2—
Essentials of a Program to Provide Psychological Well-Being

We should emphasize the following points: freedom or reasonably spacious quarters, fresh air and sunshine, preferably coupled with marked variations in temperature, cleanliness of surroundings as well as in the body; clean and carefully prepared food in proper variety and quantity; a sufficient and regular supply of pure water; congenial species companionship and intelligent and sympathetic human companionship, and finally, adequate resources, both in company and in isolation, for work and play (Yerkes 1925).

Current regulations require that facilities develop, document, and follow a plan for promoting the psychological well-being of captive nonhuman primates (9 CFR, Subchapter A). The plan must address the social needs of the primates housed in a facility and provide some form of environmental enrichment, that is, opportunities for the expression of species-typical activity. Beyond those general requirements, however, the specifics are left to individual institutions. This strategy is a direct acknowledgment of the impossibility of developing a single, over-arching plan that can promote psychological well-being in all individual members of every species of nonhuman primates in all possible housing conditions.

Psychological well-being is directly related to life history and to the unique adaptations of each species to its ecological niche (Novak and Suomi 1991). Psychological health is also a function of the unique life experiences of individual animals. Thus, the environmental conditions that promote the psychological well-being of primates will necessarily differ as a function of developmental experiences, species, sex, and individual differences (Lehman and Lessnau 1992;



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--> 2— Essentials of a Program to Provide Psychological Well-Being We should emphasize the following points: freedom or reasonably spacious quarters, fresh air and sunshine, preferably coupled with marked variations in temperature, cleanliness of surroundings as well as in the body; clean and carefully prepared food in proper variety and quantity; a sufficient and regular supply of pure water; congenial species companionship and intelligent and sympathetic human companionship, and finally, adequate resources, both in company and in isolation, for work and play (Yerkes 1925). Current regulations require that facilities develop, document, and follow a plan for promoting the psychological well-being of captive nonhuman primates (9 CFR, Subchapter A). The plan must address the social needs of the primates housed in a facility and provide some form of environmental enrichment, that is, opportunities for the expression of species-typical activity. Beyond those general requirements, however, the specifics are left to individual institutions. This strategy is a direct acknowledgment of the impossibility of developing a single, over-arching plan that can promote psychological well-being in all individual members of every species of nonhuman primates in all possible housing conditions. Psychological well-being is directly related to life history and to the unique adaptations of each species to its ecological niche (Novak and Suomi 1991). Psychological health is also a function of the unique life experiences of individual animals. Thus, the environmental conditions that promote the psychological well-being of primates will necessarily differ as a function of developmental experiences, species, sex, and individual differences (Lehman and Lessnau 1992;

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--> Line and others 1991; Novak and Suomi 1988; Novak and others 1993; O'Neill and Price 1991; Suomi and Novak 1991). Nevertheless, it is possible to identify the important elements that should be considered in designing a program to promote the psychological well-being of captive nonhuman primates. The maxims presented by Yerkes (1925) many years ago concerning the husbandry and well-being of apes still serve as useful guidelines as we move beyond taking care of only the physical needs of nonhuman primates to try to provide for their psychological needs. Yerkes's views on social housing, the importance of work and play, the need for congenial and capable caregivers—all presaged contemporary views about primate psychological needs. We believe that a well-designed plan to provide for psychological well-being should promote balanced or positive temperament as defined in the previous chapter. To achieve these goals, the plan should include Appropriate social companionship. Opportunities to engage in behavior related to foraging, exploration, and other activities appropriate to the species, age, sex, and condition of the animals. Housing that permits suitable postural and locomotor expression. Interactions with personnel that are generally positive and not a source of unnecessary stress. Freedom from unnecessary pain and distress. Social Companionship Social interactions are considered to be one of the most important factors influencing the psychological well-being of most nonhuman primates. A social environment enables nonhuman primates to perform many species-appropriate activities, including grooming, play, sleeping huddles, and sexual behavior. Moreover, partners contribute to meeting other psychological needs by providing variation (e.g., social interactions that are not completely predictable), challenge (e.g., competition for access to objects), and opportunity for control (e.g., play bouts) (Mineka and Kihlstrom 1978; Mineka and others 1986). Most primates normally live in social groups, and they should be socially housed if they are to express many aspects of their normal behaviors. However, the introduction of strange cagemates should be done gradually under conditions that minimize the likelihood of injurious aggression. For example, compatibility might be assessed by observing animals while they occupy adjacent cages, before allowing them to interact (Reinhardt 1989a). Knowing that most primates benefit from social interactions, it should be obvious that they can be harmed by a lack of social interaction. Harlow and Suomi (1971), Harlow and others (1971), Novak (1979), and numerous others have elicited profound behavioral problems by rearing infant and young macaques

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--> without mothers or peers. Davenport and others (1973) and Fritz (1986) reported on problems encountered in the resocialization of chimpanzees that had been maintained without appropriate social conspecific interaction. The manifestations of inadequate early rearing include a broad range of species-inappropriate behaviors, such as the inability to cope with stress as evidenced by self-biting; lack of appropriate breeding and parental skills; rocking, eye-poking, and other stereotypic behaviors; coprophagy; and inability to interact appropriately in social situations. Many of these behaviors are refractory to change and persist for life; at best remediation programs are labor intensive and expensive. Clearly, the goal of housing nonhuman primates is to avoid the development of behavior problems through the careful planning, execution, and assessment of an institutional strategy, or plan, for ensuring the psychological well-being of the animals. Although social housing is a critical component of psychological well-being, careful consideration is required in developing the procedures to achieve this objective. Because of the xenophobic reactions of many primate species, which can result in severe aggression to strangers, attempts to pair monkeys or create social groups must be handled with care (Clarke and others 1995). A number of different strategies—which vary according to the species, age, sex, and social experience—are possible for forming pairs or groups of primates (Coe 1991; Cooper and others 1997; Crockett and others 1997; Fritz 1986, 1989, 1994; Reinhardt 1988, 1989a, 1991a; Vermeer 1997). It should be remembered, however, that many species of primates express social dominance, and fighting between animals can occur (Bayne and others 1995). Although unfamiliar rhesus monkeys can be introduced to one another and become compatible pairs (Reinhardt 1989a), it is not so easy to introduce a rhesus monkey into a previously established group, because of the likelihood of a severe group attack. Rhesus groups are best formed with total strangers so that individuals are protected by the ''organized chaos" of the group (Bernstein 1964). Other species, with different social dynamics, such as capuchins, present different challenges (Fragaszy and others 1994). As with all close human-nonhuman primate interactions, personnel safety should receive the utmost consideration when forming pairs or groups of primates. The ability to separate incompatible animals should be well planned before new introductions. Although a social living situation is important, there can be practical and scientific reasons for using individual housing, such as research protocols, medical conditions, the possibility of disease transmission, hyperaggressiveness, and hypersubmissiveness. When experimental protocols require individual housing, nonhuman primates should, whenever it is possible, have visual, auditory, or olfactory contact with each other. Animals that have been individually housed, even for long periods, have been successfully resocialized when efforts have been made to find compatible companions.

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--> Opportunities to Engage in Species-Typical Activities The ideal environment for a nonhuman primate fosters the expression of desirable species-typical activities and does not distort the expression of normal behavior. In order to discuss the environment, however, one should first have an understanding of what species-typical activities will support a conclusion that the environment is achieving the goal of enabling individual well-being. Several factors should be considered, and knowledgeable judgment should be used in applying them: Species-typical activities in the wild. A basic understanding of the behavior of a species in the wild is essential if that species is to be maintained in captivity. That is, does the species live in large groups like squirrel monkeys, or is it relatively solitary like orangutans? What type of social group does it have; do either young males or females emigrate from the parent group? Are social groups stable, or are they loosely connected and do they come together primarily for mating? Does the species locomote and sleep in trees, or on the ground? Does it make nests? Does it eat a variety of foods, including some meat, like macaques, or is it more limited to leaves and other plant parts like the colobus? There are many other similar questions one might ask, each varying in importance among the species. These are discussed in more detail in Chapter 5 through 9. In addition to knowing what each species does, an understanding of the "time budget" devoted to its principal activities (i.e., foraging, eating, locomoting, grooming, and sleeping) is desirable (Marriott 1988), but an absolute mirroring of this time budget in captivity is neither practical nor necessary. Some animals might devote the majority of their waking time to foraging, but in the process they might cover many miles. Providing the same time budget for foraging in captivity, without the associated exercise-related activity of locomotion, will likely produce obesity. This suggests the need to provide other types of activities and to reexamine diets. Other behaviors adapted for the wild, such as alarm calls for snakes or hawks should be recognized as alarm calls for unexpected occurrences (such as a broken water pipe, escaping steam, or an animal escaped from its cage) in the captive environment. On the other hand, captive environments that are created without a reasonable appreciation for how animals spend their time in the wild can result in expressions of qualitatively normal behaviors that are quantitatively harmful. Grooming of self or others to the point of baldness is a common example. Knowledge of individual animal's previous history. As important as understanding "normal" species-typical activities in the wild is an appreciation for how an animal has been raised in captivity. A normally social animal raised for years in a semi-social environment (e.g., a room with multiple animals all in single cages) might not readily adapt to a normal social grouping, although studies have shown that this is not invariably the case. Some become adapted to people and

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--> develop close bonds with them, whereas others are highly stressed when people are near. Nature of the research. Some research requires housing conditions that restrict the movement or social interactions of animals. In such cases, efforts should be redoubled for these animals, when it is compatible with the protocol, to compensate for their well-being in other ways, e.g., provision of food treats and "toys" with which they will interact. Types of research facility and housing opportunity. Metropolitan medical centers have less space for holding animals than suburban settings. Not all facilities can have the option of large multi-acre outdoor facilities, but that does not make indoor or indoor-outdoor settings less capable of providing for the well-being of the animals. Each has its strengths and limitations—animals in a large paddock are more difficult to treat when they are hurt than are those in smaller environments—but each has the potential to provide all aspects of the well-being of most species. Each of those considerations—behaviors in the wild, rearing conditions, nature of the research, and type of housing—should be addressed in answering the question, What is meant by a suitable expression of species-typical activities with which an animal's well-being can be assessed? The answer to that question is what this book is all about. Many captive environments do not allow for the expression of the full range of desirable species-typical activities, such as foraging and exploration, unless they are enhanced by providing devices that foster such activities. Key to the establishment of environmental enrichment and the enabling of species-typical behaviors are the concepts of habituation and interest. Objects that retain their interest for the animal have a higher probability of contributing to the well-being of an animal, whereas objects that lose interest for the animal or to which the animal becomes habituated contribute little to well-being. Assessment of interest should be a continuing aspect of all environmental enrichment programs. Throughout this text we use the terms species-typical and species-appropriate to refer to behavior that knowledgeable observers might consider normal and desirable. The most reasonable interpretation of what behaviors are normal and appropriate should take into account behavior of the species in the wild; time budgets, or quantity of time devoted to each behavior; and the quality of the behavior as exhibited in captivity. For example, social grooming is commonly seen in the wild and is considered a desirable species-typical activity in captivity. But when grooming is exhibited at the expense of other normal behavior, it becomes an undesirable excess of a species-typical behavior. Whereas grooming is desirable, overgrooming is not, and it represents a time budget out of balance and a warping of the quality of the behavior that results in a distortion of the numerous behaviors that the species commonly exhibits. (See also Erwin and Deni 1979.) Providing animals with opportunities to engage in species-typical activities

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--> includes providing opportunities for them to control and predict environmental changes. Providing suitable opportunities for self-initiated activities (e.g., wood chips to permit foraging, and social companions with which to groom or play) allows animals some degree of control. When a routine is under human control (e.g., cleaning, feeding, and experimental manipulations), clear signals of the nature of the activity allow animals to anticipate and adapt to events. When a routine is essentially innocuous to the animal, clear signals that identify an environmental change as part of a familiar routine can be beneficial. On the other hand, pleasant surprises, such as treats and favored activities, need not be so routinized. Similarly, when procedures involve some level of discomfort to an animal, long anticipatory periods signaling the impending event can be a source of distress. Individual animals can control some features of their environment through self-initiated activity if opportunities are provided. Even though an activity might be repetitive and the material familiar, animals can control some of the changes in their environment. This control, or "work," is a common feature of the activity of animals in natural settings and can take many forms (Reinhardt 1993, 1994a). A degree of environmental control and challenge and the opportunities to engage in species-typical activities can be provided through enrichment techniques that provide opportunities for voluntary interaction. Such opportunities should be oriented to the animals' physical and cognitive capabilities, rather than aesthetic appearance. Enrichment devices should be carefully selected on the basis of the behavior that needs opportunities for expression. An enrichment program should be customized to the animals and the institution; what is successful in one facility might not work in another (Bayne and others 1993b). Enrichment devices can be used for both individually and socially housed primates; in the latter case, the devices should stimulate social interest and play, not competition that leads to fighting. Environmental enrichment is a broad classification that encompasses various methods. For example, such cage furnishings as perches, shelves, and tunnels have been used to increase the comfort of animals by allowing them to get off the cage floor, assume a variety of physical postures, engage in various physical activities, and escape the attention of others when socially housed (Neveu and Deputte 1996). Methods to increase species-typical behaviors, such as foraging activities, include hiding food in wood shavings or wood wool spread on the enclosure floor (Chamove and others 1982), using foraging puzzles that require an animal to discover the presence of food in a container and implement a strategy to obtain it (Hayes 1990; Murchison 1995), spreading particulate food on foraging boards to increase the time spent in collecting it (Bayne and others 1992b), and placing food in different locations within the primary enclosure and so requiring an animal to move around its home to obtain food. The use of such devices can vary widely, and provision should be made to ensure that every

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--> animal receives its daily ration of food. Devices suitable for animals of some ages and species might not be suitable for all ages and species. Manipulable objects should be sanitizable or replaceable and not harmful to animals or the caging and physical-plant utility systems. Objects (often durable toys) that animals can explore visually, orally, and tactually are often used because they are inexpensive and easy to sanitize. Some metal and plastic pieces can become ingested or entangled over the head and limbs and cause considerable harm to the animals (Murchison 1993). Small objects can go down the drains and clog sewer systems or damage sewage lift pumps. Moreover, these objects might be of little value if the species in question is not particularly manipulative or if animals readily lose interest in them. In general, a combined strategy of risk assessment and cost-benefit analysis should be used for the selection of these objects. Clearly, not all devices that present some risk should be avoided if they are thought to benefit the animals. Straw and burlap bedding, cargo nets, and destructible (and edible) objects can be injurious to animals, but if they are carefully selected and the animals are frequently observed, we believe that the benefits of many of these types of objects outweigh their potential harm. A number of devices and toys have been reported on in the literature. None appear to be universally suited to all animals. A toy that appears to be beneficial for one rhesus might be ignored by another in the same colony. We do not believe it possible to recommend which toys are best for any species, but we do believe that some general guidelines can be developed. Several categories of devices have been used for nonsocial enrichment. An exhaustive list is not possible, and some of the best are noncommercial products, such as recycled cardboard, telephone directories, and plastic bottles alone or filled with frozen juice or food. For the sake of simplicity, we think of these devices in three categories: manipulable objects (toys), foraging situations or apparatuses (Line and others 1990a), and furniture for climbing, resting, perching, or locomoting above the floor. Toys consist of commercial or home-made manipulable objects of plastic, hard rubber (e.g., Kong® toys, see Crockett and others 1989), paper (such as telephone directories), or wood (Reinhardt 1997b). In general, they consist of man-made objects not used by the animals in the wild but of some possible benefit for some animals through handling, mouthing, and use as "tools," which often result in the destruction of the items. The novelty of the items seems to wear off rapidly for many animals, and new and different toys are needed to restimulate animals to use them (Lutz and Farrow 1996; Paquette and Prescott 1988; Taylor and others 1997a). Toys might be rotated through the colony on the basis of such characteristics as texture, shape, and color to help sustain interest. Foraging boards and puzzles stimulate foraging activity and are discussed in many sections of this report. In the furniture category are ropes, swings, perches, and climbing structures; deep bedding with or without browse, such as grains and popcorn; nest boxes and other structures to permit privacy and escape; and mir-

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--> rors and video monitors. The list is limited only by the imagination of each person who has some responsibility for the welfare of animals. The type of enrichment selected is often based on whether an animal is singly housed or pair or group-housed. Toys have been used most commonly for singly housed animals, but might show promise for group-housed animals (Brent and Belik 1997; Novak and others 1993). Other variables are involved in the selection and evaluation of these devices, including the species for which they are used. Additional discussion of this topic is provided in Chapters 5–9. Technologically more complex enrichment devices, such as joystick-operated computer games that challenge cognitive and motor capabilities, have proved of interest to chimpanzees and several species of monkeys for long periods. Unfortunately, they are relatively expensive and require considerable maintenance. Some single-housed primates will watch television that depicts activities of their own species (Brent and others 1989; Rumbaugh and others 1989) and a recent report suggests that rhesus monkeys watch television if the scenes change rapidly (Platt and Novak 1997). In addition to the properties of an enriching device itself, other factors affect whether and to what extent an animal might find it "enriching." These factors include the mode of presentation, such as the spacing of puzzle feeders to avoid competition (Maki and others 1989); order of presentation and time of exposure to minimize declining interest (Cardinal and Kent 1998; Crockett and others 1989; Leming and Henderson 1996; Paquette and Prescott 1988); visibility; and ease of access. Other authors have discussed these issues as well (Bayne 1991; Fritz and Howell 1993a; Bloomsmith and others 1991). Some foods provide both nutrition and opportunity for manipulation, such as scattering corn, popcorn, or other items in the bedding (Beirise and Reinhardt 1992; Grief and others 1992). Food treats can also be given in the form of unprocessed fruits and vegetables. Unpeeled bananas, artichokes, potatoes, and coconuts increase animals' processing time of the food and can provide entertaining moments for the animals and care staff (Bloomsmith 1989; Nadler and others 1992). Fruit juices, as liquid or frozen into cubes, are also enjoyed by many animals (Goodwin 1997). Even increasing the frequency of feeding seems beneficial (Nadler and others 1989; Taylor and others 1997b). There are many opportunities for creativity in the use of food treats and presentation of food as part of well-being programs. The diet should be nutritionally balanced and raw food treated to decrease the likelihood of infection (NRC 1996, p. 40). Housing Design Housing should permit the expression of species-typical postures and locomotion. Species, age, sex, and individual histories are important factors to consider when evaluating housing designs. Performance standards based on postural adjustments and locomotor activities preclude specification of dimensions

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--> on the basis of any single criterion, such as body weight or dimension. Use of legal cage sizes will not always meet an animal's behavioral requirements. Species that normally move by brachiation (swinging from hand to hand while hanging from supports) or vertical leaping and clinging require substantially different cage designs from conventional quadrupedal striders even if all are of similar body weight. Cage design should reflect units of usable space, that is, space in the cage through which the animal can move. For example, a high glass-walled cage with no vertical perches or climbing structures might look like a two-dimensional environment to its inhabitants whereas a smaller cage, with a smaller floor area and multiple climbing surfaces, might provide more usable space for many nonhuman primates. Species-typical behavior can be promoted by various aspects of cage design. There should be sufficient space and furnishings, and they should be allocated and placed in a manner that supports basic locomotor patterns and postural adjustments. Special additions to a cage, such as feeding devices, can be placed so as to foster species-typical posture and locomotion. Features of the environment that appeal to humans (such as vertical smooth walls, tidy floors, minimal odors, and soft toys) are not necessarily conducive to the well-being of all nonhuman primates. For example, soft toys might be suitable for infants of some species but dangerous to adults that might try to eat the toys. When animals are housed socially, the committee believes the spatial requirements of the group need not be calculated by assessing the spatial requirements for one animal to express normal postures and locomotion and multiplying by the number of animals. For example, if housing needs to be 2 m high to permit brachiation, a cage for two animals does not need to be 4 m high. Likewise, floor areas need not be simple multiples. In fact, for arboreal species that normally flee up and spend most of their time climbing, floor area might be secondary to vertical space in providing for postural and locomotor opportunities. The volume of usable space could be the appropriate dimension to consider, and individual animals must have sufficient usable space to express normal postures and locomotion when the space occupied by each cage companion is taken into account. When two animals are housed together by interconnecting their cages, greater spatial opportunities exist for both than when each is housed in its separate cage. Thus, modification of current cage size regulations ought to be considered. Ten animals might not require 10 times the floor space of a single animal to ensure adequate space for normal postures and locomotion, but some animals might need more space than others (NRC 1996), for example, for fleeing from the aggression of dominant animals (old, sedentary, or infirm animals might use less space than younger animals). We agree strongly with Subpart D, paragraph 3.80(c) of the Animal Welfare Standards, which states that "innovative primary enclosures not precisely meeting the floor area and height requirements provided in paragraphs (b)(1) and (b)(2) of this section, but that do provide nonhuman primates with a sufficient

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--> volume of space and opportunity to express species-typical behavior, may be used …" That statement and paragraph 3.81(a) (Social Groupings) properly encourage social groupings and behaviorally defined cage space. However, many nonhuman primates are now singly housed because of paragraph (b)(2)(iv) which states that: "when more than one nonhuman primate is housed in a primary enclosure, the minimum space requirement for the enclosure is the sum of the minimum floor area space required for each individual nonhuman primate…." We believe that the latter statement is indefensible and that cage design (volume and furnishing) should result from a thoughtful understanding of the needs of the animals, not from multiples of body weight of the inhabitants. We further believe that many nonhuman primates in single cages today would benefit from a compatible cagemate, even if the cage sizes do not precisely meet the letter of the law (Eaton and others 1994; Reinhardt and Hurwitz 1993); such is the strength of our belief in the value of social housing. This attitude is also expressed in the Guide for the Care and Use of Laboratory Animals (NRC 1996). Providing housing environments with materials, surfaces, and structures that support species-normal activities might make them more difficult to sanitize. For example, the use of wood shavings and wooden structures has often been discouraged in primate enclosures for sanitation reasons. However, at least one study (Chamove and others 1982) has found a decrease in bacterial content over time in wooden shavings placed on the cage floor and an increase in behavior classified as desirable in five of six species of nonhuman primates studied. Some natural wood products contain bactericidal compounds that provide self-sanitation (D.O. Cliver, University of Wisconsin-Madison, unpublished data, 1993). Straw or woodchip bedding, ropes of natural materials, branches, and cardboard products can all increase the variety of surfaces and objects in a cage. When these materials have been replaced because of wear or soiling, they have not been found to constitute a health hazard. The colony manager, veterinarian, and institutional animal care and use committee (IACUC) should monitor the effectiveness of these cage modifications to ensure they enhance well-being consistent with good sanitation and the requirements of the research project. (See also NRC 1996.) Although chewed wooden structures might not be aesthetic, some species need to chew wood or other suitable material to keep their teeth and gums in good condition. Other species require wooden or porous surfaces for scent-marking (Epple 1986). The use of wooden structures and objects to support locomotor and manipulative activity should require only that appropriate schedules be developed for replacement to meet valid sanitation concerns. Likewise, open water in streams, pans, or puddles supports varied activities in many species and should be acceptable, given reasonable procedures to maintain sanitation. The frequency of changing soiled or worn materials and access to streams or puddles requires reasonable care to ensure that they do not present a health hazard. Access to streams or puddles need not be routinely prevented (NRC 1996, p. 41). Those who develop plans for psychological well-being and those evaluating

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--> and inspecting such plans should be aware of the benefits of using natural objects that support varied natural activities (Reinhardt 1997b). Thinking about the nature of suitable caging material in absolutes should be discouraged in favor of carefully crafted plans that take into account the housed animals' psychological needs to engage in species-typical activities. Personnel Interactions It is essential that both the providers of animal care and those overseeing the animal care program receive training regarding the physical and behavioral needs of each species in a facility (9 CFR Ch. 1 (Animal Welfare Regulations) paragraph 3.85; CCAC 1993; NRC 1991, 1996). Training should be part of all technicians' jobs and should be supplemented with institution-sponsored discussions and training programs and with reference materials applicable to their work and to the species with which they are engaged (Kreger 1995). Coordinators of institutional training programs can seek assistance from the Animal Welfare Information Center (AWIC), Beltsville, Md., U.S. Department of Agriculture, Agricultural Research Service, National Agricultural Library (see also NRC 1991). Relevant personnel should be skilled in procedures, such as capture and cage sanitation, both to minimize animal distress and to maximize caregiver safety. They should learn to identify individual animals and to recognize normal and abnormal behavior of individual animals. They should also know about species-typical patterns of social organization so that they can form appropriate social groups and understand which animals in a social group are most vulnerable to aggressive attacks and injuries. Finally, it is important to be aware that social interactions with familiar human caregivers can have marked positive effects (Baker 1997; Bayne and others 1993a; Wolfle 1985; 1987) and, conversely, that an animal can behave quite differently, even somewhat abnormally, toward unfamiliar persons, such as new animal technicians or visitors (Chamove and others 1988; Miller and others 1986). Chapter 3 presents some detailed comments on training personnel and animals in necessary routines that involve human-animal interactions. A good program for animal care should include plans for monitoring, intervention, remediation, and appropriate documentation. Observations of animals, especially of large outdoor nonhuman primate colonies, is a shared responsibility that varies greatly among facilities and includes the animal care staff, behavioral scientists and technicians, and other investigators. The key is that each animal should be observed daily (although we recognize that this might not be possible in island colonies and similar situations) by people appropriately trained to do so in a manner consistent with the constraints of the facility and welfare of the animals. Records should include identification of unusual behavior, provisional diagnoses (including assessment of the current condition and aspects of an

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--> animal's history that are necessary for its interpretation), and attempted remediation and its effectiveness (NRC 1996). Documentation In order to "develop, document, and follow an appropriate plan for environmental enhancement adequate to promote the psychological well-being of nonhuman primates" (9 CFR 3.81), each institution's plan should contain a statement of goals, specify the methods that will be used to achieve the goals, and describe the criteria that will be used to evaluate the effectiveness of the program. A guiding principle is that the program should be based on an understanding of the natural history of a species and its traits and, where necessary, should take into account the histories of individual animals. It is important to recognize that programs to promote the psychological well-being of nonhuman primates are living documents subject to change and updating as new information is acquired. Each facility should have protocols for diagnosing the cause of physical impairments and abnormal behavior, determining when remediation is necessary, developing remediation plans, assessing effectiveness of remediation, and maintaining appropriate records; they should specify who will be responsible for each aspect of diagnosis, remediation, assessment, and documentation. Personnel making the decisions should have training in the aspects of veterinary medicine and primate behavior necessary to ensure that diagnoses and treatments are developed in a knowledgeable manner. It is recognized that there might be no known methods for remediating some physical impairments and abnormal behavior (Novak and others, in press) and that for some individual animals all known methods of remediation might prove ineffective. In those cases, it is important that personnel responsible for animal care document good-faith efforts to use all currently available information in attempting remediation. The well-being of research animals is not just a consideration of the animal care staff. In many cases, it begins with the research protocols. Research methods should be evaluated regularly; as less stressful or less invasive methods are developed, their adoption should be considered. Methods of enhancing animal well-being must be consistent with the requirements and goals of the research (NRC 1996). Checklist for a Plan to Promote the Psychological Well-Being of Nonhuman Primates This outline constitutes a sample checklist of points to consider in the development of institutional plans to provide for the psychological well-being of non human primates. The institutional plan should clearly reflect species variations. However, few plans can be expected to be equally beneficial for all individuals of a species, and professional judgment should be exercised to address the needs of

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--> individual animals. It should be remembered that, as with the Guide (NRC 1996) itself, this checklist provides the goals but implementing standards should be developed by individual institutions to achieve the goals in their settings, with their personnel, and for the individuals and species being considered. The authors of this report believe that no single plan developed here or by a particular facility, can be entirely adequate for all facilities. We also understand that the initial development of a plan by an institution that has not previously developed one, can be daunting. We have therefore referenced items in the following checklist to the discussion in the text, which should enable construction of a plan suitable to each institution's goals and species. Additional information about the construction of plans can be found in Appendix A. Also, institutions designing enrichment plans for nonhuman primates are encouraged to take advantage of the periodic bibliographies on related subjects provided by the U. S. Department of Agriculture's Animal Welfare Information Center (AWIC 1992). (See also AWI 1998.) Statement of Goals The plan should contain a statement of the goals of the facility in terms of the following topics that apply: Research. (p. 19) Breeding. (pp. 12, 17, 42–43) Sales. Education. (p. 25) Exhibition. Other. The plan should contain a statement of the aims of the well-being program in terms of the following topics that apply: Providing opportunities for the expression of a broad range of species-typical behaviors. (pp. 18–22) Providing cognitive stimulation. (pp. 21–22) Decreasing self-injurious behavior. (pp. 11, 17, 19, 21, 33–35) Decreasing stereotypies (such patterns as pacing and eye-poking). (pp. 12–14, 17) Providing predictability of routine procedures and events. (p. 20) Providing opportunities for animals to alter their environment. (pp. 20, 33) Training personnel and animals for husbandry and biomedical routines. (pp. 25, 37, 40–42) Other.

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--> Pertinent Information The plan should contain a brief summary of relevant information on the natural history and behavioral ecology of each species of nonhuman primate in the facility in the context of scientific justification for the enrichment strategies implemented. The clinical records should indicate both the medical and behavioral status of the animals and treatment(s) to be administered. Environmental or behavioral enrichments might include such treatments as the following: Habitat diversity. Feeding habits. (pp. 18, 20, 39–40) Social organization. (pp. 13–14, 16–17, 25, 42–43) Manipulable objects and toys. (pp. 21–22) Other The plan should provide a mechanism for maintaining and using animal records if such a plan is not already part of the facility program, including the following types of information, if known: Source of animal (born at facility or acquired from person and/or institutional source). (pp. 13, 19) Rearing history (wild-born, reared at facility in mixed-sex groups, peer-reared, etc.). (p. 19) Housing history (type of cage and types of partners). (P. 12) Health and behavior records and miscellaneous observations. (pp. 26, 38–39) Other. Social Interactions (pp. 13–14) The plan should contain a discussion of how social interactions are to be provided, including one or more of the following: Continuous housing in pairs or groups. (pp. 16–17) Intermittent housing in pairs or groups, e.g., 1h or more several times a week (a standard procedure for social unit formation should take into account the risks in group formation). (p. 17) Visual, auditory, and olfactory contact with conspecifics. (pp. 17, 33) Positive interaction with animal care technicians. (p. 25) Interactions with other species (e.g., chimpanzees with dogs). (p. 108) Environmental Enrichment The plan should contain a discussion of techniques used to provide opportunities for foraging and exploration, such as those in the following list. It is recommended that techniques from the categories

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-->     given below be combined so that enrichment might accomplish multiple objectives. Techniques to promote foraging, including ''processing" of raw vegetables and fruits. (pp. 20–22) Techniques to promote manipulation. (pp. 20–22, 34) Techniques that allow animals to control aspects of the environment (opening doors and peep holes, influencing temperature and light, etc.). (p. 20) Techniques to promote other species-typical activity, including locomotion. (pp. 18–22) Techniques to reduce self-injurious behavior. (pp. 11, 17, 19, 21, 33–35) Techniques that require learning of novel responses for appetitive reward. (pp. 20–22, 40–42) Techniques that provide varied sensory stimuli (e.g., texture, density, shape, size, color, taste, and smell). (pp. 21–22) Other. Special Considerations The plan should make specific provisions for unusual situations and develop strategies for considering psychological well-being in these contexts, including one or more of the following: Strategies for hyperaggressive animals. (pp. 17, 33) Strategies for animals exhibiting injurious behavior. (pp. 34–38) Strategies for individual housing required because of veterinary care or research protocols. (pp. 17, 19–22, 33) Strategies for animals tethered or under restraint. (pp. 19, 40–42) Strategies for young (infant or juvenile) primates. (pp. 16–17, 22–23, 45) Strategies for very old primates. (p. 23) Other. Monitoring Various measures can be used to assess the well-being of nonhuman primates, including the following: Daily physical health checks by caregivers to assess Activity. (pp. 25, 45–46) Physical signs (eye and nose discharges, feces, urine production, menses, food ingestion, etc.). (pp. 11, 45–46) Daily monitoring of behavioral state by caregivers to identify Atypical behavior patterns. (p. 25)

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--> Changes in proportion of normal behavioral activity. (pp. 18–19) Recording reactions to routine husbandry events. (pp. 26, 45) Recording ability to respond to training. (pp. 40–42) Recording responses indicative of distress. (pp. 11, 13, 26) Other. The plan should discuss various elements of remediation (p. 21), including Means of documenting successful and unsuccessful attempts at remediating diagnosed animals. (pp. 12–13, 17) Protocols for followup of remediation efforts. (pp. 25–26) Steps taken to accommodate animals that do not respond to remediation. (p. 26) Establishment of end-point criteria (e.g., serious self-biter). (p. 35) The plan is considered to be effective and properly implemented if one of the following conditions is satisfied: Individual animals are judged to be in a state of well-being, or The cause of distress or atypical behavior in any animal can be shown to be derived from antecedent conditions of abnormal development, inappropriate rearing conditions, or an approved research protocol; practices are identified and implemented for the benefit of future generations of animals; and facility records exist for the presence, etiology, and remediation or accommodation of observed cases of lack of well-being.