Those who conduct research with nonhuman primates or exhibit and view them are increasingly concerned about the psychological well-being of the animals. Psychological well-being is not easily defined and has been interpreted in various ways by those who view, use, display, or regulate nonhuman primates. US Public Law 89-544 (as amended in 1970, 1976, and 1985) specifies that all research facilities in the United States that maintain nonhuman primates must develop a plan for environmental enhancement adequate to promote the psychological well-being of captive animals. The plan must address social needs and provide for group housing of compatible animals when possible. In 1991, the Animal and Plant Health Inspection Service (APHIS) of the US Department of Agriculture (USDA) adopted Title 9 of the Code of Federal Regulations (CFR), Part 3, Subpart D, “Specifications for the Humane Handling, Care, Treatment, and Transportation of Nonhuman Primates.” The subject of Section 3.81 is, “Environment enhancement to promote psychological well-being of nonhuman primates.” Because of concern about the lack of clarity and specificity in the regulations and a perceived lack of enforceability, an APHIS Animal Care Primate Environment Enhancement Team developed a final report on this subject that served as the basis of the USDA APHIS draft policy published in the Federal Register on July 15, 1999 (APHIS, 1999). The 79-page final report includes background on the intent and language of the Animal Welfare Act, the response of the public and the research and exhibit communities, a review of primate-care practices in other countries, and a discussion of the difficulties inherent in measuring psychological well-being. The report also contains a literature review dealing with behaviors of primate species in their natural environments and responses of captive primates to various environmental enhancements. The Institute for Laboratory Animal Research of the National Research Council has published a comprehensive document, The Psychological Well-Being of Nonhuman Primates (National Research Council, 1998).
The consensus of the literature is that “species-typica” or “species-appropriate” behavior should be the goal of environmental-enhancement programs, as should a full range of normal behavior. It is clear that normal behavior depends on the species. APHIS policy states that to adequately promote psychological well-being, consideration should be given to species-specific requirements for social grouping, social needs of infants, environmental structures and substrate, foraging opportunities, and manipulanda. These issues are too complex for full discussion here, and the reader is referred to the APHIS final report (APHIS, 1999).
Food and foraging for food are clearly involved in the psychological well-being of captive nonhuman primates. It has been shown that food and nonfood items can be used in ways that stimulate natural feeding behaviors, extend feeding activity, and inhibit stereotypy (Fajzi et al., 1989; Knapka et al., 1995). Foraging enrichment can be used to disperse animals, occupy their time, and reduce tension and aggressive interactions (Boccia, 1989). Social aggression in chimpanzees has been reduced by behavior modification with food (Bloomsmith et al., 1994), but it is clear that methods of food distribution that are appropriate for one species might be inappropriate for another. As opposed to floor- or ground-based feeding by terrestrial species, vertical clinging is a normal feeding posture for many arboreal primates, such as nocturnal prosimians, tarsiers, and callitrichids (Fleagle, 1998). Tail length and tail-suspension postures during feeding also influence enclosure design and food placement (Poole, 1991; Reinhardt et al., 1996).
Enclosure size can interact with nutrient and energy needs and influence diet composition. Enclosures that are
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 13 Food as a Component of Environmental Enhancement Those who conduct research with nonhuman primates or exhibit and view them are increasingly concerned about the psychological well-being of the animals. Psychological well-being is not easily defined and has been interpreted in various ways by those who view, use, display, or regulate nonhuman primates. US Public Law 89-544 (as amended in 1970, 1976, and 1985) specifies that all research facilities in the United States that maintain nonhuman primates must develop a plan for environmental enhancement adequate to promote the psychological well-being of captive animals. The plan must address social needs and provide for group housing of compatible animals when possible. In 1991, the Animal and Plant Health Inspection Service (APHIS) of the US Department of Agriculture (USDA) adopted Title 9 of the Code of Federal Regulations (CFR), Part 3, Subpart D, “Specifications for the Humane Handling, Care, Treatment, and Transportation of Nonhuman Primates.” The subject of Section 3.81 is, “Environment enhancement to promote psychological well-being of nonhuman primates.” Because of concern about the lack of clarity and specificity in the regulations and a perceived lack of enforceability, an APHIS Animal Care Primate Environment Enhancement Team developed a final report on this subject that served as the basis of the USDA APHIS draft policy published in the Federal Register on July 15, 1999 (APHIS, 1999). The 79-page final report includes background on the intent and language of the Animal Welfare Act, the response of the public and the research and exhibit communities, a review of primate-care practices in other countries, and a discussion of the difficulties inherent in measuring psychological well-being. The report also contains a literature review dealing with behaviors of primate species in their natural environments and responses of captive primates to various environmental enhancements. The Institute for Laboratory Animal Research of the National Research Council has published a comprehensive document, The Psychological Well-Being of Nonhuman Primates (National Research Council, 1998). GOAL OF ENVIRONMENTAL ENHANCEMENT The consensus of the literature is that “species-typica” or “species-appropriate” behavior should be the goal of environmental-enhancement programs, as should a full range of normal behavior. It is clear that normal behavior depends on the species. APHIS policy states that to adequately promote psychological well-being, consideration should be given to species-specific requirements for social grouping, social needs of infants, environmental structures and substrate, foraging opportunities, and manipulanda. These issues are too complex for full discussion here, and the reader is referred to the APHIS final report (APHIS, 1999). ROLE OF FOOD AND FORAGING Food and foraging for food are clearly involved in the psychological well-being of captive nonhuman primates. It has been shown that food and nonfood items can be used in ways that stimulate natural feeding behaviors, extend feeding activity, and inhibit stereotypy (Fajzi et al., 1989; Knapka et al., 1995). Foraging enrichment can be used to disperse animals, occupy their time, and reduce tension and aggressive interactions (Boccia, 1989). Social aggression in chimpanzees has been reduced by behavior modification with food (Bloomsmith et al., 1994), but it is clear that methods of food distribution that are appropriate for one species might be inappropriate for another. As opposed to floor- or ground-based feeding by terrestrial species, vertical clinging is a normal feeding posture for many arboreal primates, such as nocturnal prosimians, tarsiers, and callitrichids (Fleagle, 1998). Tail length and tail-suspension postures during feeding also influence enclosure design and food placement (Poole, 1991; Reinhardt et al., 1996). Enclosure size can interact with nutrient and energy needs and influence diet composition. Enclosures that are
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 too small can restrict growth and movement enough to produce noticeable muscle atrophy (Faucheaux et al., 1978). That effect can be a reflection both of limited exercise and an associated lower energy need, which lead to lower food consumption and inadequate protein intake by young primates from low-protein, high-energy diets. Substrates used on enclosure floors are manipulable items, can provide comfort, and can be part of foraging enrichment (Westergaard and Munkenbeck-Fragaszy, 1985; Bayne et al., 1992; Byrne and Suomi, 1995). Straw, hay, wood-wool, shredded paper, wood chips, blankets, corncobs, and soil have been used. Species or individual animals can show preferences for and more effective use of some substrates than others (Ludes and Anderson, 1996). It is, however, important that gastrointestinal disorders caused by ingestion of substrate or of pathogens in substrate be minimized by care in selecting, storing, and manipulating these materials (Baer, 1998). Wild Environment versus Captivity In the wild, primate diets are diverse and include leaves, stems, flowers, fruits, seeds, gums, insects, spiders, lizards, eggs, and other animal matter. The items selected vary with the species, and the proportions selected can vary from month to month without a clear association of the selections with seasonality of the habitat (Chapman and Chapman, 1990). Precisely gathered information on natural dietary habits is scarce, and field studies that include quantitative nutrient-intake data are exceedingly rare. Data gathered at different sites over time to account for location and seasonal differences and in which food use has been quantified and food composition determined can provide guidance for the development of rational captive dietary systems. To succeed in the wild, primates must learn by example to select foods that, in toto, provide nutrient requirements and that are not toxic. Acquisition of nutrient needs requires that wild primates spend 25—90% of their waking hours in foraging for and consuming food (Clutton-Brock and Harvey, 1977). In contrast, conventionally fed primates in captivity can fulfill their nutrient and energy needs in just a few minutes. Thus, successful enrichment programs involving food are usually designed to extend foraging time by requiring primates to ‘‘work’’ for food and to spend more time in food processing. Nutritionally complete extrusions can be placed in covered plastic buckets and suspended by ropes from structures in primate enclosures. Primates can jump onto the buckets or slide down the ropes and reach through holes in the buckets to acquire food. Buckets with smaller holes allow access by small primates while ensuring that larger, dominant animals will not take more than their share. In this instance, environmental enhancement is accomplished through the means of providing the standard diet rather than through addition of treats that might be nutritionally incomplete. Novel foods are often presented in the form of treats, although predictable presentations of treats are soon no longer novel. Treat feeding, in which the treat is handed to the primate, can foster trust and bonding with the care-taker and provide short-term sensory stimulation, but it differs greatly from natural foraging in occuping so little time (Fajzi et al., 1989). Furthermore, evidence of nutritional wisdom among nonhuman primates is not convincing. It is obvious that free-living primates have successfully evolved with their wild food supply and have learned which foods to choose and which to avoid. But there is ample evidence that captive primates given a selection of cultivated foods or treats of various nutrient densities do not consistently choose a complete diet (Ullrey, 1989; Oftedal and Allen, 1996). It also should be noted that the botanic classification of wild foods into categories, such as fruit, has commonly led to the misuse of cultivated fruits (for example, bananas, oranges, and apples) as though they were comparable with their wild equivalents in nutrient composition, color, texture, and proportions of inedible husks or shells. In fact, wild plants and their various parts are quite different from the cultivated plants used for human food (Edwards et al., 1990a, 1990b; Oftedal and Allen, 1996). In particular, wild foods tend to be higher in fiber, and that fiber is often of low digestibility. Nutrient bioavailability also varies with source (Ammerman et al., 1995) and can be different between wild foods and cultivated foods. Nearly all captive primate species should be provided a nutritionally balanced dry food as the predominant item in their daily ration. If it is appropriately formulated, it will have a positive effect on oral health, and the addition of particular vegetables or fruits will not seriously distort nutrient balance until their proportion approaches 50% on a wet basis (Edwards, 1997). The main reasons for this are that such items as green beans, celery, carrots, and kale are all good sources of many nutrients and that they are also high in water (88–94%). Thus, even though they might make up a high proportion of dietary wet weight, they have a relatively small influence on the balance of nutrients supplied by pellets or extrusions that are typically 5–13% water. However, if high-moisture vegetables or fruits are fed with a nutritionally balanced food that is high in moisture (canned or gel products) and the primates being fed are as small as marmosets and tamarins, it might be difficult for them to consume sufficient dry matter to meet nutrient and energy needs (Barnard et al., 1988). If dry, very palatable foods that are nutritionally incomplete are offered, as is the case with many seeds and nuts (Ullrey et al., 1991), these preferred items might be con-
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 sumed to the exclusion of nutritionally balanced foods, and nutrient distortion of the diet can be serious. The use of vitamin and mineral supplements is not a dependable way to correct these problems, because supplements might be inappropriately formulated for the purpose (not all supplements are alike), and they are often administered without measuring, so there are risks of overdosing or underdosing. With respect to selecting foods to extend foraging time, novel colors, sizes, shapes, smells, and textures and the presence of shells or husks that require removal can be sensory stimulants (Schapiro et al., 1996; Noonan, 1998). If cognitive tasks are required to acquire food, the associated mental stimulation appears to be rewarding beyond the acquisition of calories (Reinhardt, 1997). Singly housed marmosets foraged for up to 6 h when food was mixed with sawdust (Scott, 1991). Juvenile patas monkeys have been reported to leap several feet in the air to reach fruit stuck on branches in a zoo, even when adequate amounts of fruit were available on the ground (McGovern, 1994). A comparative study found that cynomolgus monkeys preferred foraging activities more than other enrichment methods (Bryant et al., 1988). When various foraging enrichment devices were presented to squirrel monkeys, the devices that increased foraging times and that were manipulated the most were a capped polyvinyl chloride (PVC) pipe with food-dispenser holes and food dispensers made from 2-L plastic beverage containers (Boinski et al., 1994). Provision of a PVC feeding device and more frequent feeding reduced abnormal behaviors in singly housed baboons (Brent and Long, 1995). Puzzle feeders requiring manipulation to acquire treats were more effective than treats alone in reducing locomotor stereotypies in singly housed rhesus macaques. However, the effects lasted only as long as the manipulation time (about 1 h) that was required to acquire the treats. If puzzle difficulty was increased, the monkeys tended to give up (Novak et al., 1998). Thus, it might be important to distinguish between provision of treats with little or no foraging activity and promotion of foraging activity for acquisition of principal food sources. Species Differences Different species use different foraging techniques, and promotion of foraging activity in captivity should consider species differences. Are the primates principally frugivores, folivores, insectivores, gummivores, or omnivores? Are they principally terrestrial or arboreal foragers? Are they manually dextrous? Do they use their hands or tools? What is their relative cognitive ability? Those factors are all relevant in determining which foraging enhancements may be most effective. Specialized foraging adaptations and food preferences of several species have been described. Ring-tailed lemurs have been reported to prefer fresh new leaves in the wild, whereas brown lemurs preferred mature leaves. Lemurs processed fruit very little and licked the open end of bananas rather than peel them (Jolly, 1985). Golden-lion tamarins forage for insects by manipulation; they sift through substrate, search for insect holes, remove bark, and break open wood in their quest for food. But cotton-top tamarins feed opportunistically on insects that they encounter as they move through dense tangles of branches and vines (Steen, 1995). Lorises are able to capture only slow-moving and often relatively unpalatable prey, whereas galagos capture more rapid and more palatable prey (Charles-Dominique, 1977). In captivity, patas monkeys preferred browse from poplar trees (Populus spp.) but used it more for bark-chewing than leaf-eating; for effective use, it was necessary to mount the browse in a metal sleeve to hold it in a natural, upright position (McGovern, 1994). Surfaces of novel devices containing food are inspected by sniffing, touching, and licking by captive squirrel monkeys but are more likely to be persistently manipulated by capuchins (Fragaszy and Adams-Curtis, 1991). Great apes, baboons, macaques, and capuchins explore the properties of objects and appear to have the cognitive ability to relate them to each other. These skills are basic to tool use, something that wild chimpanzees practice regularly in nut-cracking and in foraging for termites and ants. Although other apes and the monkey species mentioned above rarely use tools in the wild, they adapt readily to use of tools when they are provided in captivity (Tomasello and Call, 1997). Manipulation of Foraging Opportunities Food can be used to enrich a captive environment by manipulating foraging opportunities in time and space. If outdoor exhibit or holding areas are available, food can be placed on the ground or in trees, as it might be found in a wild environment. Foraging time also can be extended in inside areas by scattering food in a substrate, such as leaf litter, straw, hay, wood shavings, or shredded paper. Hidden foods can include the primary nutrient source, usually an extrusion, and low-density items, such as popcorn and some dry breakfast cereals. Whole fruits and vegetables that require husking or peeling before eating can also be useful. Time spent in feeding was increased when lion-tailed macaques were presented whole versus chopped foods (Lindburg and Smith, 1988). Stereotypies in singly caged baboons were reduced by offering corn on the cob (Bennett and Spector, 1989). It is particularly important to place food in multiple locations in group enclosures so that aggression and food monopolization are minimized. Studies with Diana monkeys (Cercopithecus diana), Allen’s swamp monkeys (Cercopithecus nigroviridis), lion-tailed macaques (Macaca silenus), and Hamlyn’s monkeys (Cercopithecus hamlyni) in
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 group enclosures found that food acquisition was equitable and foraging time greatest when cut-up apples and oranges were scattered in straw on the wire of enclosure roofs (Buchanan-Smith, 1995). Roof feeding promotes a variety of locomotor postures, muscle use, and physical fitness (Britt, 1993). Environmental enhancement is particularly difficult, but still possible, with individually caged primates (NIH, 1991; Dean, 1999). Replacement of a standard hopper feeder with a foraging device that required manipulative and cognitive skills reduced self-directed behaviors in cynomolgus macaques. Periodic introduction of novel foods maintained interest in the device (Holmes et al., 1995). Moving extrusion feeders out of the cages of individually housed rhesus macaques and reattaching them to the outside of a 22 x 22-mm mesh cage front increased feeding time from 0.2 min to 18.3 min (Reinhardt, 1993). Placing extrusions on top of a chain-link ceiling enclosure also extended foraging time (Reinhardt, 1997). However, total foraging time was a small proportion of the day. Raisins and seeds have been stuck in Astroturf® attached to hanging logs (Bollen, 1995). Acrylic food puzzles and various other devices that require manipulation with tools to acquire food have been attached to the outside of enclosures (Schapiro et al., 1991). Foraging devices hung from the ceiling are unpredictable in movement and stimulating when two primates attempt to use them simultaneously (Buchanan-Smith, 1997), and a free-spinning feeder log hung on a wire out of easy reach was particularly challenging to spot-nosed guenons and white-faced capuchins (Dorian, 1993). Pine cones stuffed with peanut butter and raisins, frozen juice cubes, frozen fruits and vegetables, and fruits and vegetables speared and hung on bamboo canes have been used for environmental enrichment with some success. Foraging devices are not all effective in a given situation (Lutz and Farrow, 1996), and different species, ages, and individuals may prefer different types (Watson, 1997). Live Prey Live prey can promote foraging activity, and some invertebrates can be important sources of nutrients for obligate insectivores. Beetles, caterpillars, moths, grasshoppers, locusts, ants, crickets, mealworms, wax moth larvae, butterflies, centipedes, millipedes, spiders, slugs, snails, lizards, mice, rats, and frogs have been offered. Mealworm feeders have been devised to reduce stereotyped behavior in common marmosets (Vignes et al., 2001). Goldfish in fishing pools have been used to stimulate foraging in squirrel monkeys (King and Norwood, 1989). Because of limited commercial availability of most invertebrates, crickets from commercial suppliers have been used most often. Calcium concentrations in these insects (and many others, including mealworms and wax-moth larvae) are very low and not dependably corrected by dusting with calcium supplements. Variable amounts of the calcium dust are lost as the crickets move about or clean their body surfaces. A special high-calcium insect diet should be fed to crickets, mealworms, or wax-moth larvae for about 1–2 d before they are offered as food. Consumption of this high-calcium diet by these insects leaves a high-calcium gut residue that makes the whole insect a more nutritionally complete meal for the consuming vertebrate (Strzelewicz et al., 1985; Allen and Oftedal, 1989; Roberts and Kohn, 1993). When insects were scattered among wood chips on the floor of their enclosure, cotton-top tamarins that are insectivorous (Rowe, 1996), but mostly arboreal, were enticed to forage on the floor (McKenzie et al., 1986). Passive dispensers hung from enclosure ceilings or walls will also allow slow dispersal of live prey. Active dispensers can be made from PVC or bamboo with holes of a size appropriate to admit a finger, hand, or arm for search and retrieval of prey mixed in a substrate, such as wheat bran. Such active dispensers also have been used with other foods (Banchero, 1995; Demlong, 1993; Glick-Bauer, 1997; Steen, 1995; Wassel and Race, 1994). Consumption of live prey is not without risk. Laboratory mouse pups that have been proposed as food for prey-eating primates have been identified as a reservoir of a lymphocytic choriomeningitis virus that causes hepatitis in callitrichids (Montali and Bush, 1999); free-living cockroaches caught and eaten by callitrichids can be a source of pathogenic nematodes. Exudates and Gums Feeding on tree exudates or gums has been observed in 45 species of animals in the wild, including prosimians, marmosets, tamarins, and Old World monkeys (Kelly, 1993). Although gums do not appear to be obligatory ingredients in diets for these species, their use provides environmental enrichment and enhances the visitor viewing experience. Gum arabic (from Acacia senegal) is used in frozen desserts and in bakery, confectionery, and dairy products. As a consequence, it is commercially available, and gum mixtures can be presented in liquid dispensers or in holes drilled in trees, branches, or dowels (Brennan and Russel, 1986; LeBlanc, 1993). Water Water also can be used in environmental enrichment, particularly if presented in novel ways (Parks and Novak, 1993). Primates drink it directly from a water source, from their cupped hands, or by squeezing it into their mouths from water-soaked leaves, as from a sponge. Japanese
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 macaques submerge potatoes and grains in water to remove dirt (Itani and Nishimura, 1973), and several macaque species dive and swim to retrieve food (Malik and Southwick, 1988; Suzuki, 1965). Higher-Fiber Foods Leafy vegetables, browse, and higher-fiber commercial extrusions have been used to provide environmental enhancement and may be important for physiologic reasons in highly folivorous species, such as howlers and the Colobinae. Lemurs and great apes also can benefit from appropriate sources and amounts of high-fiber foods (Gould and Bres, 1986; Edwards, 1995; Popovich et al., 1997). These foods tend to increase the time spent in feeding, can reduce aberrant behavior, favor the production of formed rather than liquid stools, and are useful in the control of obesity. The National Zoological Park in Washington, DC, has a list of East Coast browse species that were judged to be safe for primate feeding. They include alder, amaranths, arborvitae, aspen, bamboo, beech, birch, blackberry, bush honeysuckle, butterfly bush, cattails, chicory, clover, comfrey, cottoneaster, cottonwood, daylily, dogwood, elaeagnus, elm, fig, forsythia, grasses, greenbriers, hackberry, hawthorn, hazelnut, hibiscus, Japanese silver grass, kerria, kudzu, linden, maple (except red maple), mock orange, mulberry, nasturtium, Oregon grape holly, pear, pickerel-weed, poplar (except tulip poplar), purslane, raspberry, redbud, rose, snowberry, violets, water hyacinth, and willow (Gross, 1990; Shumaker, 1995; McClung, 1999). Browse species that have been listed in peer-reviewed publications may be found in Chapter 10. Studies at the Duke University Primate Center demonstrated that several local plants could be substituted for mango leaves in captive sifaka diets. Plant-species preferences were exhibited by both lemurs and sifakas, and there were seasonal preferences for particular plant parts (Pereira et al., 1989). Because some browses contain toxic chemicals or have a tendency to form indigestible phytobezoars, they must be selected and used with care (Ensley et al., 1982; Fowler, 1986; Knapka et al., 1995). EPILOGUE Nothing is more basic to the health and well-being of captive nonhuman primates than proper nutrition and dietary husbandry. Deficiencies or excesses of specific nutrients have been shown to produce specific signs of illness that reflect their metabolic roles (National Research Council, 1978; Machlin, 1990; Knapka et al., 1995; O’Dell and Sunde, 1997). Furthermore, there is a well-established relationship between nutritional status and susceptibility to infectious disease (Ullrey, 1993). Thus, the provision of a nutritionally balanced diet in amounts sufficient to meet daily energy and nutrient needs must not be subverted by well-intentioned but ill-advised uses of food in systems of environmental enhancement. 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