaviorally restrictive, barren environment. No one, including inspectors, would have any basis for criticism, until there is proof of "poor performance". Unfortunately, there is no agreement on what "poor performance" looks like. There might be virtually no performance parameter or outcome that could be proven to have been caused by an inadequate environment.

2. Lack of Enforceability

APHIS Animal Care employees recognize that there is a legal question concerning the enforceability of performance standards. Some inspectors said they could recognize a plan that was not in accordance with professional literature or was not "adequate to promote psychological well-being". However, they had concerns about Agency support for particular interpretations or judgement because of the vague language and nature of the performance standard.

3. Minimalistic and One-Sided Enhancement Programs

A common refrain among inspectors was that too many enhancement programs consisted of only one or two types of enrichment, such as feeding of treats or provision with a simple rubber toy, in an otherwise barren, stimulus-poor environment. There is agreement that acceptable enhancement programs should stimulate a variety of normal activities and meet all major areas of behavioral need in a species-typical manner, rather than concentrate on a few limited aspects of behavior (Olfert et. al. 1993, Poole 1991b). Many employees supported the idea that enhancement programs be required to address several different aspects of a primate's environment and behavior, beyond the superficial breakdown given in 9 CFR §3.81 ("social", "physical", and "special"). The team received many helpful suggestions on this issue.

4. Questionable Implementation of the Facility Plans

Another problem has been the difficulty in proving actual implementation of an enhancement plan. Animal Care inspectors recommended facilities be required to provide better documentation of implementation.

5. Low Levels of Appropriate Social Grouping

Some Animal Care inspectors felt that there were too many singly housed primates. This is especially true at research facilities and among small licensed exhibitors. Inspectors who inspected public exhibits with singly housed chimpanzees said that the reasons most frequently given for housing these animals singly were that the exhibitor: preferred to have only one chimpanzee at a time; considered them more tractable when single-caged; was ill-equipped to permit socialization of one single-caged chimpanzee with another; and/or was unwilling to transfer or loan a single chimp to other facility, even one equipped to provide a socially enriched environment. All of these reasons reflect convenience for the owner(s), not primary consideration for the psychological needs of the animals.

6. Practices that Perpetuate Socially Incompetent Individuals or Abnormal Behavior

Animal Care inspectors were concerned that dealers involved in the pet trade continue to remove infants from their care-giving parent(s) at an inappropriately early age, for reasons other than medical necessity. These practices are known to produce socially incompetent adults and contribute to the low levels of social grouping already identified.

7. Poorly Furnished Environments

Inspectors reported facilities with cages that did not have a single elevated perch, shelf, or similar structure. Inspectors said they often did not cite the above situations as noncompliant in inspection reports, although they believed the situations were not in accordance with the intent of the Animal Welfare Act, because they believed the Agency could not or would not support them.

Inspectors mentioned other problems with enhancement plans. Some plans are static, not updated to reflect whether they are working effectively. Some are not updated to be consistent with changes in the facility's population and use of animals. Some plans do not consider variation in individual animals' personalities and rearing histories. Others fail to avoid latent effects of harmful housing or rearing conditions. Inspectors said some facilities solve the problem of abnormal or psychological distress-related behavior by simply selling or transferring the primates to other parties. Facilities that sell or transfer primates after relatively short periods of use have little motivation to concern themselves with cumulative or latent effects on the behavior of their primates because these behaviors will be manifested at another facility.

The urgency of these problems or issues raised by their colleagues motivated the members of the Primate Environment Enhancement Team to move forward with the design of a conceptual model and policy. Another factor they had to consider was how to promote psychological well-being for nonhuman primates in the context of the larger political environment. A strategy had to be developed to fulfill the original intent and language of the Animal Welfare Act, while considering the response of the community affected by any new policy, the approach of other nations and societies also facing similar problems, and the difficulties inherent in scientifically measuring psychological well-being. These topics are discussed in Chapter II.

The Animal Welfare Act states that "The Secretary [of Agriculture] shall promulgate standards... The standards.. shall include minimum requirements .. for a physical environment adequate to promote the psychological well-being of primates" [AWA Sec. 13 (a)(1), emphasis added.]

The Animal Welfare Act was intended to promote the psychological well-being of nonhuman primates, not just prevent abnormal behaviors from occurring. Because there were no standards for primate psychological well-being prior to 1991, no measurable comparisons can be made as to whether the use of performance-based standards has improved the welfare of the animals as intended. As previously stated, most inspectors feel the lives of primates have been improved some, but that overall not enough is being done to provide a "physical environment adequate to promote the psychological well-being of primates", especially in the area of social grouping.

The concept of psychological well-being does not lend itself to precise definition. Facilities are allowed latitude in how they meet the requirements, as long as they achieve the desired results or outcomes. Therein lies the problem, as no one has defined the results desired in terms of something that can be easily observed and recognized.

Some facilities claim their environment enhancement programs are adequate because there are no distressing behaviors or appearances of ill health with their primates. This is a short-sighted view since waiting to improve a minimally enriched environment until a primate starts showing signs of psychological distress was not the intent of the Animal Welfare Act.

The Primate Environment Enhancement Team believes the intent of the Animal Welfare Act was to provide nonhuman primates with the opportunity to express a wide range of non-injurious, species-appropriate behaviors. The team's goal with this policy is to re-emphasize attention to adequate environmental conditions before abnormal behaviors develop.

Both the regulated community and the interested public have responded to the increasing awareness of the importance of the psychological well-being of nonhuman primates. There is now a wealth of scientific and anecdotal information on the topic. The exhibition and research communities have sponsored scientific research and professional meetings to further knowledge of the subject. The National Research Council (NRC) Institute for Laboratory Animal Research (ILAR) recommended ways in which to assess and promote psychological well-being. The NRC independently arrived at many of the same points that APHIS has arrived at and its 1998 report is an excellent resource for most purposes. "The purpose of this volume is to help scientists, veterinarians, curators, inspectors, duly appointed committees, and others concerned with the psychological well-being of nonhuman primates to deal more effectively with this complex issue" (NRC/ILAR 1998:4).

At the same time, there has been concern over the implementation of the provisions, and members of the public and an animal welfare organization brought a legal suit against USDA [Animal Legal Defense Fund, Inc. et. al. v. Daniel R. Glickman (Docket Nos. 97-5009, 97-5031, and 97-5074).]

There is a movement in other nations and professional societies abroad to develop similar provisions for meeting primates' psychological needs. Some have specific recommendations or requirements for achieving them. Jones (1996) has reviewed and compared recommendations of three major bodies influencing European laws on primates produced, held or used for research: the IPS (International Primatological Society 1993); the PVEN (Primate Vaccine Evaluation Network) (Poole and Thomas 1995); and the Berlin Workshop, an international workshop on the Accommodation of Laboratory Animals in Accordance with Animal Welfare Requirements held in Berlin, Germany in 1993 (Poole et. al. 1994). Common to all are the following:

1. Physical, physiological, and behavioral needs must be satisfied.
2. The environment must contain sufficient useable space, complexity, and enrichment.
3. Social housing should be the general rule and individual housing should be the exception.
4. The environment should promote a species-appropriate repertoire of behavior.
5. Primates should not be weaned from their mothers at an age that will produce psychological abnormality, prior to 6 months of age.

In addition, the PVEN emphasizes providing climbing structures and vertical space, novelty in the animal's environment, and giving the animal opportunity to exercise control over some aspects of its environment. The Berlin Workshop (Poole et. al. 1994) specifies provision of sleeping boxes, climbing structures, and gnawing wood for Callitrichidae (marmosets and tamarins); environmental novelty and variety; and the use of animal training to decrease the stress of handling. It also gives minimum space requirements. Although these requirements are divided into slightly different weight classes than USDA's requirements are, the minimum dimensions required by the Berlin Workshop are generally 1.5 to 3 times larger than USDA's minimums. The Berlin Workshop also states primates kept for long periods should be housed in even larger spaces, but it does not define what constitutes a "long" period.

The United Kingdom Code of Practice (Home Office 1989) contains language that is more specific. The cage volume should enable the animal to exhibit vertical flight reactions, jump, climb, and sit on perches with neither its head nor its tail touching the cage. For Callitrichidae, it specifies "wooden perches, a swing, a wooden nest box, a shelf for feeding, and sufficient shavings to allow foraging." The animals should also be allowed to "jump horizontally from one perch to another." The same cage structures are specified for arboreal, polygamous primates, such as squirrel monkeys. Group-housed macaques and baboons must be given escape routes, sleeping areas with several entrances, and multiple food and water stations.

The Canadian Council on Animal Care (CCAC) provides minimum cage space requirements for primates in research that, for most species, are the same or slightly larger than U.S. minimums. Single housing is "strenuously discouraged" (Olfert et. al. 1993). A number of other recommendations are made with respect to social grouping, cage enrichment, exercise and foraging activities (Olfert et. al. 1993).

The Australian National Health and Medical Research Council's (NHMRC) official policy requires the following: appropriate social grouping, unless individual caging is justified by an animal ethics committee; grooming opportunities for individually housed primates; access to outdoor enclosures for animals held longer than six weeks; training of isolated animals to facilitate handling; adequate enclosure size to accommodate group housing and varied activities; and foraging opportunities (National Health and Medical Research Council Animal Welfare Committee 1997).

The laws and regulations of some nations concern themselves with the specifics of primate environment enhancement just as the U.S. policy being developed here does. However, they differ from it in other ways. One of these is the animals to which the requirements apply. In the U.S., the enhancement regulation applies to all primates in facilities regulated by USDA. The requirements apply to primates in zoos and circuses as well as to primates in research⁽³⁾, breeding, and many other types of facilities. In Europe, the housing of primates in zoos is governed by standards developed under the UK Zoo Licensing Act of 1981 and/or the 1994 standards of the European Association of Zoos and Aquaria (EAZA). These regulatory documents for zoos are far more general than the other European regulatory documents reviewed above, which apply to animals in research laboratories. The EAZA standards state that the welfare of zoo animals is a matter of both "physical and social well-being" (EAZA 1994). Both the UK Zoo Licensing Act standards and the EAZA standards require the provision of enclosure space and environmental structures and substrates appropriate to the needs of the species.

Developing regulatory language with specific details about environment enhancement does not appear to have caused serious problems for the nations above who have tried it (Boisvert 1997, Poole 1997a, and Popovic 1997). In the present era of increasing concordance in regulatory matters to facilitate international trade and commerce, it will be advantageous for the U.S. to adopt criteria and language that will meet with acceptance by other nations.

The ultimate objective of 9 CFR §3.81 is "psychological well-being" (PWB), a subjective state experienced internally by each animal. It is difficult to define this term and currently there are no ways to measure it directly. Working definitions presume characteristics that are manifested in various indicators (Broom and Johnson 1993, Duncan et. al. 1993, Mason and Mendl 1993, Novak and Petto 1991b, Poole 1992).

The indicators that have been proposed include: (1) physical values such as longevity, growth rate, reproductive success, hair coat, and body condition, etc; (2) physiologic values such as heart rate, blood pressure, body temperature, levels of serum cortisol and other hormones, and rates of lymphocyte proliferation or suppression; (3) behavior; or (4) a synthesis of many such measures, perhaps weighted by evolutionary or other contexts (Boinski et. al. 1999, Broom and Johnson 1993, Line 1987, Snowdon and Savage 1989).

The assessment of the PWB of each primate relies to some degree on subjective interpretation of these indices, some of which may suggest opposite conclusions (Mason and Mendl 1993, Sackett 1991). For example, Coe found that a change in the social environment of older rhesus monkeys produced positive behavioral changes, but also evidence of reduced immune competence (C. L. Coe 1991). An ideal approach would combine many different measures and take into account differences between individual animals. This is often not feasible and the measurement of many of the parameters would be unnecessarily invasive.

An animal's behavior is still the index most commonly accepted for assessing PWB. It is also the index most readily and consistently available (Olfert et. al. 1993, Poole 1991b). To assess PWB, one may look at the animal's general activity level, the percentage of time it spends doing various things, its use of cognitive skills, its maternal behavior, locomotor behavior, play, communication, appetitive and self-maintenance behaviors, its avoidance of predators, its response to novelty and routine husbandry, affiliative behavior, and vocalizations. Environmental effects on vocalizations may provide a rich opportunity for psychological assessment that is only beginning to be applied to animal welfare (Crowell Comuzzie 1993, Mulligan et. al. 1994).

How can the welfare implications of an animal's behavior be interpreted and what does it tell about the adequacy of its environment? The performance of abnormal behaviors, such as stereotypies, is interpreted to reflect a lower level of well-being and an inadequate environment (Bayne et. al. 1992a, Broom and Johnson 1993, Maple 1979, Olfert et. al. 1993). Some may assert that the absence of such behavior indicates well-being and therefore an adequate environment. But stereotypies do not always indicate current suffering or currently inadequate environments. Current abnormal behavior may reflect past, not present, environments (Brent and Hughes 1997, Broom and Johnson 1993, G. J. Mason 1991a and 1991b, Mason and Mendl 1993). Two conditions known to result in aberrant behavior that may persist into adulthood or be expressed long after infancy are: (1) restricted social environments during development; and (2) early infant separation from the mother. Some aberrant behaviors resulting from these conditions are resistant to treatment (Capitanio 1986, Mason and Berkson 1975, Novak and Drewson 1989:166, O'Neill 1989). Some are eventually reversible after considerable ameliorative efforts (Fritz 1989, Kessel and Brent 1997).

This underscores the importance of directing major regulatory efforts toward requiring environments and practices less likely to be associated with the expression of aberrant behaviors, either immediately or later in life. Put in a constructive way, facilities should be required to enhance the environment of nonhuman primates in a way that promotes the expression of a wide variety of positive, normal behaviors. Prevention is better than treatment, in mental health as in physical health (Schapiro et. al. 1996a). The USDA's obligations under the Animal Welfare Act include requiring standards aimed at prevention of problems.

The performance of stereotypies remains an important and valid indicator of welfare problems for most situations (Broom and Johnson 1993, Olfert et. al. 1993, Toates 1995, Wemelsfelder 1993). The benefit of any interpretive doubt should go to the animals (Bekoff 1994, Duncan et. al. 1993). Many authors have concluded that welfare should also be seen as more than just absence of negative behavior (Bayne 1989:27, Broom and Johnson 1993, Poole 1992, Segal 1989 Preface). The expression of species-typical or species-appropriate behavior should be the goal of an enhancement program.

There has been some debate about whether normal behavior reflects adequate well-being or whether the performance of specific behaviors themselves is necessary to cause well-being (Petherick and Rushen 1997, Veasey et. al. 1996). In either case, it is important that USDA regulations require facilities to provide captive primates with an environment where they can express a wide range of normal behaviors.

USDA regulations state, "The physical environment in the primary enclosures must be enriched by providing means of expressing non-injurious species-typical activities" [U. S. Department of Agriculture, Animal and Plant Health Inspection Service 1998: 9 CFR 3.81(b)].

What constitutes STB or a normal behavioral repertoire in captivity? A primate in captivity will not be able to exhibit the full range of behaviors that occur in nature. Colony managers would not want to promote infanticide or harmful aggression. The primate itself would not wish to suffer infanticide, predation, or other conditions that sometimes occur in nature. In passing the Animal Welfare Act, Congress did not intend such extremes to be promoted in the maintenance of captive primates. Therefore, in this policy, the term "species-appropriate behavior" has been adopted instead of the more common term, "species-typical behavior."

The pitfalls of attempting to stimulate every natural behavior have been discussed by Veasey et. al. (1996). (See also Rosenblum and Andrews 1995.) Putting aside the extremes, behavior observed in nature serves as one of the most useful guides to what a captive environment should allow (McGrew 1981). Observations of captive but free-ranging primates may provide the best of both worlds (Newberry 1995, O'Neill et. al. 1990). Environmental preference testing can also be used to clarify the picture (Bayne et. al. 1992a, Line 1987). As Kaumanns (1997) stated, captive conditions "should still fit within [the] adaptive potential" of the animal. Differences between individuals of a species, as well as between species, must also be taken into account (Clarke and Boinski 1995, Laudenslager and Boccia 1996, Suomi and Novak 1991).

In summary, although difficulties are inherent in applying USDA's regulation concerning environment enhancement to promote the psychological well-being of nonhuman primates, we have learned a great deal since the amendments to the Animal Welfare Act were passed in 1985 and 9 CFR §3.81 was adopted in 1991. USDA now has a basis for creating more specific guidance on environment enhancement and for bringing the U.S. program into step with international developments. The central idea is that nonhuman primates must be given an environment in which they can express the wide range of behaviors practiced by others of their species in nature. Their captive environments must be enhanced to give them opportunities to exhibit these behaviors. When such conditions are achieved, the intent of the Animal Welfare Act to promote their psychological well-being will be fulfilled.

There is a consensus emerging in the literature on primate enrichment that "species-typical" or "species-appropriate" behavior should be the goal of enhancement programs, and that it is important for the animal to be able to express a "normal repertoire" or a "full range" of normal behavior--a range that is complete and balanced (Brent and Long 1995, Brent and Stone 1996, Chamove and Anderson 1989, Fragaszy 1991, Olfert et. al. 1993, Poole 1991b and 1992, Rose 1994, Toates 1995, Line 1987). Scientists believe that it is not enough for individual or groups of primates to express just a few "normal" behaviors. Environments should be complex enough to allow a variety of activity and stimulus-response options. Also, it is difficult to interpret an animal's behavior and activity levels if it has relatively few realistic choices of behavior in that environment.

Captive animals are limited in their ability and/or motivation to move about freely and carry out many of the behaviors their species normally exhibit in a natural environment. As stated in Chapter 1, USDA inspectors have found that many current enhancement programs are narrow and address only one or two aspects of the animal's life. In order to correct this problem, USDA must stimulate the addition of diverse environmental elements that can promote a wider repertoire of species-appropriate behavior. This need has motivated the Primate Environment Enhancement Team to develop the concept of critical elements.

There are distinct categories of activity or behavior, each of which should be present to some extent to round out a normal behavioral repertoire. Similarly there are categories of enhancement strategies or elements of an environment that address these behavioral needs and/or promote the expression of these behaviors. Such categorizations are useful for providing structure to an enhancement program and to regulations and policies. Numerous sources in the primate enrichment literature show similar categorizations of these elements (Bloomsmith et. al. 1991, Bowden 1988, Keeling et. al. 1991, Line 1987, Maple 1979a, Newberry 1995, Olfert et. al. 1993, Poole 1992 and 1998, Rosenblum and Andrews 1995, Schapiro and Bloomsmith 1995). They share the idea that it is critical to touch upon each element appropriately, rather than concentrate on one or two aspects of the normal behavioral repertoire.

The National Research Council in its report on The Psychological Well-Being of Nonhuman Primates discusses four main determinants of psychological well-being:

The report emphasizes the importance of flexibility since no single approach will be effective for all animals. Measuring and validating the effectiveness of an environment enhancement program is also vital to ensure that psychological well-being is actually improved.

Nevertheless, a comprehensive program to improve the psychological well-being of nonhuman primates will attend to each of the variables and include a means to test and assess the influence of each [NRC/ILAR Report 1998:2, emphasis added].

Other documents outline similar methods with several elements or variables (International Primatological Society 1993, Olfert et. al. 1993, Poole et. al. 1994, Poole and Thomas 1995).

These differ vastly from minimalist programs in which facilities adopt a single element such as feeding food treats as the mainstay of their enhancement, while keeping the enclosures barren and neglecting other environmental features. Minimalistic programs such as these do not stimulate a wide range of species appropriate behaviors and probably increase the potential for obesity. A recent study by Boinski et. al. (1999) exemplifies the importance of variety and a minimum level of enrichment. Providing both a foraging device and two toys to single housed Cebus apella markedly increased species-appropriate behavior and decreased abnormal behavior. These behavioral changes were correlated with expected effects on plasma cortisol. The overall positive effect was dramatically greater with both of these enrichments than it was with either enrichment alone, and the baseline environment already included cage furniture and daily multiple feedings of standard diet and treats.

One-sided programs have persisted at some regulated facilities because the current USDA regulations appear to allow them. Stimulation of only one type of normal behavior should not be considered adequate for compliance. Such programs can be compared to a diet that contains an excess of some nutrients and inadequate levels of others. A nutritionally balanced diet will provide certain vitamins and minerals plus a number of calories distributed among different forms of metabolizable energy. A food pyramid can be constructed to represent the relative importance of the essential food groups. A variety of individual foods are available within each food group to provide the necessary nutrients in appropriate proportions. Many food items are equivalent in value, but some are more palatable or costly than others.

This food pyramid model is analogous to the critical element concept in the Primate Environment Enhancement policy being developed for USDA here. The policy states that five elements are critical to environments that adequately promote the psychological well-being of nonhuman primates:

1. Social grouping
2. Social needs of infants
3. Structure and substrate
4. Foraging opportunities, and
5. Manipulanda.

A minimally acceptable program of environment enhancement will contain all five. A given enhancement strategy or environmental feature may simultaneously address more than one element. The extent to which each enhancement strategy may be deemed to satisfy more than one element simultaneously is a matter of professional judgement and should be evaluated on a case-by-case basis. In addition to the five critical elements, any enhancement plan should give consideration to two other aspects of the environment: stimulating all five senses; and providing the animal novelty and control over aspects of the environment.

Regulated facilities must target each critical element in their primates' environments, address it in their plan, and implement the plan in a balanced way. To meet the desired objective for each critical element, a variety of options exist. The options chosen should be appropriate for the species and individual characteristics of the animal as well as its intended use by the facility. The facility must observe the effects on the animals' health and behavior and continue to make modifications as necessary.

The essence of the performance-based standard approach is that regulated facilities assume responsibility for the end results and are given flexibility in how they approach achieving them. For this to be successful, facilities must clearly understand the goals and try different methods until they get the desired results.

We believe the majority of regulated facilities intend to voluntarily comply with the law to the extent they are able. However, educational efforts alone are not sufficient to gain compliance. There always exist some facilities that must be compelled by enforcement. USDA cannot overlook the failures of members of the second group or it will hurt the members of the first group. Fairness in government requires that if regulations exist, they are enforced uniformly and consistently. Those who voluntarily comply with the intent of the law should not be penalized for it by suffering a disadvantage relative to others who circumvent regulations.

In order for minimum standards to be enforceable, the standards must have definition and structure. It must be clear to all facilities when violations occur and enforcement action is necessary. The concept of minimum criteria has been useful in government regulations because it objectifies what is unacceptable and increases fairness. Some regulatory areas such as primate psychological well-being are so complex that specifying criteria in detail would require volumes of legal language and years to develop. There will always be the need for the careful judgement of a qualified professional who is trained in Agency policy based on regulatory experience, ethics, and applied ethology. USDA's policy has been developed to capture these principles and while allowing facilities as much flexibility as necessary.

In order to develop the new policy on environment enhancement to promote psychological well-being of nonhuman primates, USDA's Primate Environment Enhancement Team conducted a review of professional literature related to the ecology, natural history, and behavior of primates. The findings of this literature review are presented and discussed in the order the five critical elements are listed in Chapter III: social grouping; social needs of infants; structure and substrate; foraging opportunities; and manipulanda. After the five critical elements are discussed, findings are presented for two additional considerations that should be built into each environment enhancement plan--sensory stimulation, and novelty and control. This chapter is intended to explain the reasons for the policy, but it may also be useful to those who own primates and wish to understand their needs generally before beginning a detailed quest for information on the species in their care.

The team reviewed publications of scientists who have observed primate behavior in nature and under zoo and laboratory conditions. It also looked for advice and strategies directed to those who manage colonies of primates. It sought to understand what scientists and practitioners today know about each critical element and what the requirements to each one should be. The field of knowledge has grown tremendously since the Animal Welfare Act's 1985 amendments were passed. The number of articles published is increasing every year, as are the number of electronic mail discussions and sites on the World Wide Web devoted to the topic. Although the team was not able to survey all the literature, it was able to review enough sources to draw conclusions about what environmental conditions promote the psychological well-being of nonhuman primates. Sources are listed at the end of this paper. The interested reader who is unable to locate information sought may try the Animal Welfare Information Center of the National Agricultural Library, 10301 Baltimore Boulevard, Beltsville, Maryland 20705, (301) 504-6212. The Center's Email address is: AWIC@NAL.USDA.GOV. For document delivery, another resource is the Wisconsin Regional Primate Research Center Library at the University of Wisconsin in Madison, Wisconsin 53715-1299, (608)263-3512. The Email address is: jacobsen@primate.wisc.edu. The webpage address is: http://www.primate.wisc.edu/pin/primpro.html. The Primate Information Center at Box 35730, University of Washington, Seattle, WA 98195-7330, (206) 543-4376, is an indexing service for scientific literature on all aspects of nonhuman primate research. Its manager, Jackie Pritchard, is at: plj@u.washington.edu. The webpage address is: htt://www.rprc.washington.edu/pic1.htm.

USDA regulations state that, "The environment enhancement plan must include specific provisions to address the social needs of nonhuman primates of species known to exist in social groups in nature." [U. S. Department of Agriculture, Animal and Plant Health Inspection Service 1998:9 CFR §3.81(a)].

Social interactions are considered to be one of the most important factors influencing the psychological well-being of most nonhuman primates. (NRC/ILAR Report 1998:13)

Nearly all primates have some tendency to seek the company of their own kind at times other than mating (McGrew 1981, Rowe 1996, Pereira et. al. 1989b, Fleagle 1998). Even within those few species known as "solitary"--orangutans and most nocturnal prosimians--individuals of certain age or sex classes can still be found in social associations at certain times (Bearder 1987, Rodman and Mitani 1987, Rowe 1996, Van Schaik and Van Hoof 1996). Despite their solitariness in the wild, adult orangutans have been kept in compatible social groups in captivity (Maple 1979a, Perkins 1992), such as at the Singapore Zoo (Poole 1987), where allogrooming and social play among adult females was much higher than one would predict from behavior observed in the wild (but see also Markham 1990). The remarkable sociality of the primate order in general is the most relevant characteristic for their humane housing. This social tendency may be redirected toward animals of other species, including humans (Collazo 1989, Hediger 1964, Mason and Kenney 1974).

The gregariousness of a primate in nature varies not only with its species, but may also vary with its age, sex, kinship to others, the season, the habitat, and the particular activity. The composition of a group that sleeps together is not necessarily the same as that of the foraging or breeding group (Cheney et. al. 1987, Jolly 1995, Rowe 1996). Group sizes can range from two, as in a monogamous pair of gibbons with no offspring, to 400, as in some hamadryas baboon troops (Rowe 1996). Bolivian squirrel monkeys live in large, but sexually segregated groups, enforced by the females, except during the breeding season (Williams and Abee 1988). Foraging associations between some primate species also occur and may provide a basis for mixed-species housing (Bernstein 1991, Bramblett 1989a, Thomas and Maruska 1996).

Jolly (1985) summarizes the breeding systems of many species. Monogamy, polygamy, polyandry, and multi-male, multi-female groups are all represented among the many primate species and those social structures are species specific. Some species can exhibit more than one breeding system, for example, many Callitrichidae can be either monogamous or polyandrous. Generally one male or multi-male groups are the rule among Old World Anthropoids; monogamy and polyandry, as well as multi-male, multi-female groups, are common in New World Anthropoids.

Close social bonds may exist between heterosexual breeding partners and/or between adult males, adult females, among juveniles, between parents and offspring, between infants and other kin, between non-kin. These patterns of bonding and association are also species specific and are often determined by degree of kinship (DeWaal 1993, Gouzoules and Gouzoules 1987). For many species, kinship appears to be the ultimate cause of social bonds between non-mated individuals in nature. But in captivity, if certain conditions are met and group formations are made with care, affiliative bonds can readily form between unrelated individuals that would not otherwise associate peacefully in nature (Gust et. al. 1996, Meshik 1994, Vermeer 1997, Williams and Abee 1988).

The generalized fear of strangeness or xenophobia that appears to characterize many primates accounts for the difficulties associated with socializing unfamiliar individuals together in captive settings (Bernstein 1991). Even relationships between primates in an established pair or group are not without stress and hostility, in the wild or in captivity. Primate societies are rarely composed of members of equal social rank, but rather consist of dominant and subordinate members. Some species tend to show strict and stable dominance hierarchies while others have more unstable or non-linear arrangements (Jolly 1995, Fragaszy 1994). Changes in group structure or dominance status are associated with physiologic evidence of stress, which may persist long after the event (C. L. Coe 1991, Ray and Sapolsky 1992, Van Schaik et. al. 1991).

In species such as guenons that normally live in groups consisting of one adult breeding male with several related females and immature offspring, two adult males are not likely to be compatible companions for each other in captivity (Cords 1987). But this does not mean that either male is unsuitable for social housing. It may simply be a matter of finding the right kind of social partner(s). Guenons are reportedly tolerant of social partners of other species (Bramblett 1989).

Patterns of emigration from the natal group and immigration or transfer into other groups is also species specific. Knowledge of these patterns is essential for successfully forming pairs or groups in captivity, managing group sizes, and assuring the proper developmental environment for captive juveniles (Williams and Bernstein 1995). When it is necessary to remove individuals, it should be done in a way that minimizes disruption of stable social structures, and removals should approximate natural patterns of change to the extent practical (McGrew 1981).

In some species such as gelada baboons or gorillas, young males leaving their natal groups may travel alone for a while or may join together in bachelor groups. For a given individual in the wild, this arrangement is usually temporary, since the objective is to join a reproductive group (Jolly 1995). In captivity, squirrel monkeys, guerezas, lion-tailed macaques, and gorillas have been managed as bachelor groups (Harcourt 1988, Vermeer 1997, Watts and Meder 1996). In chimpanzees, young females normally emigrate from their natal groups and males form the cohesive core of societies (Goodall 1986). Chimpanzee males may also be kept in bachelor groups (Alford 1995).

One of the most important primate behaviors associated with social living is the wealth of signals that communicate emotional states or other information between individuals. The signals may be visual, vocal, olfactory, or tactile. They can convey dominance, submission, intent to attack, anxiety, reconciliation, reassurance, alliance, sexual receptivity, a solicitation for grooming or play, a willingness to nurse, territorial boundaries, and so on (Estes 1991, DeWaal 1989, Rowe 1996, Zimmerman et al. 1980). Knowledge of these communicative and associated sensory abilities have led to various sensory enrichment ideas (Buchanan-Smith 1997, Shepherdson et. al. n.d.).

Visual signals include facial expressions, gestures, postures, and athletic displays of jumping, running, and object manipulation (Cheney et. al. 1989, Estes 1991, Goodall 1986, Zimmerman 1980). Vocal expressions can be context and gender specific (A. P. Clark and Wrangham 1994, Palombit 1992, Scott 1997). Prosimians and most New World Monkeys use odors to mark territory, indicate status, or compete with rivals (Jolly 1995, Ruiz 1993, Zimmerman et. al. 1980).

Grooming is the most important form of tactile communication and stimulation for primates (Olfert et. al. 1993). Social grooming can account for 10-13% of the daily activity budgets of rhesus macaques (Malik 1986). Chopra et. al. (1992) found that grooming was the most frequent social interaction in rhesus monkey troops in various habitats, generally beginning immediately after the first feeding period in the morning and continuing throughout the day. In capuchins (Cebus spp.) grooming is the primary activity during daytime rest (Robinson and Janson 1987). One grooming bout observed between a wild chimpanzee and her adult son lasted 2 hours and 45 minutes (Goodall 1986).

Grooming is the most critical activity in maintaining social bonds for most species (Prince et. al. 1989, Williams and Bernstein 1995). Jolly (1985) has called grooming "the social cement of primates from lemur to chimpanzee." Relaxed and affectionate grooming bouts between two primates are frequently seen by human care givers as an indication of successful affiliative bonding (Crockett et. al. 1997, Reinhardt et. al. 1995b). Grooming is not the only tactile interaction important for social cohesion and harmony: embracing, huddling, patting, kissing, and the tail-twining seen in titi monkey pairs are others ( Cheney et. al. 1987, Jolly 1985).

Communication between animals can be used by managers to recognize affiliative or stable bonds as well as aversion or impending aggression (Bernstein 1991, Rosenblum and Andrews 1995). Dominance relations can be established between laboratory macaques through visual signals between two individuals in adjacent cages and are an important tool for predicting successful pair introductions (Lynch 1998, Reinhardt 1995b).

It is therefore important that captive environments for primates allow for the adequate expression of social signals by the sender and reception by the receiver. Where postures and positions are part of the behavioral repertoire by which individuals normally establish or maintain social relationships, cages must supply enough room to safely express them. Other characteristics of the physical environment, such as furnishing and cage placement, must accommodate signaling. Threat signals can be a source of distress for recipients. In one case, a singly-caged male rhesus macaque persistently expressed abnormal behavior and severe anxiety when housed where he was in direct view of a dominant male. The situation was improved somewhat by moving the subordinate male's cage out of view of the other animal (Baer 1998a).

The expression of olfactory and tactile cues requires appropriate substrates for scent-marking and opportunities for contact, proximity, and avoidance. Cage boundaries do not stop olfactory signals. In common marmoset (Callithrix jacchus) colonies, olfactory and visual cues given by dominant females can suppress ovulation in subordinate females housed in separate cages in the same room (Tardif et. al. 1994). Because of the importance of scent-marking to New World species, it is highly recommended that sanitization of various surfaces and furniture within the cage be done sequentially, rather than all at once, so that a familiar territorial scent is always present (Buchanan-Smith 1997, NRC/ILAR 1998).

Whether a primate correctly uses and interprets social signals depends on its social experience and rearing history. A primate learns the customs of its own kind from adults or older peers during periods of early development (Fairbanks 1993, Fritz 1986, Jolly 1985). Young rhesus macaques with restricted social rearing may launch into "suicidal" attacks on mature adult males, apparently because the abnormally-reared animals are unable to recognize the danger (Mitchell et. al. 1966). A rhesus harem headed by a male reared in isolation had more problems with aggression and wounding than harems led by males reared by their mothers or peers (L. Watson et. al. 1995). Bernstein (1991) suggests that lack of shared communication mechanisms might explain instances where groupings of animals of different species began without overt hostility but later deteriorated into violence.

Primates are clearly social beings and social housing is the most appropriate way to promote normal social behavior and meet social needs. However, there is no doubt that there are risks and negative impacts associated with both individual and social caging in captivity.

The relative benefits and costs to the animal of either alternative have been discussed extensively in primatological literature and are reviewed here. There is an emphasis on species used in laboratories, where single caging continues to be more common than in other types of facilities.

Many authors have described the pronounced association between abnormal behaviors and/or physiological disturbance and single cage housing (Bayne et. al. 1991, Brent and Hughes 1997, Goosen 1988, Goosen et. al. 1986, Schapiro et. al. 1996a, Visalberghi and Anderson 1993, Watts and Meder 1996, Woolley 1997). In one study, chimpanzees that were moved from group housing to single caging exhibited increased stereotypical behaviors in the short term (Brent et. al. 1989). Individual caging of infants and juveniles impairs animals' social skills, makes them more difficult to socialize later in life, and may result in abnormal reaction to stimuli (Capitanio 1986, Fritz 1986, Louwerse et. al. 1997, Mason, W. A. 1991, Prince et. al. 1989, Young et. al. 1996). Walsch et. al . (1982) have stated that "even relatively complex laboratory environments, in the absence of opportunity for interaction with conspecifics, disrupt and seriously damage psychological processes in the chimpanzee".

Many beneficial effects of social housing are well documented. Social grouping reduced abnormal behavior in previously individually caged macaques and baboons at a pharmaceutical laboratory (Woolley 1997). Group-housed squirrel monkeys exhibited more normal behavior than individually-housed ones (Spring et. al. 1997). Social enrichment for young rhesus macaques both increased species-typical behavior and reduced abnormal behavior (Schapiro et. al. 1996a). The well-being of adult female rhesus macaques, based on behavior, was improved after a switch from single to pair housing; measures of physiology and reproduction did not indicate that the pairing caused significant stress (Eaton et. al. 1994). In juvenile squirrel monkeys, the presence of a peer mediated stress responses (stress vocalizations and plasma cortisol) to manual capture and exposure to a strange environment (Hennesy 1984). A familiar conspecific plus a familiar environment mediated the stress response to maternal separation (C. L. Coe et. al. 1987). Similar results have been obtained for pigtailed macaques and bonnet macaques (Laudenslager and Boccia 1996). In another study, cell-mediated immune function in pair-housed adult rhesus was superior to that of single-caged controls (Schapiro et. al. 1997b). Social companions lowered blood pressure in baboons (Coelho et. al. 1991), and pig-tailed macaques being groomed by conspecifics had reduced heart rates (Boccia 1989). Where nonhuman primates are subject to frequent manipulation and exposure to unfamiliar environmental stimuli, the presence of a compatible conspecific may be significant in helping them to cope with these realities of captive life (Gust et. al. 1994).

There have also been concerns over potential detrimental effects of pair or group caging versus individual caging. These effects can include social stress, competition for food, disease transmission, woundings, and the possible need for contraception. Gust et. al. (1996) found that cortisol levels were increased in pig-tailed macaques after group formation. Christopher Coe (1991) detected reduced cell-mediated immunity in geriatric rhesus monkeys when paired with juveniles, though such effects were not evident in the geriatrics' behavior. There is certainly also a risk of wounding during social caging, especially in reportedly "aggressive" species like macaques. However, pair housed rhesus at one facility required less veterinary treatment than rhesus in single or group caging (Schapiro and Bushong 1994). The conventional wisdom has been that species with this type of social organization are too difficult to pair or group in laboratories (Rhine and Cox 1989, Williams and Bernstein 1995). One resocialization of formerly single caged rhesus macaques resulted in aggression and increased stereotypies (Ljungberg et. al. 1997).

But there are also many instances of compatible pairs or groups of these species (Seelig 1998). Long periods of individual housing do not appear to reduce the need or desire for social contact (Taylor et. al. 1998). Animals that have been socially isolated have been successfully resocialized (Fritz 1989, Kessel and Brent 1997, Reinhardt 1994b). At one facility, adult male rhesus were paired with an 80% success rate, even though they had a history of being single-caged (Reinhardt 1994a).

Reinhardt et. al. (1995b) analyzed evidence for and against social housing of macaques in research facilities and concluded that the commonly given reasons for avoiding it were not supported by evidence. Even some of the infectious disease research commonly performed with chimpanzees does not appear to require single caging (Prince et. al. 1989). Visalberghi and Anderson (1993:8) have stated: "The gap between principles derivable from constantly updated knowledge on primates' psychological and physiological well-being and many existing regulations and practices is wide and unfortunate."

In creating appropriate social groupings in captivity, there are many factors to consider: Should animals be paired or in larger groups? What will be the group structure in terms of age and sex? What is the rearing history and personality of the candidates? How will group size be regulated? By what method will the group be formed and members added or removed artificially, if necessary? By what means will compatibility be determined? What equipment and enclosures will be needed and how will space be structured? How will humans fit into their social life, and will a behavioral conditioning program be implemented? How will the purpose and use of the animals, or their medical treatment, affect social stability? What will be done with socially incompetent individuals?

Many criteria for selecting partner candidates and methods of introduction and group formation have met with success and failure, perhaps even in the same setting. Many factors may impinge on the likelihood of success of any pairing or grouping, including individual personality (Reinhardt et. al. 1995b). Some grouping methods seem less prone to risk than others, and certain precautions seem well-advised.

Infants and juveniles of most species are easiest to introduce to established groups, to adults, or to each other. For animals like male macaques, an infant or juvenile can make good social partner (Fragaszy et. al. 1994, Reinhardt et. al. 1987, Schapiro et. al. 1994). All introductions should be closely monitored for as long as possible before leaving animals unattended, and there should be a plan for separating animals quickly if there is an attack. Since virtually any social change is a stressor, it is best that initial introductions occur at a time when other environmental factors are stable (Capitanio 1998). Beyond that, advice for pair or group formation among the major social types of primates varies. Different reports have yielded conflicting information on the role of prior familiarization, age differences, presence of the opposite sex, "neutral" cage environments, and other factors (Alford et. al. 1995, Bernstein 1991, Brent et. al. 1997, Crockett et. al. 1994, Reinhardt 1994a, Seelig 1998).

The method of introduction, as well as the rearing history, age, and sex of partners, may influence pairing success in macaques (Schapiro et. al. 1994). Crockett et. al. (1994) were able to compatibly establish only 6 of 15 attempted pairs of male cynomologous macaques (Macaca cynomologus) in a two week period. However, pairs were separated and re-paired daily. Higher rates of success in the same species and sex occurred at a facility where pairs were not continually re-separated (Lynch 1998). At this laboratory, 16 of 17 attempted male cynomologous pairs were established and remained compatible after one to two years. These researchers used a nine step partner evaluation and introduction technique that has been successful elsewhere in establishing long-term compatible pairs of adult male rhesus, adult female rhesus, adult male stump-tailed macaques and adult female stump-tailed macaques (Reinhardt et. al. 1995b). In Lynch's laboratory, an additional six pairs of male cynomologous were formed using an exercise cage (Lynch and Baker 1998). Similar techniques have been used to form compatible isosexual pairs of cynomologous macaques (Mack 1998) and to socialize pig-tailed and bonnet macaques (Taylor and Laudenslager 1998). At an animal sanctuary 18 former laboratory cynomologous macaques have been paired (Asvestas 1998).

Seelig (1998) contrasted the methods used in five studies on the pairing of adult male cynomologous macaques. The widely varying success rates in these studies suggest that adult male cynomologous macaques are more challenging to pair than other combinations of species and sexes. Where full-contact housing is not successful for these adult males, a safe alternative is adjacent caging with privacy panels and vertical bars that permit allo-grooming. In a test of one such design, all male-female and all female-female pairings were successful. Forty of 45 male-male pairs were successful, and nearly half of these successful pairs had not been compatible when previously housed together in one continuous enclosure (Crockett et. al. 1997). These cages can be used with partners of the opposite sex without resulting in unwanted pregnancies.

There are other reports of successful pairing or grouping of many species in pharmaceutical, toxicological, and other research settings: cynomologous macaques (Brinkman 1996, Buerge and Weber 1997, Heath 1989); rhesus macaques (Macaca mulatta) (Bowditch et. al. 1997, Buerge and Weber 1997, Fligiel and Reinhardt 1994, Louwerse et. al. 1997); pig tail macaques (Macaca nemestrina) (Gust et. al. 1996); rhesus macaques (Brown et. al. 1997); capuchins (Cebus) (Fragaszy et. al. 1994); chimpanzees (Pan troglodytes) (Alford 1995); squirrel monkeys (Saimiri) (Salzen 1989); bonnet macaques (Macaca radiata) (Taylor et. al. 1998).

Squirrel monkeys seem particularly well-suited to being kept in large groups, in a free-ranging room (King and Norwood 1989). An tame adult brown capuchin (Capucinus apella) who had formerly been a pet was successfully introduced to an existing group (Anderson et. al. 1991). Juvenile and adult female capuchins can be introduced to existing groups without great difficulty; males can also be integrated into groups that have no resident adult males (Fragaszy et. al. 1994).

For other descriptions of introduction techniques, see the following sources: Baer 1994, Byrum and St. Claire 1998, Cooper et. al. 1997, Kurth and Bryant 1998, Schapiro et. al. 1994, Reinhardt et. al. 1995b, Fritz 1994, Watts and Meder 1996, Ljungberg et. al. 1997, Morland et. al. 1992, Fragaszy 1994, Alford et. al. 1995. Behavioral conditioning (training) has been used to improve compatibility (Bloomsmith et. al. 1994).

5. Separations

Once animals have been compatibly paired or grouped, separating them is stressful. Any disruption of attachments will be stressful, whether it is separation from the mother, a sibling or nursery peer, a cage partner, or a room-mate in a separate cage (Capitanio 1998, Mendoza and Mason 1986, Prince et. al. 1989, Suomi et. al. 1975). Separations occur naturally in the wild, as part of normal weaning, death, and emigration. Stressful effects may be reduced in group-living species by the presence of group mates and/or minimizing other environmental changes (Coe et. al. 1987b, Gerber et. al. 1997, Reinhardt 1995b).

After pairing, the frequency and duration of unnecessary separation of an animal from its companion should be minimized (Olfert et. al. 1993). In the past, traditional laboratory settings made this nearly impossible. More recently, refinements in animal handling and restraint methods are making separations for husbandry, treatment, and experimental purposes increasingly unnecessary. Primate pairs have been trained to cooperate in a variety of clinical and husbandry procedures (Brown et. al. 1997, Gilbert and Wrenshall 1989, Reinhardt 1997d, Reinhardt et. al. 1995b, Turkkan 1989). Where separation is necessary, social partners should be able to maintain as much visual and auditory contact as possible (Lynch 1998, Reinhardt et. al. 1995b, Washburn and Rumbaugh 1991). It is also beneficial to prevent total separation by providing opportunities for tactile contact. If this cannot be done, providing items for tactile stimulation is the next best alternative (Lam et. al. 1991).

We have established that social housing is superior for most social primates, but should it be pair or group housing? In captivity, primates tend to be held as single animals, in pairs, or small social groups. Maintaining groups of three or more in captivity can be more difficult than maintaining pairs. Many of the references examining overt aggression in group housing situations involve groups of three or more in confined spaces (Bernstein 1991, Reinhardt 1991, Rhine and Cox 1989). Reinhardt et. al. (1995b) discusses why housing animals in pairs may be the best compromise between single and group caging for the majority of laboratory situations, even though the pair is not a species-typical social arrangement for most of the species commonly kept in laboratories.

For monogamous pair-bonding primates such as Aotus, Callicebus, and some Callitrichidae, only two adults will likely be tolerated, and these must usually be of opposite sexes (Baer 1994, NRC 1998).

Larger groups may be necessary for some species such as chimpanzees and squirrel monkeys (K. C. Baker 1996, Maclean et. al. 1987, Mendoza and Mason 1989, Olfert et. al. 1993, Prince et. al. 1989, Young et. al. 1996). K. C. Baker (1996) concludes that even one or two conspecifics are not sufficient to meet the extraordinary social needs of chimps in stimulus-restricted environments. Macaques, vervets, and squirrel monkeys have been successfully kept in medium-sized groups. So far, large social groups exist only at a few zoos and laboratory breeding colonies.

Social compatibility can be influenced by environmental structure and complexity (Chance et. al. 1983). Appropriate enclosure size, design, and furnishings can make attempts at social housing and the process of introduction more successful. In one group of chimps, aggressive behavior increased as enclosure space decreased (Howell et. al. 1993). Two unfamiliar individuals, at first pairing, may actually require more than twice the minimum space required by USDA for each individual alone because of the distance they feel they must maintain from each other. As previously discussed, there must also be room enough for appropriate social signals.

Physical features such as visual barriers, privacy panels, mesh dividers, multiple shifting points, escape routes, refuges, and perches have all been recommended to increase chances of successful pairing or grouping (Adang et. al. 1987, Aureli et. al. 1997, Bettinger et. al. 1994, Bramblett 1989a, Fouts 1989, Fritz 1986, Fritz 1989, Goosen et. al. 1984, Mendl and Newberry 1997, Prince et. al. 1989, Seier 1996, Watts and Meder 1996). Williams et. al. (1988) found that among mixed-sex group-housed squirrel monkeys, housed in cages with perches at multiple levels, males (which are subordinate to females) occupied perches below those preferred by females. Without a choice of perches, males were forced to stay on the floor. Mesh tunnels, connecting passages, coupled cages, and large exercise pens have been used to facilitate social introductions and periodic social contacts (Buchanan-Smith 1997, Field et. al. 1992, Lynch and Baker 1998, Marriott et. al. 1993). Primates in zoos need appropriate visual barriers or psychological distance from human visitors (Chamove et. al. 1988).

Food, water, shelter, and enrichment devices should be distributed to reduce hoarding (Lynch 1998 ). Foraging enrichments that disperse individuals and occupy their time can reduce tension and distract them from aggression (Boccia 1989). Behavior modification techniques, such as those used for most animal training, reduced social aggression in chimps (Bloomsmith et. al. 1994).

Nearly any two conspecifics might be housed together "compatibly" given just the right environment. For some individuals, this could entail huge, complex enclosures that contain a large inter-individual distance. Even two very compatible individuals may become aggressive towards one another if crowded into a barren space for a long period and subjected repeatedly to additional inescapable stress. These extreme hypothetical cases illustrate that social compatibility exists along a continuum that can vary with other factors. Animals should not be judged unsocializable on the basis of their behavior under conditions approaching the latter example. Rather, an appropriate physical setting must be provided to accommodate social living.

There is no doubt that successful pair or group housing of primates requires the proper caging and equipment. In order to maximize the potential psychological benefits of social housing and minimize the risks to animal well-being, individuals must have the right kind of space for social adjustments. In addition to the enclosure dimensions that accommodate interaction, the space must be shaped and furnished so that postural and other social signals can be used by the animals to maintain relationships, as in the wild. Caging systems need to be adapted to suit appropriate social grouping rather than the reverse. Resources such as food and water, resting sites, and enrichment devices also need to be chosen and distributed to respect mechanisms for maintaining social relationships.

Positive interaction with humans can improve the social environment for captive primates (Bayne et. al. 1993b, Bloomsmith et. al. 1997, K. C. Baker 1997b ). Although it should not replace the conspecific social interaction intended by the regulations, positive interaction with humans is valuable in two situations:

Many regard a positive, relaxed relationship with human keepers as one of the most important components of captive primate well-being (Poole 1997b, Reinhardt 1997e). Reinhardt warns of potential problems with keepers who appear dominating and intimidating. Those who work with primates must be knowledgeable about primate gestures and vocalizations to avoid inadvertently threatening or stressing primates with their own movements and body language (National Research Council, Institute for Laboratory Animal Research 1998).

The activities and presence of humans may also have significant negative effects on primates. At three chimpanzee breeding facilities, births occurred significantly more often during periods of low human activity (at night and on weekends). This was attributed to the greater privacy and reduced stress during such times (Alford et. al. 1992). Line et. al. (1989b) found that even routine events like cage cleaning caused elevated heart rates for several hours. On the other hand, Line (1995) also found in another project that study observers had no significant effect on most primate behaviors and that "a period of habituation to an observer...is not always necessary". Thus, unfamiliar humans who must enter a primate area occasionally to make observations, may be able to avoid influencing behavior unduly just by remaining calm and avoiding threatening actions, such as direct stares.

At many facilities, programs of animal training using positive reinforcement techniques have been successful in reducing the stress that normally accompanies manipulations by humans. The cognitive stimulation and pleasurable interaction with humans that such training entails may in itself be enriching (Laule and Desmond 1998). Reinhardt (1997d) collected 46 published reports on the training of primates to cooperate with clinical and husbandry procedures such as shifting from cage to cage, capture, venipuncture, urine collection, and drug administration. Traditional stressful methods of manual restraint and handling are often unnecessary (Reinhardt et. al. 1995a). In only 21 days, Drea (1998) trained a colony of 55 rhesus macaques to repeatedly divide themselves into two groups for a social behavior study. Scott (1990) criticizes training methods using food deprivation. Gifted animal trainers in the film and animal exhibit industry have successfully trained many animals to consistently perform complex tasks, without resorting to water or food deprivation.

The social needs of most primates cannot be completely met by single housing. As previously discussed, social primates are very much physical contact animals. Continuous full contact housing, in pairs or appropriately structured social groups allows primates to express sophisticated social adaptations (Jane Goodall Institute 1988, Prince et. al. 1989, Visalberghi and Anderson 1993). Walsch et. al. (1982) concluded that chimpanzees' "opportunities for visual and auditory contact with conspecifics, in the absence of tactile contact, do not appear to significantly reduce levels of disturbance." In situations where continuous social housing is not appropriate, due to the health or personality of the individual animal or to research protocol requirements, caging allowing periodic full contact or even partial contact with conspecifics can be justified with appropriate supporting evidence (Bayne 1991, Taylor et. al. 1998). The more socially restrictive the housing arrangement is, the more rigorously it must be justified.

This does not mean that every individual primate must be forced into social contact. There will be situations where single housing would still be preferable to contact with unsuitable conspecifics. For example, an adult male owl monkey would be more appropriately housed alone, than with another adult male, if that is the only social partner available (Baer 1994).

Companions do not just meet innate social needs in primates. A compatible companion supplies environmental novelty, multi-sensory stimulation, something to manipulate, and opportunities for cognitive challenge and control. Appropriate social enhancement is one of the most versatile and option-laden forms of enhancement we can provide.

Psychological well-being in primates depends on appropriate infant development. Reproductive success (including reproductive behaviors, fertility, prenatal adequacy, parturition, and parental care) is generally considered to be the strongest indicator of psychological well-being in captive nonhuman primates (Novak and Suomi 1991). It is necessary for primate individuals to learn appropriate behaviors to allow them to function in their captive environments. Experiencing effective parenting at an early developmental stage allows the young primate the opportunity to grow into a healthy and responsive adult. The young primate ideally will translate positive early experiences into subsequent social skills, including parenting (Suomi 1986.)

Developmental sequences in young primates may be characterized in the following manner. The neonatal primate is termed an infant until the time it can survive its mother's death. This period encompasses weaning. Infancy is followed by the juvenile stage, which takes the young primate up to the onset of puberty. After puberty, but before reproduction, the primate is considered an adolescent. It must be noted that these definitions are imprecise and are not used consistently across species (Walters 1987).

Infancy in primates is characterized by a variable period of helplessness and dependency. The mother provides nourishment, transportation, protection, and education. The newborn's survival is critically dependent on establishing and maintaining a satisfactory relationship with its mother (W. A. Mason 1986). It must also be recognized, the infant is an active participant in its own postnatal development. W. A. Mason (1971) characterizes the developmental trends in infant primates as a balance between two functional systems: filial ("mother-directed") and exploitative ("other-directed"). Both functional systems exist concurrently in varying degrees throughout the life of the developing primate. As expected, mother-directed behaviors predominate in the neonate: clinging, rooting, and sucking. These behaviors reduce infant arousal and anxiety. This, in turn, enhances the formation of filial attachment. A shift toward exploitative behaviors, such as investigation and play, evolves as the infant develops and interacts with its environment.

Weaning commences as the infant matures. The weaning process consists of two concurrent processes: behavioral weaning and nutritional weaning. Nutritional weaning is completed at the time the infant is no longer dependent on the mother for total provision of food. As the infant grows, the diet is increasingly supplemented with other foods eaten by members of the same species, including insects, fruit, and vegetation. Typically this is a gradual process. Behavioral weaning extends beyond the conclusion of nutritional weaning. This transition encompasses the period during which the infant may nurse, not primarily to obtain food, but to obtain comfort and reassurance during times of stress (Byrne and Suomi 1995, Goodall 1986, Van Roosmalen and Klein 1988). The infant will seek to prolong this period as a means of maintaining the mother-infant bond.

Harvey et. al. (1987) have noted the weaning age in primates is strongly correlated with neonatal body weight. Ranges for weaning ages extend from the relatively brief (2 months for some callitrichids) to very long (52 months for some gorillas).

Continuing development in the young primate is influenced by a variety of factors. The age at which an infant will attain independence varies by species. Social structure and group dynamics may play a role in development, depending on species and situation (Milton 1993, Nash 1993, Watts and Pusey 1993). In some species, the presence of alloparents and/or peer conspecifics is essential to promote appropriate development (Worlein and Sackett 1997, Young et. al. 1996). Resource availability, such as proper nutrition, adequate usable space, and privacy, may have profound impact on development. The ability to play with others, including parent(s), conspecific peers, or surrogates, enhances the acquisition of locomotor and social skills (Fagen 1993, Fairbanks 1993, Govindarajulu et. al. 1993). Individual variations within a species must also be considered: a confident, secure animal may show independent characteristics earlier than a weak, submissive one.

The optimal situation in which any primate should develop is one that permits the infant to remain with its biologic mother through weaning in the company of a species-normal social group (Pazol and Bloomsmith 1993, W. A. Mason 1991, ). International Primatological Society (1993) guidelines recommend the young of most species should be allowed to remain in contact with the mother until at least 12-18 months old. Primate Vaccine Evaluation Network (PVEN) guidelines state infants should not be weaned before 6 months and recommend weaning at 12 months old (Poole and Thomas 1995).

Early studies by Harlow and Harlow (1965, 1972) tested the importance of affectional systems in the developing primate by subjecting newborn rhesus macaques to an array of deprivation. Reared in total or partial social isolation, these infant monkeys could not function socially as they matured. They demonstrated inadequate play, social behaviors, and, later, abnormal sexual and maternal behaviors. Other studies by Harlow et. al. (1963) showed that motherless infant rhesus monkeys could be reared with more success in peer groups. These monkeys bonded strongly with each other, as manifested by increased clinging behavior. When the clinging behavior was discouraged, however, the infants exhibited play behaviors which approximated adequate social adjustments. Surrogate studies by Harlow revealed infants separated from their mothers and reared in the presence of various surrogates (inanimate models) exhibited varying degrees of disturbed behaviors. However the degree to which these youngsters displayed aberrant behaviors was less than it was for maternally-deprived infants reared without any surrogate interaction. Other surrogate studies have evaluated the use of simple objects such as shaped wire forms, the complex interactions with conspecific peers in a nursery environment, and interactions with unrelated adults or phylogenetically remote surrogates such as dogs (Pazol and Bloomsmith 1993, Rumbaugh et. al. 1989, W. A. Mason and Kenney 1974, W. A. Mason and Capitanio 1988). In general, these studies found the closer the surrogate approaches species-specific maternal nurturing behaviors, the better the infant's chances are to develop adequate and appropriate behavior. No combination of maternal, surrogate, and/or peer contact is quite as effective as the species-typical, mother-peer group in producing completely normal animals. However, for rhesus monkeys, surrogate rearing with daily, but not continuous, contact appears to be the best approximation among the commonly compared regimens (Bayne and Novak 1998, NRC/ILAR 1998).

The response of the infant nonhuman primate to the loss of the mother-figure has been the focus of considerable research effort. These inquiries have sought to elucidate the dynamics of the mother-infant relationship. For the infant, maternal separation or loss is accompanied by a complex series of behavioral and physiological changes. Initially, an agitation/protest phase is observed, characterized by increased locomotion, distress vocalizations, and oral and ingestive behaviors. This phase is followed by a depressive/despair phase, in which the infant becomes increasingly withdrawn and despondent, manifesting reduced locomotion, slouched postures, and diminished interest in play activity. The degree to which an individual infant will exhibit these phases is influenced by a variety of factors: species, age, familiarity with the environment, presence or absence of alloparenting or other social support figures, and intra specific individual variations (Mineka and Suomi 1978, Worlein and Sackett 1997).

In many species, a history of nursery rearing is correlated with various abnormal behaviors in juveniles and adults. These include self-aggression, self-clasping, bizarre postures, rocking, regurgitation with reingestion, locomotor stereotypies, and others (Capitanio 1986, Gould and Bres 1986, Marriner and Drickamer 1994, Platt et. al. 1996). In chimpanzees, it is associated especially with body-rocking and self-clasping (Walsch et. al. 1982). Spijkerman et. al. (1994) found that of various rearing conditions, only rearing by the chimpanzee mother in the presence of peers did not result in development of rocking behaviors. Others found neither human contact nor peer contact were as effective as dogs in mitigating body rocking (Pazol and Bloomsmith 1993).

Infant physiological parameters are also profoundly affected by the disruption of the mother-infant bond. Studies of separated infant squirrel monkeys by C. L. Coe et. al. (1985) demonstrated changes in the level of circulating complement proteins and immunoglobulins and decrease in the capacity to mount an antibody response to an antigenic challenge. These findings are supported in other primate species: titi monkeys (Mendoza 1991) and bonnet and pig-tailed macaques (Laudenslager et. al. 1990). a study comparing pig-tailed macaques remaining with their mothers for the first 1.5 years of life to pig-tailed macaques separated from their mothers for as little as two weeks during the first year of life showed an association between separation and deficient immune responses in adulthood (Laudenslager et. al. 1985). The detrimental immunologic effects of maternal separation in primates can be buffered by allowing the infant to remain in the home cage and providing a familiar companion (C. L. Coe et. al. 1987a, Laudenslager and Boccia 1996). Disruption of the maternal-infant bond decreases heart and body temperature, as well as disturbs sleep patterns and EEG activity (Reite et. al. 1981). For reviews of the immunologic effects of maternal separation, see C. L. Coe (1993) and Capitanio (1998).

Research efforts have provided much information about negative effects on developmental processes, especially detrimental effects of isolation and early maternal separation. For many species we have an idea of what constitutes lack of well-being. (See Fouts et. al. 1989). It is much more difficult to quantify the positive side of well-being. Psychological well-being is not merely the absence of behavioral pathology and abnormality, however defined. It is something positive. But what? We have gained some insight into what situations to avoid when raising primates, but are only beginning to understand the components of a beneficial, species-appropriate environment. Optimal, as opposed to merely adequate, social and nonsocial infant development, is still to be defined.

A plan to enhance appropriate infant development within a primate population must address many factors. Physical environment is an obvious starting point. First, the plan must ensure that there is adequate space to express species-typical behavior. Both floor space and vertical space must be considered. Increased cage complexities (for example, ropes, swings, and shelves) allow for expression of species-typical locomotor activity and provide opportunities for play. Nesting materials, visual barriers, and refuges can add comfort to an enclosure. Some degree of control over their environment can offset stress in many individuals (Mineka et. al. 1986). Provision of manipulanda and the ability to move freely within the existing environment can ameliorate an animal's sense of helplessness and also decrease the level of frustration inherent in some types of captivity.

Social factors are also essential considerations in planning appropriate infant development. Family history, social groupings, age/sex mix, social rankings, individual personality and temperament play important roles, in addition to intrinsic species variations. Witnessing good mothering first hand allows females to observe and learn appropriate nurturing behaviors that they may later apply to their own infants (Miller-Schroeder and Patterson 1989).

To summarize, in most situations, the developing infant's optimal captive environment approximates what it would encounter in the wild, if the natural habitat were undisturbed and risk free. Expression of species-typical behaviors among members of the natal group permits the young primate to learn its role within the culture of its species community. When this structure is provided, infant development can flourish.

Although we have stressed the importance of not disrupting the bond between the infant and its parents or natal group, there are situations in which allowing the infant to remain may also be a source of problems. Cases of infanticide, parental neglect, and abuse of offspring have been noted in both wild and captive environments. Aggression directed toward infants may be perpetrated by family members or unrelated members of the troupe. In captivity, this situation may necessitate removal of the infant from the hostile environment for its own safety. The decision to separate mother and infant introduces a constellation of factors to consider, including: species; health status; age and level of development and independence; availability of foster or surrogate care givers or peer groups; and the feasibility of later re-introductions.

The social, developmental, and physical environment are interdependent in enhancing psychological well-being. The most basic components of the physical or inanimate environment are the enclosure structure (its size, shape, and design) and the substrates within it (J. Coe 1989, Maple and Perkins 1996, Poole 1991b). Although the term "substrate" commonly refers to the "base on which an organism lives" and would include flooring, turf, sand, soil, and bedding materials, in this section we include furnishings, perches, swings, ropes, ledges, nest boxes, barrels, culverts, and water features as well. These components should combine to create opportunities for species-typical resting, exploration, play, and foraging, as well as social interaction and adjustments (Prince et. al. 1989, Schapiro et. al. 1991, Thompson 1996). The enclosure should allow normal postures and a range of locomotion (Buchanan-Smith 1997, Dahl 1989, EEC 1986, Home Office 1989, International Primatological Society 1993, Marriott et. al. 1993, Olfert et. al. 1993, Poole 1991b, Poole and Thomas 1995, Poole et. al. 1994, Reinhardt 1997b, Snowdon and Savage 1989, Whitney and Wickings 1987).

In order to accommodate species-typical behavior, the enclosure must have adequate space. Use of legal cage size will not always meet an animal's behavioral requirements (NRC/ILAR 1998:18).

Adequate space is not just a question of numeric dimensions or total volume, but also one of shape and design. The space must be structured to be useable and species appropriate. This can be achieved through a variety of furnishings, projections, contours and floor coverings (Chamove and Anderson 1989, Maple and Perkins 1996, NRC/ILAR 1998, Poole 1991b, Schapiro et. al. 1991).

Primates display a variety of different comfort postures during resting and sleeping similar to those of other animals and humans: lying down; sprawling out prone, sternally or laterally; sitting upright; and crouching (Fleagle 1998, McGraw 1998). Vertical clinging is a normal resting, feeding and vigilance posture for many nocturnal prosimians, tarsiers, and callitrichids (Fleagle 1998). There must be something in the cage to which these animals may cling. Squirrel monkeys sleep hunched with their tails curled between their legs and up over their shoulders (Baldwin 1985). According to Abee (1985), large diameter tubular perches provide comfortable, contoured, and stable resting surfaces for squirrel monkeys and prevent the development of pressure sores at the base of the tail associated with the use of flat shelves or boards. Many prosimians, callitrichids, and owl monkeys use nests or cavities for sleeping (Rowe 1996).

In nature, great apes build night and day nests of soft materials. They appear to be painstakingly constructed for comfort (Fruth and Hohmann 1996, Maple and Perkins 1996, Van Lawick-Goodall 1968). While orangutans build their nests only in trees, chimpanzees, bonobos, and gorillas also build them on the ground (Tuttle 1986). Chimpanzee night nests are generally more elaborate than those constructed for day time naps (Van Lawick-Goodall 1968 ). Chimpanzee nest building skill appears to be learned from elders, with first attempts at eight months of age (Fruth and Hohmann 1994). Human-raised, captive chimpanzees removed from their mothers at birth were unable to construct good nests in adolescence or adult-hood, although some made rudimentary efforts and all manipulated the materials (Bernstein 1962). Suitable materials to facilitate development and expression of nest building include both artificial materials, such as blankets and shredded paper, as well as more naturalistic materials. Even chimps with no prior exposure to nest-construction benefit from these materials as manipulable items (Jane Goodall Institute 1988, K.C. Baker 1997a). Some ape breeding colonies and sanctuaries have provided chimpanzees with elevated "tire hammocks" (tires chained together in clusters), their contour and shape mimicking an arboreal nest.

In designing enclosures for primates with long tails, one must take into account the position, angle and length of the tail so that it may be unobstructed and held comfortably in a normal manner (NRC/ILAR 1998). Goosen et. al. (1984) recommend that for long-tailed macaques, shelves should not be flush against a wall but should have a space between the edge and the wall through which the tail may hang. Poole (1991b) and Reinhardt et. al. (1996) demonstrate that many of the standard legal-sized laboratory cages for adult long-tailed macaques, including those given in the weight-based table of the minimum standards under the Animal Welfare Act, are not tall enough to permit a normal perching posture. Either the animal's head will be obstructed or its tail must be held up to avoid dragging in the waste pan. Cages of this height are inadequate for the "normal postural adjustments" and certainly for the "normal postural adjustments with adequate freedom of movement" required by USDA regulations in 9 CFR Section 3.80(a)(2)(xi). Species with certain anatomical features "might require a taller cage than other species of the same body weight." (NRC/ILAR 1998:26)

As previously discussed, a variety of postures, including tail positions, may be used in social adjustments. An enclosure should have proper dimensions to allow this. Vervets may hold their tails straight out from the body, more than doubling their effective body length while quadrupedal (Estes 1991). New World species use their prehensile tails as a fifth limb (Fleagle 1998). Tail-suspension postures are used in feeding and exploration and for locomotion (Gebo 1992). Prehensile or non-prehensile tails may also be used for support or counterbalance (Baldwin 1985, Fleagle 1998). The Canadian Council on Animal Care (CCAC) Guidelines specify that to engage in normal postures, New World primates with prehensile tails should be provided with linear vertical space about four times the length of their body (Olfert et. al. 1993).

All of the apes use their arms and/or feet for suspensory postures. In chimpanzees and gorillas these are more commonly observed in juveniles than in adults (Baldwin 1985, Goodall 1986, T