3
Carbohydrates and Fiber

Carbohydrates are the most abundant of the compounds in living plants, other than water, and serve as a principal repository of photosynthetic energy. They are in above-ground parts (stem, leaves, flowers, fruits, and seeds) and belowground parts (roots and tubers); constitute about 50-80% of the dry matter in leaves, fruits, and seeds; and generally furnish 40% or more of the metabolizable energy in the diets of most primate species, including humans (Asp, 1994). Although their chemical structure and distribution in foods can be described, independently of the animals that eat them, information on the digestion and metabolism of carbohydrates is derived largely from studies of laboratory animals, domestic animals, and humans (Van Soest, 1994; Szepesi, 1996; Levin, 1999). The relevance of the information to nonhuman primates is uncertain, and it is reasonable to expect both similarities and differences among species.

CARBOHYDRATE CLASSIFICATION, CHARACTERISTICS, DIGESTION, AND METABOLISM

Carbohydrates are classified according to size as monosaccharides, disaccharides, oligosaccharides, or polysaccharides.

Monosaccharides

Monosaccharides, often called simple sugars, are single carbohydrate units that contain three to seven carbon atoms. The six-carbon monosaccharides (hexoses) that are particularly important in animal nutrition are glucose, fructose, and galactose.

Glucose is a moderately sweet simple sugar present in honey, ripe fruits, and some vegetables in free form and combined with fructose, forms the disaccharide sucrose (Matthews et al., 1987). It is the chief end-product of starch digestion in rats, pigs, and humans. It is absorbed through the intestinal wall, is transported via the portal vein to the liver, circulates in the blood, and is the primary carbohydrate used by the body’s cells for energy. Amounts in excess of immediate need can be stored as glycogen or fat. Although glucose can be used for energy by all cells, it is essential for erythrocytes and brain cells. If unavailable in the diet or glycogen stores, glucose can be produced in small amounts from non-carbohydrate sources (gluconeogenesis). Thus, glucose—and carbohydrates in general— in the short term is not considered a dietary essential, but there are energetic costs associated with gluconeogenesis, and it is likely that minimum dietary concentrations of carbohydrates probably must be present for optimal health and metabolic efficiency. Acquisition of minimal amounts of carbohydrate does not pose a practical problem, because diet formulations designed to meet essential protein (amino acid), fatty acid, mineral, and vitamin requirements have adequate space for any conceivable carbohydrate need.

Fructose is a very sweet simple sugar present in honey, ripe fruits, and some vegetables in free form and combined with glucose in sucrose (Matthews et al., 1987). The enzymes in the mucosal cell brush border appear to adapt to increased intakes of sucrose or fructose, and fructose transport into plasma is accelerated by high intakes of fructose or sucrose in the rat (Mavrias and Mayer, 1973; Reiser et al., 1975) and baboon (Crossley and MacDonald, 1970). Limited amounts of fructose may be used directly for energy or converted into glucose by intestinal mucosal cells. Most of the fructose that reaches the liver via the portal vein is converted to glucose, lipid, or lactate.

Galactose is a simple sugar that is not very sweet and is seldom present free in foods (Matthews et al., 1987). It is usually bound with glucose in the disaccharide lactose, which is found in mammalian milks. Digestion of lactose releases glucose and galactose; after absorption, galactose is converted to glucose in the liver, although the kidney and erythrocyte may be involved in galactose metabolism to a minor extent.



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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 3 Carbohydrates and Fiber Carbohydrates are the most abundant of the compounds in living plants, other than water, and serve as a principal repository of photosynthetic energy. They are in above-ground parts (stem, leaves, flowers, fruits, and seeds) and belowground parts (roots and tubers); constitute about 50-80% of the dry matter in leaves, fruits, and seeds; and generally furnish 40% or more of the metabolizable energy in the diets of most primate species, including humans (Asp, 1994). Although their chemical structure and distribution in foods can be described, independently of the animals that eat them, information on the digestion and metabolism of carbohydrates is derived largely from studies of laboratory animals, domestic animals, and humans (Van Soest, 1994; Szepesi, 1996; Levin, 1999). The relevance of the information to nonhuman primates is uncertain, and it is reasonable to expect both similarities and differences among species. CARBOHYDRATE CLASSIFICATION, CHARACTERISTICS, DIGESTION, AND METABOLISM Carbohydrates are classified according to size as monosaccharides, disaccharides, oligosaccharides, or polysaccharides. Monosaccharides Monosaccharides, often called simple sugars, are single carbohydrate units that contain three to seven carbon atoms. The six-carbon monosaccharides (hexoses) that are particularly important in animal nutrition are glucose, fructose, and galactose. Glucose is a moderately sweet simple sugar present in honey, ripe fruits, and some vegetables in free form and combined with fructose, forms the disaccharide sucrose (Matthews et al., 1987). It is the chief end-product of starch digestion in rats, pigs, and humans. It is absorbed through the intestinal wall, is transported via the portal vein to the liver, circulates in the blood, and is the primary carbohydrate used by the body’s cells for energy. Amounts in excess of immediate need can be stored as glycogen or fat. Although glucose can be used for energy by all cells, it is essential for erythrocytes and brain cells. If unavailable in the diet or glycogen stores, glucose can be produced in small amounts from non-carbohydrate sources (gluconeogenesis). Thus, glucose—and carbohydrates in general— in the short term is not considered a dietary essential, but there are energetic costs associated with gluconeogenesis, and it is likely that minimum dietary concentrations of carbohydrates probably must be present for optimal health and metabolic efficiency. Acquisition of minimal amounts of carbohydrate does not pose a practical problem, because diet formulations designed to meet essential protein (amino acid), fatty acid, mineral, and vitamin requirements have adequate space for any conceivable carbohydrate need. Fructose is a very sweet simple sugar present in honey, ripe fruits, and some vegetables in free form and combined with glucose in sucrose (Matthews et al., 1987). The enzymes in the mucosal cell brush border appear to adapt to increased intakes of sucrose or fructose, and fructose transport into plasma is accelerated by high intakes of fructose or sucrose in the rat (Mavrias and Mayer, 1973; Reiser et al., 1975) and baboon (Crossley and MacDonald, 1970). Limited amounts of fructose may be used directly for energy or converted into glucose by intestinal mucosal cells. Most of the fructose that reaches the liver via the portal vein is converted to glucose, lipid, or lactate. Galactose is a simple sugar that is not very sweet and is seldom present free in foods (Matthews et al., 1987). It is usually bound with glucose in the disaccharide lactose, which is found in mammalian milks. Digestion of lactose releases glucose and galactose; after absorption, galactose is converted to glucose in the liver, although the kidney and erythrocyte may be involved in galactose metabolism to a minor extent.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Disaccharides A disaccharide consists of two monosaccharide units linked together, such as the disaccharide sucrose which is a plant energy reserve. Monosaccharides and disaccharides are known collectively as soluble sugars. Sucrose (glucose + fructose) is present in high concentrations in sugar cane and sugar beets and in much lower concentrations in fruits, vegetables, seeds, and nuts (Matthews et al., 1987). Adults have no problem in digesting sucrose, but very young baby pigs show little ability to use dietary sucrose or fructose (Becker et al., 1954a, 1954b) unless gradually adapted to them (Manners and Stevens, 1972). Although apparently not studied in nonhuman primates, that finding suggests caution in the selection of carbohydrates for use in primate milk-replacers. Lactose (glucose + galactose) is present in most mammalian milks. Some adult humans exhibit lactose intolerance associated with limited intestinal lactase activity; intolerance to lactose also has been reported in captive macaques (Hart et al., 1980; Streett and Jonas, 1980). Maltose (glucose + glucose) is seldom present free in foods but is an intermediate formed during the digestion of starch to glucose. Oligosaccharides An oligosaccharide is a polymer of three or more monosaccharide units. Some are intermediates in the synthesis or degradation of polysaccharides. Oligosaccharides include raffinose (a trisaccharide: fructose + glucose + galactose), stachyose (a tetrasaccharide: fructose + glucose + two galactose molecules), and verbascose (a pentasaccharide: fructose + glucose + three galactose molecules) (Taiz and Zeiger, 1998). Raffinose and stachyose have been found, and their concentrations determined, in some grains, leguminous seeds, nuts, and vegetables (Matthews et al., 1987). Polysaccharides Polysaccharides are large, and often complex, polymers of multiple monosaccharide units. They can be divided into two categories, starch and starch-like compounds, which are the only polysaccharides directly digestible by mammals, and non-starch polysaccharides. Non-starch-polysaccharides can be further divided into two sub-categories, insoluble non-starch polysaccharides, also referred to as insoluble fiber, and soluble non-starch polysaccharides, or soluble fiber. STARCH AND STARCH-LIKE POLYSACCHARIDES Starch, a polymer of glucose, is a plant energy reserve and occurs in granules that consists of amylose and amylopectin in various proportions (Taiz and Zeiger, 1998). Amylose is primarily a straight-chain polymer of glucose units linked by α-1→4 glycosidic bonds. Amylopectin is a branched-chain polymer of glucose units linked by α-1→4 and α-1→6 glycosidic bonds. Starch solubility ranges from soluble to highly insoluble but tends to form a gel in water unless physical or enzymatic treatment is applied to promote dissolution (Lee et al., 1992; Van Soest, 1994). Starch digestion by endogenous mammalian enzymes involves salivary and pancreatic α-amylases and yields maltose, maltotriose, some glucose, and limit dextrin (three to five α-1,4-glucose units and one α-1,6-glucose unit). Further digestion to glucose is accomplished principally by maltase in the intestinal brushborder. Resistant starch escaping enzymatic digestion or foregut fermentation may undergo microbial fermentation in the hindgut. Starch concentrations in diets fed to captive primates are commonly higher than found in wild foods (Clutton-Brock, 1975; Hladik, 1977; McKey et al., 1981). When high-starch diets are fed, excessively rapid fermentation may lead to digestive upsets, characterized by signs of abdominal discomfort and poor stool quality. This is particularly serious when high-starch, low-fiber foods are consumed by foregut fermenting primates, and may result in death (Go öltenboth, 1976). Glycogen is an animal energy reserve consisting only of amylopectin and is of little quantitative significance in the diets of most nonhuman primates. Dextrins are polymers of glucose and are intermediates in the digestion of amylopectin (principally from starch). NON-STARCH POLYSACCHARIDES Insoluble non-starch polysaccharides do not dissolve in water, nor do they generally swell in water to form a gel. Cellulose and hemicelluloses are structural polysaccharides making up the bulk of plant cell wall and also are referred to as insoluble fiber. They are commonly included in measures of fiber, along with non-carbohydrate components of cell wall, such as the highly complex phenylpropanoid lignin and the fatty substances cutin, suberin, and waxes. Other non-carbohydrate substances variously associated with cell wall (but not usually a part of fiber) are silica, calcium carbonate, tannins, resins, volatile oils, and crystalline pigments (Esau, 1965; Taiz and Zeiger, 1998). Cellulose is a polymer of 1,000 or more glucose molecules bound together by β-1→4 linkages that cannot be broken (digested) by endogenous mammalian enzymes. Symbiotic gastrointestinal anaerobes can release the energy of cellulose through microbial fermentation and the production of volatile fatty acids, although digestion may not be complete. The principal volatile fatty acids are acetic, propionic, and butyric acids (in descending order of usual abundance) plus small and variable amounts of isobutyric, valeric, and isovaleric acids. Much of the butyric acid (and some acetic acid) can be used directly for energy by intesti-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 nal cells. The other volatile fatty acids are absorbed and enter metabolic pathways (Cummings, 1981; Cummings and Branch, 1986; Bourquin et al., 1992). Wheat bran is an example of a food source of cellulose. Hemicelluloses are a heterogeneous group of single and mixed polymers of arabinose, xylose, mannose, glucose, fucose, galactose, and glucuronic acid closely associated with cellulose and lignin. Examples are xyloglucans, xylans, glucomannans, arabinoxylans, and glucuronoxylans (Taiz and Zeiger, 1998). Most hemicelluloses are water insoluble, but a few will form a viscous or gel-like solution (Gaillard, 1962). Like cellulose, hemicelluloses cannot be digested by endogenous mammalian enzymes, although they can be partially hydrolyzed in the acid stomach. Anaerobic fermentation is required for effective use of the energy that hemicelluloses contain, and the products of fermentation are essentially the same as those of cellulose. Humans and chimpanzees ferment hemicelluloses somewhat more completely than they do cellulose (Keys et al., 1970; Wiggens and Cummings, 1976; Milton and Dement, 1988). Soluble non-starch polysaccharides do not dissolve in water completely but swell to form a gel or a gummy solution. Nevertheless, they are referred to as soluble fiber. They are nonstructural polysaccharides, some of which serve as plant energy reserves, but they are not as digestible as starch, although fermented quite completely by ruminal and intestinal bacteria (Salyers et al., 1977; Van Soest, 1994; Bourquin et al., 1996). Included among the non-starch plant energy reserves are fructans, mannans, and galactans. Fructans (also known as fructosans, and including inulin) are polymers of fructose that are stored in grasses and composites (Smith, 1969), as well as in parts of some food crops (Ernst and Feldheim, 2000). Fructans are broken down in an acid environment (Smith, 1969), so passage through the acid stomach may result in release of some fructose monomers that can be absorbed in the small intestine (Ernst and Feldheim, 2000). Mannans are polymers of mannose found in sea weeds, algae, nuts, and seeds (Buckeridge et al., 2000; Sachslehner et al., 2000). Galactans are polymers of galactose found in sea weeds, algae, and with pectin in fruit pulps (Femenia et al., 1998). Pectic substances are not plant energy reserves but are associated with the plant cell wall. Despite this association, their relative solubility results in their inclusion among the soluble non-starch polysaccharides along with soluble β-glucans and other gums. They are closely related to hemicelluloses, but have no covalent linkage with lignin, and occur as protopectin, pectin, and pectic acid. They are heterogeneous polysaccharides, characteristically containing galacturonic acid, rhamnose, galactose, and arabinose bound by α-1→4 linkages (Taiz and Zeiger, 1998), that cannot be digested by endogenous mammalian enzymes. Like cellulose and hemicelluloses, however, they can be degraded by fermentation, and microbial degradation of pectic substances is often quite complete (Cummings et al., 1979; Stevens et al., 1988 ). Gumsand mucilagesare related to pectic substances, with which they share the property of swelling in water. Gums include β-glucans (soluble relatives of cellulose found in cereals, especially oats and barley), xyloglucans, and mannoglucans. Gums appear in plant exudates mainly as a result of physiologic or pathologic disturbances that induce breakdown of cell walls and cell contents. Mucilages occur in gelatinous or mucilaginous cell walls of aquatic plants and in seed coats. Sources are gum arabic, tragacanthic acid, locust bean gum, guar gum, xanthan, and tamarind. The algal polysaccharides are agar, alginates, and carrageenins. Psyllium or isopaghula is an indigestible mucilage used as a laxative by humans. Fermentation of cellulose, hemicelluloses, and pectic substances is quantitatively important in meeting the energy requirements of herbivorous primates that have specialized pregastric (Colobinae) or postgastric (howlers) digestive compartments. Even in primates that have no specialized compartments, anaerobic fermentation of dietary carbohydrates in the colon and cecum can account for up to 28% or more of the total metabolizable energy supply, based upon natural dietary habits and analogies with simple-stomached animals, such as the pig (Parra, 1978). Many soluble fibers tend to ferment faster than do insoluble fibers and may be more energetically important to simple-stomached animals and hind-gut fermenters (Cork et al., 1999). Marmosets and tamarins may derive some of their nutrient and energy requirements by digesting or fermenting plant exudates, including gums, sap, and latex. Some callitrichids, notably the pigmy marmoset (Cebuella pygmaea) and Callithrix spp., have relatively large lower incisors adapted for tree-gouging and intestinal tract structure adapted for digesting the exudates released (Coimbro-Filho et al., 1980; Rylands and de Faria, 1993). Other callitrichids, such as Saguinus spp. and Leontopithecus spp., do not have specialized incisors for tree-gouging but feed on exudates opportunistically when they are available because of insect or mechanical damage to plants (Garber, 1993; Rylands, 1993). Microbial fermentation of carbohydrates in the gastrointestinal tracts of some primates appears to support biosynthetic production of protein from recycled urea and some vitamins, such as vitamin B12 (Bauchop, 1978). On the basis of field observations by Jay (1965), it is probable that urea recycling and its associated water conservation contribute to colobines’ tolerance of climates that include an extended dry season. A classification of common dietary carbohydrates and associated digestive enzymes or digestive processes is shown in Table 3-1.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 3-1 Common Dietary Carbohydrates and Their Digestion (Kronfeld and Van Soest, 1976) Carbohydrate Simple-Sugar Components Digestion Digestive Products Maltose Glucose Maltasea Glucose Sucrose Glucose, fructose Sucrasea Glucose, fructose Lactose Glucose, galactose Lactaseb Glucose, galactase Starch Glucose Amylasesa Glucose Fructans Fructose Gastric acida Fructose Galactans Galactose Fermentative Volatile fatty acids Mannans Mannose Fermentative Volatile fatty acids Pectins Arabinose, galactose Fermentative Volatile fatty acids Hemicelluloses Arabinose, xylose, mannose, galactose, glucuronic acids Fermentative Volatile fatty acids Cellulose Glucose Fermentative Volatile fatty acids aIn primates with pregastric digestive compartments, digestion is primarily fermentative, yielding volatile fatty acids. Carbohydrates escaping digestion by endogenous enzymes in primates without pregastric digestive compartments may be digested fermentatively in the hindgut. bLactase activity declines after weaning in some species, and lactose may be digested fermentatively. ANALYTIC PROCEDURES FOR CARBOHYDRATES AND FIBER Analytic procedures for carbohydrates and for fiber are still under development despite a long history (DeVries et al., 1999). Their development is driven by the variability and complexity of carbohydrates and particularly of fiber and by recognition that some compounds in these categories have unique physiologic significance. Van Soest (1994) reviewed the relevant issues and described the limitations and advantages of various analytic techniques, emphasizing the characterization of fiber and pointing out that no protocol is appropriate for all samples. For other reviews of methodology, see Englyst and Cummings (1990) and Spiller (1992). A basic challenge for the nutritional chemist is to place plant cell components in categories that have physiologic meaning for the plant consumer. One category might include plant components, such as cell contents, that have the potential to be completely available, depending on the rate of digestion and the rate of digesta passage. The category would be comprised of protein, lipids, organic acids, and nonstructural carbohydrates, such as sugars, starch, and fructans; pectic substances, normally associated with the plant cell wall, might be included because of their high availability through fermentation. A second category might include plant components that are incompletely available and that are refractory to hydrolysis by endogenous enzymes but subject to fermentation by gastrointestinal microbes; this category would comprise the structural carbohydrates, cellulose and hemicelluloses. The third category could include plant cell-wall components that are unavailable, such as lignin and cutin, plus indigestible Mail-lard products resulting from protein denaturation and condensations between denatured proteins and carbohydrates during excessive heat exposure. Crude Fiber Crude fiber (CF), as measured in the 19th century Weende procedure, is the insoluble organic residue remaining after sequential treatment of samples with acid and alkali to mimic digestion in the human stomach and intestine. Crude fiber was intended to represent the fibrous fraction of the plant cell that was indigestible. However, the Weende procedure results in substantial solubilization of hemicelluloses and lignin, thus seriously underestimating the structural fiber content (Englyst and Cummings, 1990; Spiller, 1992; Van Soest, 1994). As a consequence, variable proportions of these substances appear in the nonstructural carbohydrate fraction (or nitrogen-free extract [NFE]) by difference. Hemicelluloses, although they are carbohydrates, cannot be digested by endogenous enzymes and yield energy to the host only after gastrointestinal fermentation. Lignin is a noncarbohydrate phenolic polymer that cannot be digested by endogenous mammalian enzymes or fermented by gastrointestinal microorganisms. Thus, the placement of these compounds in NFE is a serious error. These errors in crude-fiber determination have been known for years, but crude fiber continues to be used by regulatory agencies in characterizing animal feeds, apparently because of lack of agreement on alternative procedures. Total Dietary Fiber DeVries et al. (1999) suggested that Hipsley in 1953 might have been the first to use the term dietary fiber for the indigestible constituents that make up the plant cell wall. The indigestible constituents were known to include cellulose, hemicelluloses, and lignin, and dietary fiber was intended to distinguish more clearly between the indigestible components and components being measured as crude fiber. The definition of dietary fiber was subsequently

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 broadened to include “remnants of edible plant cells, polysaccharides, lignin, and associated substances resistant to (hydrolysis) digestion by the alimentary enzymes of humans.” Included in dietary fiber were cellulose, hemicellulose, lignin, gums, modified celluloses, mucilages, oligosaccharides, and pectins and associated minor substances, such as waxes, cutin, and suberin. After collaborative studies, AOAC Method 985.29 (1995) and AACC Method 32-05 (1995) were officially declared defining procedures for measuring dietary fiber. Modifications to separate total, soluble, and insoluble fiber were adopted as AOAC Method 991.43 (1995) and AACC Method 32-07 (1995). A reference standard with analytic values for those fractions is now available (Caldwell and Nelson, 1999). Total dietary fiber (TDF) (Prosky et al., 1985) is a more recent analytical method recognized as an official method of the AOAC, which has taken on an important role and is used extensively in human nutrition. Concentrations of TDF in human foods are included in the food composition tables in Chapter 12. Despite that progress, analytic problems in defining dietary carbohydrates and fiber persist (Delcour and Eerlingen, 1996). Starch that is resistant to hydrolysis by digestive enzymes has physiologic effects in humans that make it comparable with dietary fiber. The formation, structure, and properties of enzyme-resistant starch have been reviewed (Eerlingen and Delcour, 1995), and its physiologic properties have been described (Annison and Topping, 1994). Type I resistant starch is trapped in the food matrix. For example, starch granules in cell contents can be physically separated from amylolytic digestive enzymes by an unbroken cell wall, and enzymatic digestion will proceed if the cell wall is ruptured by chewing or by food processing, such as grinding. Type II resistant starch is native granular starch that is resistant to enzymatic digestion because of its compactness and partially crystalline structure; this resistance can be overcome by gelatinization (heating in the presence of water to disrupt hydrogen bonding and destroy crystallinity). Type III resistant starch is formed during retrogradation (recrystallization), primarily of amylose, although retrogradation of amylopectin can also be involved. The implications of the preceding paragraph for “accuracy” of the current AOAC and AACC methods depend on the intent to include or not include resistant starch in the dietary-fiber residue. Type I resistant starch generally would not be included in the residue, because type I resistance is destroyed during grinding of the sample in preparation for the analysis. Type II resistant starch would not appear in the residue, because the temperature to which it is exposed during the analysis (100°C) results in gelatinization, and it would be hydrolyzed by the added heat-stable a-amylase. Type III resistant starch consisting of retrograded amylopectin generally would not be included in the residue, because heating to 100°C would destroy most or all of the enzyme resistance. Retrograded amylose would be included in the residue because its enzyme resistance would not be destroyed until it reached a temperature of about 150°C, which is above the temperature used in the analysis. Neutral-Detergent Fiber and Related Fractions Progress is being made in defining the physiologically functional components of dietary fiber in human foods, but few TDF determinations have been made on the foods consumed by nonhuman primates in natural ecosystems or on the complete primate foods consumed in captivity. Except for crude-fiber values required by regulatory agencies on commercial feed labels, most measurements of fiber in the foods have been expressed as neutral-detergent fiber (NDF), acid-detergent fiber (ADF), and/or acid-detergent lignin (ADL), commonly using the procedures described by Van Soest et al. (1991) with the modifications described by Robertson and Horvath (1992). Although this detergent system of analysis does not quantify soluble fibers, quantification of insoluble fibers is comparable to that of the TDF system just described (Lee et al., 1992; Popovich et al., 1997), and soluble fiber concentrations may be estimated by subtracting NDF from TDF (Baer et al., 1997). The scheme shown in Figure 3-1 illustrates plant cell components that one would expect to find in the various analytic fractions of the commonly used sequential detergent system devised by Robertson and Van Soest (1981). NDF includes the total insoluble fiber in plant cell wall, primarily cellulose, hemicelluloses, and lignin. ADF is primarily cellulose and lignin, and the quantity of hemicelluloses may be estimated by subtracting ADF from NDF. When ADF is treated with sulfuric acid, cellulose is dissolved, leaving a residue designated acid-detergent lignin (ADL) or acid lignin (AL). Lignins are polyphenols that not only are themselves indigestible and unfermentable but interfere with the fermentability of other fractions in the cell wall by physically and chemically entrapping them (Southgate and Englyst, 1985; Cummings and Branch, 1986; Van Soest, 1994), especially lignin-bound proteins (Pichard and Van Soest, 1977). The various fiber fractions also may include tannins, waxes (such as cutin and suberin), and latexes (Van Soest, 1994; Conklin and Wrangham, 1994). Chitin (an unbranched polymer of ß-1,4-linked N-acetyl-D-glucosamine), found in the cell walls of bacteria and fungi and in the exoskeletons of insects and crustaceans (Vonk and Western, 1984), is similar in structure and chemical behavior to cellulose and can be measured in the ADF fraction when analyzing chitin-containing foods of omnivorous or insectivorous primates (Allen, 1989). Chitin can be

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 FIGURE 3-1 Plant cell components in the analytic fractions of the sequential detergent system of Robertson and Van Soest (1981). Alternatively, acid-detergent residue may be oxidized first with KMnO4, leaving a cellulose, cutin, and insoluble-mineral residue, with lignin measured as weight loss. Subsequent hydrolysis of the cellulose, cutin, and insoluble-mineral residue with H2SO4 leaves a cutin and insoluble-mineral residue, with cellulose measured as weight loss. Ashing the cutin and insoluble-mineral residue at 550°C leaves an insoluble mineral residue, with cutin measured as weight loss. *Acid-detergent lignin (or acid lignin) can be measured as weight loss after the lignin, cutin, and insoluble-mineral residue is ashed at 550°C and includes lignin + cutin.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 hydrolyzed to chitobiose by chitinase, and chitobiose can be hydrolyzed to N-acetyl-D-glucosamine by chitobiase (Stevens and Hume, 1995). Because these enzymes are found in many indigenous gut microorganisms, their presence in the gastrointestinal tract does not infer endogenous production. However, chitinase has been found in the gastric mucosa of a number of animal species (Jeuniaux, 1962), including the primates, Cebus capucinus (Jeuniaux and Cornelius, 1978) and Perodicticus potto (Beerten-Joly et al., 1974). CARBOHYDRATES IN WILD FOOD PLANTS Few studies of carbohydrates in wild food plants have identified or measured the specific carbohydrates found in plant parts consumed by free-ranging primates. In some instances, analytic procedures were used to measure concentrations of moisture, crude protein, ether extract, ash, NDF, ADF, and ADL in consumed plant parts (fresh basis). When the sum of moisture, crude protein, ether extract, ash, and NDF percentages was subtracted from 100% of fresh weight, the residual fraction was presumed to be mostly nonstructural carbohydrates, largely sugars, starch, and soluble fiber not included in NDF. NDF includes mainly cellulose, hemicelluloses, and lignin, so NDF minus ADL would approximate the structural-carbohydrate concentration; and NDF minus ADL plus nonstructural carbohydrates would yield an approximate measure of total carbohydrates. Of course, such estimates are subject to the errors associated with inaccuracies, imprecision, or lack of specificity in analyses of the other plant components. In addition, the category total carbohydrates combines carbohydrate fractions that differ tremendously in digestibility by endogenous alimentary enzymes. Carbohydrates in the insoluble fiber fraction (NDF-ADL) are relatively low in digestibility, those in the soluble fiber fraction (TDF-NDF) generally are moderately to highly digestible, whereas soluble sugars and starch are highly digestible. Calvert (1985) collected 36 samples of stems, leaves, shoots, and fruits from 27 species of plants eaten by western gorillas (Gorilla g. gorilla) in Cameroon, West Africa. Mean nonstructural-carbohydrate concentrations (dry basis) were estimated to be 28, 5, 24, and 20% in leaves, shoots, stems, and fruits, respectively. Estimates of mean structural-carbohydrate concentrations (cellulose plus hemicelluloses) were 27, 62, 45, and 38%, respectively. Thus, total carbohydrate concentrations were about 55, 67, 69, and 58% in leaves, shoots, stems, and fruits, respectively. Edwards (1995) collected plant parts (representing 90% of feeding time) consumed by red howlers (Alouatta seniculus) in the central llanos of Venezuela. Mean dietary nonstructural-carbohydrate concentrations (dry basis) were 29% during the wet season and 37% during the dry season. Structural carbohydrate concentrations (dry basis) were 32% and 31% during the wet and dry seasons, respectively. Thus, total carbohydrate concentrations were 61% and 68%. Conklin-Brittain et al. (1997) analyzed 408 samples of 194 plant parts representing 94% of the plant-feeding time among chimpanzees (Pan troglodytes), gray-cheeked mangabeys (Cercocebus albigena), blue monkeys (Cercopithecus mitis), and redtail monkeys (Cercopithecus ascanius) in the Kibale Forest, Uganda. Reported mean concentrations (dry basis) of simple sugars were 10-15% and of total nonstructural carbohydrates from 34-39%. (Conklin-Brittain et al., 1998). Mean concentrations of structural carbohydrates (cellulose plus hemicelluloses) were 23-26%. Thus, total carbohydrate concentrations in the plant parts eaten were 57-65%. Others have conducted nutrient analyses of the natural foods of gorillas in the Lopé Reserve, Gabon (Rogers et al., 1990), baboons (Papio anubis) on the Laikipia Plateau in Kenya (Barton et al., 1993) (Table 3-2), red colobus (Colobus badius) and black-and-white colobus (C. guereza) in the Kibale Forest in Uganda (Baranga, 1982), and silvered leaf monkey (Trachypithecus auratus) in the Pangandaran Nature Reserve, West Java (Kool, 1992) (Table 3-3). The proportions of items in wild diets that were analyzed are lower in Table 3-3 than in Table 3-2. The data generated do not permit estimates of total nonstructural carbohydrates or total carbohydrates, but measurements of ADF make it clear that fiber concentrations were variable in chosen foods and often high compared with those in fruits and vegetables cultivated for human consumption and in commercial primate diets. Rogers et al. (1990) noted that plant diversity was high in the mature forest inhabited by gorillas in Gabon compared with the impoverished disturbed forest occupied by gorillas in Cameroon (Calvert, 1985). Fruit availability in Gabon was much greater, and Lopé Reserve gorillas eagerly consumed ripe fruits, particularly succulent flesh that tended to be more sugary and less fibrous than unripe fruit or the fruit parts that were uneaten. Mean water-soluble carbohydrate concentration in the dry matter of 46 fruits and fruit parts that were eaten was 35%, and mean ADF concentration 24%. Surprisingly, consumed fruit parts often were higher than nonconsumed fruit parts in condensed tannins and total phenols. Conklin and Wrangham (1994) analyzed nine fig species eaten by frugivorous primates in the Kibale Forest, Uganda, and found that water-soluble carbohydrates (free simple sugars) in the pulp organic matter (dry matter minus ash) were present at 7-23%, whereas NDF was present at 24-65%. For purposes of comparison, total sugar concentrations exceed 33% in the dry matter of the edible portion of raw figs consumed by humans when calculated by adding analytic

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 3-2 Fiber Concentrations in Wild-Primate Diets (% of Dry Matter) in Studies in Which over 70% of Items in Diet Were Analyzed Species Neutral-Detergent Fiber (NDF) Acid-Detergent Fiber (ADF) Acid-Detergent Lignin (ADL) Crude Fiber (CF) Cellulose Reference Notes New World monkeys Alouatta palliata 34.0a — — — 13.6 Hladik et al. (1971) Weighted meand—cellulose in many plant foods Ateles geoffroyi 27.5a — — — 11.0 ibid. ibid. Cebus capucinus 19.0a — — — 7.6 '' '' Saguinus geoffroyi 18.2a — — — 7.3 '' '' Alouatta palliata 50.8b 40.8 — — — Glander (1981) Mean—fruit 47.5b 37.5 — — — ibid. Mean—mature leaves 43.7b 33.7 — — — '' Mean—young leaves 47.3b 37.3 — — — '' Mean—all items Alouatta seniculus 50.6 35.8 17.1 — — Oftedal (1991) Mean—flowers 53.8 35.2 16.6 — — ibid. Mean—fruit 57.2 40.5 20.4 — — '' Mean—mature leaves 54.4 36.4 21.1 — — '' Mean—young leaves 54.0 37.0 18.8 — — '' Mean—all items Prosimians Avahi laniger 53.3 — — — — Ganzhorn et al. (1985) Mean—all items Daubentonia madagascariensi 28.9 22.5 16.8 — — Sterling et al. (1994) Mean—diet items Old World monkeys Macaca fuscata 45.4c — — 22.7 — Iwamoto (1982) Mean—leaves-shoots 41.8c — — 20.9 — ibid. Mean—fruit-seeds 23.0c — — 11.5 — '' Mean—invertebrates 36.8c — — 18.4 — '' Mean—all diet items Cercocebus torquatus 33.2b 23.2 — — — Mitani (1989) Weighted meane—diet items Papio anubis 27.1b 17.1 — — — Barton et al. (1993) Mean—foliage 37.2b 27.2 — — — ibid. Mean—fruit 24.8b 14.8 — — — '' Mean—seeds 29.7b 19.7 — — — '' Mean—all diet items Lophocebus albigena 33.0 20.4 8.2 — — Conklin-Britain et al. (1998) Weighted meane—annual diet Cercopithecus ascanius 31.5 19.4 8.1 — — ibid. Weighted meane—annual diet Cercopithecus mitis 32.8 20.0 8.1 — — ibid. Weighted meane—annual diet Cercopithecus mitis 40.2b 30.2 — — — Beeson (1989) Mean—dry-season diet 35.3b 25.3 — — — ibid. Mean—wet- and dry-season diet Colobines Colobines (several) 44.1b 34.1 — — — Waterman and Kool (1994) Weighted meane—leaves Presbytis senex [67.4] — — — — Hladik (1988) Estimated diet NDF Presbytis entellus [61.8] — — — — ibid. Estimated diet NDF Procolobus badius 36.0b 26.0 — — — Mowry et al. (1996) Mean—young leaves 40.0b 30.0 — — — ibid. Mean—mature leaves 35.6b 25.6 — — — '' Mean—flowers 62.2b 52.2 — — — '' Mean—fruit 43.5b 33.5 — — — '' Mean—all diet items Apes Hylobates lar 33.8c — — 16.9 — Vellayan (1981) Estimated mean—low-fiber diet 51.2c — — 25.6 — ibid. Estimated mean—high-fiber diet

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Species Neutral-Detergent Fiber (NDF) Acid-Detergent Fiber (ADF) Acid-Detergent Lignin (ADL) Crude Fiber (CF) Cellulose Reference Notes Gorilla g. gorilla 46.0 42.6 19.4 — — Calvert (1985) Mean—leaves 55.9 44.4 11.4 — — ibid. Mean—stems 73.2 52.0 11.3 — — '' Mean—shoots 64.6 44.8 26.9 — — '' Mean—fruit 59.9 46.0 17.3 — — '' Mean—all diet items 38.8b 28.8 — — — Rogers et al. (1990) Mean—foliage 33.7b 23.7 — — — ibid. Mean—fruit 34.6b 24.6 — — — '' Mean—seeds 54.9b 44.9 — — — '' Mean—stems-bark 40.5b 30.5 — — — '' Mean—all diet items Pan troglodytes 33.6 19.6 7.8 — — Conklin-Brittain et al. (1998) Weighted meane—annual diet Pongo pygmaeus 17.0 — — — — Knott (1999) Weighted meanf—high fruit 69.0 — — — — ibid. Weighted meanf—low fruit aNDF estimated by multiplying analyzed cellulose by 2.5. bNDF estimated by adding 10 to analyzed ADF. cNDF estimated by multiplying analyzed crude fiber by 2. dWeighting coefficient based on proportions of plant foods in stomach. eWeighting coefficient based on time spent in feeding on each food item. fWeighting coefficient based on calculated mass of each food item eaten. values of 17.7%, 13.4%, and 1.9% for glucose, fructose, and sucrose, respectively (Matthews et al., 1987). Galactose, trioses, and tetroses also were known to be present but were unmeasured. Assuming that the unmeasured sugars were present in low concentrations, failure to consider them should produce only a minimal error in the estimate of total sugar concentrations. Total carbohydrate (including the water-soluble sugars) concentration was reported to be 90.2%, and fiber concentration 5.3% (Watt and Merrill, 1963). Because the latter figure was determined with the Weende crude-fiber procedure, it is probably too low; and because the total carbohydrate value was determined by difference from 100% after analysis of moisture, crude protein, ether extract, crude fiber, and ash, it is probably too high. Nevertheless, the domesticated fig is appreciably lower in fiber and higher in nonstructural carbohydrates than the wild figs consumed by free-ranging primates. SIGNIFICANCE OF FIBER Among primate species, acceptable concentrations of fiber in the diet and the ability to digest it tend to be highest in Colobinae (with pregastric fermentation similar to that in ruminants). Human diets are generally low in fiber and elevated levels may decrease fat and protein digestibility, although apparent digestibility of TDF has been shown to range from 67 to 82% (Baer et al., 1997). Certain fibers have a high cation-exchange capacity and may influence mineral metabolism by reducing absorption of iron, calcium, copper, and zinc (Schneeman, 1990). That is not to say that fiber in the diet is an entirely adverse factor. In humans, dietary fiber is useful in managing obesity (Burley and Blundell, 1990; Rytigg et al., 1990). Some fiber appears to lower plasma lipid and cholesterol (Anderson et al, 1990; Sugano et al., 1990), modulate the postprandial glycemic and insulinemic response (Trowell, 1990; Wolever, 1990), and improve large bowel function (Stephan, 1985) in humans. Soluble fiber that undergoes fermentation may contribute little to laxation (Stephen and Cummings, 1980; Southgate and Englyst, 1985), and insoluble fibers of cereal brans are more effective than fiber in domestic fruits and vegetables for increasing fecal bulk (Stephen, 1985). However, fine grinding of cereal brans may greatly reduce this laxation effect (Brodribb and Groves, 1978; Floch and Fuchs, 1978; Wrick et al., 1983; Van Soest, 1994). The risk of diverticular disease (Painter, 1985) and colon cancer (Hill and Fernandez, 1990; Lanza, 1990) in humans may be reduced by increased fiber intake from fruits and vegetables, but the data are not conclusive (Schatzkin et al., 2000). It is difficult to separate the effects of fruit and vegetable fiber from other potentially beneficial components of these foods or from the decrease in relative intake of other foods that may have components that increase disease risk (Gallaher and Schneeman, 1996). Whether fiber in the diet of nonhuman primates promotes the health benefits proposed for humans has not been sufficiently studied. It has been shown that some fiber or fiber sources may be associated with increases, decreases, or no change (depending on fiber type) in serum lipid and cholesterol concentrations and the incidence of atherosclerosis and colonic mucosal damage in rhesus (Macaca mulatta) and vervet or green (Chlorocebus aethiops) monkeys (Heine et al., 1984; Kritchevsky et al., 1986,

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 3-3 Fiber Concentrations in Wild-Primate Diets (% of Dry Matter) in Studies in Which under 70% of Items in diet Were Analyzed Species Neutral-Detergent Fiber (NDF) Acid-Detergent Fiber (ADF) Acid-Detergent Lignin (ADL) Crude Fiber (CF) Total Dietary Fiber (TDF) Reference Notes New World monkeys Alouatta palliata 27.5 — — — — Milton (1979) Mean—young leaves 36.4 — — — — '' Mean—mature leaves Leaves 48.2% of diet Alouatta palliata 34.4a — — 17.2 — Estrada (1984) Mean—young leaves (39.3% of diet) 53.6a — — 26.8 — '' Mean—mature leaves (10% of diet) Alouatta palliata 42.8a — — 21.4 — Estrada & Coates-Estrada (1986) Mean—young leaves (36% of diet) 53.2a — — 26.6 — '' Mean—mature leaves (10% of diet) Prosimians Avahi laniger 63.0 46.2 — — — Ganzhorn (1988) Mean—leaves (folivore) Cheirogaleus major 63.1 43.0 — — — '' Mean—leaves (frugivore) Eulemur fulvus 58.7 49.0 — — — '' Mean—leaves (frugivore) Hapalemur griseus 70.4 29.7 — — — '' Mean—leaves (folivore) Indri indri 61.4 47.5 — — — '' Mean—leaves (folivore) Lepilemur mustelinus 62.1 45.1 — — — '' Mean—leaves (folivore) Old World monkeys Macaca fuscata 49.6c — — — — Hill & Lucas (1996) Mean—petioles 66.4c — — — — '' Mean—leaf midrib 42.0c — — — — '' Mean—leaf lamina Colobines Colobus guereza 34.8 20.2 — — — Oates (1978) Mean—eight foods (68% of diet) Presbytis johnii 38.1 30.0 13.6 — — Oates et al. (1980) Mean—young leaves (35.4% of diet) 41.6 32.6 15.3 — — '' Mean—mature leaves (26.8% of diet) Colobus badius 49.4b 39.4 — — — Waterman & Choo (1981) Mean—leaves Colobus satanas 65.2b 55.2 — — — '' Mean—leaves Presbytis johnii 52.1b 42.1 — — — '' Mean—leaves Colobus badius 48.4b 38.4 — — — Choo et al. (1981) Mean—mature leaves 38.8b 28.8 — — — '' Mean—young leaves Colobus satanas 70.8b 60.8 — — — McKey et al. (1981) Mean—mature leaves 58.6b 48.6 — — — '' Mean—young leaves Leaf 43%, seeds 57% of diet Colobus badius, 44.0b 34.0 10.2 — — Baranga (1982) Favored foliage (mean of two) C. guereza 48.4b 38.4 17.0 — — '' Less-favored foliage (6) Trachypithecus auratus 40.0b 30.0 — — — Kool (1992) Mean—mature leaves 45.0b 35.0 — — — '' Mean—fruit Presbytis entellus 34.6b 24.6 — — — Kar-Gupta & Kumar (1994) Mean—winter foliage 32.6b 22.6 — — — Mean—spring foliage Nasalis larvatus 63.9 34.7 16.5 — — Yeager et al. (1997) Mean—mature leaves 44.4 31.4 16.0 — — '' Mean—young leaves Rhinopithecus brelichi 46.2 37.0 18.9 — — Bleisch et al. (1998) Mean—leaves Apes Pan troglodytes 50.5 33.7 4.5 — — Wrangham et al. (1991) Mean—pith (nine species) Pan troglodytes 35.6 — — — — Wrangham et al. (1993) Mean—pulp (eight fig species) 63.7 — — — — '' Mean—seeds (eight fig species)

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Species Neutral-Detergent Fiber (NDF) Acid-Detergent Fiber (ADF) Acid-Detergent Lignin (ADL) Crude Fiber (CF) Total Dietary Fiber (TDF) Reference Notes Pan troglodytes 55.7b 45.7 — — — Conklin & Wrangham (1994) Mean—26 fig species from literature 41.3 34.3 15.3 — — '' Mean—8 fig species from Uganda Pongo pygmaeus 36.0b 26.0 — — — Leighton (1993) Mean—nonfig pulp 34.0b 24.0 — — — '' Mean—nonfig seeds 60.4b 50.4 — — — '' Mean—nine favored fig species Pongo pygmaeus 51.3b 41.3 — — — Hamilton & Galdikas (1994) Weighted mean—8 items Pongo pygmaeus 28.7 — — — — Knott (1999) Mean—five favored fruits (high abundance) 62.2 — — — — '' Mean—five typical fruits (low abundance) Gorilla g. gorilla 64.2 47.7 — — 65.5 Popovich et al. (1997) Mean—16 leaves 80.4 54.5 — — 86.9 '' Mean—eight stems 79.5 64.6 — — 66.5 '' Mean—two vines 78.7 65.4 — — 83.8 '' Mean—five fruits Analyzed 15% of items eaten aNDF estimated by multiplying analyzed CF by 2. bNDF estimated by adding 10 to analyzed ADF. cNDF estimated from wet weight assuming 25% DM. 1988; Paulini et al., 1987). There is strong evidence of beneficial roles for dietary fiber in the diets of several orders of herbivorous animals (Salley and Bryson, 1957; Cummings et al., 1978; Edwards, 1995), including nonhuman primates, particularly those whose gastrointestinal tracts are specialized for foregut or hindgut fermentation by symbiotic microorganisms (Stevens and Hume, 1995). In fact, the occurrence of morbidity associated with gastrointestinal disease in captive specimens of these specialist primates has been attributed to the low concentrations of fiber in their diets (Gö ltenboth, 1976; Griner, 1977, 1983; Janssen, 1994). The more fermentable (soluble) fraction of dietary fiber may be energetically important for some simple-stomached or hindgut-fermenting nonhuman primates (Cork et al., 1999). Some callitrichid species show evidence of high use of gum arabic included in captive diets, on the basis of measures of dry-matter digestibility (Power and Oftedal, 1996). PROPOSED FIBER INTAKES BY NONHUMAN PRIMATES Minimal required dietary concentrations of specific kinds of fiber, such as cellulose, or of a broad fiber category, such as NDF, have not been—and perhaps cannot be— established in the same sense as minimal requirements for essential nutrients. However, adverse effects of inappropriate fiber intakes have been reported in nonhuman primates, particularly in species with specialized foregut or hindgut fermentation, and it might be helpful to draw analogies with other well-studied species. Fiber Recommendations for Other Species The National Research Council has recommended that the dietary DMof the dairy cow (a foregut fermenter) should contain no more than 30-40% nonstructural carbohydrate to avoid acidosis and other metabolic problems (National Research Council, 2001). Minimum recommended NDF concentrations for dairy cattle of various ages and productive states range from 25-33% of dietary DM(National Research Council, 2001). When expressed as ADF, the recommended minimal range is 17-21%. The National Research Council has recommended that the horse (a hindgut fermenter) receive sufficient forage to minimize digestive dysfunctions attributable to sudden dietary change and the feeding of excessive concentrate (inadequate fiber) (National Research Council, 1989). Depending on age and activity, recommended proportions of forage in the total dietary dry matter fed to horses range from 30-100%. Corresponding values for dietary NDF or ADF were not provided. Fiber in Wild Food Plants as Guides for Captive-Diet Fiber Concentrations Fiber concentrations in the diets of free-ranging nonhuman primates can serve as guides for fiber in the diets of captive species, and data on fiber concentrations in wild-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 3-4 Fiber Levels (% of Dietary Dry Matter) Fed to Primates in Captivity Species Neutral-Detergent Fiber (NDF) Acid-Detergent Fiber (ADF) Acid-Detergent Lignin (ADL) Crude Fiber (CF) Total Dietary Fiber (TDF) Reference Notes Macaca mulatta   4.4a — — 2.2 — Morin et al. (1978) Commercial extruded diet; 20.8% intestinal disorders 4.8a — — 2.4 — '' Baked experimental diet; 11.1% intestinal disorders 14.0a — — 7.0 — '' Baked experimental diet; 1.4% intestinal disorders 19.6a — — 9.8 — '' Baked experimental diet; 12.5% intestinal disorders Alouatta palliata 40.6 25.7 11.4 — — Milton et al. (1980) Wild-fruit diet; ADb of NDF = 23% 39.7 22.7 10.6 — — '' Wild-leaf diet; AD of NDF = 41% Colobus guereza   25.1 — — — — Watkins et al. (1985) Commercial extruded diet; AD of NDF = 81.3% Pan troglodytes   34.5 10.0 2.8 — — Milton & Demment (1988) Commercial extruded diet; AD of NDF = 54.3%, AD of ADF = 32.9% 15.3 5.2 1.1 — — '' Commercial extruded diet; AD of NDF = 70.6%; AD of ADF = 57.2% Macaca fuscata, M. mulatta   37.5 15.1 — — — Sakaguchi et al. (1991) Commercial extruded diet; AD of NDF = 48.3%; AD of ADF = 34.5% 18.0 4.7 — — — '' Commercial extruded diet; AD of NDF = 78.0%; AD of ADF = 60.7% Semnopithecus cristatus   37.5 15.1 — — — '' Commercial extruded diet; AD of NDF = 68.9%; AD of ADF = 61.8% Nasalis larvatus   14.0 — — — — Dierenfeld et al. (1992) Commercial extruded diet; AD of NDF = 86.4% 14.5 — — — — '' Commercial extruded diet; AD of NDF = 86.2% Callithrix jacchus — — — — 16.0 Power & Oftedal (1996) Gel diet; AD of DM = 77.2% Cebuella pygmaea — — — — 16.0 '' Gel diet; AD of DM = 83.7% Leontopithecus pithecus — — — — 16.0 '' Gel diet; AD of DM = 85.4% Saguinus fusicollis — — — — 16.0 '' Gel diet; AD of DM = 74.3% Saguinus oedipus — — — — 16.0 '' Gel diet; AD of DM = 83.0% Varecia variegata   24 15 — — — Edwards & Ullrey (1999a) Experimental extruded diet; AD of NDF = 20.4%; AD of ADF = 9.4% 42 30 — — — '' Experimental extruded diet; AD of NDF = 20.7%; AD of ADF = 12.6% Alouatta caraya   24 15 — — — Edwards & Ullrey (1999b) Experimental extruded diet; AD of NDF = 46.5%; AD of ADF = 40.5%; 42 30 — — — '' Experimental extruded diet; AD of NDF = 45.8%; AD of ADF = 37.7% Alouatta seniculus   24 15 — — — '' Experimental extruded diet; AD of NDF = 43.3%; AD of ADF = 43.1%; 42 30 — — — '' Experimental extruded diet; AD of NDF = 44.8%; AD of ADF = 39.5% Alouatta villosa   24 15 — — — '' Experimental extruded diet; AD of NDF = 43.7%; AD of ADF = 43.8% 42 30 — — — '' Experimental extruded diet; AD of NDF = 52.6%; AD of ADF = 46.2% Colobus guereza   24 15 — — — '' Experimental extruded diet; AD of NDF = 77.0%; AD of ADF = 80.1% 42 30 — — — '' Experimental extruded diet; AD of NDF = 74.3%; AD of ADF = 56.2% Pygathrix nemaeus   24 15 — — — '' Experimental extruded diet; AD of NDF = 66.5%; AD of ADF = 66.6% 42 30 — — — '' Experimental extruded diet; AD of NDF = 69.8%; AD of ADF = 67.6% Trachypithecus francoisi   24 15 — — — '' Experimental extruded diet; AD of NDF = 79.3%; AD of ADF = 82.3% 42 30 — — — '' Experimental extruded diet; AD of NDF = 75.7%; AD of ADF = 76.9% aNDF estimated by multiplying analyzed CF by 2. bAD = apparent digestibility.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 3-5 Proposed Fiber Concentrations in Total Dietary Dry Matter of Extruded Diets for Primate Species Grouped by Relative Ability to Utilize Plant Cell Walla Fiber Form and Percentage Species Group I   NDF 10 Callithrix spp. ADF 5 Cebuella spp. Leontopithecus spp. Macaca spp. Saguinus spp. Group II   NDF 20 Pan troglodytes ADF 10 Varecia variegata Group III   NDF 30 Alouatta spp. ADF 15 Colobus spp. Nasalis larvatus Propithecus spp. Pygathrix nemaeus Semnopithecus entellus Trachypithecus spp. aThese concentrations were reported to have desirable effects on gut health and fecal consistency. Complete diets with higher fiber concentrations are difficult to extrude with present technology, and waste is unacceptably high. primate foods are presented in Tables 3-2 and 3-3. However, it is questionable whether field studies are sufficient for deducing optimal dietary fiber concentration, in that the foods consumed in the wild depend on what foods are available, both regionally and seasonally. It might be necessary for primates to consume higher-fiber foods in a degraded habitat, and a number of studies have noted a tendency for primates to select against highly fibrous plant parts when less-fibrous foods are available. Of course, concentrations of other components—such as protein, sugars, and tannins—in these plant parts might influence food choices in the wild. Primate populations that appear healthy and that are reproducing at an expected rate are probably not harmed by a seemingly high fiber intake. At some field sites and sampling times, however, certain primates appear to be just maintaining a viable population. Consequently, fiber levels consumed in the wild may represent maximum levels that still allow for growth and reproduction but may not be optimal. Fiber Digestion by Nonhuman Primates as a Guide for Captive-Diet Fiber Concentrations The digestive capabilities of several primate species have been studied with multiple fiber concentrations in controlled studies (Table 3-4). Animal response was, as one would expect, related to the gastrointestinal adaptations of the species involved. In one study, the relative digestibility of NDF by primates with foregut fermentation (colobines), hindgut fermentation (howlers), and a simple gastrointestinal tract (ruffed lemurs) was comparable with that seen in domestic mammalian species that have similar digestive tract adaptations (Edwards, 1995). Proposed NDF and ADF Concentrations in Captive Nonhuman-Primate Diets On the basis of the data in Table 3-4, we propose NDF and ADF in total dietary dry matter as shown in Table 3-5 for three groups of primate species that have various demonstrated abilities to use plant cell wall. These concentrations are not intended as minimal requirements for fiber, but represent guidelines for diet formulation that are rational and achievable and appear to be consistent with primate health. REFERENCES AACC Method 32-05. 1995. Total dietary fiber. Approved Methods of the American Association of Cereal Chemists, 9th ed. St. Paul, MN: The Association. AACC Method 32-07. 1995. Determination of soluble, insoluble and total dietary fiber in foods and food products. Approved Methods of the American Association of Cereal Chemists, 9th ed. St. Paul, MN: Am. Assoc. Cereal Chem. Allen, M.E. 1989. Nutritional Aspects of Insectivory. Ph.D. Dissertation, Mich. State Univ., E. Lansing, MI. Anderson, J.W., D.A. Deakins, and S.R. Bridges. 1990. Soluble fiber: hypocholesterolemic effects and proposed mechanisms. Pp. 339-364 in Dietary Fiber: Chemistry, Physiology, and Health Effects, D. Kritchevsky, C. Bonfield, and J.W. Anderson, Eds. New York: Plenum Press. Annison, G., and D.L. Topping. 1994. Nutritional role of resistant starch: chemical versus physiological function. Annu. Rev. Nutr. 14:297-320. AOAC Method 985.29. 1995. Total dietary fiber in foods - enzymatic-gravimetric method. Official Methods of Analysis, 16th ed. Gaithersburg, MD: Assoc. Official Anal. Chem. AOAC Method 991.43. 1995. Total, insoluble and soluble dietary fiber in food - enzymatic-gravimetric method, MES-TRIS buffer. Official Methods of Analysis, 16th ed. Gaithersburg, MD: Assoc. Official Anal. Chem. Asp, N. 1994. Nutritional classification and analysis of food carbohydrates. Am. J. Clin. Nutr. 59S:679S-681S. Baer, D.J., W.V. Rumpler, C.W. Miles, and G.C Fahey, Jr. 1997. Dietary fiber decreases the metabolizable energy content and nutrient digestibility of mixed diets fed to humans. J. Nutr. 127:579-586. Baranga, D. 1982. Nutrient composition and food preferences of colobus monkeys in Kibale Forest, Uganda. Afr. J. Ecol. 20:113-121 Barton, RA, A. Whiten, R.W. Byrne, and M. English. 1993. Chemical composition of baboon plant foods: implications for the interpretation of intra- and inter-specific differences in diet. Folia Primatol. 61:1-20 Bauchop, T. 1978. Digestion of leaves in vertebrate arboreal folivores. Pp. 113-204 in The Ecology of Arboreal Folivores, G.G. Montgomery, Ed. Washington, DC: Smithsonian Instit. Press. Becker, D.E., D.E. Ullrey, and S.W. Terrill. 1954a. A comparison of carbohydrates in a synthetic milk diet for the baby pig. Arch. Biochem. Biophys. 48:178-183. Becker, D.E., D.E. Ullrey, S.W. Terrill, and R.A. Notzold. 1954b. Failure of the newborn pig to utilize dietary sucrose. Science 120:345-346.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Beerten-Joly, B., A. Piavaux, and M. Goffart. 1974. Quelques enzymes digestives chez un prosimien, Perodicticus potto. C.R. Séances Soc. Biol. (Paris) 168:140-143. Beeson, M. 1989. Seasonal dietary stress in a forest monkey (Cercopithecus mitis). Oecol. 78:565-570. Bleisch, W.V., Z-M. Liu, E.S. Dierenfeld, and J-H. Xie. 1998. Selected nutrient analysis of plants in the diet of the Guizhou snub-nosed monkey (Rhinopithecus brelichi). Pp. 241-259 in The Natural History of the Doucs and Snub-Nosed Monkeys, N.G. Jablonski, Ed. Singapore: World Scientific Publishing. Bourquin, L.D., E.C. Titgemeyer, K.A. Garleb, and G.C Fahey. 1992. Short-chain fatty acid production and fiber degradation by human colonic bacteria: effects of substrate and cell wall fractionation procedures. J. Nutr. 122:1508-1520. Bourquin, L.D., E.C. Titgemeyer, and G.C. Fahey. 1996. 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