Response to USDA Draft Policy on Environment Enhancement for Non-Human Primates

Docket No. 98-121-1
Regulatory Analysis and Development
PPD, APHIS, Suite 3C03
4700 River Road Unit 118
Riverdale, MD 20737-1238

To Whom it May Concern:

We wish to submit the following comments pertaining to Docket No. 98-121-1, described in the Federal Register (Vol. 64, No. 135) as 'Draft policy on environment enhancement for nonhuman primates' (hereafter referred to as the 'Policy').

The present comments originate from an ad hoc committee of the American Society of Primatologists, convened to study the Policy and to determine whether the Society should make a response. The committee-members, listed at the end of this document (Appendix 1), agreed that a response to the Policy would be appropriate. Comments were solicited from the Society's membership, as well as from non-members who are likely to be involved in the implementation of the policy (including staff scientists at primate facilities, colony management personnel, veterinarians, and IACUC members) in an effort to understand concerns from a broad range of perspectives. Comments were also made by the committee-members, who are primatologists and have expertise in well-being issues. The comments were collated, and multiple drafts created before a final draft was submitted to the Society's Board of Directors. The present comments reflect a final version, approved by the Society's Board (members of which are also listed at the end of this document in Appendix 1). We note at the outset that while not every individual who submitted comments to the committee (nor every Society-member) may agree with every recommendation contained in this document, that the present comments reflect a good faith effort to provide useful comments that reflect a) the interests of many members of the Society; b) a response that reflects a surprising degree of consensus among the committee-members and that is acceptable to the Society's Board of Directors; and c) recommendations based both on scientific evidence that the original framers of the draft policy may have been unaware of, and the substantial expertise of committee- and Society-members with nonhuman primates. We hope that these comments are considered useful.

We wish to express our appreciation to USDA for permitting the public to comment on the Policy. We realize that public comment was not required, and presume that it was solicited because of the importance of the topic, both to those who are regulated and to the public at large. We also appreciate USDA's willingness to extend the comment period for 30 days, in order to generate a more full set of comments. Finally, we wish to commend those involved in the literature review (published as the 'Final Report on Environment Enhancement to Promote the Psychological Well-being of Nonhuman Primates') that underlies these recommendations. As the reference section of that document indicates, it is a voluminous literature, and its comprehensive review was no small feat.

We hope that USDA finds these comments useful.

Sincerely,

Nancy G. Caine, President
American Society of Primatologists

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Executive Summary

The ad hoc committee of the American Society of Primatologists identified a number of areas in the USDA's 'Draft policy on environment enhancement for nonhuman primates' (hereafter referred to as the 'Policy') that were of concern. These areas reflect:

1. a concern about variability in expertise in nonhuman primate behavior among all regulators, which could lead to inconsistent interpretation and enforcement of the Policy;
   
   
2. the cost and timing of implementation of the Policy's recommendations;
   
   
3. a need to rethink the hierarchy of social housing options proposed in the Policy;
   
   
4. the idea that many aspects of experimental manipulation and training activities of animals can be positive experiences for animals, and should not be summarily excluded as a component of a facility's environmental enhancement program;
   
   
5. that the social needs of infants can be met in ways that do not necessarily involve the infant remaining with its parent until age of independence;
   
   
6. vagueness in what constitutes 'documentation';
   
   
7. and that the issues of 'novelty' and 'control' are more complex than is currently considered in the Policy.

The document discusses these and other issues in some detail, and includes suggestions for USDA's consideration. We also offer the expertise of our members, and the venue of our annual meetings, to facilitate information exchange, training, and compliance with the Policy.

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I. General comments.

I.A. Expertise.

I.A.1. The stated goal of the Policy is to 'assist regulated entities by clarifying what actions we consider necessary in order to comply with the requirements of Section 3.81' [of subpart D of 9 CFR Part 3]. From USDA's perspective, having some explicit guidelines can make the job of assessing compliance easier. We wish to note, however, that from our perspective (i.e., we are members/employees of regulated entities) such guidelines can also serve to address what many of our Members have indicated is a continuing concern: variation in judgments about what constitutes compliance or violation. That is, the regulators and the regulated may see these guidelines from different perspectives (although both aiming for the same goals, consistency in compliance with the Animal Welfare Act). An important reason that ASP is responding to this Draft Policy is to provide USDA with some ideas about where in the proposed guidelines members of the regulated community see potential for differences in interpretation among regulators.

I.A.2. A major concern is variation in primate behavioral expertise, at all levels of regulation, from the facility's enrichment coordinators, to the facility veterinarian, to the institutional animal care and use committee (IACUC), to the USDA Inspector, to the Deputy Administrator of Animal Care (to whom a regulated entity may turn for approval of a plan that is not in accordance with the Draft Policy [p. 38146]). In an important sense, psychological well-being is a behavioral concern. Many members of the Society have devoted their careers to understanding primate behavior, and can appreciate the richness within the primate Order that is a reflection of species differences, individual differences, the roles of early history, age, and endocrine status, the importance of life-history variables such as foraging and activity patterns, social status, and so on. ASP is concerned that important decisions, which could limit the intended use of the animals (whether for research, exhibition, or education), could be made by individuals who possess a limited background in primate behavior, who may be unaware of the relevant scientific literature (related to what is, as well as what is not, known), and who may be unfamiliar with the particular species under consideration. Many of our comments below reflect the Committee's understanding of the scientific literature on primate behavior. More importantly, some of our comments reflect important gaps in our knowledge of these animals; in the absence of empirical data, what criteria should be used by regulators to make a decision in a particular case? The variation that exists among individuals in their knowledge of the complexity of primate behavior, and of the scientific literature, is likely to continue to be a major cause of why different inspectors and personnel at different institutions vary in their interpretations of the regulations.

I.A.3. We propose some options for remedying this concern. First, the American Society of Primatologists is willing to assist the USDA in any way USDA deems relevant to educate individuals across all levels of regulation with the most up-to-date scientific information that is available. Furthermore, when scientific information is not available, we offer the expertise of our members in attempting to find a solution to a problem. This assistance can take many forms, from staging seminars for regulators, to assisting in the development of an expert panel that might be consulted for unusual or difficult cases, to recommending specific individuals who would agree to be consulted to provide information on a case by case basis.

I.A.4. As a second possible remedy, we offer to provide methodological expertise in developing an assessment strategy that inspectors could use for facilities, that demonstrates good measurement characteristics, namely, reliability (different individuals make the same judgements about the same situation with a reasonable level of confidence) and validity (judgements are related to important and demonstrated outcomes). This could involve developing a set of scenarios that regulators could use for training purposes, or other materials that facility, institutional, and federal regulators can turn to in order to create as much consistency as possible between institutions and between inspectors in the shared goals of compliance with the regulations.

I.A.5. Third, we suggest the USDA consider having a small number of inspectors who specialize in nonhuman primates. Such individuals could have extensive experience (or receive targeted training) in nonhuman primate behavioral biology. A specialist team would also greatly increase consistency among inspectors in applying criteria for compliance. Given the unique position of nonhuman primates within the regulatory environment (i.e., phylogenetic proximity to humans; greater expense involved in their care and maintenance; greater need for psychological stimulation; as well as the greater concern that this taxon of animals has generated among the lay public), such a remedy may be a particularly effective way to achieve our common goals.

I.B. Cost and timing of implementation.

I.B.1. The cost of implementing some of the recommendations in the Policy may be excessive. For example, mandating that animals must have access to continuous tactile contact with another animal would involve the purchase of new (or the retrofit of old) cages that could number into the hundreds at any given facility. Moreover, the personnel costs to implement the Policy are also likely to be extreme. For example, a large number of animals may need to be housed individually, due to research protocols involving infectious diseases. Requiring individually housed primates to have 'daily positive interaction with compatible human care givers ... of sufficient type and duration to compensate for restricted social housing' could result in large primate facilities needing to hire many new staff members. Given that many large facilities are federally funded (e.g., Regional Primate Research Centers), it is not clear how compliance can be achieved within existing budgets.

I.B.2. An important issue with respect to cost is how soon institutions will be expected to comply with the Policy. We urge USDA to specify a time-frame (and, if necessary, a sequence of steps) that institutions can follow that will demonstrate good faith efforts on the part of institutions to comply, at a time when they are technically not in compliance with the Policy.

I.C. Compatibility with the different functions of regulated institutions.

I.C.1. The Policy is intended to apply to 'dealers, exhibitors, and research facilities'. We are concerned that these three types of facilities have very different goals and functions, and that portions of the Policy, which may have been drafted to deal with one type of facility, could adversely impact the aims of another type of facility. For example, as currently written, only 4 options are available for social housing, the most restrictive of which involves animals housed without continuous access to visual, olfactory, auditory, and tactile contact. These animals must, however, be provided with daily positive interaction with humans, as described in paragraph I.B.1. above. It may not be feasible to provide animals on infectious disease studies with extensive human contact, for biohazard and liability reasons. Such a rule could seriously impede the aims of the research facility. Meeting the requirement for tactile contact in housing may be easier to achieve in a zoological garden, however, where the biohazard concerns and personnel options (e.g. greater use of volunteers) may be quite different. We recognize, however, that trying to fix this problem by broadening the options for social housing (which we in fact propose below), could lead to other problems at other types of facilities. Because we do not know all of the complexities involved in the unique operations and problems with compliance among these three types of facilities, we suggest that USDA consider specific recommendations for specific types of facilities, and designate the recommendations as applicable only to those facility-types.

I.D. Alternative plans.

I.D.1. As indicated in paragraph I.A.1. above, the stated goal of the Policy is to 'assist regulated entities by clarifying what actions we consider necessary in order to comply with the requirements of Section 3.81' [of subpart D of 9 CFR Part 3]. Yet, on page 38146, we read that 'if a dealer, exhibitor or research facility wants assurance that an alternative plan (not in accordance with the draft policy) is in compliance with S. 3.81, they may request approval of the plan in writing from the Deputy Administrator of Animal Care.' It is unclear how an entity can escape accordance with a Policy that specifies 'necessary' actions, but remain in compliance with S. 3.81.

II. Social grouping.

II.A. General concerns.

II.A.1. We have no argument with the general conclusion that primates have social needs that must be met to adequately promote their psychological well-being. However, we believe there are several problem areas that could benefit from changes in wording and emphasis.

II.A.2. The emphasis that a facility's environmental enhancement plan "must address the social needs of nonhuman primates of species known to exist in social groups in nature" ignores the social needs of primate species that spend little time in groups. Nocturnal prosimians (e.g., galagos), fission-fusion species (e.g., spider monkeys), and "solitary" primates such as the orangutan should not be excluded from a plan to address social needs. We believe that all primate species have social needs that should be addressed in environmental enhancement plans. Therefore, we recommend deletion of the phrase "of species known to exist in social groups in nature" from the first sentence of this section of the policy.

II.A.3. We also feel strongly that in providing the opportunity for social interaction, members of the same species should be favored over other compatible species. The preferred option should be "compatible primates of the same species."

II.A.4. We disagree that a "species typical grouping" is necessarily the best method for meeting social needs in all captive situations. "Species-typical" groupings are most often the result of adaptations to the particular ecological situation in which wild primates find themselves. For example, baboons and macaques live in multi-male, multi-female groups in the wild, but such groups in captivity are successful ONLY when there is sufficient space for subordinate males to distance themselves from more dominant males. If such space is not available, subordinate animals will be harassed and may be killed. Therefore, in some captive situations, other social options may be preferred, such as harem groups (one male, several females). For captive harem groupings of species of the female-bonded type, such as macaques and baboons, groupings including female kin that are seldom disrupted are particularly compatible. In general, we know of no data supporting the assertion that social needs in captivity are best met in social groupings (group size and composition) mimicking those found in the natural habitat.

II.A.5. There are important issues of timing of social grouping, especially with respect to the start of an experiment. Not cited in the literature review ('Final Report on Environment Enhancement to Promote the Psychological Well-being of Nonhuman Primates') was an important recent study (Capitanio, J.P., Lerche, N.W. Social separation, housing relocation, and survival in simian AIDS: A retrospective analysis. Psychosomatic Medicine, 1998, 60, 235-244) demonstrating that the strongest predictor of shorter survival in SIV-inoculated rhesus monkeys was social housing (specifically, pair- or group-housing, but not infant-mother). The authors speculated that the reason for this negative effect was at least partially due to how and when the groups/pairs were formed, in this case involving animals that had mixed familiarity, and with groups mostly formed just prior to SIV inoculation. Thus, there are circumstances where providing social housing can seriously interfere with the conduct of the research. The cited study illustrates that facility management prior to primates' assignment to a research project can impact that study's outcome.

II.B. Housing options.

II.B.1. We disagree with the assertion that continuous social grouping is always the best way to meet social needs in captivity. In the natural habitat, animals can separate themselves from others spatially and do not engage in social interactions continuously. The spatial constraints of captivity, especially in pair-housing or small-group caging, can be stressful, especially to subordinates of species with strongly delineated dominance hierarchies. Thus, part-time physical social contact may be the best way to promote psychological well-being for individuals of particular species, temperaments, ages, sex, or housing types. For example, animals might be pair-housed for part of the day, and separated by closing panels for the rest of the day. Or they might be housed in adjacent caging with bar or mesh spacing large enough to permit social grooming. We wish to point out that continuous social housing may be inconsistent with the additional Policy criterion of "Control," (Section X below) and that the smaller the enclosure, the greater the limitations to enclosure design in providing visual and physical escape. Furthermore, injury and overt compatibility are not the only measures for assessing whether psychological well-being has been promoted. The possibilities of social stress, depression, and immune system compromise seem to be ignored in the Policy.

II.B.2. Tactile (physical) contact can be provided in three ways: 1) in an enclosure or cage large enough for two or more individuals (i.e., shared space); 2) in adjacent cages specifically provided with bars or mesh that are spaced widely enough to allow comfortable social grooming (e.g., Washington Regional Primate Research Center's grooming-contact cages, Crockett, C. M., Bellanca, R. U., Bowers, C. L. & Bowden, D. M. 1997. Grooming-contact bars provide social contact for individually caged laboratory macaques. Contemp. Top. Lab. Anim. Sci., 36, 53-60); and 3) by reaching out of the cage in an unintended, usually awkward manner to touch a neighbor. Clearly, we can rate number three as the least desirable way, but there are some situations in which grooming-contact (providing more choice and control) is preferable to shared space. Social contact in shared space may be especially important for infants and juveniles to permit contact play behavior, but it need not be continuous to allow for normal behavioral development. In fact, continuous social contact with peers appears to be detrimental to infant pigtailed macaques raised without adults (see references listed in Section III.C.2. below).

II.B.3. We feel that the Draft Policy does not acknowledge significant facility type, species, and individual differences that must be taken into account in meeting social needs while simultaneously promoting psychological well-being. The Policy indicates that Option 1 (continuous social grouping) is designated as the preferred option, and any deviation must be justified in an institution's plan. If Option 1 is not the best for all primates, however, facility managers will find themselves in the position of having to justify in writing why the USDA recommendation is inappropriate for their circumstances. Furthermore, we do not find evidence in the published literature to support ranking Option 1 over Options 2 and 3. Note that Option 4, as written, implies that the animals are housed alone in isolation.

II.B.4. If daily visual, olfactory and auditory contact is the extent of a primate's "social interaction," then the Policy recommends the animal should be given extra enrichment and daily positive interaction with compatible human care givers. Note that Section A, Option 4, as written, implies that the animals eligible for extra human interaction are housed alone in isolation. There are some important issues with the concept of providing "substitute" social interaction by human care givers.

1. First of all, only some nonhuman primates readily interact with humans in a positive manner, e.g., allowing grooming.
   
   
2. Second, there is a biohazard inherent in human-nonhuman primate interaction that is especially acute in retrovirus-infected animals.
   
   
3. Third, by specifically excluding interactions during husbandry, veterinary, experimental manipulation, and training activities, the Policy negates the important role of these aspects of facility management in promoting psychological well-being. Instead of denying the relevance of these activities, the Policy should identify aspects of these activities that serve as positive social interaction. Training, in particular, can be used by the care giver to encourage a positive response by the nonhuman primate toward human primates. Human social interaction in the context of training, experimental manipulation, exhibition, and many aspects of husbandry and veterinary activities can be very positive and provide a meaningful structure for the social interaction. The interactions involving positive reinforcement should be distinguished from those involving punishment or negative reinforcement.
   
   
4. Fourth, while interaction with humans may be helpful to the animals, there is very little research in this area. In particular, we do not know if human interaction COMPENSATES for lack of interaction with a conspecific. It is possible that this may ultimately be shown to be an ineffective form of social enrichment.
   
   

II.B.5. We therefore propose that Critical Element A be revised from the terminology "Social Grouping" to "Social Interaction" or "Social Opportunities" or "Opportunities for Social Interaction." We think it is a serious mistake to set a policy whereby continuous social grouping (housing in shared space) is the default standard, and any other options for providing the opportunity for social interaction must be justified. We think instead that a facility's environmental enhancement plan should specify the minimum social interaction that will be provided without requiring specific exemptions (either by IACUC or Attending Veterinarian) and those circumstances that will require an exemption. The minimum standard should be permitted to vary depending on the type of facility as long as it is "in accordance with currently accepted professional standards as cited in appropriate professional journals or reference guides." Social interaction involving tactile contact with a conspecific is generally preferable to no physical contact, but intermittent (e.g., a period of time daily) or controlled contact (e.g., grooming-contact cages) may be preferable to continuous group housing and should be allowed under a facility's environmental enhancement plan. Consequently, we propose the following 5 housing options, and recommend that for Options a), b), and c) that the plan must provide an explanation and justification for the circumstances under which the various options are used. For Options d) and e) exemptions must be granted by the Attending Veterinarian or by the Institutional Animal Care and Use Committee:

1. Housing in an enclosure with one or more compatible primates of the same species. For group living species, species-typical groupings are encouraged when housed in appropriately designed space of sufficient quantity to support such a group.
   
   
2. Housing in an enclosure without another compatible primate of the same species, but with the animal having the opportunity for continuous visual, auditory, olfactory, and tactile contact with another compatible primate (such as through adjacent wire mesh or bars). For primate species in which grooming other primates is an important social function, sufficient tactile contact range is particularly important.
   
   
3. Housing with the animal having the opportunity for continuous visual, auditory, and olfactory contact with another compatible primate of the same species, but with tactile contact of Options a) or b) provided on a periodic basis, through scheduled social interaction with one or more compatible primates of the same species.
   
   
4. Housing with the animal having the opportunity for continuous visual, auditory, and olfactory contact but with limited or no tactile contact with a compatible primate of the same species. When consistent with biosafety considerations, additional daily positive interaction with compatible human care givers may improve the psychological well-being of some animals housed under this option.
   
   
5. Housing without continuous visual, auditory, and olfactory contact and no tactile contact with a member of the same species (e.g., housed alone in a room for quarantine), or housing providing social interactions only with a member of another species is least desirable. When consistent with biosafety considerations, additional daily positive interaction with compatible human care givers may improve the psychological well-being of some animals housed under this option.
   
   

II.B.6. Other suggestions.

1. We cannot find the specific provision in 3.81a "to be housed with other primates whenever possible." Therefore, we recommend deletion of this sentence entirely: "In order to address the social needs of nonhuman primates under Sec. 3.81(a), the plan must provide for each primate of a species known to be social in nature to be housed with other primates whenever possible."
   
   
2. With respect to reasons for exemptions from Options a), b), and c) as described above, we recommend USDA retain the four reasons listed in the draft report. We strongly recommend, however, that USDA provide clear guidance on what constitutes 'documentation' for reason number 2: 'Documented unavailability of compatible individuals'. We feel this could be interpreted to mean that all possible attempts (e.g., pairings) must have been tried before an animal is housed individually. At large primate facilities, this could be a herculean task.
   
   

II.B.7. Although we recognize that our primary comments on this section should be based on meaningful ways to promote psychological well-being through addressing social needs, the cost of the present draft policy must be reiterated (see also Section I.B.).

1. Section C of the Policy (Environmental Enrichment - Structure and Substrate), includes the following sentence: "Enclosures should be designed, constructed, and furnished to facilitate social introduction, reintroduction, separation, or temporary restraint." We fully agree that well-designed caging is necessary to provide for suitable social interaction. Many laboratory primate cages are inappropriate for providing meaningful tactile contact, and marginally capable of providing visual contact. Suitable caging is expensive, and facilities and their funding agencies must recognize that cost-cutting should not be done in the area of primate caging.
   
   
2. Introducing, assessing, monitoring, and documenting the compatibility of social partners is a nontrivial, labor-intensive activity. Staff assigned to such duties must be trained in nonhuman primate behavior.
   
   
3. Provision of significant positive social interaction to individually housed primates involving even 5-minutes per animal per day to 100 primates would be a full-time job for a single employee doing nothing else.

III. Social needs of infants.

III.A. General comments.

III.A.1. We agree that special attention should be given to infants and young juveniles, and that in most situations the optimal environment for infant development is one that allows the infant to remain with its biological mother through weaning in the company of a species-normal social group. However, there are both experimental and husbandry reasons why such rearing may not always be feasible. The following is intended to clarify two issues involved in alternative rearing: 1) the age at which animals can reasonably be separated from their mothers; and 2) the features of alternative rearing environments necessary to produce normal developmental patterns.

III.B. Age at separation.

III.B.1. We would suggest changing the sentence in Paragraph 3 from "Infants should not be permanently removed from the care giving parent(s) before an age that approximates the age of infant independence in nature" to "Ideally, infants should not be permanently removed from the care giving parent(s) before an age that approximates the age of completed weaning in nature". The definition of the original term "independence" is quite vague, and could be interpreted to mean anything from the infant's total reliance on solid food to the physical separation that emigrating males undergo at puberty. Where well-established norms are not available for a species, a conservative rule of thumb could be to use the normal spacing between infants in nature (e.g. for rhesus macaques, this spacing between infants is approximately 12 months). There is considerable evidence, however, that, using the 'reproductive success' criterion described in this section of the Policy, that separation from mother at an age that corresponds to only 25% - 50% of the completed weaning age may have no adverse impact AS LONG AS THERE IS A STRONG SOCIAL COMPONENT TO THE SUBSEQUENT HOUSING SITUATION. We believe the USDA should explicitly acknowledge this in the Policy, in order to prevent regulators and inspectors from adhering too rigidly to the criterion we propose. We emphasize that what should really matter is that the animals' social needs are met, not necessarily that they are met by a specific individual. We suggest adding the following sentence to the Policy, between the current first and second sentences in paragraph 4 of this section: "...than is optimal. We emphasize that meeting the animals' social needs, and producing healthy animals that are competent both reproductively and socially is the overarching goal, and we recognize that this goal can be met by earlier separation combined with foster-rearing and/or peer socialization with conspecifics. When infants must..."

III.B.2. In Paragraph 3, we would add at the end of the last sentence "or as part of an IACUC-approved protocol".

III.B.3. In Paragraph 4, we would replace "age of separation in nature" with ".age of completed weaning in nature", for the reasons given above.

III.B.4. In Paragraph 4, we would change "hand-raising" to "alternative rearing".

III.C. Alternative rearing environments.

III.C.1. Crucial features of any alternative rearing environment include not only some form of socialization, but also sufficient environmental complexity/stimulation to encourage infant exploration and the development of independence.

III.C.2. In general, we would recommend that infants NOT be peer-reared on a continuous basis. Full-time peer access, whether in a dyad or in a larger peer group, tends to promote intense clinging to the social partner(s) and delayed behavioral maturation--in large part because clinging is incompatible with exploration and development of complex social repertoires. As adults, continuously peer-reared animals show heightened aggression, decreased sexual performance, and minimal affiliative behavior. In contrast, surrogate-rearing or even single-cage rearing with daily peer contact (as little as 30 min./day, 5 days/wk) produces animals with quite normal behavioral and developmental profiles. The following papers (and others cited in these works) address these issues: (Champoux, M., Shannon, C., Airoso, W.D., Suomi, S.J. 1999. Play and attachment behavior of peer-only reared and surrogate/peer-reared rhesus monkey infants in social groups. In: Play and Culture Studies, Vol. II, Ed. by S. Reifel. Ablex Publishing Corp., Conn., pp 209-217; Ruppenthal, G.C., Walker, C.G. and Sackett, G.P. 1991. Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages. Am. J. Primatol., 25, 103-113.) We recognize, however, that the bulk of the research on this issue has been conducted with Old World Cercopithecine monkeys (and principally macaques), and that there may be important species differences in whether continuous peer-rearing is detrimental.

IV. Environmental enrichment -- Structure and substrate.

IV.A. Cage design and size.

IV.A.1. The Policy recommends that primates should be able to engage in 'social adjustments'. Presumably this means spatial adjustments to conspecifics. Further along in this section, the Policy recommends that 'enclosures be designed, constructed, and furnished so that individual primates may reasonably avoid other individuals or frightening stimuli.' Some members of species whose social organizations involve social dominance, when continuously housed in pairs, may need space or structures to escape from unwanted social initiations by higher-ranked cage mates. Given that macaques and baboons, the most common laboratory primates, are such animals, this section seems incompatible with the goal of continuous social housing as the preferred housing option, unless cages are redesigned (at great expense) to accommodate this stipulation. One solution is for continuous housing to be considered only one of several preferred options for housing, as described in Section II.B. above.

IV.A.2. We find somewhat ambiguous the paragraph that indicates 'Primate of species with long tails should be provided with sufficient vertical space to permit normal upright resting postures without restriction of tail position, or placement of the tail outside the enclosure or into waste pans'. This could be interpreted to mean that long-tailed macaques (also called cynomolgus monkeys, Macaca fascicularis) may need to have cages tall enough that they can sit on a perch without their tails contacting the floor. A second interpretation is that these animals must have sufficient floor area that their tails should be able to lie straight (i.e., not be curled up). Either interpretation would require that new cages be purchased for these animals, and that housing rooms would have to be radically re-designed to accommodate the larger cages. Such costs could be enormous. Alternatively, fears have been raised that such a rule could either end research with individually housed long-tailed macaques, or encourage surgeries that could be detrimental to the animals (e.g., tail-docking). Certainly long-tailed macaques in the wild sit on low perches with their tails lying partially on the ground. Moreover, our experience has been that these animals behave as if they are aware of their tail's location, and do not allow it to hang haphazardly. The problematic phrase here may be 'without restriction of tail position'. This phrase should be clarified.

IV.B. Space for running.

IV.B.1. It is unclear why patas monkeys were singled out for having 'regular access to large exercise areas that accommodate running'. This sounds like it may be a recommendation to solve a particular problem at a particular facility; this degree of specificity may create problems for other facilities (see Section I.C.1. above).

IV.C. Species that scent-mark.

IV.C.1. We are pleased to see provision made for species that scent-mark. We should note, however, that in the wild such marks persist for days. This is likely to be incompatible with current husbandry practices involving daily cage cleaning. In fact, performance of daily cage cleaning (which removes the scents) could lead to exaggerated, continual marking behavior, which might be inconsistent with well-being. We see this area as one in which two laudable goals, scent-marking and cage hygiene, are potentially incompatible. The concern is that different inspectors may focus more on one or the other goal, with the result being inconsistent interpretation of the Policy. We recommend that USDA provide further guidance in this area.

V. Environmental enrichment -- foraging opportunities.

V.A. General considerations.

V.A.1. There is a difference of opinion among some of those who study the behavior of primates about the justification that since wild primates spend a significant portion of their time foraging, substantial foraging time is a necessary or beneficial thing in captivity. An animal forced to forage for its entire daily ration might experience stress, and may suffer nutritionally. In addition, if foraging is performed in a social situation, competition may result in a reduction in an individual's experience of control over the environment (see Section X below). Therefore, we recommend that the Policy emphasize that nonhuman primates be offered species-appropriate foraging opportunities to supplement their daily nutritional needs, not to replace them entirely.

V.A.2. The policy states that "Captive nonhuman primates that are not provided with enough time-consuming foraging tasks may self-mutilate, over-groom, or become aggressive" (page 38149). This statement is not supported by the literature. We know of no studies demonstrating a causal link between a lack of foraging activities and the development of aggressive or abnormal behavior. There is, however, evidence that some foraging tasks can ameliorate the display of some forms of stereotyped behavior. Some severely abnormal behavior (such as self-inflicted wounding) seems to be resistant to a variety of forms of enrichment, including foraging strategies. To better reflect findings from published studies, we suggest rewording of the Policy to state, "Captive primates that engage in stereotyped or other atypical forms of behavior (e.g., repeated rocking, somersaulting, or other motor stereotypies, coprophagy, over-grooming) may reduce the expression of these behaviors when given opportunities for species-appropriate, time-consuming foraging tasks."

V.A.3. We feel there should be a statement added about the foraging needs of nocturnal primates. Effective foraging and feeding opportunities for such species should be at appropriate times in their day-night cycle, and this may not be during daylight hours.

V.A.4. The reference to "high" processing time should read "long" processing time.

V.A.5. While the literature suggests that regular foraging opportunities would be effective in altering foraging behavior (and in some cases other behavior) in species-appropriate directions, this may be impractical to implement on a broad scale immediately. Foraging enrichment opportunities may require equipment design, cage alterations, the acquisition of a variety of foods, personnel to make, clean, and stock devices, additional storage facilities, and personnel to evaluate effectiveness. We suggest that provision of regular (at least 3X/week) foraging opportunities is one area in which each facility should be allowed to develop a staged plan to work toward this as a goal (see also Section I.B. above).

V.B. Experimental manipulation.

V.B.1. The policy states that ". we do not consider activities that are part of experimental manipulation to be adequate" for enrichment for animals who are on restricted diets. We do not feel that this discounting of activities that are a part of experimental manipulations is always appropriate. For example, some types of cognitive testing appear to be very stimulating for the animals involved. These animals voluntarily participate in the experimental tasks, some of which may be effective forms of enrichment offering a type of stimulation not commonly available through other enrichment venues. In fact, in the Final Report issued with the policy, it states that "Mental stimulation may be provided to animals by requiring them to complete cognitive tasks to obtain their food." (page 35). This seems to contradict what is stated in the Policy. We suggest that the Policy be reworded to state that "activities that are part of experimental manipulations may serve as a form of foraging enrichment if the primates are being rewarded with palatable food." We should note that members of the committee drafting this document disagreed on whether animals working under conditions involving pre-test deprivation should be included in this consideration. We do note that there is wide variation in the extent to which animals are subject to such deprivation. In many cases, for example, animals are tested prior to their daily feeding. This disagreement notwithstanding, we do agree that at least some experimental manipulations (including manipulations involving non-food rewards) have positive effects on the animals' well-being, and urge USDA to adopt language that reflects this.

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V.B.2. The term "continuously restricted diets" is confusing. Since even animals on restrictive experimental protocols do eat, the meaning of that phrase is not clear. We suggest stating that such animals should receive at least part of their restricted diet in the form of time-consuming foraging tasks, if that is possible within the limits of the experimental protocol.

V.B.3. Foraging for "nonfood rewards" (as stated in the policy) is an oxymoron since the word "foraging" implies food acquisition. Toys may be rewards, but animals do not forage for them. We suggest replacing the word "foraging" with "manipulation", although this may then no longer fit in this section of the Policy on foraging opportunities.

VI. Environmental enrichment - manipulanda.

VI.A. Variety of items.

VI.A.1. The Policy states that nonhuman primates should be provided with a variety of portable or moveable items for manipulation. It is unclear from this statement whether nonhuman primates should have access to several objects at a time or be provided with one object that is changed on a regular (perhaps weekly) basis. If the intent is the former, then we have the following concerns:

1. The presence of several objects in a cage substantially increases the probability that an object will interfere with the squeeze mechanism thereby making it difficult to access the animal in medical emergencies or to carry out basic husbandry.
   
   
2. There are a limited number of objects that meet the criteria for safe, stimulating, durable, and sanitizable. If nonhuman primates must have exposure to multiple objects at a time, this requirement will reduce the pool from which novel objects can be drawn. We recommend that the objective be variety and not mere numbers of objects and that the phrase be changed to read "The plan should provide for each primate to have a portable or moveable item for manipulation that is changed as often as necessary to maintain variety."
   
   

VI.B. Access to objects or substrates for grooming.

VI.B.1 The policy states that nonhuman primates caged without tactile contact (presumably social grouping 4) should have daily access to suitable substrates or objects for grooming. There are a number of significant concerns about this issue.

1. There are very few devices currently available that would serve this purpose (e.g., grooming boards being the only apparatus that could be used with macaques).
   
   
2. There is little evidence to suggest that monkeys groom the board independently of obtaining crumbles from the board. We believe that foraging is being confused with grooming.
   
   
3. As mentioned in the workshop on enrichment held at ASP's annual meeting in August 1999, grooming boards are one of the most expensive devices requiring very high maintenance by technicians because of issues surrounding sanitation.
   
   

VI.B.2 The implication of the policy is that grooming substrates will serve a grooming function in species that normally groom each other. However, we raise the following points with respect to this idea.

1. Grooming substrates do not elicit grooming activity in the majority of animals given such devices.
   
   
2. The policy assumes that it is the motor acts of grooming that are of paramount importance. In fact, social grooming in nonhuman primates is about social relationships, not about motor movements. We doubt that the provision of grooming substrates can take the place of these social factors. Furthermore, grooming appears to benefit the recipient more than the individual performing the motor movements.
   
   
3. We recommend that grooming substrates be considered as fulfilling the foraging requirement and that the grooming requirement in this section be eliminated inasmuch as it does not accomplish the purpose of stimulating actual grooming behavior.
   
   

VI.C. Number of enrichment activities.

VI.C.1. The policy appears to require that all of the environmental enhancements be implemented for individual monkeys on a daily basis. Thus, if monkeys were housed individually and given increased human contact (option 4), they would also have to have a different daily foraging event, multiple objects placed in their cage probably on a weekly basis, and a grooming board mounted on their cage daily. We have the following concerns.

1. This level of activity around the cage might be stressful for some nonhuman primates.
   
   
2. The time needed to carry out all these enrichment procedures along with the time required for basic husbandry would leave only a very narrow window of time to conduct basic research, particularly for behavioral, reproductive or cognitive studies.
   
   
3. There would have to be a substantial increase in the number of technicians to carry out this work, as suggested in Section II.B.7. above.
   
   

VII. Considerations for meeting the critical elements.

VII.A. Intent of this section.

VII.A.1. It is unclear whether each of the six issues identified in this section must be related, in a facility's plan, to each of the five critical elements contained in the draft Policy. We believe that this section needs more of an introduction or explanation. Maybe add a sentence such as: "The following six issues must be addressed in a facility's Environmental Enhancement Plan."

VIII. Documentation.

VIII.A. Wording.

VIII.A.1. We recommend several changes to the wording in this section to avoid the interpretation that an institution's plan must by updated whenever there is a change in numbers of animals or change in the needs of specific animals (bullets 2 and 3). Specifically, we recommend changing the second sentence to read: The plan should "incorporate" rather than "document".

VIII.A.2. We recommend changing the second bullet to read "general specification of how changes in the facility's primate population will be accommodated".

VIII.A.3. We recommend changing the third bullet to read "general specification of how changes in the needs of individual primates will be accommodated".

VIII.B. Clarification.

VIII.B.1. It is unclear what the documentation should consist of. For example, as currently written, this section does not indicate that the implementation of a facility's environmental enhancement plan even needs to be described, nor does it indicate the level of detail that would reflect adequate documentation. We see this as an area that is open to wide interpretation by regulators.

VIII.B.2. It is unclear what comprises 'assessments of the effectiveness' of a facility's environmental enhancement plan. This could range from impressions formed by an animal care technician who has no formal training in primate behavior, to a quantitative assessment program designed and executed by a staff behaviorist. We urge USDA to specify clearly what the documentation must contain, and how effectiveness is to be assessed.

IX. Novelty.

IX.A. Considerations.

IX.A.1. The Policy defines novelty as 'variation in enrichment devices and strategies', yet aspects of this section suggest the intent is not novelty per se, but rather variety. The difference is between having 5 different types of items that are rotated throughout the colony, but that the animals experience repeatedly on an irregular basis, versus having animals only experience a given object (or class of objects) once, necessitating the continued purchase of 'novel' objects. (See also Section VI.A. above.) We recommend clarification of the relationship between novelty and variety in this section.

IX.A.2. The Policy indicates that 'the cognitive abilities of primates should be considered in the choice of novelty provided.' Species and individuals also vary widely, however, in temperament/reactivity. An active area of research in primatology has been documenting variations in temperament, and a common procedure has been to provide novel objects, or place the animal in novel surroundings, and assess the animals' responses. Whereas members of one species may rapidly approach a novel object placed in its cage, other members of the same (or members of a different) species might avoid the same object for days. This has more to do with temperament than with cognitive ability. We recommend adding 'temperament' to this sentence.

IX.A.3. Other sections of the Policy note quite correctly that separations and relocations can be stressful to animals. Thus, there are some forms of 'novelty' (i.e. new partners, new cages) that facilities might not want to provide, and in fact might be discouraged from providing.

X. Control over the environment.

X.A. Practical considerations.

X.A.1. While we welcome USDA's recognition that a large body of psychobiological research has indicated that lack of control is stressful (and potentially incompatible with well-being), we point out that this recommendation can conflict with the earlier recommendation of continuous social housing as the preferred housing option. Specifically, for species whose social relationships involve social dominance (such as macaques and baboons, which are among the most common species in research facilities), continuous pair-housing in small cages may result in great disparities in the experience of control over the (social) environment. In fact, such differences in control can compromise research, if subordinate and dominant animals show different endocrine or immunological profiles. Such internal physiological differences may not be apparent at the behavioral level, yet may influence physiological processes important to the conduct of a research program. We believe that this is yet another reason why continuous social housing should not be considered the preferred housing option for all species in all captive settings.

X.A.2. The examples of control involving temperature or lighting seem ill-advised, inasmuch as such decisions would most probably affect many more animals than the one exerting the control. If one animal can control the environment of 20 animals, then 19 animals have a loss of control.

X.A.3. We note that some control can have unintended negative consequences. For example, an animal that is allowed the freedom to control the positioning of its cage back, might inadvertently reduce its access to water.

X.A.4. In another section of the Policy, foraging activities that are part of experimental manipulations were judged inadequate as providing foraging opportunities as enrichment. In Section V.B. above we argue that this should be reconsidered. In the current context, however, one could argue that an animal's participation in a Sidman avoidance task (in which making a response results in avoidance of a noxious stimulus) constitutes 'control' over its environment. In this situation, we would argue that such a task should not be considered as environmental enhancement, yet it does conform, in an important way, to the description in this section of 'avoiding noxious stimulation'. In short, the issue of 'control' is a complex one, involving what is available to be controlled, and the practical fact that not all animals can be given control of all aspects of their environment. We urge USDA to reconsider this section.

XI. Sensory stimulation.

XI.A. General considerations.

XI.A.1. It is difficult to imagine how an animal in captivity can have the opportunity to avoid excessive exposure to frightening stimuli, or how the plan might provide for it. On the other hand, management policies might be designed to minimize exposure to such stimuli. The distinction is between designing an environment permitting escape versus minimizing disturbing activities or sounds in the proximity of the primates. A zoo example might be what the USDA has in mind, e.g., don't house the prey in close visual and olfactory contact with a predator. This is unlikely to be relevant in a research facility, however (see Section I.C. above).

XI.A.2. Does distancing oneself from a frightening stimulus also pertain to incompatible social partners? If so, then this section (as with Section X above) may have implications for housing strategies.

XII. Exemptions.

If an animal is exempted from various aspects of the plan due to experimental protocol, additional compensation as suggested by the last sentence in the Policy may not be consistent with that protocol. This further underscores the points made in Sections II.B.4. and V.B.1. that positive human interaction, tasks, and food reward received as a part of an experimental protocol should, in many cases, be allowed to fulfill the environmental enhancement elements of compensatory social interaction and foraging opportunities.

XIII. Individuals in persistent psychological distress.

This section needs amplification. There must be a plan for detecting and diagnosing the behavioral problems and suggesting interventions for treatment, and assessing the treatment's efficacy. Suggested rewording:

"The plan should provide for detecting, diagnosing, and treatment of behavioral problems of primates in persistent psychological distress. If the facility's staff does not include an on-site behaviorist, the plan must specify that a primate behaviorist or veterinarian with formal training and experience in primate behavior will be consulted."

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Appendix 1

Members of the ad hoc committee of the American Society of Primatologists that drafted this document:

Dr. John P. Capitanio, University of California, Davis, Chair
Dr. Mollie Bloomsmith, Zoo Atlanta & Yerkes Regional Primate Research Center
Dr. Carolyn Crockett, University of Washington
Dr. Melinda Novak, University of Massachusetts
Dr. Kathlyn Rasmussen, National Institutes of Health

Members of the Board of Directors of the American Society of Primatologists:

Dr. Nancy Caine, California State University, San Marcos, President
Dr. John P. Capitanio, University of California, Davis, President-Elect
Dr. Melinda Novak, University of Massachusetts, Past President
Dr. Steven Schapiro, University of Texas M.D. Anderson Cancer Center, Treasurer
Dr. Janette Wallis, University of Oklahoma Health Science Center, Executive Secretary