10
Diet Formulation, Effects of Processing, Factors Affecting Intake, and Dietary Husbandry

DIET FORMULATION

The goals of diet formulation are to integrate natural dietary habits, digestive morphology and physiology, nutrient requirements, and the physical characteristics and nutrient composition of potential feedstuffs to make diets that will be eaten in amounts sufficient to meet nutrient needs.

Natural Dietary Habits

Information on natural dietary habits is derived from field studies of free-ranging primates in their natural habitat (see Chapter 1). Such studies have been conducted with a number of species, and the results are published in varied detail in research journals, books, and theses (Clutton-Brock, 1977; Milton, 1980; Newton, 1992; Edwards, 1995; Nijboer and Dierenfeld, 1996; Mowry et al., 1997; Dierenfeld and McCann, 1999; Silver et al., 2000).

Digestive System Morphology and Physiology

Descriptions of primate digestive systems (Langer, 1988; Stevens and Hume, 1995) have been derived opportunistically from necropsies performed for other purposes or from necropsies conducted specifically to gather this information. Data on digestive physiology are usually obtained from studies of living primates in captivity (Bauchop, 1978; Edwards, 1995).

Nutrient Requirements

Estimated nutrient requirements derived from a review of published research are presented in Chapter 11, Table 11-1. However, the values listed there represent minimal needs in that they were derived largely from studies with purified diets in which biologic availability was assumed to be 100%. In general, the bioavailabilities of nutrients in natural-ingredient diets are lower (Ammerman et al., 1995), and it might be necessary to compensate for their lower availability by increasing nutrient concentrations above minimal requirements, as recommended in Table 11-2. Factors influencing nutrient requirements are described in relevant chapters of this report dealing with specific nutrients and general considerations regarding adequate dietary nutrient concentrations are described in Chapter 11.

Feedstuffs

Feedstuffs with potential for use in primate diets are shown in Chapter 12, Tables 12-1 through 12-6. Ultimately, it is necessary to match the nutrient composition and physical characteristics of feedstuffs with the nutrient requirements and the structural and physiologic characteristics of the gastrointestinal tract of the primate in question.

Diet Formulation

Although the calculations required in formulating diets can be made with a calculator, diet formulation is easier and faster with a computer that uses software designed specifically for the purpose. Diet-formulation software is available (Anonymous, 1999), and commercial programs are commonly designed to select and incorporate feedstuffs on a least-cost basis. If a consistent, unvarying formula is desired, that option is also available.



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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 10 Diet Formulation, Effects of Processing, Factors Affecting Intake, and Dietary Husbandry DIET FORMULATION The goals of diet formulation are to integrate natural dietary habits, digestive morphology and physiology, nutrient requirements, and the physical characteristics and nutrient composition of potential feedstuffs to make diets that will be eaten in amounts sufficient to meet nutrient needs. Natural Dietary Habits Information on natural dietary habits is derived from field studies of free-ranging primates in their natural habitat (see Chapter 1). Such studies have been conducted with a number of species, and the results are published in varied detail in research journals, books, and theses (Clutton-Brock, 1977; Milton, 1980; Newton, 1992; Edwards, 1995; Nijboer and Dierenfeld, 1996; Mowry et al., 1997; Dierenfeld and McCann, 1999; Silver et al., 2000). Digestive System Morphology and Physiology Descriptions of primate digestive systems (Langer, 1988; Stevens and Hume, 1995) have been derived opportunistically from necropsies performed for other purposes or from necropsies conducted specifically to gather this information. Data on digestive physiology are usually obtained from studies of living primates in captivity (Bauchop, 1978; Edwards, 1995). Nutrient Requirements Estimated nutrient requirements derived from a review of published research are presented in Chapter 11, Table 11-1. However, the values listed there represent minimal needs in that they were derived largely from studies with purified diets in which biologic availability was assumed to be 100%. In general, the bioavailabilities of nutrients in natural-ingredient diets are lower (Ammerman et al., 1995), and it might be necessary to compensate for their lower availability by increasing nutrient concentrations above minimal requirements, as recommended in Table 11-2. Factors influencing nutrient requirements are described in relevant chapters of this report dealing with specific nutrients and general considerations regarding adequate dietary nutrient concentrations are described in Chapter 11. Feedstuffs Feedstuffs with potential for use in primate diets are shown in Chapter 12, Tables 12-1 through 12-6. Ultimately, it is necessary to match the nutrient composition and physical characteristics of feedstuffs with the nutrient requirements and the structural and physiologic characteristics of the gastrointestinal tract of the primate in question. Diet Formulation Although the calculations required in formulating diets can be made with a calculator, diet formulation is easier and faster with a computer that uses software designed specifically for the purpose. Diet-formulation software is available (Anonymous, 1999), and commercial programs are commonly designed to select and incorporate feedstuffs on a least-cost basis. If a consistent, unvarying formula is desired, that option is also available.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Commercial feed manufacturers offer a variety of closed-formula diets for nonhuman primates. Although the specific amounts of each ingredient in the formula are not usually revealed, most manufacturers will furnish estimates of typical nutrient content in printed form or on a Web site. The information from the manufacturer can then be compared with the estimated nutrient requirements listed in Table 11-1. However, commercial feed manufacturers routinely alter feed formulations based on the quality and availability of feed ingredients, and customers are typically not notified when these formulation changes occur (Knapka, 1997). Although changes might only involve alterations in the ratios of the ingredients listed, in order to control the variation in the dietary nutrients of interest and perhaps permit use of low cost ingredients, changes might also occur in dietary constituents that are not being measured. For example, dietary ingredient changes can result in alterations of phytoestrogen concentrations, which are not typically reported, but can have a significant effect on reproductive efficiency and tumor rates in laboratory animals. These changes in feed composition can have potential impacts on the health of the animals being fed and the quality of research conducted with experimental animal colonies. Because of the potential variation in nutrient composition and other nonnutrient factors that may have physiologic effects, closed formula diets are not recommended for many research situations. If closed formula diets are used in research, they should be used with extreme caution and the researcher should conduct independent analyses of the diets throughout the experimental period. Researchers and caretakers should maintain detailed knowledge of the composition of diets, and those dietary constituents—nutrients and nonnutritive components—that may be of special interest. Persons conducting research with primates often use an open-formula diet, publishing the amount and identity of each ingredient. Information on diet composition has utility in the interpretation of research findings, but one should be wary of uncritically adopting diets based on formulas published in the past. The definitions of feed ingredients (and their nutrient compositions) tend to change, and it might be difficult or even impossible to formulate diets as originally specified. For example, an open formula might specify the use of a fishmeal containing 70% protein. Fish-meal containing 70% protein has traditionally been derived from processing of sardines and is no longer widely available. The fishmeal used in most feed mills today is derived either from menhaden (60% protein) or from anchovies (65% protein), and few commercial feed mills have more than one type of fishmeal on hand. Another example is related to the use of wheat in an open-formula diet. The many types of wheat (such as soft white winter, hard red winter, and durum) vary in protein concentration from 10% to 15%. Most feed manufacturing plants will have only one type of wheat, and that makes it difficult to meet specifications that require a particular type of wheat or wheat with a particular protein level. An example of an ingredient specification that is not consistent with current technology is related to the form of vitamin C. Most older published diet formulations specify ascorbic acid, whereas modern formulas use L-ascorbyl-2-polyphosphate, a biologically active vitamin C form that is much more stable. Because of concern that natural-ingredient diet formulas published in this document would be used without critical consideration of the issues raised above, we have chosen instead to refer the reader to relevant literature. A National Institutes of Health open-formula high-fiber diet that was developed to study the effect of fiber on rhesus monkeys during quarantine has been used as a maintenance ration in a number of colonies (Morin et al., 1978; Knapka et al., 1995). Diets used for longevity studies with rhesus and squirrel monkeys, in which food was restricted, have been published by Ingram et al. (1990). Diets for marmosets (Flurer et al., 1983; Barnard et al., 1988) and diets for lemurs, howlers, colobus, langurs, mangabeys, and drills (Edwards, 1995) also have been described. A number of investigators have used purified diets in their research, and these diets are referred to in many of the studies cited in this report. Purified-diet formulas for macaques (Macaca spp.) (Kark et al., 1974; Kemnitz et al., 1993; Thornberg et al., 1995), African green monkeys (Cercopithecus aethiops) (Scobey et al., 1992), and squirrel monkeys (Saimiri sciureus) (Rasmussen et al., 1979; Martin et al., 1972) and a liquid diet used for alcohol investigations with baboons (Papio spp.) (Leiber and DeCarli, 1974) have been published. They can be used as a starting point by those wishing to formulate a diet for a specific purpose. The original publications should be studied carefully and formulas modified as appropriate. Adjustment of nutrient levels is particularly important for diets that were used to produce nutrient deficiencies. EFFECTS OF PROCESSING Feed processing typically includes grinding of dietary ingredients to produce particles of approximately equal size suitable for mixing and then pelleting or extrusion. Such processing promotes diet homogeneity and reduces the likelihood that primates will select and consume only the ingredients that appeal to them, regardless of their relative nutritional importance. Many primates manipulate their food and generally prefer the physical characteristics of extrusions or pellets to ground meals. Manufactured diets for nonhuman primates usually are prepared by extrusion. This process involves passing steam-moistened feed through a high-pressure, high-temperature chamber and forcing it through a small opening. The pres-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 sure is sufficiently high that steam is formed and the starches are gelatinized and made more digestible (Camire et al., 1990; Knapka et al., 1995). Thus, difficult-to-digest starches are less likely to escape endogenous digestion in the upper gastrointestinal tract of simple-stomached primates and are less likely to produce digestive disturbances as a consequence of excessively rapid microbial fermentation in the lower gut. Variable effects on lipids, proteins, and minerals have been noted (Camire et al., 1990); much of this variability is associated with the sources and chemical nature of these nutrients and variations in the conditions of extrusion. The temperatures and pressures of extrusion are high enough to greatly reduce dietary microbial concentrations, although in most commercial operations recontamination occurs to some degree during cooling and bagging. If the conditions are proper, the final product will expand or “puff” so that a low-density biscuit is formed; this low-density extrusion tends to be more palatable than pellets. If diets are prepared by pelleting, sources of carbohydrate that provide sugars or gelatinized starch should be used to ensure adequate carbohydrate digestibility. Such a pelleted diet was formulated by Barnard et al. (1988). If extruding or pelleting equipment is not available, baked diets can be prepared (Knapka et al., 1995). Some primate diets are canned. The general procedure includes grinding of the major ingredients, precooking in a continuous cooker with live steam, addition of mineral and/or vitamin mixes, blending of all ingredients, and filling of cans while hot. The cans are vacuum sealed and transferred to a retort for sterilization. Temperature and time of cooking depend upon steam pressure, size of can, can contents, and rate of can movement. After retorting, the cans are rapidly cooled to about 38° C, dried, labeled, and placed in cases (Ockerman and Hansen, 2000). The canning process significantly reduces potential for microbial contamination. Extruding, pelleting or baking can have destructive effects on the vitamins in feed. Some nutrients—for example, vitamin A, vitamin D, vitamin E, vitamin C, thiamin, and folacin—are particularly susceptible to destruction during feed manufacture and storage unless included in the proper form. Vitamin A is quite unstable in its free form, retinol, and is commonly stabilized by creating an ester, retinyl palmitate, and by microencapsulation within a coating that contains antioxidants. Vitamin D also is stabilized by microencapsulation. The ester form of vitamin E, a-tocopheryl acetate, that is commonly added to manufactured feeds is much more stable tha a-tocopherol. Protective coatings also have been used to stabilize vitamin C, but creation of the ester L-ascorbyl-2-polyphosphate has been even more successful. Thiamin and folacin each have a free amino group that makes them susceptible to losses in activity during heat treatment in the presence of reducing sugars, such as glucose and lactose; these losses can be exaggerated by close association with some mineral mixes and must be compensated for by supplementation. Thiamin mononitrate appears to be more stable than thiamin hydrochloride (Gubler, 1991). The most labile vitamin is ascorbic acid; 40-70% of ascorbic acid can be destroyed during extrusion (Lovell and Lim, 1978; Grant et al., 1989). Ascorbic acid in a manufactured diet continues to be lost during storage. The rate of loss depends on feed composition and on the temperature and humidity at which the feed is stored. The traditional recommendation is that primate feeds be used within 90 days of the date of manufacture unless a stable form of vitamin C is used or a supplementary form of ascorbic acid is provided. Vitamin pills, fresh fruit, or orange-flavored drinks containing additional ascorbic acid have been used as supplements. L-Ascorbyl-2-polyphosphate, a form of vitamin C that is stable to oxidation, is now available. It is a phosphate ester of ascorbic acid, and has full biologic activity in primates (Machlin et al., 1979). The phosphate stabilizes the ascorbate molecule in feed, but the ester is cleaved by intestinal phosphatases when consumed and releases ascorbic acid for absorption. Although there can be some loss of ascorbyl polyphosphate during extrusion, that present in the final manufactured feed is quite stable (Grant et al., 1989); manufactured feeds containing the polyphosphate form of vitamin C may be stored for 180 days or longer before feeding. If high-quality, stable forms of vitamins are added at concentrations sufficient to compensate for manufacturing and storage losses and the feed is stored under cool, dry conditions, manufactured diets can be held for several months (Coehlo, 1996). FACTORS AFFECTING INTAKE The feeding ecology of several wild primate species has been studied, but the methods of study generally provide an idea of what rather than how much is eaten. For primates living in the wild, the adequacy of the food supply varies with the health of the ecosystem and with the season. Wild primates must identify what is food, avoid toxicants, and distinguish between edible and inedible items. Experience and the organoleptic senses are both important (Lang, 1970). Visual, olfactory, taste, and tactile clues are used, and young primates commonly mimic the foraging behavior of adults, such as the mother and older family members. In captivity, the supply and quality of food are under the control of humans, but unless it is eaten, its nutrient composition is of limited significance. Observations of other primates consuming a food, including trusted

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 humans, can encourage tasting by a primate for which consumption of the food is a novel experience. Influence of Visual, Olfactory, Taste, and Tactile Clues on Food Acceptance Color vision in nonhuman primates has been little explored, but some colors or shadings of food can influence acceptance. Color preferences probably have a role in selection of foods in the wild; in captivity, juvenile orangutans consumed more of colored extruded diets, and adults took less time to consume the colored food (Barbiers, 1985). Olfactory and taste characteristics also seem important, and it is common to see some primates responding to tastes and odors, particularly citrus and other fruity flavors and odors (Wene al., 1982). There is evidence that nonhuman primates have taste responses to sweet substances, as do humans. Most, but not all, primate species like the sweetness associated with sucrose, fructose, and glucose (Glaser, 1979; Kemnitz et al., 1986; Simmen, 1992a; Laska, 1996), and it is common to add sugar to commercial primate diets composed of natural ingredients. Sweet and fruity tastes generally enhanced dietary palatability for Callitrichidae (Callithrix jaccus, Saguinus fuscicollis, S. labiatus, S. mystax, and S. oedipus) but not when the fruity flavors were artificial (Flurer et al., 1983). Banded leaf monkeys (Presbytis melalophos) and red (P. rubicunda) leaf monkeys were found to favor seeds and fruits that had high concentrations of storage carbohydrates or fats but not those rich in simple sugars (Davies and Bennett, 1988). Taste-preference studies with spider monkeys (Ateles geoffroyi) and squirrel monkeys (Saimiri sciureus) showed a preferential response to sugar concentrations that were lower than those detected by other nonhuman primates and suggest that these species use sweetness as a criterion for food selection that is correlated with their dietary specialization (Laska et al., 1996; Laska, 1996). Squirrel monkeys preferred sucrose over starch-derived polysaccharides when taste preferences were compared with those of bonnet macaques (Macaca radiata). The latter preferred the starch-derived sugars maltose and polycose (Sunderland and Sclafani, 1988). Taste-preference profiles were consistent with the natural food preferences of those two species. When near-threshold concentrations of fructose solutions (30-60 mM) were provided, they were strongly preferred by Goeldi’s monkeys (Callimico goeldii) and tamarins, whereas most marmosets, especially Cebuella pygmaea, were least attracted (Simmen, 1992b). Those findings are consistent with the dietary strategies exhibited by tamarins (Saguinus and Leontopithecus) and Goeldi’s monkeys, which are predominantly frugivores and nectarivores that feed mainly on foods rich in soluble sugars, and the marmosets (Cebuella pygmaea and Callithrix jaccus), which meet much of their energy requirement from plant exudates. Captive and free-living gentle lemurs (Hapalemur griseus alaotrensis) exhibited a hierarchy of food preference based on the age of plant parts. New growth, containing greater crude-protein and lower indigestible-fiber concentrations, was preferred to mature growth (Fidgett et al., 1966). When damaged plant parts were encountered, they remained untouched. Quinine hydrochloride added to the drinking water of Macaca fascicularis was rejected. However, these monkeys did not find moderate concentrations of hydrochloric acid aversive (Pritchard et al., 1994). Mouth “feel” and tactile responses during food manipulation appear to influence food acceptability. Special attention should be paid to the final form of extruded and pelleted diets. If a pellet or extruded biscuit is too hard or too dense, an animal might not be able to bite it comfortably. The final hardness or density can be controlled through manipulation of manufacturing procedures. The size of the extruded biscuit or pellet is also important, particularly for the smaller species of primates. A feed morsel should be small enough to be readily held and taken into the mouth. To promote intake, some animal caretakers soak extruded biscuits in water or juice to make them softer. That practice is not recommended: soaking the biscuits can result in loss or destruction of some vitamins (particularly ascorbic acid), facilitate spoilage by molds and bacteria, and increase the incidence of oral health problems. Regulation of Food Intake Normal feeding behavior appears to involve adjustment of oral intakes to balance the energy acquired with the energy needed. When rhesus macaques (M. mulatta) received an intragastric infusion of food energy during a meal, oral energy intakes were reduced by an amount equivalent to the energy provided by the infusate (Hansen et al., 1977). After being rendered obese by intragastric hypercaloric feeding, male rhesus macaques orally consumed fewer kilocalories of metabolizable energy (ME) per kilogram of body weight (BW) during restabilization to pre-overfeeding weights than they had consumed before induction of obesity (Jen and Hansen, 1984). When a liquid diet providing ME at 1.35 kcal·ml-1 was diluted with water to create four diets with ME densities of 1.35-0.5 kcal·ml-1, rhesus macaques were able to maintain a constant average ME intake of 84±0.7 kcal·kg-1 of BW for a period of 15 d (Hansen et al., 1981a). However, if the liquid diets were very dilute or were offered for only a limited time, the animals were unable to ingest enough food to meet the day’s needs (Hansen et al., 1981b).

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Although, in general, primates eat to meet their energy requirements, some captive primates seem to consistently eat in excess of immediate energy needs and become obese. Thus, it might be necessary to limit intake of diets that are energy-dense and very palatable. Long-term studies (Ingram et al., 1990) exploring the effects of restricted energy intake on life span have demonstrated that primates can adjust to moderate energy restriction as long as nutrient intakes are sufficient to maintain basic body functions. They do it either by decreasing accretion of body tissue, particularly fat, or by decreasing physical activity to match energy consumption. High protein intakes can have satiating effects beyond the calories provided. When Jen et al. (1985) administered a liquid intragastric infusate containing casein as 36% of ME calories, satiation of rhesus macaques receiving the infusate and consuming a nutritionally adequate solid diet occurred more quickly than when the same percentage of ME in the infusate was provided by either carbohydrate or fat. The putative effects of high-protein diets in suppressing appetite were concluded to have potential for weight control. When adult male rhesus macaques received 50% of their ME intake as protein (oral plus intragastric infusion) compared with 14%, a doubling in plasma branched-chain amino acid (valine, isoleucine, and leucine) concentration and a consistently reduced caloric intake (by 24.7%) were noted (Hannah et al., 1990). Gibbs and Smith (1977) found that gastric preloads of L-phenylalanine, but not of D-phenylalanine, produced large reductions in meal size among rhesus monkeys, as did intravenous infusions of cholecystokinin, a gut hormone released in response to L-phenylalanine and regarded as an endogenous “satiety signal.” Young adult male baboons (Papio cynocephalus) responded with a 44% decrease in meal size when cholecystokinin octapeptide at 25 ng·kg-1 of BW was given intravenously before a 30-min meal (Figlewicz et al., 1995). Plasma concentrations of glucose and insulin modulate feeding behavior, and blood concentrations of these compounds can be influenced by diet composition. When solutions of maltose, sucrose, or glucose (molar concentrations not specified) were provided to rhesus macaques at the beginning of a 24-h feeding period, the intake of a commercially prepared complete diet was significantly reduced, and total energy intake matched need. However, when fructose solutions were offered, reduction in food intake was only 37% of that induced by the other sugars. The difference in food intake was evident 3 h after presentation of the sugar solutions; this suggested an association with absorptive or immediate postabsorptive events and was presumably due to the failure of fructose to increase plasma glucose concentrations, as do the other sugars, or to elicit an insulin response (Kemnitz and Neu, 1986). Variations in the concentrations of essential vitamins and minerals and the presence of aversive compounds, can also influence food intake and animal performance substantially (Newberne, 1975). DIETARY HUSBANDRY Primary Food Source Most feeding programs for nonhuman primates in captivity use dry extrusions as the chief source of nutrients. In some management systems, food is offered ad libitum; in others, a fixed amount of food is presented one or more times per day. Some animal caretakers feed the same number or volume of extrusions. However, the densities and sizes of extrusions vary, not only between products made by different manufacturers but between batches of the same product. Thus, feeding by number or volume can lead to unintended changes in energy and nutrient intake. Weight is the recommended measure upon which the amount of food offered should be based. The nutritional implications of feeding pellets ad libitum or in amounts limited to what can be consumed in 1 h, twice a day, to baboons (Papio cynocephalus) have been explored by Phillips and Clemens (1981). Food consumption and digestibility were not significantly different, nor were there differences in total transit times of fluid and particulate digesta markers. However, ad libitum-fed baboons passed 2-mm and 10-mm particulate markers more quickly and had a shorter 85% marker-recovery interval than did limit-fed baboons. Supplements Extrusions can make the entire diet or be supplemented with other foods, such as nutritionally complete treats, vegetables, fruits, and insects. Such supplements often are more palatable than the extrusions, and supplement intake must be controlled lest overall intake become nutritionally unbalanced (Shimwell et al., 1979). With the exception of browse for such primates as colobus monkeys (Colobus spp.), langurs (Presbytis spp.), and howlers (Alouatta spp.), which have a well-developed digestive capacity for fermenting fiber, supplemental foods are commonly fed for environmental enrichment rather than for nutritional reasons. When used, such foods should be nutritionally complete or result in minimal nutritional distortion of the diet. In some cases, nutritionally complete “treats” are available from commercial manufacturers, but care should be taken to assure that the supplement is nutritionally complete before incorporating it into a feeding program. Aside from nutritionally complete supplements or treats, appropriate environmental enrichment food choices would be those high in moisture and low in calories, such as vegetables and some fruits, rather than

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 10-1 Plant Species Used in Feeding Captive Primates Plant Species Reference Alder (Alnus spp.) Dierenfeld et al., 1992; Kirschner et al., 1999 Alfalfa (Medicago sativa) Bauchop and Martucci, 1968 American holly (Ilex opaca) Dierenfeld and McCann, 1999 Bamboo (Pseudosasa spp., Phyllostachys spp.) Gould and Bres, 1986 Beech (Fagus spp.) Gould and Bres, 1986 Blackberry (Rubus betuifolius) Dierenfeld and McCann, 1999 Brush cherry (Syzgium paniculatum) Griner, 1977; Ullrey et al., 1982; Janeke, 1995 Buckthorn (Bumelia tena) Dierenfeld and McCann, 1999 Cabbage palm (Sabelpalmetto) Dierenfeld and McCann, 1999 Carolina cherry laurel (Prunus caroliniana) Dierenfeld and McCann, 1999 Chinaberry (Melia azedarach) Dierenfeld and McCann, 1999 Common nightshade (Solanum nigrum) Dierenfeld and McCann, 1999 Cup-of-gold (Solandra guttata) Griner, 1977 Fig (Ficus carica) Janeke, 1995 Fig (Ficus glomerata) Janeke, 1995 Fig (Ficus macrophylla) Janeke, 1995 Fig (Ficus nittida) Janeke, 1995 Fig (Ficus retusa) Janeke, 1995 Fig (Ficus rubiginosa) Janeke, 1995 Fig (Ficus rumphii) Janeke, 1995 Fig (Ficus thonningii) Janeke, 1995 Flowering dogwood (Cornus florida) Dierenfeld and McCann, 1999 Grape (Vitis spp.) Hill, 1964; Dierenfeld et al., 1992 Giant cane (Arundinaria gigantean Dierenfeld and McCann, 1999 Hackberry (Celtis occidentalis georgiana) Dierenfeld and McCann, 1999 Hercules’ club (Zanthoxylum clava-herculis) Dierenfeld and McCann, 1999 Hibiscus (Hibiscus rosa-sinensis) Hill, 1964; Griner, 1977; Ullrey et al., 1982; Janeke, 1995 Kudzu (Pueraria hirsuta) Gould and Bres, 1986 Live oak (Quercus virginiana) Dierenfeld and McCann, 1999 Loblolly pine (Pinus taeda) Dierenfeld and McCann, 1999 Mangrove (Rhizophora spp.) Dierenfeld et al., 1992 Maple (Acer spp.) Gould and Bres, 1986 Mexican tea (Chenopodium ambrosiodes) Dierenfeld and McCann, 1999 Mistletoe (Phoradendron flavescens) Dierenfeld and McCann, 1999 Mulberry (Morus spp.) Hill, 1964; Gould and Bres, 1986; Dierenfeld et al., 1992; Janeke, 1995 Muscadine grape (Vitis rotundifolia) Dierenfeld and McCann, 1999 Mushrooms (unkown spp.) Dierenfeld and McCann, 1999 Nut muscadine (Vitis cinerea) Dierenfeld and McCann, 1999 Persimmon (Diospyros virginiana) Dierenfeld and McCann, 1999 Red bay (Persea borbonia) Dierenfeld and McCann, 1999 Red cedar (Juniperus silicicild) Dierenfeld and McCann, 1999 Resurrection fern (Polypodium polyploides) Dierenfeld and McCann, 1999 Small pignut (Carya ovalis) Dierenfeld and McCann, 1999 Southern bayberry/wax myrtle (Myrica cerifera) Dierenfeld and McCann, 1999 Southern magnolia (Magnolia grandiflora) Dierenfeld and McCann, 1999 Spanish moss (Tillandsia usneoides) Dierenfeld and McCann, 1999 Sparkleberry (Vaccinium arboreum) Dierenfeld and McCann, 1999 Sugarberry (Celtis laevigata) Dierenfeld and McCann, 1999 Virginia creeper (Parthenocissus quinquefolia) Dierenfeld and McCann, 1999 Weeping Chinese banyan (Ficus benjamina) Janeke, 1995 Willow (Salix spp.) Höllihn, 1973; Gould and Bres, 1986; Dierenfeld et al., 1992; Kirschner et al., 1999 Yaupon (Ilex vomitoria) Dierenfeld and McCann, 1999 energy-dense and nutritionally incomplete foods, such as raisins and nuts. Cultivated fresh fruits and vegetables typically contain about 80-93% moisture. If the contribution of produce is restricted to 40% of dietary wet weight, it will furnish less than 10% of total dietary dry matter (DM) and will distort nutrient balance minimally. However, if that restriction is exceeded, it might be necessary to take special steps to ensure that nutritional needs are met. Browse The diets of some captive primates may include plant materials propagated or harvested as a source of nutritional

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 and behavioral stimulation (Gould and Bres, 1986; Woods, 1992). Plant materials may include leaves, twigs, shoots, flowers, and fruits (Oftedal et al., 1996). These materials are collectively referred to as browse. In most situations, browse includes plant species indigenous to the geographic location where the primates are housed. Some institutions have made efforts to propagate plant species that are consumed in natural ecosystems by the free-ranging counterparts of the primates under their care. Regardless of the source, prospective users of browse must recognize two key points: nutrient composition varies greatly among plant species and among plant parts within a species (one plant species or part is not necessarily analogous to another) and plants have various protective mechanisms (some toxic) that have evolved as feeding deterrents to limit or prevent ‘‘predation’’ by herbivores (Kingsbury, 1964; Harris, 1970; Rosenthal and Janzen, 1979; Cheeke, 1985). Free-ranging primates are highly selective in their feeding. Captive-born primates do not have the same experience as wild primates in food selection and avoidance of potentially hazardous material. The presumption that naive animals are innately capable of recognizing nutrient concentrations or toxicants within a food source (nutritional wisdom) is not supported by evidence (Ullrey, 1989). Even if nutrition is not the primary reason for providing browse, the plant species offered should be evaluated as though they will be consumed. The morbidity and mortality related to primate-browse interactions have increased proportionately with the inclusion of browse in diets of captive primates (Ensley et al., 1982; Robinson et al., 1982; Janssen, 1994). The relatively high concentration of indigestible lignin (23.6% acid-detergent lignin, DMbasis) in Acacia longifolia and A. saligna leaves contributed to the formation of gastrointestinal obstructions (phytobezoars) and death when these browse species were offered to leaf-eating primates (Presbytis entellus and Pygathrix nemaeus). Similar problems might be expected when browse species with lower leaf lignin concentrations are fed in restricted amounts, thus encouraging leaf-eating primates to eat not only leaves but also high-lignin plant parts, such as bark. Ingestion of indigenous plants containing toxic secondary plant compounds has resulted in poisoning of nonhuman primates. Some secondary plant compounds may be bitter or cause mild digestive disorders, whereas others may be acutely toxic and lead rapidly to death (Oftedal et al., 1996). Three ruffed lemurs (Varecia variegata variegata) exhibited signs of alkaloidal glycoside exposure— including depression, lethargy, ataxia, diarrhea, and death—after consuming hairy night shade (Solanum sarrachoides) (Drew and Fowler, 1991). A capuchin monkey (Cebus apella) consumed fruits of English ivy (Hedra helix) and died 3 days later with severe gastroenteritis (Fowler, 1980). The lethal dose of dried oleander leaf for capuchin monkeys (Cebus apella) was found to be 30-60 mg·kg-1 of BW (Swartz et al., 1974). The alkaloid senecionine in Senecio spp. produced toxicity in nonhuman primates (Wakim et al., 1946), and rhesus macaques (Macaca mulatta) were found to be susceptible to pyrrolizidine alkaloids in Crotalaria spectabalis (Allen et al., 1965). With those warnings, appropriately selected browse can be an important dietary supplement for captive primates, especially highly folivorous species. Griner (1977) suggested that fresh vegetation should make up a major portion of the daily diet of captive proboscis monkeys (Nasalis larvatus), especially during high-stress periods, such as quarantine and acclimation to captivity. Table 10-1 lists some plant species that have been offered to captive primates or that were consumed by provisioned, semi-free ranging primates (with published documentation). 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