NATIONAL INSTITUTES OF HEALTH NONHUMAN PRIMATE MANAGEMENT PLAN REVISED 1/22/91 Office of Animal Care and Use National Institutes of Health Bethesda, Maryland 20892 (301)496-5424 CONTENTS Preface ........................................................3 List of Figures ................................................4 List of Tables .................................................5 Chapter 1 - Introduction........................................6 Chapter 2 - Evaluation of the Status of NHP Care and Use at NIH--Survey Results.............................7 Chapter 3 - Potential Environmental Enrichment Options for Nonhuman Primates ....................................12 Chapter 4 - Translation of the Nonhuman Primate Management Plan Into Action ..............................22 Appendices 1 Behaviors Considered to be Abnormal...................33 2 Chimpanzee Enrichment Program ........................34 3 Glossary of Terms.....................................37 4 Sample Facility Enrichment Plan.......................38 References ....................................................43 PREFACE The director of the National Institutes of Health (NIH) requested in March 1987, "state-of-the-art" housing for the nonhuman primate population at NIH. As a result of this, the National Center for Research Resources (NCRR) hired Dr. Kathryn Bayne to coordinate the development of this document, conduct a survey of nonhuman primate utilization and conduct independent research on environmental enrichment. She was also directed to work with scientists and veterinarians working with nonhuman primates, the Office of Animal Care and Use (OACU), and the Veterinary Resources Program (VRP) in the formulation of this plan. The document, then, presents the results of the survey and recommendations of a diverse group of researchers, care providers and administrators to meet the 1985 congressional mandate for improved "psychological well-being" of nonhuman primates. This Plan does not attempt to set the standard for nonhuman primate housing across the country, but rather is a research oriented program through which various means of environmental enrichment can be tested and implemented at NIH. LIST OF FIGURES Figure 1: Environmental Enrichment - Social ..................50 Figure 2: Environmental Enrichment - Non-social ..............51 Figure 3: Example of Creative Animal Holding Room Design ...........................................52 Figure 4: Factors Proposed by NIH Scientists to Assess Psychological State...............................53 Figure 5: Recommendations by NIH Veterinarians for Measuring Psychological Well-Being................54 LIST OF TABLES Table 1: Percent of Nonhuman Primates Utilized at the National Institutes of Health by Species ...........26 Table 2: Methods Utilized by National Institutes of Health Investigators to Measure Nonhuman Primate Psychological Well-Being ...................27 Table 3: Listing and Frequency of Suggestions Made by Investigators at the National Institutes of Health for Modifications of the Cage Environment.........................................28 Table 4: Methods of Measuring Nonhuman Primate Psychological Well-Being Utilized by National Institutes of Health Veterinarians .................29 Table 5: Recommendations by National Institutes of Health Veterinarians for Nonhuman Primate Housing Changes ....................................30 Table 6: Categorization of References by Method of Assessing Well-Being................................31 CHAPTER 1 INTRODUCTION Healthy and normal nonhuman primates are required for many biomedical research studies. Although guidelines and regulations exist for the maintenance of healthy nonhuman primates which include standards for nutrition, sanitation, and the micro- and macro-environments, the 1985 amendment to the Animal Welfare Act (PL 99-198) mandated additional requirements with the introduction of the term "psychological well-being." Since the passage of the Act, many investigators have been attempting to define "psychological well-being" in an objective and measurable fashion. To date, no one definition has been described which can be applied equally to all individuals or species of nonhuman primates. As a state of well-being is similarly difficult to describe universally for all human beings, it is not surprising that such a definition is at present lacking in the primatological literature. Many means of measuring "psychological well-being" are currently used. The most commonly utilized measures include behavioral and physiological parameters. Erwin and Deni (1979) have described in great detail the abnormal behaviors frequently seen in rhesus monkeys (Macaca mulatta) maintained in laboratories (see Appendix 1). Similar descriptions for other nonhuman primate species are also available. Physiological measures, such as cortisol and ACTH levels as well as immune status tests (e.g., IgG levels) are objective values that can be monitored at regular intervals. However, the validity of relying on measures of stress as the sole determination of psychological well-being has not been verified. Also, the ubiquitous usefulness and reliability of any measure for even one species of nonhuman primates is unlikely as individual variation in situational responsiveness is high in nonhuman primates. CHAPTER 2 EVALUATION OF THE STATUS OF NONHUMAN PRIMATE CARE AND USE AT THE NATIONAL INSTITUTES OF HEALTH -- SURVEY RESULTS - 1987 In 1987, a survey of 56 investigators and five veterinarians from 10 ICD's was conducted to assess the status of housing and management procedures and experimental requirements for the nonhuman primate population at NIH. A follow-up survey was conducted in 1990. The results of this survey are as follows: o The largest proportion of nonhuman primates at NIH is the rhesus monkey (Macaca mulatta). See Table 2 for a rank ordering of the usage of other nonhuman primate species. o 58.1% of the investigators studying nonhuman primates at NIH use rhesus monkeys (see Table 3). o 96.4% of the time the subject animal is removed from the home cage during the course of the experiment (47% of the time the animal is removed 1-2 times each week). o If the animal is removed, 64.1% of the time it is sedated or anesthetized. o In 29.1% of the protocols, positive reinforcement is used. o When positive reinforcement is used, 62% of the time a liquid (water or juice) is the form of the reinforcer. o The length of time an individual nonhuman primate is used for a research protocol at NIH ranges from one day (typically these animals are placed in the recycling program if they are not euthanized) to a lifetime, with the mean time being 9.6 months. o 58.2% of the time the subject is euthanized at the end of the study. o 62% of the investigators surveyed feel that the nonhuman primate's environment is "suitable". Continued - Survey Results - 1987 o 53% of the investigators surveyed feel that the nonhuman primate's environment is enriched. Many thought this enrichment was due to the experiment itself. o The average nonhuman primate research project has 4.2 investigators working directly or indirectly with the animals. o Animals that are chair restrained as part of the study spend a mean time of 5.7 hrs (mode =3.0 hrs) in the chair during the course of the day. o 30.9% of the investigators chair restrain their subjects as part of the protocol. o 16.4% of the investigators tether their subjects as part of the experimental protocol. o 14.3% investigators keep their animals on collars and chains in the home cage. A total of 20.5% use chains to transfer animals to chairs. o 4.5% utilize the pole and collar system to transfer animals. o 9.1% of the investigators train their subjects to enter transport cages, so they can move them while the animals are conscious. o The mean number of hours the nonhuman primates are worked each week for all Institutes is 14.6 hrs (ranging from 1 hr to 56 hr per week). o 84.9% of the investigators surveyed house their adult nonhuman primates singly. Approximately 70% of the nonhuman primates at the NIH are singly housed. Of these approximately 4% are housed in isolation chambers for purposes of quarantine or infectious disease studies. o 51.8% of the investigators currently are or would be willing to pair or group house their subjects. o 8.9% of the animals are on special diets as part of the experimental protocol. o 56% of the investigators surveyed try to assess the psychological well-being of their nonhuman primate subjects. Many, however, felt unskilled in their attempts and felt a "trained observer" (i.e. an individual skilled in making behavioral assessments) would be more reliable. Continued - Survey Results - 1987 o 80% of the veterinarians interviewed attempt to assess the psychological well-being of the nonhuman primates in their care. o See Table 3 for a list of the current methods utilized by NIH investigators to measure the psychological well-being of their nonhuman primates. o See Table 4 for a list of suggestions by investigators for environmental enrichment for nonhuman primates made by investigators at NIH. o See Table 5 for the list of methods utilized by attending veterinarians at NIH for assessing the psychological well- being of nonhuman primates. o See Table 6 for recommendations for housing made by the attending veterinarians. EVALUATION OF THE STATUS OF NONHUMAN PRIMATE CARE AND USE AT THE NATIONAL INSTITUTES OF HEALTH -- SURVEY RESULTS - 1990 o The largest proportion of nonhuman primates studied at the NIH is the rhesus monkey (Macaca mulatta). 63% of the investigators studying nonhuman primates at NIH use rhesus monkeys. o 98% of the time the subject animal is removed from the home cage during the course of the experiment (64% of the time the animal is removed 1-5 times each week). o If the animal is removed, 63% of the time it is sedated or anesthetized. o In 50% of the protocols, positive reinforcement is used. o When positive reinforcement is used, 32% of the time a liquid (water or juice) is the form of the reinforcer; 59% of the time food is used and 9% of the time other forms of reinforcement are utilized. o The length of time an individual nonhuman primate is used for a research protocol at NIH ranges from one day (typically these animals are placed in the recycling program if they are not euthanized) to a lifetime, with the mean time being 3 years. o 69% of the investigators surveyed feel that the nonhuman primate's environment is enriched. Many thought this enrichment was due to the experiment itself. o The average nonhuman primate research project has 3.2 investigators working directly or indirectly with the animals. o Animals that are chair restrained as part of the study spend a mean time of 3.4 hours (mode = 3.0 hours) in the chair during the course of the day. The time ranges from 1 hour to 8 hours uninterrupted. o 27.5% of the investigators chair restrain their subjects as part of the protocol. o 12% of the investigators tether their subjects as part of the experimental protocol. o 6% of the investigators keep their animals on collars and chains in the home cage. o 4% utilize the pole and collar system to transfer animals. o 22% of the investigators transport cage train their subjects so they can move the animals while they are conscious. o 61% of the investigators surveyed house their adult nonhuman primates singly. Approximately 78% of the nonhuman primates owned by the respondents are singly housed. o 45.8% of the investigators who currently are not social housing their animals would be willing to pair or group house their subjects. o 36.7% of the animals are on food controlled diets and 20.4% fluid controlled as part of the experimental protocol. o 83% of the investigators surveyed try to assess the psychological well-being of their nonhuman primate subjects. CHAPTER 3 POTENTIAL ENVIRONMENTAL ENRICHMENT OPTIONS FOR NONHUMAN PRIMATES Introduction: Figures 1 and 2 depict an option diagram which is presented for use by the investigator, veterinarian or facility manager. It suggests a variety of options for housing and managing the laboratory nonhuman primate. These options may be selected as befits the particular research study of which the animal is a part. Many of the potential methods were suggested by investigators during the survey process. Factors Potentially Promoting Well-Being: I. Social Enrichment A. Contact Experience It is agreed by most behavioral investigators that a conspecific cage-mate can be a dynamic and enriching stimulus to the environment (Novak & Suomi 1988; Novak & Drewsen 1988; Stanton et al. 1985; Simpson 1984; Kraemer & McKinney 1979; Chamove et al. 1973; IPS 1988). It is recommended that social housing be considered one appropriate means of providing enrichment in cases where the ICD-ACUC approved animal study proposal does not prohibit it. Both pair and group housing conditions are categorized as social housing. It is recognized that group housing may limit access to the subject animals in many protocols, therefore, it is recommended that pair housing be considered for those studies requiring frequent investigator/subject contact. This social housing may be full-time or part-time, again as the protocol permits. It should be noted that the formation of social units of animals should be done with care. Part- time pair housing may be applicable for protocols requiring food or water restriction or for studies which require routine removal of the animal from the home cage. The determination of the animal composition of the social housing unit should be flexible as recent data indicate that successful social housing can be accomplished with mixed or like ages (e.g., mother/infant dyads, peer groups, mixed age/unrelated groups or extended family units), and with mixed or same sex (Reinhardt et al. 1987a; Reinhardt et al. 1987b; Reinhardt 1989; Snowden 1985). As maternal and peer separation studies have clearly shown detrimental effects on nonhuman primate species-typical behaviors and reproductive capacity, it is recommended, unless the approved protocol requires otherwise, that infant nonhuman primates should be housed with the mother and/or with peers until a species- appropriate weaning time is reached (Ruppenthal et al. 1976; Suomi et al. 1976; Suomi et al. 1973; Suomi et al. 1971; Suomi et al. 1970). Partial social contact may also occur outside of the home cage in a designated exercise area through which the animals are rotated. This exercise area may encompass an entire room in the animal facility or be a large pen in a separate room or in the middle of an occupied animal room (thereby providing social stimulation to the animals remaining in their home cages). In the case of exercise pens, the exercise area would be equipped with devices and "toys" to increase the activity and interest levels of the occupant(s). If a room is dedicated to this purpose, multiple pens could be placed in the room, thus increasing the frequency of rotation through the exercise area. As preliminary evidence (O'Neill 1988) indicates that different aged animals of some species (e.g., rhesus monkeys) have significantly different preferences for various types of enrichment (e.g., swinging apparatus for juveniles versus floor toys for adults), a multitude of strategies should be present in each pen, or different pens should be designed for various age groups. Special consideration should be given to the introduction of nonfamiliar animals in the exercise area, and provision should be made for only familiar pairs or groups of animals to be in the exercise area at the same time. Also, training of the animals to a transport cage may facilitate both introduction to and removal of the animals from the exercise area. Training programs have even been proposed for reducing stress levels in laboratory nonhuman primates (Layng & DauDelin 1988). Provision for the increased time and personnel needed for these methods of social contact must be made. The time allotted to animals for socialization and/or exercise may occur between studies of the same protocol, or between protocols for the same investigator, or while animals are awaiting assignment to a different investigator. Rehabilitation through exposure to other animals can result in various degrees of social recovery (Huebner & King 1984; Dienske et al. 1980; Fritz & Fritz 1979; Novak 1979; Suomi et al. 1976; Novak & Harlow 1975; Suomi & Harlow 1972; Harlow et al. 1971; Harlow & Suomi 1971; Suomi 1973). Pairs of animals designated for socialization/exercise could be identified and then introduced to each other in a neutral environment. Again, it must be emphasized that caution must be exercised when introducing unfamiliar animals. Incidents of aggression can occur even between familiar animals, resulting in varying degrees of harm to the monkeys involved. The dyad could be composed of two naive animals or composed of one socially experienced animal and one naive animal. Alternatively, a group of naive animals could be formed and introduced to the neutral environment. A serious consideration in social housing of nonhuman primates is the induction of separation anxiety. This phenomenon results when animals which have bonded together (mother/infant or peer/peer) are physically removed from each other (Suomi et al. 1970; Suomi et al 1973; Suomi et al. 1976). Typically the social bonding between two animals has occurred early in life. A considerable amount of variability in the impact of separation on the behavior of the animals involved has been reported (Suomi 1983). Suomi (1983) has also noted that the number of cases of disturbance resulting from separation (mother/infant, peer/peer) are outnumbered by cases where little disturbance has been observed. The incidence of separation anxiety in animals that were paired as adults will in all likelihood be less. Thus, if social units of nonhuman primates are to be formed, due consideration by the individuals forming the pairs must be made to the species, age and rearing history of the animals. Another factor which must be closely monitored is the increase in health risks for animals in social units. Clearly, the possibility of a greater incidence of disease transmission and traumatic wounds must be taken into account when considering socially housing animals which are part of a research project (Novak & Drewsen 1988). A level of acceptable risk should be established by both the investigator and the attending veterinarian. Another form of enrichment via social contact involves participation by humans. Socialization of dogs to improve handling and reduce behavioral abnormalities has been well documented (Vanderlip et al. 1985a; Vanderlip et al. 1985b). However, this area of environmental enhancement for nonhuman primates has to-date not been thoroughly investigated (see Cooper & Markowitz 1979 for the effect of a keeper on chimpanzees). In addition, questions of precise methodology and potential ramifications remain unanswered. B. Non-Contact Social Experience Other appropriate means of enriching the environment may occur in a social, but non-contact context. A viable solution to the problem of allowing social interaction between animals in a room whose physical configuration prohibits direct visualization of cage neighbors, is the provision of mirrors along an otherwise empty wall. This would allow the animals to visually communicate with each other via reflections (Gallup 1977; Gallup et al 1980; Gallup 1982). It has also been shown that many species of nonhuman primates will use social signals when viewing their own reflections in mirrors. This has been demonstrated in stumptail macaques (Anderson 1983), patas monkeys (Hall 1962), Japanese macaques (Itakura 1987), rhesus monkeys (Gallup et al. 1980), cynomolgus monkeys (Gallup 1977), and squirrel monkeys (MacLean 1964). The importance of olfactory and visual signals for communication purposes in nonhuman primates has been clearly outlined for the various species (Zeller 1987). Single housed monkeys do experience a limited degree of social interaction with other animals in the room by auditory, olfactory and visual communication (Novak & Suomi 1988). Social stimulation of several species of nonhuman primates can also be accomplished by means of nonthreatening, non- contact methodologies. An increase in grooming behavior by the provision of an artificial fleece attached to the home cage has been examined at the NIH (Bayne et al., In press ). Visual contact between what are generally considered "social" species (i.e., living in formal troops or more loosely structured groups) can often ease the stress from what would otherwise be an isolated environment if special attention is paid to the animal arrangement. It is probable that the maximum benefit from this arrangement comes from housing like species across from each other. The provision of visual contact between these animals can be accomplished by requiring that the animals in a room be housed across from each other as much as is possible (clearly an odd number of animals will result in one animal relying on diagonal social viewing). For rooms with a square rather than rectangular design, the physical arrangement of the cages can be planned to maximize visual contact between the animals. Visual contact between animals can also be increased by providing the home cages with a mutual wall of translucent materials (for example, impact-resistant plastics such as polycarbonates). This would prevent injuries resulting from loosely woven metal cages and increase neighbor-viewing over the current cages with one solid wall. For those buildings with rooms too narrow to have cages along both walls, windows in the walls between such rooms (also constructed of impact resistant plastics) could be provided. As many species of nonhuman primates seem to be very curious about activities in the corridors outside their rooms, windows in the doors to the rooms provide a strong focal point for interest. The cages closest to the door, then, should not remain empty. Much auditory communication occurs between the animals in a room. Communication between rooms might provide further stimulation for these animals (similar to one troop communicating with another). In some facilities, this may be accompliished by having a mesh component to the wall at the ceiling level. Other electronic solutions are conceivable as well. However, there is little available data in this area, and the effects of auditory communication on behavior need to be tested. II. Non-Social Enrichment A. The Environment 1. The room Little is known about the design of an animal room to optimize environmental enrichment. However, the survey process revealed some concern by the investigators about the room itself as a pleasant living environment for the nonhuman primate. Many of their suggestions could be implemented in a typical animal room. For example, the color of the room could be changed without compromising USDA regulations or AAALAC standards. A few investigators were of the opinion that the average animal room is too small. Perhaps increasing the inter-animal distance by increasing the net square footage of the room would improve the well-being of the more subordinate animals. The shape of the room could be considered an important element of an enrichment program as a shape which confers more visibility between animals (see above) is desirable. By designing a creative shape to a room or with the placement of additional walls, animals may be able to increase or decrease their visual contact with each other by their choice (see Figure 3). Additional features of the room which could enhance the environment of the animals include a capacity for sound to be available at times (e.g. music or naturalistic sounds) throughout the day. Research in this area is still underway but preliminary data indicate a reduction in aberrant behaviors (Novak & Drewson 1988; O'Neill 1989). Some zoos provide an opportunity for television viewing to their great apes. They report variable success (Shumaker, personal communication; Hinshaw personal communication). This strategy is also currently under investigation, and differences in animal responsiveness between commercial television viewing and viewing of animal documentaries is being determined. It is possible that the form of lighting in the room is important to the psychological well-being of the nonhuman primates housed there. Currently, standard fluorescent lighting is used in most rooms. There is preliminary evidence in both the nonhuman primate (O'Neill 1989) and human literature (Fenton & Penny 1985; Colman et al. 1976) that broad spectrum lighting can have a positive effect on behavior. Some components of the behavioral repertoire of group housed animals have been modified by the use of this form of light (Novak & Drewsen 1988). Its effect on singly housed animals, however, is only now being investigated (Pearce & Beauchamp 1988) and needs further examination. Broad spectrum bulbs are commercially available and are one means of providing "natural" lighting. Of course, windows and skylights are also potentially viable options. The physical location of the room may prove to be a critical element of an enrichment program. Its proximity to the people working in the building may encourage authorized personnel to "visit" the room, thereby providing the animals with increased human interaction. The proximity of one animal room to other animal rooms may also have an impact on the well-being of its inhabitants (see non-contact social enrichment). 2. The cage At the present time there are many guidelines concerning the cage environment, and only preliminary evidence concerning the impact of cage size on the incidence of aberrant behaviors in the nonhuman primate (Bayne & McCully 1989; Draper & Bernstein 1963; Erwin 1979). Recommendations on cage size and capability for sanitation are clearly outlined in the Guide. Debate still continues concerning the minimum cage size which will allow for psychological well-being (Novak & Drewsen 1988; Nash & Chilton 1986; Elton & Anderson 1977; Erwin 1979; Paulk et al. 1977; Alexander & Roth 1971; Southwick 1967). Until this issue is resolved, Guide recommendations should be considered minimum suggestions. The design of the cage can be greatly altered by utilization of a variety of cage materials (plastics versus metal) and shapes (using the modular concept). Plastic materials for cage construction offer some benefits: 1) less noise is produced by daily activities surrounding the maintenance of the cage; 2) an opaque or translucent environment can be created without compromising the safety of the animals or the people working with the animals; 3) plastics are warmer for the animal; and 4) sanitation principles would not be compromised. However, plastic materials have notable disadvantages as well. They scratch more easily than metal cages, they reduce air movement within the cage and the accumulation of waste material on the cage walls becomes more obvious (thereby reducing the visibility of the animals). The potential for having a variety of sizes and shapes of cages as a result of a modular concept available for different species and ages of nonhuman primates is desirable. The provision of an escape place for each animal is more likely to occur with a modular design than a fixed design. A modular design is also flexible for partial or full-time pair housing of animals as well. Enrichment of the home cage environment is most commonly being attempted with a variety of devices or manipulanda. The presence of manipulanda has been shown to have a positive effect on a variety of nonhuman primate species including stumptail macaques (Chamove et al. 1984) and rhesus monkeys (O'Neill 1988; Line 1987). These devices address two main categories of behavior: 1) foraging; and 2) play or manifestation of interest. Currently foraging behavior is being increased by the use of food puzzles, raisin boards and several substrates in which food items can be hidden (e.g. artificial fleece, wood wool, hay, astro-turf). However, it should be noted that it has long been recognized that monkeys will operate devices without a food reward (Dennis 1955). The induction of play behaviors or the increase in behavioral interest (i.e. exploratory behavior) can be accomplished by many means. The provision of cage furniture from which to swing, such as ropes, hoses, chains with crates or tires or PVC piping will result in a decrease in behavioral problems (Erwin 1986; Bryant et al. 1988). Perches made out of cage material or wood are routinely used by nonhuman primates (O'Neill 1987; Reinhardt 1989; Schmidt et al. 1989; Wolff 1989). Other objects such as stuffed animals and blankets are very appropriate for young nonhuman primates. It is recommended that for those species of nonhuman primates in which the females routinely form a nest for sleeping or reproductive purposes (Bernstein 1967; Hediger 1977; Horn 1980; Baldwin et al. 1981; Anderson et al. 1983) be provided with a substrate (e.g. towels) with which to do this. A variety of "toys"-- both responsive and nonresponsive-- have been shown to be used routinely by several species of nonhuman primates (Evans 1984; Renquist & Judge 1985; Westergaard & Fragszy 1985; Champoux et al. 1987; Westergaard & Lindquist 1987; O'Neill 1988; Bayne et al. 1989; Crockett et al. 1989; Watson et al. 1989). There is some preliminary evidence that the portability of an object in a cage can increase that object's interest factor for the singly caged nonhuman primate (Baldwin & Suomi 1974; Bayne 1989). 3. Food Nonhuman primates which forage for food located in dispersed patches rest less, exhibit more competition over a food source and spend more of their active period engaged in searching and feeding behaviors (Oates 1987). Thus, feeding time in the laboratory represents one of the most important events in the day for the captive primate. Therefore, it is probable that environmental enrichment via food presentation is likely to be successful. This strategy is currently being investigated at several facilities (Bayne et al. In press; Bloomsmith et al. 1988; Nadler 1988- unpublished). Foraging boards, flexible PVC tubing filled with food treats and Kong toys filled with frozen juice are methods which have been used with success (Bayne et al. 1989; Bloom et al. 1989; Brent et al. 1990; Murchison 1990; Bayne et al., In press; Bayne et al., submitted). Nutritionally balanced food treats should be used for enrichment purposes. Considering the potential importance of foraging as an enrichment technique, further research needs to be done in this area. Three components to the food delivery process that can be altered for enhancement of psychological well-being include: 1) a varied diet, including treats; 2) an increase in the frequency of food delivery (either by mechanical devices or foraging opportunities); and 3) a systematic analysis of who is the best person to feed the animals (Is the animal care technician who cleans the room and disturbs the animals the same individual who should be feeding?). B. Control Over The Environment It has been hypothesized by many (Line 1987a; Line 1987b; Novak & Drewsen 1988; Mineka et al. 1986) that giving the nonhuman primate the opportunity to change its environment whenever it chooses to do so improves psychological well- being. Many of the features of the room and cage environment can be made flexible in presentation so that the animals can choose to alter their micro- or macro- environment. These features include sound, lighting, and food delivery time and type. To prevent animals from battling each other over the amount of light and sound, banks of light and individual speakers would be required to have independent controls and settings. Some control over the environment could be provided to each animal by allowing the animal to remove himself, hide, from the macro-environment (e.g. with a small interior box or with a sliding panel which would close off an area). C. Exercise (see previous discussion) Exercise activities do not have to be a social event. Many nonhuman primates will use swings (Bayne et al. 1989) and other play objects without a social partner to stimulate interest. Thus, for some animals individual exercise periods to enhance psychological well-being should be considered. The use of spherical cages, which the animals can roll from inside the cage, in an occupied room is being explored for purposes of exercise and social enrichment of both the animal in the cage and animals watching from their home cages. III. Species Specific Recommendations As available information is limited for many species of nonhuman primates, further study needs to be conducted to expand the variety of enrichment options from which to choose. A. Macaca mulatta See Figures 1 & 2 B. Saimiri sciureus Perches (Williams et al. 1989) C. Macaca fasicularis See Figures 1 & 2 D. Callithrix sp./ Saguinus sp. 1. nest boxes 2. perches 3. wood for scent marking (can be incorporated into perch or nest box) E. Aotus trivirgatus 1. lighting Light intensities can modulate both behavioral and physiological parameters of owl monkeys (Eckert and Grober 1986). Unless scientific or husbandry practices requires otherwise, red lighting should be provided during daylight hours while fluorescent or broad- spectrum lighting be provided at night. 2. nest boxes All animals should be provided with a nest box. 3. other Branches or other natural perching material are recommended as owl monkeys are arboreal (Dixson 1987). F. Macaca arctoides nb: These animals empirically appear to be very prone to the development of behavioral pathology as a result of single housing. Consider mandating pair housing or other means of avoiding this as typically the behaviors are self-destructive. G. Cebus apella nb: As these animals are renowned for their manual dexterity, they should always be provided with some form of manipulanda. Additionally, a social environment may be preferred for this species (Bayne et al., submitted). H. Pan troglodytes For an example of an enrichment program, see Appendix 2. I. Erythrocebus patas nb: As these animals are natural runners, large (sq.ft. undetermined) exercise areas may be beneficial. CHAPTER 4 TRANSLATION OF THE NONHUMAN PRIMATE MANAGEMENT PLAN INTO ACTION Implementation of the Nonhuman Primate Management Plan will be accomplished via a three phase program. This implementation will predominantly be composed of a research and demonstration project at the NIH and at other research laboratories across the country. A phase-in program will be based on the research program currently under the direction of Dr. Kathryn Bayne, OACU. Phase 1 will test enrichment methodologies and consider other findings to ensure they are not detrimental to the ongoing research effort. Phase 2 will examine their efficacy in a small number of laboratories which have volunteered to participate in this effort. Both Phases 1 & 2 will have a bias toward cost-effective enrichment techniques. Phase 3 will encompass the broad-scale implementation of a number of enrichment options that have passed through Phases 1 & 2 in a larger number of laboratories at NIH. The options from which the scientific and veterinary communities can choose will be based on research studies. A rating scale of the behavioral indices used to evaluate the psychological state of a nonhuman primate has been developed. This rating scale is based on data from enrichment studies conducted at the NIH (Bayne et al., submitted). The responsibility of the design of an enrichment program for each animal study proposal will rest with each investigator. The Veterinary Behaviorist, ICD-ACUC, ICD veterinarian, and facility manager can all assist to various degrees with the design and implementation of the enrichment plan. If an approved enrichment technique proves to be unsuccessful under some conditions of use, assistance will be available from the Veterinary Behaviorist and her staff. In addition, the Veterinary Behaviorist will maintain current files on the variety of enrichment methodologies that have been tested or proposed, thereby serving as an information source for the intramural community. I. Environmental Enrichment Alternatives Figures 1 and 2 depict option diagrams which are presented for use by the investigator, veterinarian or facility manager. They suggest a variety of alternatives for housing and managing the laboratory nonhuman primate and represent the first techniques that can be addressed in Phase 1 of the implementation program. The scope of techniques which produce the desired effect (Phases 1 & 2) of these enrichment alternatives, is not entirely known at this time. Two main categories of enrichment are presented. They are 1) social and 2) non- social strategies. Laboratories wishing to participate in the evaluation of these methodologies may pick and choose strategies of interest and most suitable for their animals and then coordinate an assessment of their safety and efficacy with Dr. Bayne. Some of the questions which will be addressed by the research program are the relative merits or effects of: 1) animal-animal contact, 2) human-animal contact and 3) enrichment devices on the nonhuman primate's behavioral repertoire. The risks/benefits of human-animal interaction will be examined at the NIH. A program of human/nonhuman primate interaction must address several points. First, should such a program utilize a single individual or is the animal's environment enhanced by interaction with several familiar individuals? Who should act in this role in each facility? How are safety and liability issues addressed? What form of security screen will be in place to ensure that the integrity of the building and the safety of the other personnel and animal population remain intact? Certainly commercial animal breeders (especially dog breeders for laboratory animal research purposes) have had a great deal of success with their socialization programs utilizing paid professionals. A similar program could be established at the NIH so that a trained individual could do continuous monitoring of the behavior and enrichment program of the NIH nonhuman primate population. Many of the nonhuman primates on active protocols already have a great deal of human contact. Research will address questions such as whether this type of contact improves the behavioral state of the animals involved; can this be documented; and should auxiliary contact by an individual(s) be provided outside of the experimental context? Other questions of interest include how frequently should human interaction with the nonhuman primate occur? Should it be provided on a daily basis or on a weekly basis? How long should each interactive period last? What form should this interaction take? Two methods that have been suggested include the provision of food treats and interactive devices. Since any form of interaction with the animals implies proximity between the animal and designated personnel, a program of screening for various diseases (e.g. for macaques; Herpes B; SAIDS; shigella; salmonella) may be indicated to protect the personnel at risk. Additionally, training of personnel regarding safety measures is strongly encouraged. Personnel should also participate in an Animal Exposure Surveilance Program. II. Training Program A. Who participates? 1. Principal investigator 2. Technicians 3. Animal Care Personnel B. How? 1. What format? o video o seminar 2. How often? o annual 3. Who will conduct? Training Officer may select the faculty, as is currently being done with the investigators training course. C. Content/Goals III. Formation of Pairs/Groups of Nonhuman Primates A. Who identifies animals, monitors process? -- personnel issues B. Formation of a schedule or program by which social units are formed C. Where? -- facility and caging needs D. Identification of investigators interested in allowing their animals to pair/group housed IV. Continuation of Research Program to Evaluate Enrichment Proposals in Plan A. Identification of investigators willing to do independent or collaborative work in this area 1. Formulation of a working definition of "psychological well-being" based on data collected 2. Testing of new or novel cage enrichment strategies B. Continuation of research program through the OACU. V. Formation of a Nationwide Network for Information Exchange A. Participants would include investigators, animal care providers, and veterinarians working with nonhuman primates 1. Of particular interest and use to investigators working in the area of environmental enrichment for sharing evaluations of enrichment strategies B. Would require a "manager"-- personnel issues C. BITNET and Compuserve packages seem the most likely candidates at this time VI. Incorporation of a Description of the Enrichment Methodologies Available to the Intramural Nonhuman Primates in the Animal Study Proposals and Semi-annual Reports Table 1 Percent of nonhuman primates utilized at the National Institutes of Health by species Species Percent Macaca mulatta 61.5 Macaca fascicularis 12.1 Saimiri sp. 11.3 Callithrix sp./Saguinus sp. 6.8 Aotus trivirgatus 4.5 Pan troglodytes 2.2 Macaca arctoides 1.3 Cebus apella 0.3 Table 2 Methods utilized by NIH investigators to measure nonhuman primate psychological well-being o physiological measures o performance during experiment o behavior changes o behavioral abnormalities (stereotypies, self-abuse, masturbation, coprophagy, urine-drinking) o level of aggression o facial expressions o hair coat quality o response to people o dominance over cage neighbors o general behavior normal for species o appetite and body weight o quality of vocalizations o attention to surroundings o immunologic state o consistency in behavior Table 3 Listing and frequency of suggestions made by investigators at the National Institutes of Health for modification of the cage environment o Increase size of cage/more vertical space 20.2% o Apparatus, toys, rope, swings 17.0% o Perches, shelves (including the use of wood) 10.8% o Pair/group house 7.7% o Vary the diet 7.0% o Natural lighting 3.9% o Provide T.V., music 3.9% o Use materials other than metal for the cage 2.3% o Decrease the number of animals in a room 2.3% o Increase the size of the rooms 2.3% o Provide a central exercise area 2.3% o Improve quality of caretaker time with animals 2.3% o Paint the walls with colors 1.6% o Wire mesh walls to increase visibility of cage 1.5% neighbors o Central social area 1.5% o Control over the environment 1.5% o Provide the animals with hiding places 1.5% o Improve the cage washing system 1.5% o Improve the watering system 1.5% o Provide nesting material for pregnant females 0.8% o Flexible barriers between animals 0.8% o Padded cages for recovery from anesthesia 0.8% o Mirrors, house across from each other 0.8% o Provide time outdoors 0.8% o Feed throughout the day 0.8% o Improve room lighting 0.8% o Increase predictability of daily routine 0.8% o Outdoor view, e.g via a window 0.8% Table 4 Methods of measuring status of nonhuman primate psychological well-being utilized by NIH veterinarians o self-mutilation o stereotypies o over-reaction to a stimulus o distress calls o physical appearance o appetite Table 5 Recommendations by NIH veterinarians for nonhuman primate housing changes o social housing o perches in the cage o manipulanda in the cage o puzzle feeders on the cage o transport cage train the animals o exercise area o visual barriers for group housed animals o computerized watering system for isolator cages Table 6 Categorization of References by Method of Assessing Well-Being METHOD AUTHOR SPECIES Behavioral Alexander & Roth 1971 Japanese macaque Anderson 1983 Stumptail macaque Baldwin & Suomi 1974 Rhesus Bayne 1989 Rhesus Bayne et al. 1989 Rhesus Bayne & McCully 1989 Rhesus Bernstein 1967 Chimpanzee Bloom et al. 1989 Rhesus Bloomsmith 1988 Chimpanzee Bryant et al. 1988 Cynomologus Chamove et al. 1973 Rhesus Chamove et al. 1984 Stumptail Champoux et al. 1987 Rhesus Colman et al. 1976 Human Cooper & Markowitz 1979 Chimpanzee Crockett et al. 1989 Macaques Dennis 1955 Capuchin Dienske et al. 1980 Rhesus Draper & Bernstein 1963 Rhesus Eckert & Grober 1986 Owl Elton & Anderson 1977 Baboons Erwin 1979 Pigtail Erwin & Deni 1979 Rhesus Erwin 1986 Rhesus, Pigtail Evans 1984 Marmosets Fenton & Penny 1985 Human Fritz & Fritz 1979 Chimpanzee Gallup 1977 Cynomolgus Gallup et al. 1980 Rhesus Gallup 1982 Monkeys & Apes Hall 1962 Patas Harlow et al. 1971 Rhesus Harlow & Suomi 1971 Monkeys & Apes Horn 1980 Chimpanzee Huebner & King 1979 Rhesus Huebner & Kong 1984 Squirrel Itakura 1987 Japanese macaque Kraemer & McKinney 1979 Rhesus Line 1987a Rhesus Line 1987b Rhesus MacLean 1964 Squirrel Mineka et al. 1986 Rhesus Nash & Chilton 1986 Galago Novak & Harlow 1975 Rhesus Novak 1979 Rhesus Novak & Drewsen 1988 Rhesus Oates 1987 Monkeys & Apes O'Neill 1987 Rhesus O'Neill 1988 Rhesus O'Neill 1989 Rhesus Paulk et al. 1977 Rhesus Reinhardt et al. 1987a Rhesus Reinhardt et al. 1987b Rhesus Reinhardt 1989 Rhesus Renquist & Judge 1985 Rhesus Ruppenthal et al. 1976 Rhesus Schmidt et al. 1989 Rhesus Simpson 1984 Rhesus Southwick 1967 Rhesus Suomi et al. 1970 Rhesus Suomi et al. 1971 Rhesus Suomi & Harlow 1972 Rhesus Suomi et al. 1973 Rhesus Suomi 1973 Rhesus Suomi et al. 1976 Rhesus Suomi 1983 Rhesus Watson et al. 1989 Cynomologus Westergaard/Fragaszy 1985 Cebus Westergaard/Lindquist 1987 Lion-tail macaque Williams et al. 1989 Squirrel Wolff 1989 Squirrel Ecological Baldwin et al. 1981 Chimpanzee Anderson et al. 1983 Chimpanzee Horn 1980 Chimpanzee Physiological Pearce & Beauchamp 1988 Cynomolgus Stanton et al. 1985 Squirrel Line 1987b Rhesus Immunological Coe et al. 1985 Squirrel & Rhesus Coe et al. 1988 Squirrel APPENDIX 1 Behaviors Considered to be Abnormal* Qualitatively Abnormal Behaviors Bizarre Postures Floating Limb Self-Biting Self-Clasping & Self-Grasping Saluting Stereotyped Motor Acts Stereotyped Pacing Head Weaving or Tossing Bouncing in Place Somersaulting Rocking Appetitive Disorders Coprophagia Urine Drinking Sexual Disorders Autoerotic Stimulation Quantitatively Abnormal Behaviors Increased or Decrease Activity Appetitive Disorders Hyperphagia Hypophagia Polydipsia Agonistic Disorders Hyperaggression * Based on Erwin & Deni, 1979. APPENDIX 2 Chimpanzee Enrichment Program Southwest Foundation for Biomedical Research Brent, L.; D.R. Lee and J.W. Eichberg SOCIAL INTERACTION WITH CARETAKER Note: This is in addition to the regular attention the chimp receives from the caretaker. Grooming infant chimps - or let chimp groom you o with hair brush or emery board - don't give to chimp if not returned Play with infant chimps o tag - chase or be chased o tickle o tug of war with chain, etc. (select chimps) Blow bubbles - in areas where mask is to be worn; wave wand or hold wand in front of air conditioner to make bubbles Show pictures in magazines, books, photos do not let chimp have item New objects for chimp to see mechanical toys, tools, etc. FUN FOODS Amount per chimp Nuts in shell - peanuts, not salted 1 cup Sunflower seeds 1/2 cup Popcorn, no salt or butter 1 cup Frozen fruit or vegetables 1 piece Peanut butter in cup 1/4 cup Raisins 1/4 cup Oatmeal - flavored 1/2 cup Cereal 1/2 cup Yogurt, nonfat 1/2 cup Fruit juice 1 cup PUZZLES Raisin tubes - fill small plastic tube with raisins Koolaid tub with straw - frozen koolaid in tub outside cage, provide paper straw or tube Popcorn in bag - lunch size bag for individuals or large paper bag for group, place on top of cage Pipe feeder - attached outside cage, filled with honey, juice, etc. Puzzle box with peanuts, raisins, primatreats - on top of cage King kong toys filled with food Frozen koolaid, juice, applesauce ice cubes or ice blocks NON-FOOD ITEMS Unbreakable mirror Toothbrush and toothpaste - only give toothbrush to animals that will not destroy it immediately Magazine - several pages per chimp Newspaper - several pages per chimp Crayons/Paint/Chalk with paper - one piece paper and small piece of crayon, paint, or chalk per chimp (encourage chimp to give picture back) Toys (if approved) Toilet paper - one roll per group, or several feet per individual Boxes Feed sack - no string or plastic GUIDELINES 1. Use good judgement. Every chimp has a personality and mood of its own. Be careful of chimps that may grab at you. Not all activities will be possible with all chimps. Have any new toys or items approved with supervisor or veterinarian. 2. Do not force frightened chimps to participate. Some animals may take some time to become accustomed to the new routine (especially in the huts). They may react by withdrawing or being aggressive to new items. 3. Show lots of enthusiasm. Build up the excitement when entering the area. Talk favorably to the chimps and be very interested in the activity. Food grunts or hoots will help. Remember - in some cases you are the only variety and stimulation these animals receive. They are depending on you! 4. Urge animals to return items to you (such as toothbrush, toys, pictures) and reward them if they do. A wider variety of play items can be used with animals that return things. Also, urge chimps to come to the front of the cage to engage in the activity. This training may help the technicians when they need to sedate an animal. 5. Before hosing down each area, pick up or sweep up pieces of bags, boxes, toys or other items that will not go down the drain. Each caretaker will be responsible for cleaning up the area properly. If brooms or new drain covers are needed, contact your supervisor. 6. Be sure to fill out Enrichment data sheet completely. This is important for several reasons. Since the U.S. Congress has mandated that we provide for the psychological well- being of non-human primates, this is concrete evidence that we are doing our best to do so. Secondly, the data from the rating scale is invaluable in recommending further activities for particular animals, in testing the effectiveness of certain activities, and in plotting changes in behavior or possible early signs of illness. Also, the information may be used to publish data on environmental enrichment. 7. This enrichment program is also for the caretakers. You should develop a better relationship with the chimps, and have fun doing it. Your job is very important, and you should be proud of the excellent care you are capable of giving our primate cousins! ENRICHMENT SCHEDULE (EXAMPLE) Week 1 Week 2 Week 3 Week 4 MONDAY Emery Board Bubbles Tickle/Tag Brush TUESDAY Unshelled Frozen banana Popcorn Raisins nuts WEDNESDAY Raisin tube Popcorn bag Koolaid Pipe feeder (honey) THURSDAY Yogurt cup Sunflower Peanut Oatmeal seeds butter cup FRIDAY Toilet paper Feed sack Crayons/ News- chalk paper Tang and vitamins every day. Televisions and radios on at varied times. Appendix 3 GLOSSARY OF TERMS Bonding: The formation of social attachments which when temporarily or permanently disrupted result in a psychologically distressing syndrome known as separation anxiety. Positive Reinforcement: The receipt of a pleasant stimulus by an animal after a specified response is made, thereby increasing the probability that the same response will be made again. Negative Reinforcement: Occurs when an unpleasant stimulus is stopped when an animal makes a specified response, thereby increasing the probability that the response will be made again. Social Housing: A living environment in which two or more animals are maintained together. Social housing necessitates compatibility and may or may not result in bonding. Social Signal: A visual, tactile, or auditory cue made by one animal in a social situation and interpreted by another animal or the same animal. Appendix 4 FACILITY NONHUMAN PRIMATE ENRICHMENT PLAN Facility Name_____________________________________________ Reporting Period (e.g., fiscal year)______________________ Name of Responsible Individual____________________________ Those species of nonhuman primates which have been observed to live in social groups in a free-ranging state are currently being socially housed in their primary enclosure a) in a manner similar to the natural social structure b) in accord with generally accepted practices described in the literature for captive members of this species c) based on information contained in the NIH Nonhuman Primate Intramural Management Plan Each animal is being maintained in a pair/group housing condition which has been determined to be compatible by regular behavioral observations (conducted by ________________________, at __________________________[time] interval) and based on the professional judgement of the attending veterinarian (name). Animals which are individually housed are maintained in this manner for reasons of over-aggression, health status, or due to justified experimental constraints (see attached for a complete listing of individually housed animals), and have been approved by the Animal Care and Use Committee and facility veterinarian. Cage complexities (perches, toys, foraging devices, etc.) made available to socially and individually housed primates include the following: _________________________________________________________________ _________________________________________________________________ _________________________________________________________________ _________________________________________________________________ Environmental enrichment is being given special consideration to (select the type(s) that apply): 1) Individually housed primate infants or juveniles 2) Individually housed primates that are unable to see or hear primates of their own or compatible species 3) Nonhuman primates in psychological distress, as determined by behavior or appearance 4) Nonhuman primates participating in approved animal study proposals which require restricted activity 5) Great apes weighing more than 110 lbs (50 kg) Nonhuman primates experiencing restraint for more than 12 hours are provided daily with the opportunity for unrestrained activity for at least one continuous hour during the period of restraint, unless continuous restraint is required by an approved animal study proposal. A summary of the enrichment program available to each species in the facility and standard operating procedures for its implementation are attached. LISTING OF INDIVIDUALLY HOUSED NONHUMAN PRIMATES JUSTIFICATION FOR ANIMAL IDENTIFICATION INDIVIDUAL HOUSING ENVIRONMENTAL ENRICHMENT TECHNIQUES IN USE: Species Name: Social Enrichment _____ Pair ____ / Group ____ Single Sex ____ / Mixed Sex ____ Related ____ / Unrelated ____ / Both ____ Nonsocial Enrichment _____ Perch(es) ____ Swing(s) ____ Mirror(s) ____ Toys ____ Type(s) of toys ___________________________________ Number of toys per primary enclosure ______________ Dietary Description _________________________________ _____________________________________________________________ _____________________________________________________________ Feeding Methods Employed ____________________________ _____________________________________________________________ _____________________________________________________________ Description of Interaction(s) with Animal Care Staff and Scientific Staff:___________________________________________ ____________________________________________________________ Other Enrichment Methodologies In Use: _____________ ____________________________________________________________ LISTING OF NONHUMAN PRIMATES EXEMPT FROM ENVIRONMENTAL ENHANCEMENT PROGRAM ANIMAL ID DATE MADE EXEMPT JUSTIFICATION SIGNATURE REFERENCES Amended Animal Welfare Act. 1985, P.L. 99-198. Anderson, J. R., E. A. Williamson & J. Carter. 1983. Chimpanzees of Sapo Forest, Liberia: Density, nests, tools and meat-eating. Primates 24(4):594-601. Anderson, J. R. 1983. Responses to mirror image stimulation and assessment of self-recognition in mirror- and peer-reared stumptail macaques. Quart. J. Expt. Psychol. 35B:201-212. Alexander, B. K. & E. M. Roth. 1971. The effects of acute crowding on aggressive behavior of Japanese monkeys. Behaviour 39:73-89. Baldwin, D. V. & S. J. Suomi. 1974. Reactions of infant monkeys to social and nonsocial stimuli. Folia Primatol. 22:307-314. Baldwin, P. J., J. Sabater Pi, W. C. McGrew & C. E. G. Tutin. 1981. Comparisons of nests made by different populations of chimpanzees (Pan troglodytes). Primates 22(4):474-486. Bayne, K. 1989. Nylon Balls Re-visited. Laboratory Primate Newsletter. 28(1):5-6. Bayne, K., H. Mainzer, G. Campbell, F. Yamada & S. Suomi. The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board. American Journal of Primatology, In press. Bayne, K., S. Suomi and B. Brown. 1989. A new monkey swing. Lab. Prim. Newsletter 28(4):16-17. Bayne, K. and C. McCully. 1989. The effect of cage size on individually housed rhesus monkeys. Lab Animal 18(7):25-28. Bernstein, I. S. 1967. Age and experience in chimpanzee nest building. Psych. Reports 20:1106. Bloom, K.R. and M. Cook. 1989. Environmental enrichment: behavioral responses of rhesus to puzzle feeders. Lab Animal 18(5):31-33. Bloomsmith, M. 1988. Successful feeding enrichment for captive chimpanzees. Am. J. Primatol. 16:155-164. Brent, L. D.R. Lee, & J.W. Eichberg. Environmental Enrichment Program for Chimpanzees at the Southwest Foundation for Biomedical Research, San Antonio, TX 87284 Bryant, C.E., N.M.J. Rupniak and S.D. Iverson. 1988. Effects of different environmental enrichment devices on cage stereotypies and autoaggression in captive cynomologus monkeys. J. Med. Prim. 17(5):257-269. Champoux, M., M. Schneider & S. Suomi. 1987. Environmental enrichment and affective responses in infant rhesus monkeys. Annual meeting- American Society of Primatologists. Chamove A. S., L. A. Rosenblum & H. F. Harlow. 1973. Monkeys raised only with peers: a pilot study. Anim. Behaviour 21:316-325. Chamove, A. S., J. R. Anderson, & V. J. Nash. 1984. Social and environmental influences on self-aggression in monkeys. Primates 25(3):319-325. Coe, C.L., S.G. Wiener, L.T. Rosenberg & S. Levine. 1985. Endocrine and immune responses to separation and maternal loss in nonhuman primates. In: The Psychobiology of Attachment and Separation. Academic Press: New York. Pp. 163-199. Coe, C.L., P. Cassayre, S. Levine & L.T. Rosenberg. 1988. Effects of age, sex and psychological disturbance on immunoglobulin levels in the squirrel monkey. Developmental Psychobiology 21(2):161-175. Colman, R.S., F. Frankel, E. Ritvo & B.J. Freeman. 1976. The effects of fluorescence and incandescent illumination upon repetitive behaviors in autistic children. J. Autism and Childhood Schizophrenia 6(2):157-162. Cooper, D. L. & H. Markowitz. 1979. Handler's effects on contact comfort behaviors of two trios of juvenile chimpanzees in the zoo. Psychol. Rep. 44:1015-1018. Crockett, C., J. Bielitzki, A. Carey and A. Velez. 1989 Kong toys as enrichment devices for singly-caged macaques. Lab. Prim. Newsletter 28(2):21-22. Dennis, W. 1955. Early recognition of the manipulative drive in monkeys. Brit. J. Anim. Behav. 3(2):71-72. Dienske, H., W. Vreeswijk & H. Koning. 1980. Adequate mothering by partially isolated rhesus monkeys after observation of maternal care. J. Abnorm. Psychol. 89:489-492. Dixson, A. 1987. The owl monkey. Pp. 582-585 In The UFAW Handbook on the Care and Use and Management of Laboratory Animals (T.B. Poole, ed.), 6th edition. Longman Scientific & Technical, London. Draper, W. A. & I. S. Bernstein. 1963. Stereotyped behavior and cage size. Perceptual and Motor Skills 16:231-234. Eckert, H. & J. Grober. 1986. Direct modulation of activity and body temperature of owl monkeys (Aotus lemurinus griseimembra) by low light intensities. Folia primatol 47:171-188. Elton, R. H. & B. V. Anderson. 1977. The social behavior of a group of baboons (Papio anubis) under artificial crowding. Primates 18:225-234. Erwin, J. 1986. Environments for captive propagation of primates: interaction of social and physical factors. In: K. Benirschke (ed.) Primates: The Road to Self-Sustaining Populations. Springer-Verlag: New York. Pp. 297-305. Erwin, J. 1979. Aggression in captive macaques: interaction of social and spatial factors. In: J. Erwin, T. Maple and G. Mitchell (eds.) Captivity and Behavior. Van Nostrand Reinhold: New York. Pp. 139-171. Erwin, J. & R. Deni. 1979. Strangers in a strange land. In: J. Erwin, T. Maple, and G. Mitchell (eds.) Captivity and Behavior. Van Nostrand Reinhold: New York. Pp. 1-28. Evans, S. 1984. Captive management of marmosets and tamarins. In: Standards in Laboratory Animal Management, Part 2. Potters Bar: Universities Federation of Animal Welfare. Pp. 250-252. Fenton, D. & R. Penny. 1985. The effects of fluorescent and incandescent lighting on the repetitive behaviours of autistic and intellectually handicapped children. Australia and New Zealand Journal of Developmental Disabilities 11(3):137-141. Fritz, P. & J. Fritz. 1979. Resocialization of chimpanzees. J. Med. Primatol. 8:202-221. Gallup, G. 1982. Self-awareness and the emergence of mind in primates. Amer. J. Primatol. 2:237-248. Gallup, G. G., L. B. Wallnau & S. D. Suarez. 1980. Failure to find self-recognition in mother-infant and infant-infant rhesus monkey pairs. Folia Primatol. 33:210-219. Gallup, G. G. 1977. Absence of self-recognition in a monkey (Macaca fascicularis) following prolonged exposure to a mirror. Develop. Psychobiol. 10(3):281-284. U. S. Department of Health & Human Services. 1985. Guide for the Care and Use of Laboratory Animals. Bethesda, MD. Hall, K. R. L. 1962. Behaviour of monkeys towards mirror-images. Nature 195:1258-1261. Harlow, H. F., M. K. Harlow & S. J. Suomi. 1971. From thought to therapy: lessons from a primate laboratory. Am. Scient. 59:538-549. Harlow, H. F. & S. J. Suomi. 1971. Social recovery by isolation-reared monkeys. Proc. Nat. Acad. Sci. 68:1534-1538. Hediger, H. 1977. Nest and home. Folia Primatol. 28:170-187. Horn, A. D. 1980. Some observations on the ecology of the bonobo chimpanzee (Pan paniscus, Schwarz 1929) near Lake Tumba, Zaire. Folia Primatol. 34:145-169. Huebner, D. K. & J. E. King. 1984. Kittens as therapists: social behavior sequences in isolated squirrel monkeys after exposure to young conspecifics. Dev. Psychobiol. 17:233-242. International Primatological Society Guidelines for Breeding and Captive Care of Nonhuman Primates. Prepared by the Captive Care Committee, July 1988. Itakura, S. 1987. Use of a mirror to direct their responses in Japanese monkeys (Macaca fuscata). Primates 28(3):343-352. Kraemer, G. W. & W. T. McKinney, Jr. 1979. Interactions of pharmacological agents which alter biogenic amine metabolism and depression. J. Affective Disorders 1:33-54. Layng, P. & C. DauDelin. 1988. Alleviating stress in the research monkey. CALAS Newsl. 20(2):40-41. Line, S. 1987a. Environmental enrichment for laboratory primates. JAVMA 190:854-859. Line, S. 1987b. Behavioral and physiologic response of rhesus macaques to an environmental enrichment device. Lab. An. Sci.37:509. MacLean, P. D. 1964. Mirror display in the squirrel monkey, Saimiri sciureus. Science 146:950-952. Mineka, S., M. Gunnar, & M. Champoux. 1986. Control and early socioemotional development: infant rhesus monkeys reared in controllable versus noncontrollable environments. Child Dev. 57:1241-1256. Nadler, R. 1988. Variance of food schedule- unpublished. Nash, L. T. & S. Chilton. 1986. Space or novelty?: effects of altered cage size on galago behavior. Amer. J. Primatol. 10:37-49. Novak, M. & K. Drewsen. 1988. Enriching the lives of captive primates: issues and problems. In: E. Segal (ed.) Psychological Well-Being of Captive Primates. Noyes (in press). Novak, M. & S. Suomi. 1988. Psychological well-being of primates in captivity. J. Amer. Primatol. (in press). Novak, M. 1979. Social recovery of monkeys isolated for the first year of life: II. Long-term assessment. Dev. Psychol. 15:50-61. Novak, M. A. & H. F. Harlow. 1975. Social recovery of monkeys isolated for the first year of life: I. Rehabilitation and therapy. Dev. Psychol. 11:453-465. Oates, J. F. 1987. Food distribution and foraging behavior. In: B. Smuts, D. Cheney, R. Seyfarth, R. Wrangham, T. Struhsaker (eds.) Primate Societies. Chicago: University of Chicago Press. Pp. 197-209. O'Neill, P. 1987. Enrichment techniques for confined primates. Scientist Center Newsletter. 9(4):5-8. O'Neill, P. 1988. Developing effective social and environmental enrichment strategies for macaques in captive groups. Lab Anim. 17(4):23-36. O'Neill, P. 1989. A room with a view for captive primates: Issues, goals, related research strategies. pp. 135-160. In: E. Segal (ed.) Housing, Care and Psychological Wellbeing of Laboratory and Captive Primates. Noyes Publications, Park Ridge, NJ. Paulk, H. H., H. Dienske & L. G. Ribbens. 1977. Abnormal behavior in relation to cage size in rhesus monkeys. J. Abnorm. Psych. 86(1):87-92. Pearce, B. & D. Beauchamp. 1988. The effects of management upon the quality of the breeding and research non-human primate. CALAS Newsl. 20(2):37-39. Reinhardt, V. 1989. Evaluation of the long term effectiveness of two environmental enrichment objects for singly caged rhesus macaques. Lab Animal 18(6):31-33. Reinhardt, V. 1989. Re-pairing caged rhesus monkeys. Lab. Primate Newsletter. 28(4):19. Reinhardt, V., D. Cowley, S. Eisele, R. Vertein & D. Houser. 1987a. Preliminary comments on pairing adult female rhesus monkeys for the purpose of environmental enrichment. Lab Prim. Newsl. 26(3):5-8. Reinhardt, V., D. Houser, S. Eisele, D. Cowley, & R. Vertein. 1987b. Behavioral responses of unrelated rhesus monkey females paired for the purpose of environmental enrichment. Amer. J. Primatol. 14:135-140. Renquist, D.H. & F.J. Judge. 1985. Use of nylon balls as behavioral modifier for caged primates. Laboratory Primate Newsletter. 24:4. Ruppenthal, G. C., G. L. Arling, H. F. Harlow, G. P. Sackett & S. J. Suomi. 1976. A 10-year perspective of motherless-mother monkey behavior. J. Abnorm. Psych. 85(4):341-349. Schmidt, E.M., G.M. Dodd & J.S. McIntosh. 1989. A perch for primate squeeze cages. Lab. An. Sci. 39(2)166-167. Simpson, M. 1984. Behavior as a guide to management of macaques. In: Standards in Laboratory Animal Management, Part 2. Potters Bar: Universities Federation for Animal Welfare. Pp. 217-224. Snowden, D., A. Savage & P. McConnell. 1985. A breeding colony of cotton-top tamarins (Saguinus oedipus). Lab Anim Sci 35:477-480. Southwick, C. H. 1967. An experimental study of intragroup agonistic behavior in rhesus monkeys (Macaca mulatta). Behaviour 28:182-209. Stanton, M. E., J. M. Patterson & S. Levine. 1985. Social influences on conditioned cortisol secretion in the squirrel monkey. Psychoneuroendocrinology 10:125-134. Suomi, S. J., M. L. Collins, H. F. Harlow & G. C. Ruppenthal. 1976. Effects of maternal and peer separations on young monkeys. J. Child Psychol. Psychiat. 17:101-112. Suomi, S. J. 1973. Surrogate rehabilitation of monkeys reared in total social isolation. J. Child Psychol. Psychiat. 14:71-77. Suomi, S. J. 1983. Social separation in monkeys as viewed from several motivational perspectives. In: E. Satinoff & P. Teitelbaum (eds.) Handbook of Behavioral Neurobiology, Vol. 6: Motivation. New York: Plenum Press. Pp.543-583. Suomi, S. J., M. L. Collins & H. F. Harlow. 1973. Effects of permanent separation from mother on infant monkeys. Dev. Psychol. 9(3):376-384. Suomi, S. & H. Harlow. 1972. Social rehabilitation of isolate-reared monkeys. Dev. Psychol. 6:487-496. Suomi, S. J., H. F. Harlow & S. D. Kimball. 1971. Behavioral effects of prolonged partial social isolation in the rhesus monkey. Psych. Reports 29:1171-1177. Suomi, S. J., H. F. Harlow & C. J. Domek. 1970. Effect of repetitive infant-infant separation of young monkeys. J. Abnorm. Psych. 76(2):161-172. Watson, D.S.B., B.J. Houston and G.E. Macallum. 1989. The use of toys for primate environmental enrichment. Lab. Prim. Newsl. 28(2):20. Westergaard, G. C. & T. Lindquist. 1987. Manipulation of objects in a captive group of lion-tailed macaques. Amer. J. Primatol. 12:231-234. Westergaard, G. C. & D. Fragaszy. 1985. Effects of manipulatable objects on the activity of capuchin monkeys (Cebus apella). Zoo Biol. 4:317-327. Williams, L.E., C.R. Abee, S.R. Barnes & R. B. Richer. 1988. Cage design and configuration for an arboreal species of primate. Lab. Anim. Sci. 38(3):289-291. Vanderlip, S. L., J. E. Vanderlip & S. Myles. 1985a. A socializing program for laboratory-raised canines. Lab. Anim. 14(1):33-36. Vanderlip, S. L., J. E. Vanderlip & S. Myles. 1985b. A socializing program for laboratory-raised canines. Part 2: The puppy socialization schedule. Lab. Anim. 14(2):27-36. Wolff, A.V. 1989. Polyvinyl chloride piping as perch material for squirrel monkeys. Lab. Prim. Newsl. 28(1):17. Zeller, A. C. 1987. Communication by sight and smell. In: B. Smuts, D. Cheney, R. Seyfarth, R. Wrangham, T. Struhsaker (eds.) Primate Societies. Chicago: University of Chicago Press. Pp. 433-439.