6
Minerals

Animals, plants, and microorganisms all require minerals. In animals, minerals function as structural components of organs and tissues, as cofactors or activators in enzyme and hormone systems, as constituents of body fluids and tissues (where they maintain osmotic pressure, acid-base balance, membrane permeability, and tissue irritability), and as regulators of cell replication and differentiation (Underwood and Suttle, 1999). If tissues and foods are burned, the mineral content is the fraction that remains; it is termed ash. The inorganic elements in ash exist principally as oxides, carbonates, and sulfates, so the percentage of total ash is higher than the sum of the individually determined inorganic elements. Some of the elements in ash are essential nutrients, but few definitive studies have been conducted in nonhuman primates to determine quantitative requirements.

The essential macrominerals include calcium, phosphorus, magnesium, potassium, sodium, chlorine, and sulfur. Concentrations of macrominerals in animal diets are usually expressed in percentages.

Trace elements known to be required include iron, copper, manganese, zinc, iodine, selenium, chromium, and cobalt (as a part of vitamin B12, cobalamin). Other trace elements (such as fluorine, molybdenum, silicon, boron, nickel, and tin) might be required (Underwood, 1977; Nielson, 1994), although little research on the qualitative or quantitative needs of nonhuman primates for these elements has been conducted. Trace element requirements are usually expressed in parts per million (ppm) or parts per billion (ppb), equivalent to milligrams per kilogram (mg·kg-1) or micrograms per kilogram (µg·kg-1), respectively.

In the wild, primates obtain minerals mostly from plant and animal tissues, depending on dietary habits, although geophagia (dirt-eating) has been observed in moustached tamarins (Saguinus mystax) (Hartmann and Hartmann, 1991), howlers (Alouatta seniculus), spider monkeys (Ateles belzebuth) (Izawa, 1993), mountain gorillas (Gorilla gorilla beringei) (Mahaney et al., 1990, 1995a), and rhesus macaques (Mahaney et al., 1995b; Marriott et al., 1996), and sometimes this practice supplements the dietary mineral supply. Green leaves and bones are usually good sources of calcium and magnesium; some gums are high in calcium, magnesium, and potassium (Bearder and Martin, 1980); and seeds, nuts, bones, muscle, and invertebrates are usually good sources of phosphorus. Primates in laboratories or zoos fulfill many of their mineral requirements from specific mineral additions to diets containing ingredients that would otherwise be nutritionally incomplete. Browse (fresh or dried foliage) offered to captive primates can also contribute to the dietary supply of essential minerals.

Quantitative mineral requirements of nonhuman primates are poorly defined, but proposed minimal dietary concentrations are presented in Chapter 11. Mineral concentrations in foods and feedstuffs commonly used in feeding captive primates are presented in Chapter 12.

The bioavailability of minerals in foods (Ammerman et al., 1995) for nonhuman primates has not been studied, but bioavailability of many minerals for many other species is less than 100%, compared with highly bioavailable standards. For example, calcium bound to oxalate and phosphorus bound to phytate appear to be largely unavailable to simple-stomached animals. Spinach contains appreciable calcium, but most is bound to oxalate, so only about 5% is available to humans (Heaney et al., 1998). The mineral concentrations in foods might require interpolation when diets are being formulated to ensure that requirements for minimal available nutrients are met.

Some mineral elements, such as cadmium, lead, and antimony, are of concern because of their potential toxicity. Primate research on this subject is sparse, although some clinical reports might contribute to definitions of lead tolerance (Zook and Paasch, 1980), and the effects of different lead intakes and low or normal dietary calcium concentrations upon chromosomal abnormalities in lymphocytes have been studied in cynomolgus (Macaca irus) monkeys (Deknudt et al., 1977). Dietary cadmium intake and its



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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 6 Minerals Animals, plants, and microorganisms all require minerals. In animals, minerals function as structural components of organs and tissues, as cofactors or activators in enzyme and hormone systems, as constituents of body fluids and tissues (where they maintain osmotic pressure, acid-base balance, membrane permeability, and tissue irritability), and as regulators of cell replication and differentiation (Underwood and Suttle, 1999). If tissues and foods are burned, the mineral content is the fraction that remains; it is termed ash. The inorganic elements in ash exist principally as oxides, carbonates, and sulfates, so the percentage of total ash is higher than the sum of the individually determined inorganic elements. Some of the elements in ash are essential nutrients, but few definitive studies have been conducted in nonhuman primates to determine quantitative requirements. The essential macrominerals include calcium, phosphorus, magnesium, potassium, sodium, chlorine, and sulfur. Concentrations of macrominerals in animal diets are usually expressed in percentages. Trace elements known to be required include iron, copper, manganese, zinc, iodine, selenium, chromium, and cobalt (as a part of vitamin B12, cobalamin). Other trace elements (such as fluorine, molybdenum, silicon, boron, nickel, and tin) might be required (Underwood, 1977; Nielson, 1994), although little research on the qualitative or quantitative needs of nonhuman primates for these elements has been conducted. Trace element requirements are usually expressed in parts per million (ppm) or parts per billion (ppb), equivalent to milligrams per kilogram (mg·kg-1) or micrograms per kilogram (µg·kg-1), respectively. In the wild, primates obtain minerals mostly from plant and animal tissues, depending on dietary habits, although geophagia (dirt-eating) has been observed in moustached tamarins (Saguinus mystax) (Hartmann and Hartmann, 1991), howlers (Alouatta seniculus), spider monkeys (Ateles belzebuth) (Izawa, 1993), mountain gorillas (Gorilla gorilla beringei) (Mahaney et al., 1990, 1995a), and rhesus macaques (Mahaney et al., 1995b; Marriott et al., 1996), and sometimes this practice supplements the dietary mineral supply. Green leaves and bones are usually good sources of calcium and magnesium; some gums are high in calcium, magnesium, and potassium (Bearder and Martin, 1980); and seeds, nuts, bones, muscle, and invertebrates are usually good sources of phosphorus. Primates in laboratories or zoos fulfill many of their mineral requirements from specific mineral additions to diets containing ingredients that would otherwise be nutritionally incomplete. Browse (fresh or dried foliage) offered to captive primates can also contribute to the dietary supply of essential minerals. Quantitative mineral requirements of nonhuman primates are poorly defined, but proposed minimal dietary concentrations are presented in Chapter 11. Mineral concentrations in foods and feedstuffs commonly used in feeding captive primates are presented in Chapter 12. The bioavailability of minerals in foods (Ammerman et al., 1995) for nonhuman primates has not been studied, but bioavailability of many minerals for many other species is less than 100%, compared with highly bioavailable standards. For example, calcium bound to oxalate and phosphorus bound to phytate appear to be largely unavailable to simple-stomached animals. Spinach contains appreciable calcium, but most is bound to oxalate, so only about 5% is available to humans (Heaney et al., 1998). The mineral concentrations in foods might require interpolation when diets are being formulated to ensure that requirements for minimal available nutrients are met. Some mineral elements, such as cadmium, lead, and antimony, are of concern because of their potential toxicity. Primate research on this subject is sparse, although some clinical reports might contribute to definitions of lead tolerance (Zook and Paasch, 1980), and the effects of different lead intakes and low or normal dietary calcium concentrations upon chromosomal abnormalities in lymphocytes have been studied in cynomolgus (Macaca irus) monkeys (Deknudt et al., 1977). Dietary cadmium intake and its

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 effects upon serum thyroxine and triiodothyronine concentrations have been studied in rhesus monkeys (Mehta et al., 1986), and chronic cadmium poisoning has been induced in cynomolgus monkeys as a model of human itai-itai disease (Umemura, 2000). The publication MineralTolerances of Domestic Animals (National Research Council, 1980) provides information on the toxicity of specific minerals in diets for farm animals, pets, and some laboratory animals. Interactions of minerals with each other and with other nutrients have been fairly well studied in laboratory and domesticated animals (Underwood, 1981; Mertz et al., 1986, 1987; National Research Council, 1995). For example, in rats, calcium absorption decreases in the presence of high dietary phosphorus (Schoenmakers et al., 1989); this relationship may be affected by magnesium intake (Bunce et al., 1965). In humans, long-term calcium supplementation did not adversely affect iron status as assessed by plasma ferritin concentrations in one study (Minihane and Fairweather-Tait, 1998), but other studies demonstrated a short-term reduction in iron absorption as dietary calcium increased (Cook et al., 1991; Hallberg et al., 2000). For many years, salt mixes (mineral premixes of published composition) have been successfully used in laboratory primate diets (Hegsted et al., 1941; Hayes et al., 1980; Hawk et al., 1994). This information has been used to formulate commercial primate biscuits or pellets that appear to meet the mineral requirements of nonhuman primates. It is important to note that substantial deviations in mineral concentrations have been found among primate diets produced by different manufacturers, and between manufacturers’ published specifications and the mineral concentrations found by analysis (Wise and Gilburt, 1981). MACROMINERALS Calcium and Phosphorus The skeleton and teeth of mammals contain over 98% of the body’s calcium (Ca) and about 80% of the body’s phosphorus (P). Because of the relative mass and density of bones and teeth, Ca and P are required in large amounts, relative to other macrominerals. In addition to their critical structural role, Ca and P are essential for normal cellular communication and modulation. Calcium binds to many cellular proteins, resulting in their activation. The functions of the proteins are diverse and include cell movement, muscle contraction, nerve transmission, glandular secretion, blood clotting, and cell division (Weaver and Heaney, 1999). When a cell, such as a muscle fiber, receives a nerve stimulus to contract, Ca channels in the plasma membrane open to admit a few Ca ions from the cytosol. The ions bind to an array of intracellular activator proteins that release a flood of Ca from intracellular storage vesicles (sarcoplasmic reticulum in the case of muscle). The increase in cytosolic Ca concentration leads to activation of the contraction complex. Troponin c, after binding Ca, initiates a series of steps leading to muscle contraction. Another Ca-binding protein, calmodulin, has many secondary messenger functions, one of which is to activate the enzymes that break down glycogen. Thus, Ca ions both trigger muscle contraction and fuel the process. P is widely distributed in soft tissue and is required to drive multiple metabolic and energy reactions within and between cells. As phosphate, it helps to maintain osmotic and acid-base balance. As a component of deoxyribonucleic and ribonucleic acids, P is involved in cell growth and differentiation. As a phospholipid, it contributes to cell-membrane fluidity and integrity. Through involvement in creatine phosphate, adenosine triphosphate (ATP), and other phosphorylated compounds, P plays a vital role in energy transfer and use, gluconeogenesis, fatty acid transport, amino acid and protein synthesis, and activity of the sodium-potassium pump (Knochel, 1999). Short-term, moderate inadequacies in Ca intake are modulated by skeletal reserves and cause few signs of deficiency, particularly in adults. However, rapidly growing young animals might exhibit hypocalcemia, hypercalciuria, and increased plasma alkaline phosphatase activity. Chronic, long-term dietary Ca deficiency can result in retarded growth and rickets in the young and osteomalacia and osteoporosis in adults. Early responses to low dietary P include a decline in plasma inorganic P concentration and an increase in plasma alkaline phosphatase activity. If the deficiency is sufficiently severe or prolonged, abnormalities of the bones and teeth can be expected, growth will slow in the young, and appetite will be depressed; and pica (depraved appetite) will be seen in some domestic animals (Underwood and Suttle, 1999). An early study of Ca metabolism in rhesus macaques concluded that a growing 3-kg monkey requires Ca at 150 mg·BWkg-1·d-1 (Harris et al., 1961). In later studies with rhesus macaques, feeding a diet containing 0.15% Ca (equivalent to Ca at 150 mg·BWkg-1·d-1 for 2- to 3-kg animals) resulted in osteoporosis (Griffiths et al., 1975). Fluoride added to such a diet at 50 ppm prevented osteoporosis by reducing bone growth rate and resorption, resulting in bones with normal density, but the added fluoride interfered with mineralization of osteoid, and led to osteomalacia. When diets containing 0.32% Ca were fed to young cynomolgus monkeys for about 3½ years, motor neuron damage resulted; the damage was exacerbated by addition of aluminum and manganese to the diet (Garruto et al., 1989). The minimal dietary Ca concentration of 0.5% (air-dry basis) previously recommended (National Research Coun-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 cil, 1978) should be sufficient to support maintenance of adult nonhuman primates, assuming appropriate P and adequate vitamin D consumption or sufficient ultraviolet B (UVB) exposure. When expressed on a dietary dry matter (DM) basis, this estimated Ca requirement would be 0.55% (assuming 10% moisture in the air-dry diet). Lactation can be expected to increase the demand for Ca, particularly in mothers with more than one offspring, but bone reserves and increased food intake during lactation can compensate to some extent in the short term. With proper diet, at least partial postweaning restoration of bone Ca reserves (depleted by lactation) has been seen in humans (Prentice, 2000). Although juveniles of the larger primate species grow relatively slowly, compared with the young of many other mammals, the period of growth will probably raise the requirement for both Ca and P over maintenance requirements. Furthermore, the growth of small species, such as marmosets and tamarins, is sufficiently rapid that Ca and P requirements will increase. Dietary protein and sodium concentrations can influence requirements for Ca. High sodium intakes result in higher sodium concentrations in glomerular filtrate, competing with Ca for renal tubular reabsorption (Nordin et al., 1993). In humans, increased Ca excretion occurs when protein and sodium intakes are high (Heaney and Recker, 1982; Matkovic et al., 1995; Nordin, 1997). The negative Ca balance associated with high protein intakes might be due to increased glomerular filtration and decreased renal Ca reabsorption as end-products of protein metabolism, such as phosphate and possibly sulfate, complex Ca in the renal tubules and carry it out in the urine (Johnson et al., 1970; Spencer et al., 1978; Nordin, 1997). However, Grynpas et al. (1993) found that free-ranging rhesus monkeys from the Caribbean Primate Research Center that had been provisioned with either a 15% or a 25% protein extruded diet for most of their lives were not different in vertebral mineral concentrations, as determined by neutron activation analysis. Calcium concentrations were 0.90% in the lower-protein diet and 1.00 to 1.15% in the higher-protein diet, as fed. Heaney (1998) argued that if Ca intake is sufficiently high, excessive dietary protein will not result in bone loss; he contended that the ratio of dietary Ca to protein is more important than the absolute dietary concentration of Ca. A ratio that was proposed as adequate to prevent bone loss was about 20 mg of dietary Ca per gram of dietary protein, although the suitability of that ratio has not been experimentally confirmed in nonhuman primates. In any case, it is likely that Ca requirements of nonhuman primates will vary to some extent with dietary habits and composition of the diet, as they do in humans (Nordin, 2000). A diagnostic distinction between protein-calorie malnutrition and Ca deficiency was noted when cadmium was administered to rhesus macaques. Metallothionein (MT) production was induced, but the major liver isoform was MTc in protein-calorie malnourished monkeys and MTb in Ca-deficient monkeys (Nath et al., 1987). As early as 1957, a relationship of bone loss, a decrease in effective Ca use, and restricted physical activity in humans was reported (Whedon and Shorr, 1957). Physical restriction of Macaca nemestrina also increased Ca excretion (Pyke et al., 1968). Osteoporosis and osteoarthritis might be more common in chronically physically restricted primates (DeRousseau, 1985a,b; Pritzker et al., 1985; Rothchild and Woods, 1992), although some authors question the occurrence or incidence of osteoarthritis in nonhuman primates (Ford et al., 1986; Jurmain, 1989; Chateauvert et al., 1990; Sokoloff, 1990). When over 1,500 nonhuman-primate skeletons of 29 species were examined, osteoarthritis was more prevalent in captive animals (presumably physically restricted) than in wild animals (Rothschild and Woods, 1992). Eaton and Nelson (1991) have proposed that Ca intakes of humans living at the end of the Stone Age were twice those of contemporary humans, and their physical exertion was greater than at present. Skeletal remains suggest that Stone Age humans developed a greater peak bone mass and experienced less age-related bone loss than 20th Century humans. Many of the diets fed to captive nonhuman primates comprise mixtures of nutritionally complete biscuits or pellets, fruits, vegetables, browse, and insects. However, given the opportunity for free choice among such an assortment of foods, the likelihood of Ca deficiency is real. With the exception of primate biscuits and some green, leafy vegetables, most of those foods are inadequate sources of Ca. In spinach, much of the Ca is bound to oxalate and unavailable. Sprinkling on Ca supplements does not necessarily prevent Ca deficiencies that might appear when mixed diets are fed. That practice was attempted with two species of lemurs (Lemur catta and L. variegatus) at the Cincinnati Zoo, but much of the supplement did not adhere to the foods; signs of nutritional secondary hyperparathyroidism were seen, including hyperphosphatemia, hypocalcemia, increased alkaline phosphatase activity, impaired mobility, bowing of the long bones, poorly mineralized skeleton, and soft tissue mineralization (Tomson and Lotshaw, 1978). Nursing neonatal New World and Old World primates, with presumably adequate Ca intakes from milk, presented signs of abnormal Ca status (Ullrey, 1986; Morrisey et al., 1995). Responses to UVB exposure or to intramuscular vitamin D injections made it look as though vitamin D supplies were inadequate to support normal Ca absorption and metabolism. The milk of species that have been examined is low in vitamin D; if solid food containing vitamin D is not consumed in sufficient amounts or if there is no UVB exposure, absorbed Ca might be inadequate to meet tissue needs. Because of solar UVB exposure, that is proba-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 bly not a problem in nursing wild primates. In humans, if infant formula thickened with an indigestible carbohydrate, such as locust bean gum, replaces mother’s milk, Ca availability is reduced compared with that in unthickened infant formula or formula thickened with a digestible carbohydrate, such as pregelatinized rice starch (Bosscher et al., 2000). Further, it has been shown that the Ca in fortified soy milk is absorbed at only 75% of the efficiency of Ca in cow’s milk (Heaney et al., 2000). Tarsiers held at the National Zoological Park were fed crickets exclusively, a particularly poor calcium source (see Chapter 12). Repeated breeding failures were experienced until a high-Ca (8%) cricket diet was made available to the free-ranging crickets in the tarsier enclosure (Roberts and Kohn, 1993). Although the Ca concentrations in cricket tissues were unchanged, the residue of high-Ca diet in the cricket gut supplied sufficient Ca to meet tarsier needs. Successful births and weanings were observed regularly after that dietary change was made. Mineral mixes (salt mixes) historically used in diets for laboratory primates appear to have provided about 0.2% of available (non-phytate) P in the diet. When they were combined with the P in food ingredients (those furnishing protein tending to be richer in P), available P concentrations (air-dry basis) in formulated diets were about 0.3-0.4% and appeared to be adequate (National Research Council, 1978). When the lowest National Research Council (1978) value is expressed on a DMbasis, the estimated dietary available P requirement would be 0.33% (assuming 10% moisture in the air-dry diet). Total P requirements in natural-ingredient diets are generally higher because the bioavailability of P tends to be less than that in inorganic P sources, particularly when associated with phytate in commonly used cereals and oil-seed meals. P bioavailability studies have not been conducted with nonhuman primates, but P bioavailability values have been reported for feed ingredients fed to pigs (National Research Council, 1998). Phytate P is believed to be only slightly available or totally unavailable to non-ruminants. In ruminants, the phytase activity of ruminal microorganisms renders nearly all of the phytate P available for absorption (National Research Council, 2001). Whether this would be true for microorganisms in the complex stomach of the Colobinae has not been established. Provision of a dietary Ca:P ratio between 1:1 and 2:1 has been emphasized in setting Ca and P requirements in the past. However, it has been shown in the pig that inorganic P, added to the diet to maintain a particular Ca:P ratio, will lower use of phytate P, and phytate lowers use of Ca (Underwood and Suttle, 1999). Furthermore, excess Ca lowers P absorption (National Research Council, 1998). Thus, it might be important to consider the Ca and P concentrations in diets used in defining Ca and P requirements and the effects of phytate on requirement estimates. In practical diet formulations for nonhuman primates, the addition of stable phytases might increase phytate P availability, on the basis of studies with other species (Cromwell et al., 1995). However, the choice of phytase, and its resistance to the heat and pressure of food processing, will influence its effectiveness (National Research Council, 1998). Magnesium It has been said that about 70% of the body’s magnesium (Mg) of ruminants is in the skeleton (Todd, 1969), although Shils (1999) has stated that bone contains about 53% of the Mg in the adult human body. Mg is a component of regulatory enzymes and enzyme systems, and over 300 essential metabolic reactions involving Mg have been identified (Shils, 1999). Mg helps to regulate muscle and nerve function and influences the metabolism of protein, carbohydrate, fat, and nucleic acids. ATP exists in all cells primarily as MgATP, and the complex plays a central role in many of these reactions. Cyclic adenosine monophosphate (cAMP), formed from MgATP and adenylate cyclase, is involved in the secretion of parathyroid hormone (PTH), and PTH exerts some of its physiologic effects through the formation and actions of cAMP. That role of Mg might partially explain the hypocalcemia seen in Mg-depleted rhesus monkeys, humans, calves, sheep, dogs, and pigs (Dunn, 1971). Studies of the effects of dietary calcium, phosphorus, or vitamin D on absorption and retention of Mg in humans have produced equivocal results (Shils, 1999). Long-term balance studies with healthy adults generally suggest that increased calcium intakes do not substantially influence Mg absorption or retention. Some reports indicated that high phosphorus intakes decreased Mg absorption, whereas others did not. Some patients, but not others, with impaired calcium absorption and both osteomalacia and osteoporosis showed improvement in Mg absorption when given vitamin D or calcitriol orally. Increased intakes of Mg have been associated with decreased calcium absorption or no effect. Signs of Mg depletion in humans include neuromuscular, gastrointestinal, and cardiovascular changes (Shils, 1999). Tremor and muscle fasciculations are seen; anorexia, nausea, and vomiting can be experienced; and in severe Mg depletion, there can be electrocardiographic changes compatible with hypokalemia or hypocalcemia. In only 4 weeks, rhesus monkeys fed a diet containing Mg at 3 mg·100 g-1 (0.003%, air-dry basis) (Dunn, 1971) exhibited hyperirritability associated with hypomagnesemia, whereas monkeys fed a control diet containing Mg at 102 mg·100 g-1 (0.1%, air-dry basis) did not. Affected macaques fed additional Mg (33% of control concentrations, equivalent to 0.034% of the diet on an air-dry basis)

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 returned to normal. Thus, it would appear that a Mg concentration of 0.04% in dietary DMshould support maintenance requirements when dietary calcium and phosphorus concentrations are relatively low. However, few studies of Mg requirements of nonhuman primates have been reported, and higher dietary concentrations of calcium and phosphorus have been shown to elevate the Mg requirements of some other species (Underwood and Suttle, 1999). Examination of natural-ingredient diets for primates and other mammals, with their higher Ca and P concentrations, indicates that 0.08% Mg is more likely to be a consistently adequate dietary level. Thus, the recommendation in Table 11-2 reflects a presumed adequate dietary level of 0.08%, whereas the estimates of 0.04 to 0.074% Mg in Table 11-1 are minimum requirements. Mg concentrations in the milk of rhesus monkeys are 32.9 ± 3 µg·ml-1 compared with 49.6 ± 12.1 µg·ml-1 in colostrum (Lonnerdal, et al., 1984). Formulas for artificial rearing should contain supplemental sources of this essential nutrient. Potassium Potassium (K) is usually found in high concentrations in plant and animal tissue. Concentrations over 3% are typical in plant DM, and deficiencies are rare. K helps to regulate tissue turgidity of plants; in animals, K is the major intracellular cation and is largely responsible, with sodium and chloride, for the maintenance of osmotic pressure and acid-base balance. A K concentration of 0.24-1.1% in dietary DMappeared to support maintenance in baboons (Hummer, 1970). However, studies with other species using natural-ingredient diets suggest that minimum K requirements may be 0.4% or more of dietary DM, and may depend upon species, life stage, and diet composition (Underwood and Suttle, 1999). Thus, recommendations in Table 11-2 reflect the higher concentrations reported to be adequate with natural-ingredient diets. In rhesus monkeys, Lonnerdal et al. (1984) found that K is higher in colostrum (367 µg·ml-1) than in milk expressed after 30 days of lactation (260 µg·ml-1). Sodium The major extracellular cation in mammals is sodium (Na). Thirst and total body water are regulated by dietary Na. Na thirst has been identified in a number of mammal species. Natural diets usually contain adequate supplies of Na, although strict herbivores might be at risk for Na deficiency. Depending on soil and environmental characteristics, plants might be poor sources of Na or phosphorus. The influence of Na on blood pressure has been extensively studied in primates because of the high incidence of hypertension in Western human populations. Increasing dietary sodium chloride (NaCl) concentrations to 3-6% increased systolic and diastolic blood pressure in African green monkeys, spider monkeys, and hamadryas baboons. Rhesus monkeys, however, failed to show an increase in blood pressure under the same conditions over a 6-week period (Srinivasan et al., 1980, 1984). The rhesus monkeys expressed a distaste for the high-NaCl diet, and a decline in body weight was associated with increasing dietary NaCl. Diets containing 0.25-0.65% Na appear to support maintenance of nonhuman primates, but are likely to exceed minimum needs (Hummer et al., 1970; National Research Council, 1978). The milk of rhesus monkeys contains Na at about 171 µg·ml-1 in the first week of lactation, but milk Na appears to decline to about 90 µg·ml-1 after a month (Lonnerdal et al., 1984). Apparently female rhesus monkeys ingest more NaCl than do males when presented the opportunity (Shulkin, 1992). However, ovarian hormones do not appear to be involved in this sex difference (Krecek et al., 1972; Krecek, 1973). Chloride The major digestive chemical in gastric secretions is hydrochloric acid. With the exception of foregut-fermenting primates, the acid stomach is the first and the major organ responsible for processing feedstuffs. Chloride (Cl) is also critical (with sodium and potassium) in the osmotic regulation of cells and tissues. Hummer (1970) fed diets containing 0.27-0.62% Cl to baboons, and they appeared to support maintenance but probably exceeded minimum requirements. The lower of the previous National Research Council (1978) recommendations of 0.2-0.55% dietary Cl would be expected to be sufficient, based on comparisons with the Cl requirements of other species. Sulfur Important compounds in the diets of primates that contain sulfur (S) include biotin, thiamin, cystine, cysteine, methionine, and taurine. A frank deficiency of S in primates has not been described, although taurine deficiency may occur in neonates (Hayes, 1980). Excessive intakes of protein high in S-containing amino acids (cystine, methionine, and taurine) might exacerbate problems of renal calcium loss. TRACE MINERALS Iron Iron (Fe) is an essential component of such proteins as hemoglobin, myoglobin, and ferritin; and some enzymes require Fe as a cofactor (Fairbanks, 1999). Iron in heme

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 allows the transport of oxygen to tissues (hemoglobin), transitional storage of oxygen in tissues (myoglobin), and the transport of electrons through the respiratory chain (cytochromes). Biologic functions that depend on Fe include energy metabolism, neurotransmitter synthesis, connective tissue metabolism, immune function, thyroid hormone metabolism, and thermogenesis. Recently, Fe has been found to bind to proteins, forming transcription factors that can affect the expression of other proteins. Thus, impaired Fe status can affect the metabolism of several nutrients. Fe is present in many natural ingredients. The biologic availability of such Fe has been studied mostly in chickens and rats, and the results might not be completely applicable to nonhuman primates. Generally, the biologic availability of Fe in natural ingredients is about 40-60% (Henry and Miller, 1995). Iron is a substantial contaminant of most sources of dicalcium phosphate, and this makes it difficult to reduce the Fe concentration of natural diets. Ferrous sulfate is customarily used as the standard in bioavailability studies and is usually assigned an Fe bioavailability of 100%. Ferrous sulfate and ferrous carbonate are the usual sources of Fe added to commercial diets, but various Fe sources are used in purified diets. Fe in ferrous sulfate, ferric chloride, ferric citrate, and ferric ammonium citrate has high biologic availability for several species. Bioavailability of Fe in ferrous carbonate and reduced iron varies with source and possibly particle size. The Fe in ferric oxide, which is occasionally added to feed as a coloring agent, is virtually unavailable (Henry and Miller, 1995). Fe absorption has been studied extensively in humans. Absorption is enhanced by the presence of ascorbic acid in the diet. Meat, fish, and chicken also enhance the absorption of Fe, whereas polyphenols, such as are found in tea and leaves, seem to inhibit absorption (Yip and Dallman, 1996; Zijp et al., 2000). An algorithm has been developed for calculating absorption and bioavailability of Fe in a number of human foods, and concentrations of phytate phosphorus and Fe-binding polyphenols in foods used in human and some nonhuman-primate diets have been published (Hallberg and Hulthé n, 2000). There are a number of nutritionally significant interactions of Fe with other minerals, although few of these have been studied in nonhuman primates. Dietary concentrations of calcium, copper, manganese, and zinc may influence Fe absorption. Plasma concentrations of chromium and manganese may influence Fe transport. Tissue concentrations of copper and zinc may influence cellular Fe uptake, and tissue concentrations of chromium, copper, and zinc may influence the size and mobility of Fe stores (O’Dell and Sunde, 1997) Fe absorption from infant formulas has been determined in infant rhesus monkeys and was found to be 20-30% from milk-based and soy-based formulas (Davidson et al., 1990; Lonnerdal et al., 1999). The effect of various dietary factors on Fe absorption has not been studied extensively in primates, but the rhesus monkey has been used as a model to study the effect of lactoferrin, a major Fe-binding protein in the milk of rhesus monkeys (Davidson and Lonnerdal, 1986) and in human milk, on Fe uptake from milk and milk-replacers (Davidson et al., 1990). It appears that a unique receptor-mediated mechanism in the small intestine facilitates the uptake of Fe from lactoferrin (Davidson and Lonnerdal, 1988, 1989). Removal of phytate from soy in a soy-based formula appeared to have little effect on Fe absorption in infant rhesus monkeys (Lonnerdal et al., 1999). Young rhesus monkeys fed a soy protein diet were found to be anemic after 2-7 months, and Fe absorption from this diet was lower than from a casein diet (Fitch et al., 1964). The diet was baked, however, and both the heat treatment and the addition of baking soda (pH) might have affected Fe bioavailability. Adequate Fe status is needed for normal hematologic characteristics. Age-related changes in hematologic measures have been described in infant rhesus monkeys (Martin et al., 1973). Packed cell volumes were high at birth, declining during the first 2 post-natal weeks. Proportions of neutrophils were high at birth and declined with age, whereas proportions of lymphocytes were low at birth but rose rapidly to adult values. Proportions of eosinophils were low at birth, increasing to adult values during the first post-natal month. Total leukocyte counts were essentially constant from birth to 2 years. The consequences of impaired Fe status on such hematologic measures as hemoglobin, hematocrit, MCV, transferrin saturation, and serum iron have been described in rhesus macaques (Wolcott et al., 1973; Mandell and George, 1991; Bicknese et al., 1993; Sreeramulu et al., 1994; Kriete et al., 1995) and cynomolgus macaques (Giuletti et al., 1991). When 30-70% of blood volume was withdrawn from adult (6.5- to 10-year-old) nonpregnant female rhesus monkeys over a long period (5-10% per week), anemia developed (Mandell and George, 1991). No firm indices for the identification of anemia or Fe deficiency have been established for nonhuman primates, and indices for human subjects are usually used. Results of a study in which dietary Fe deficiency was induced in rhesus monkeys suggest that serum ferritin is not a good indicator of Fe status in this species (Sreeramulu et al., 1994). The assay used, however, might not have recognized rhesus monkey ferritin, which is necessary if commercially available kits for assay of serum ferritin in humans are to be useful in measuring the response to dietary Fe intake in rhesus infants (Lonnerdal et al., 1996). The effect of transferrin polymorphism on total iron-binding capacity has been examined in rhesus monkeys, and it has been suggested that different types of transferrin (genotypes) affect fertility and growth of offspring (Smith, 1982).

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Fe-deficiency anemia has been produced in rhesus monkeys (Wolcott et al., 1973; Mandell and George, 1991). Weanling rhesus monkeys (3 months old) were found to be less Fe-deficient if they were raised in the nursery than if they were mother-reared (Bicknese et al., 1993), and multiparous dams were more likely to have Fe-deficient weanlings than primiparous dams. Formula-fed infant rhesus monkeys have been shown to develop Fe-deficiency anemia at the age of 3-5 months even if the formula was fortified with Fe (Kriete et al., 1995). Another study, however, showed no anemia at that age in infant rhesus monkeys fed Fe-fortified formula exclusively from birth (Lonnerdal et al., 1999). Differences in Fe endowment at birth, growth rate, number of bleedings, and Fe concentration in the formulas used might explain the disparate findings. Fe deficiency has also inadvertently been produced in monkeys fed diets low in protein (Sood et al., 1965). The Fe requirements of nonhuman primates have not been well established. Infant rhesus monkeys fed infant formula exclusively up to 5.5 months of age showed no signs of anemia (Lonnerdal et al., 1999). The formula contained Fe at 12 mg·L-1, and average consumption was 400 ml·d-1, so it appears that an Fe intake of about 5 mg·d-1, or about 3-10 mg·BWkg-1·d-1, given in formula meets the Fe requirement during infancy. Rhesus milk contains Fe at about 1.1-1.8 mg·L-1 during the first month of lactation and slightly less after that (Lonnerdal et al., 1984). Assuming that milk intake by nursed rhesus infants is similar to that by formula-fed infants, the “true” Fe requirement might be substantially lower than that estimated for formula-fed infants. Fe-deficiency anemia has been produced in adult female baboons (Papio spp.) (Huser et al., 1967) and newborn squirrel monkeys (Saimiri sciureus) (Amine et al., 1972), and an Fe-deficient diet developed for 4-year-old capuchins (Cebus albifrons) produced a negative Fe balance (Wolfe et al., 1989). But the minimal Fe requirement for those species cannot be deduced from the studies. Although Fe-deficiency anemia is of concern in most colonies, it should be recognized that giving primates high-Fe diets can result in Fe overload. Hemosiderosis has been observed in lemurs in captivity (Gonzales et al., 1984); signs were most pronounced in the black lemur (Eulemur macaco) and least in the ring-tailed lemur (Lemur catta). It was later found that all 49 lemurs in the colony that had been necropsied during a 10-year period had hemosiderosis and that severity increased with age (Spelman et al., 1989). A suggested explanation was that captive lemurs received diets high in Fe (commercial monkey diets) and in ascorbic acid (citrus fruits), which enhanced Fe absorption, while they received few inhibitors of Fe absorption, such as tannins (polyphenols), that are constituents of the diet consumed in the wild (leaves, fruits, and bark). Because hemosiderosis can lead to liver and kidney disease, the authors suggested that lemur diets should be modified to reduce this risk. Marmosets (Callithrix jacchus), too, develop hemosiderosis in captivity; it is also believed to be caused by high-Fe diets (Miller et al., 1997). When a diet lower in Fe (100 mg·kg-1) was fed, liver Fe was only one-tenth that of animals fed a high-Fe diet (500 mg·kg-1), demonstrating that lowering the Fe content of the monkey diet can reduce the risk of hemosiderosis. Experimental hemosiderosis has been induced in rhesus monkeys by injections of Fe dextran (Nath et al., 1972). Cebus monkeys, loaded with Fe dextran, were found to be a useful model for study of the effectiveness of Fe chelators in Fe overload. Desferroxamine, administered intramuscularly, and desferrithiocin, administered intramuscularly or orally, were found to significantly promote Fe excretion (Wolfe et al., 1989). To test new orally active Fe chelators, marmosets (Callithrix jacchus) have been Fe-overloaded by intraperitoneal injections of Fe hydroxide polyisomaltose (Sergejew et al., 2000). Copper Copper (Cu) is associated with a number of proteins, including many important enzymes. The Cu-containing enzymes are commonly divided into amine oxidases, ferroxidases, cytochrome c oxidase, dopamine ß-hydroxylase, superoxide dismutases, and tyrosinase. The known Cu-binding proteins are metallothionein, albumin, transcuprein, and blood-clotting factor V (Turnlund, 1999). Cytochrome c oxidase might be the most important enzyme in the mammalian cell because it is the terminal link in the mitochondrial electron-transport chain and regulates the formation of ATP. Other Cu-containing enzymes are part of the body’s antioxidant defense system, are involved in melanin formation, and function in the cross-linking of collagen and elastin during formation of connective tissue (Linder, 1996). In studies of the development of age-related macular degeneration in elderly (20 years old and older) rhesus macaques, monkeys with diagnosed drusen (hyaline excrescences in the basal choroid layer of the eye) exhibited alterations in concentrations and activities of the free-radical defense system, particularly of enzymes associated with Cu (Olin et al., 1995b). Cardiovascular defects in Cu deficiency include weakened heart and blood-vessel structure, impaired use of energy by the heart, reduced ability of the heart to contract, altered ability of blood vessels to grow and regulate their diameter, and altered structure and function of the blood cells. Those defects result principally from impaired effectiveness of the enzymes that are Cu-dependent (Saari and Schuske, 1999). Copper is usually added to manufactured feeds in the form of cupric sulfate, CuSO4, a form that is highly bioavailable. Cupric carbonate, CuCO3, a form sometimes used in rations, is intermediate in Cu bioavailability. Copper in

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 cupric oxide, CuO, is absorbed very poorly by most species (Baker and Ammerman, 1995a). However, no studies on the biologic availability of Cu in these compounds have been conducted with nonhuman primates. Excessive dietary zinc can lead to Cu deficiency in a number of mammalian species (Baker and Ammerman, 1995a). That could be important in infant primates raised with their mothers in breeding colonies in galvanized cages, such as corncribs. Under such circumstances, depigmentation of the hair (achromotrichia), alopecia, weakness, and microcytic anemia were observed in infants of rhesus (Macaca mulatta) mothers fed commercial diets but not in the adults. The achromotrichia was described as development of a steel-gray hair coat. Serum zinc was increased, and serum Cu decreased. Animals raised in stainless-steel cages and fed the same diet did not develop the syndrome. High intakes of zinc from the galvanized caging apparently induced a Cu deficiency in the infant animals (Stevens et al. 1977; Obeck, 1978; Wagner et al., 1985). Stevens et al. (1977) and Wagner et al. (1985) gave no details on diet composition. Obeck (1978) reported that the commercial diet contained zinc at 34 mg·kg-1 and Cu at 10 mg·kg-1, an insufficient amount of Cu to prevent the syndrome. Higher concentrations were not evaluated, so it is not known whether the effect of galvanized caging on infant rhesus can be overcome by increasing the Cu in rations consumed mostly by the mothers. Hypocupremia, sider-oblastic anemia, leukopenia, and neutropenia were observed in an adolescent human who ingested excessive amounts of zinc (Porea et al., 2000). Low Cu status in infant rhesus monkeys also has been induced by feeding a commercial canned infant liquid formula designed for human infants (Lonnerdal et al., 2001). Information on the form of Cu in the liquid formula and the heat treatment to which it was subjected were not revealed by the manufacturer of the product. However, the Cu concentration was described to be comparable to that in other commercial products tested at the same time. The researchers speculated that the conditions of heat processing might have reduced Cu availability, thereby inducing a Cu deficiency. Besides hypocupremia, low serum ceruloplasmin, and low erythrocyte Cu, Zn-superoxide dismutase activity, the monkeys became anemic and had a change in hair color. Fischer and Giroux (1987) fed a specially formulated commercial type of monkey diet containing zinc at 30 mg·kg-1and Cu at 6 mg·kg-1to cynomolgus (Macaca fascicularis) monkeys. The diet was supplemented with 10 or 24 mg of zinc each day. The 10-mg zinc supplement was given to the control group to meet the nutritional requirement and compensate for zinc bound to dietary phytate. The male and female animals weighed about 3.5 and 2.7 kg and ate 120 and 90 g·d-1, respectively. Monkeys that received the 24-mg zinc supplement had higher plasma zinc, lower plasma Cu, and somewhat increased plasma cholesterol. Plasma ceruloplasmin, hematocrit, and hemoglobin were not affected. Increased plasma cholesterol is a sign of Cu deficiency in rats and humans. In this experiment, zinc supplementation appeared to impair Cu status. Adult cynomolgus monkeys weighing 4.2-4.8 kg were fed purified liquid diets containing Cu at about 0.4 mg·kg-1 of DMfor 28 weeks (Milne et al., 1981). High concentrations of ascorbic acid are known to reduce Cu use in several species (Baker and Ammerman, 1995a), so the effect of ascorbic acid was evaluated by giving animals a supplement of 1 or 25 mg of ascorbic acid per kilogram of body weight. There was relatively little change in serum Cu or ceruloplasmin (a Cu-containing enzyme) concentrations, but there was a significant increase in serum cholesterol rising from 80 mg·dl-1 to 108 mg·dl-1. At the end of 28 weeks, approximately 2 mg of Cu·kg-1 of DMwere added to the diet, furnishing a total Cu concentration of about 2.5 mg·kg-1 of dietary DM. After 4 weeks on this Cu-supplemented diet, serum cholesterol concentrations of animals receiving the higher amounts of ascorbic acid were elevated above those of animals receiving the lower amounts of ascorbic acid, suggesting that ascorbic acid may have interfered with Cu absorption. Available data are not sufficient to establish a Cu requirement. Cu at 12-20 mg·kg-1 in commercial diets seems to be sufficient under most conditions (Knapka et al., 1995). However, it might not be sufficient for breeding colonies exposed to high concentrations of zinc from galvanized caging. Cu from CuSO4 at about 2 mg·kg-1 of diet was sufficient to reverse an increase in cholesterol in adult cynomolgus monkeys (Milne et al., 1981). Cu at 15 mg·kg-1 of dietary DMshould be sufficient to meet the dietary needs of animals not exposed to excessive dietary zinc. Manganese Manganese (Mn) is a constituent of several metalloenzymes, such as arginase, pyruvate carboxylase, glutamine synthetase, and Mn-superoxide dismutase. Such enzymes as oxidoreductases, lyases, ligases, hydrolases, kinases, decarboxylases, and transferases can be activated by Mn, but most of these can also be activated by other cations, particularly magnesium (Nielsen, 1999). Manganous sulfate and manganous oxide are the most common supplemental forms of Mn used in animal feeds. Compared with manganous sulfate, the bioavailability of manganese oxide in chicks was 60-77%, and that of manganous carbonate was 32-36% (McDowell, 1992). Mn deficiency has been demonstrated in a number of avian and mammalian species. Female rhesus (Macaca mulatta) monkeys fed a semisynthetic diet containing Mn at 0.5 mg.kg-1 were mated and maintained on this low-Mn diet throughout their pregnancy. Their infants were

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 continued on the same diet, and their behavior was compared with that of animals fed a diet that was similar but contained Mn at about 40 mg·kg-1. Mothers fed the deficient diet had normal pregnancies. The infants had normal birth weights and grew normally on the low-Mn diet. Behavioral development was evaluated with a series of tests. Infants fed the low-Mn diet had abnormally strong clasping and clinging responses, but their righting responses, which required release from clasping, were inadequate (Riopelle and Hubbard, 1977). Signs of Mn deficiency other than the changes in behavioral development have not been described in nonhuman primates. Typical commercial diets, which appear to be adequate, contain Mn at 70-100 mg·kg-1 (Knapka et. al, 1995). Those concentrations are probably far in excess of the minimal requirement, which is 10 mg·kg-1 for rats and 2-20 mg·kg-1 for swine in various stages of their life cycle (National Research Council 1995, 1998). The level of Mn in the control diet used by Riopelle and Hubbard (1977) would provide about 44 mg·kg-1 of dietary DMand probably exceeds primate available Mn requirements, as well. Zinc Zinc (Zn) is the most abundant of intracellular trace elements and is involved in structural, catalytic, and regulatory roles. Loss of Zn from biomembranes, as a consequence of Zn deficiency, can result in increased susceptibility to oxidative damage, structural strains, and alterations in specific receptor sites and transport systems (King and Keen, 1999). Over 200 Zn enzymes with diverse functions have been found, and Zn is involved in the metabolism of carbohydrate, protein, lipids, and nucleic acids (DNA and RNA polymerase and thymidine kinase). Extracellular superoxide dismutase activity in primates is affected by dietary Zn intake (Olin et al, 1995a). Zn also serves as a structural part of several important cellular constituents, such as transcription factors. In so-called zinc-finger structures, Zn is involved in gene expression at a very fundamental level. Growth, reproduction (pregnancy outcome), bone formation, immune function, skin integrity, morbidity, appetite, cognitive function, and behavior have been shown to be impaired in Zn deficiency in nonhuman primates and in humans. Zn deficiency affects embryogenesis, resulting in malformations, stillbirths, abortions, and smaller than normal offspring (King and Keen, 1999). Although Zn deficiency affects organisms in many ways, some might be due to the effects of Zn deficiency on cytokine synthesis and metabolism, particularly Tumor Necrosis Factor-a (TNF-a) and interleukin-2. Cell cycle events and apoptosis (programmed cell death) are affected by Zn nutriture. Zn is usually added to commercial diets as zinc sulfate, ZnSO4; zinc oxide, ZnO; or zinc carbonate, ZnCO3. The Zn in ZnSO4 and ZnCO3 has high biologic availability in livestock. In some earlier studies, Zn in ZnO was demonstrated to have high biologic availability, but more recent reports indicated a biologic availability of about 50% (McDowell, 1992; Baker and Ammerman, 1995b). A number of factors can affect Zn availability. Diets high in wheat bran lowered Zn concentrations in the serum and bone of male (but not female) baboons, despite a low phytate:Zn molar ratio and high Zn intake (Kriek et al., 1982). Dietary phytate, which can be present in significant amounts in oilseeds and cereal grains, markedly decreases the absorption of Zn in chicks, rats, and swine. High dietary calcium exacerbates the effect. The effect can be overcome by feeding higher concentrations of Zn (hence a high Zn requirement will be observed) or by the concurrent feeding of some, but not all, chelating agents (Baker and Ammerman, 1995b). Proprietary products containing Zn chelates, or other organic complexes containing Zn, are sometimes used in diets to ensure good absorption. Diets based on soy protein have been used in studies of experimental Zn deficiency in primates because soy-protein sources usually contain enough phytate to inhibit Zn absorption (Lonnerdal et al., 1988). When phytate was removed or reduced in the soy-protein diet, Zn absorption by infant rhesus monkeys increased significantly (rising from 27% to 45%) (Lonnerdal et al., 1988, 1999), to a point similar to that of Zn absorption from milk-based formulas (46%). Zn absorption from monkey milk has been shown to be about 54% (Lonnerdal et al., 1988). Absorption of Zn from a formula based on casein hydrolysate was lower than that from a regular milk formula, but the presence of a soy-protein source reduced Zn absorption further (Rudloff and Lonnerdal, 1992). It has been suggested that iron can interfere with the absorption of Zn (Solomons and Jacob, 1981). The interaction has been demonstrated in humans when high amounts of iron were given with Zn at a ratio of 25:1 in a water solution but not when iron and Zn were given in this ratio in a meal (Sandstrom et al., 1985). Studies in pregnant and lactating rhesus monkeys showed no negative effect of iron supplementation (iron at 4 mg·BWkg-1·d-1) on Zn absorption when the diet contained Zn at 4 or 100 mg·kg-1 (Lonnerdal et al., 1990b). Similarly, when infant rhesus monkeys were given infant formulas with a high iron:Zn ratio (iron at 12 mg·L-1 and Zn at 1 mg·L-1), there was no difference in Zn absorption or retention as compared with those in infants fed formula with a lower iron:Zn ratio (1:1) (Polberger et al., 1996). Rhesus monkeys (Sandstead et al., 1978) and bonnet monkeys (Swenerton and Hurley, 1980) have been used as animal models for human Zn deficiency. In both, the Zn-deficient diets contained Zn at less than 1 mg·kg-1. Signs included anorexia, apathy, weight loss, dermatitis, reproductive failure, and lowered plasma and tissue Zn

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 concentrations. Oral supplementation with Zn rapidly reversed the signs of Zn deficiency, but Zn concentrations in hair remained low for some time (Swenerton and Hurley, 1980). Although the Zn-deficient diet was fed only during the third trimester of pregnancy, behavioral effects on the infants born to these mothers were noted: they played and explored less, associated more with their mothers, and were less active (Sandstead et al., 1978). Most of the studies cited above used diets very low in Zn (less than 1 mg·kg-1) to induce Zn deficiency. In a series of studies on rhesus monkeys, moderate or marginal Zn deficiency was produced by feeding a purified diet with Zn at 2 or 4 mg·kg-1 of diet (air dry), respectively (Golub et al., 1982, 1984a,b,c, 1990a,b, 1992, 1994, 1995, 1996a,b; Baly et al., 1984; Leek et al., 1984; Haynes et al., 1985, 1987; Keen et al., 1989, 1993; Lonnerdal et al., 1990a,b). The marginal Zn deficiency resulted in changes in activity level, taste sensitivity, and immune function but not in the more severe signs of Zn deficiency, such as anorexia, alopecia, diarrhea, and dermatitis. The Zn requirement of nonpregnant female monkeys was not determined; but when a diet with Zn at 12 mg·kg-1 air-dry diet was fed, plasma Zn remained normal, whereas it decreased when the diet contained 8 mg·kg-1 or less (Golub et al., 1982). When the diet containing Zn at 4 mg·kg-1 (air dry) was fed to pregnant females, the more severe signs of dermatitis, anorexia, and low plasma Zn were observed and suggested that the Zn requirement is higher during pregnancy. Stillbirths, abortions, and delivery complications were more frequent in the group fed the low-Zn diet. Frequent observations of reduced plasma vitamin A and iron-deficiency anemia (Golub et al., 1984b; Baly et al. 1984) indicated that impaired Zn status can affect the metabolism of other essential nutrients. Effects of the low-Zn diet were observed not only in pregnant females, but also in infants born to them, which had slower than normal growth, taste dysfunction, and reduced food intake (Golub et al, 1984b). Delayed skeletal maturation and defective bone mineralization were also observed in the infants (Leek et al., 1984). Monkeys fed the marginal-Zn diet appeared to increase Zn absorption homeostatically. Pregnant and lactating dams fed the low-Zn diet showed about 25% higher Zn absorption than control dams (Lonnerdal et al., 1990a). A similar increase in Zn absorption was found in infants born to dams fed the low-Zn diet; that suggests that the Zn status was also compromised in the offspring. The Zn requirement of infant rhesus monkeys can be estimated from the study of long-term feeding with formulas that had different concentrations of Zn (Polberger et al., 1996). Although formula containing Zn at 1 mg·L-1 resulted in signs of Zn deficiency, infants consuming formula containing 4 mg·L-1 did not show any of the signs. A Zn intake of 1.6-2 mg·d-1 or 1-1.5 mg·BWkg-1·d-1 appears to meet the Zn requirement of growing rhesus infants. Rhesus milk contains Zn at about 2-5 mg·L-1 during the first month of lactation and slightly lower concentrations (1-2 mg·L-1) after that (Lonnerdal et al., 1984). Thus, inasmuch as Zn bioavailability is high in monkey milk, lower Zn intakes than from formula are adequate for nursed infants. The complexity of assessing Zn status contributes to difficulties in establishing Zn requirements. Plasma or serum Zn concentrations are often used to diagnose Zn deficiency, but substantial decreases in those concentrations often occur only in severe deficiency (King and Keen, 1999). The “normal” mean Zn concentration in cerebrospinal fluid of rhesus monkeys (Macaca mulatta) has been reported to be 1.0 µg·dl-1 (Hambleton et al., 1981). In many of the studies of marginal or moderate Zn deficiency discussed above, plasma or serum Zn concentrations were not markedly affected. Furthermore, the use of galvanized cages has been shown to increase plasma Zn (Stevens et al., 1977) and hair Zn (Marriott et al., 1996). Thus, “normal” plasma Zn concentrations cannot be used to rule out impaired Zn status. Measurement of concentrations of Zn and metallothionein in liver biopsies might be useful in assessment of long-term Zn deprivation (Keen et al., 1988). In a study with rhesus monkeys, infants fed formula with a somewhat lower than usual Zn concentration (1 vs 4 mg·L-1) had “normal” plasma Zn concentrations, but growth and neutrophil chemotaxis were significantly reduced, and a marked increase in Zn absorption indicated impaired Zn status (Polberger et al., 1996). Zn deficiency has been produced in the squirrel monkey (Saimiri sciureus) (Macapinlac et al., 1967; Barney et al., 1967). The animals were fed a semipurified diet in which low-Zn casein was the protein source. Growth was retarded, the hair coat appeared unkempt, and some alopecia occurred. Hematologic measurements in deficient animals were unchanged. Blood albumin was moderately decreased. Zn in serum and hair was decreased in deficient animals. Thickening of the mucosa of the tongue, particularly over the anterior dorsal surface, occurred within 60 days. Parakeratosis of the tongue developed and appeared to be a unique characteristic of Zn deficiency in this species. The deficiency signs were prevented with Zn at 15 mg·kg-1 of air-dry diet. The minimal dietary requirement of Zn for squirrel monkeys has not been determined, but Zn at 17 mg·kg-1 of dietary dry matter seems to be adequate for weanling animals in the absence of dietary phytate (Barney et al., 1967). Zn deficiency also has been observed in the moustached tamarin (Saguinus mystax) (Chadwick et al., 1979). Animals were fed a commercial diet containing Zn at 150 mg·kg-1 of diet, according to the manufacturer, although this value was not confirmed by analysis. The diet was supplemented with apples and oranges. The marmosets developed alopecia on the tail, thinness of hair, open sores about the anus

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 and tail, and were generally debilitated. The lesions were reversed by adding ZnSO4·7H2O to provide Zn at 40 mg·L-1 in drinking water. The alopecia returned when the animals were given Zn at 80 mg·L-1 of drinking water, and some hair regrowth occurred when Zn in the water was returned to 40 mg·L-1. The reason for the adverse effect of the higher concentration of Zn was not apparent. Increased serum Zn has been found in Senegalese baboons (Papio papio) that were moderately sensitive to light-induced seizures. Chronic oral administration of the chelating agent, D-penicillamine, lowered serum Zn and protected against the seizures (Alley et al., 1981). Iodine Iodine (I) is a part of the thyroid hormones thyroxine (3,5,3'5'-tetraiodothyronine) and 3,5,3'-triiodothyronine (Stanbury, 1996). Thus, I plays a major role in the regulation of growth and of metabolic rate. Although it is found in generous amounts in oceans, much of the I originally present in soil has been leached from surface layers by glaciers, snow, and rain. Ocean winds carry I-bearing moisture to near-shore areas, but ancient interior soils and the plants growing on them are often I-deficient. Potassium iodide, calcium iodate, ethylenediamine dihydriodide, and pentacalcium orthoperiodate are sources of I commonly added to animal diets to prevent deficiency. All four have high bioavailability. Calcium iodate, ethylenediamine dihydriodide, and pentacalcium orthoperiodate have greater physical stability (Miller and Ammerman, 1995). Schultz et al. (1965) and Pickering (1968) reported on the uptake of radioiodine by the thyroid glands of pregnant rhesus monkeys (Macaca mulatta) and their fetuses. Fetal thyroids incorporated radioiodine more rapidly than maternal thyroids. Both maternal and fetal thyroids contained substantial I-containing thyroid hormones. Thyroidectomized infant rhesus monkeys exhibited nearly all the signs of cretinism seen in humans (Pickering and Fisher, 1953a, 1953b), but frank deficiency signs were not produced by feeding I-deficient diets. It is noteworthy that low protein concentrations (2%) in the diet of Macaca nemestrina resulted in thyroidal ultrastructural changes mimicking thyroid hypofunction induced by hypophysectomy or thyroxine administration (Worthington and Enwonwu, 1975). However, the thyroidal changes may be a consequence of tyrosine deficiency associated with low protein intake and have little relationship to the I supply. Iodine deficiency has been produced in the common marmoset (Callithrix jacchus) by feeding a diet composed of natural ingredients selected for their low I content (Mano et al., 1985). The diet furnished I at about 0.36 g·d-1. On the basis of DMintake of about 12-13 g·d-1, dietary I concentration was 0.03 g·g-1 of DM. Body weights were maintained, and there were no clinical signs of ill health. However, mean plasma thyroxine concentration declined from an original value of 140.1 nmol·L-1 to 22.4 nmol·L-1, and mean plasma thyroid-stimulating hormone concentration increased from 1.8 ng·ml-1 to 9.0 ng·ml-1. Compared with newborn offspring of control marmosets receiving a potassium iodate supplement providing I at 7.9 µg·d-1 (0.65 µg·g-1 of dietary DM), the young of I-deficient females had heavier thyroid glands and lower thyroidal I concentrations. On histologic examination, their thyroid glands exhibited hypertrophy and hyperplasia; follicular colloid was absent. The infants from first and second pregnancies were evaluated in further studies. Those of mothers fed the low-I diet had sparse hair coats but were not different from controls in body weight or skeletal development. The brain weights of deficient newborns from the second pregnancies were reduced, particularly those of the cerebellum, where brain-cell numbers were reduced. Brain-stem cell size was reduced in the cerebrum. Offspring from the second pregnancies were more severely affected than those from the first (Mano et al., 1987). Young marmosets born of mothers fed an I-deficient diet in the studies of Mano et al. (1985) were fed a deficient or a normal diet (Goss et al., 1988). They were compared with animals born of mothers fed a normal diet and themselves fed a normal diet. Marmosets from I-deficient mothers and fed the deficient diet were smaller at birth and grew more slowly; whereas those fed the normal diet were smaller at birth but exhibited compensatory growth and were of nearly normal size by the age of 1 year. The I-deficient animals did not have a typical cretin face. Specific quantitative requirements for I have not been determined. The studies with marmosets indicate that 0.03 mg·kg-1 of dietary DMis insufficient but that 0.65 mg·kg-1 is sufficient. Diets containing I at about 2.2 mg·kg-1 of dietary DM were previously deemed adequate for most growing and adult nonhuman primates (National Research Council, 1978), but this concentration appears not to have been judged a minimum requirement. Estimates of I requirements for other species reported in the National Research Council nutrient requirement series do not exceed 0.35 mg·kg-1 of dietary DM. Selenium Most of the selenium (Se) in biologic systems is in amino acid constituents of proteins. Proteins that contain Se in stoichiometric amounts are called selenoproteins; selenocysteine is the primary reactive structure in the animal selenoproteins that have been identified (Burk and Levander, 1999). A number of proteins contain Se in nonstoichiometric amounts and are called simply Se-containing proteins; this Se is often found in selenomethionine, and

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 the proportion of Se in Se-containing proteins is usually related to the relative proportions of methionine and selenomethionine. Although higher plants appear not to need Se, Se enters the food chain through plants; Se exists primarily as selenomethionine and, to a lesser extent, as selenocysteine and other sulfur amino acid analogues. Selenium concentrations in plants depend on the plant species and available Se concentrations in soil, and vary widely from deficient to toxic for animals that consume them. After absorption by animals, selenomethionine appears not to be recognized specifically as a Se compound and is metabolized in the methionine pool. When catabolized, the released Se enters regulated Se metabolism and can be incorporated into selenocysteine in selenoproteins, into Se-transport compounds of unidentified composition, or into methylated Se excretory metabolites. Selenocysteine and inorganic Se absorbed by animals also enter regulated Se metabolic pathways. Selenocysteine is degraded to selenide by selenocysteine ß-lyase, whereas inorganic Se is reduced to selenide by glutathione. Selenide can enter anabolic pathways by conversion to selenophosphate or can be methylated and excreted (Burk and Levander, 1999). Eleven selenoproteins have been identified in animals; the functions of several of them are still unknown, and apparently other selenoproteins exist. The four glutathione peroxidase selenoproteins that have been characterized use reducing equivalents from glutathione to catabolize hydroperoxides. Thus, they have been generally considered to protect cells from oxidative damage. However, their different locations and substrate specificities suggest that they can also be involved in metabolic regulation (Burk and Levander, 1999). Vitamin E functions in the protection of injury from hydroperoxides; consequently, there is an interaction between dietary needs for vitamin E and Se. Nevertheless, there is a dietary requirement for Se even if sufficient vitamin E is present (McDowell, 1992). Selenium is involved in the metabolism of thyroid hormones, and combined deficiencies of iodine and Se are more severe than a deficiency of iodine alone (Levander and Burk, 1996). Iodothyronine deiodinases are selenoproteins that catalyze the deiodination of thyroxine, triiodothyronine, and reverse triiodothyronine and thus regulate the concentration of the active hormone triiodothyronine. Thioredoxin reductase is an NADPH-dependent selenoprotein containing selenocysteine and regenerates ascorbic acid from dehydroascorbic acid in animals (May et al., 1997). Selenoprotein P is an extracellular protein found in plasma and associated with endothelial cells. Its specific function has not been identified, but it accounts for about 45% of plasma Se in North American humans (Hill et al., 1996). Its concentration declines in Se deficiency, can be used for assessing Se status, and appears to be associated with oxidant defense. Selenoprotein W has been found in muscle and a number of other tissues, and its concentration declines in Se deficiency (Vendeland et al., 1993). Its biochemical function is unknown, but the binding of one form to glutathione suggests that it can undergo redox changes. Two selenophosphate synthetases that appear to be involved in Se homeostasis have been identified in animals (Guimaraes et al., 1996). The Se in natural ingredients can be highly variable in quantity and in bioavailability (Henry and Ammerman, 1995; Levander and Burk, 1996). Se is usually added to commercial feeds in the form of sodium selenite. Adult squirrel monkeys (Saimiri sciureus) appear to be more sensitive than rhesus monkeys to Se deficiency. Squirrel monkeys fed a semipurified torula-yeast diet with adequate vitamin E but without added Se showed weight loss, listlessness, alopecia, myopathy, and hepatic degeneration. The signs did not appear until the deficient diet was fed for 6-9 months. The signs were reversed by a single injection of 0.04 mg of Se from sodium selenite, and the animals were maintained by three injections of 0.04 mg at 2-week intervals followed by monthly injections. Untreated monkeys became moribund and died (Muth et al., 1971). Pregnant rhesus (Macaca mulatta) monkeys were fed a semipurified diet containing Se at 0.03 or 0.2 mg·kg-1.No deficiency signs were seen in the mothers fed the Se-deficient diets for about 4 years. The young of the females fed the low-Se diets for about 2 years exhibited no deficiency signs. Although several animals fed the deficient diets died, no pathologic lesions characteristic of Se deficiency were seen. Hair analyses demonstrated that the animals fed the low-Se diet did indeed have low tissue concentrations. Plasma and erythrocyte glutathione peroxidase activities decreased in animals fed the diet low in Se and increased in animals fed the diet supplemented with Se. Cardiomyopathy, characteristic of Se deficiency, was found in a mother and infant fed a protein-deficient low-Se diet. That suggested that simultaneous deficiencies of protein and Se are required for signs of Se deficiency to be manifested (Butler et al., 1988). Blood Se concentrations and glutathione peroxidase activities were compared in a number of species, including nonhuman primates (Butler et al., 1982; Beilsten and Whanger, 1983; Beilsten et al., 1984; Butler et al., 1988). A much greater portion of the Se was associated with glutathione peroxidase in erythrocytes of squirrel monkeys, rats, and sheep than of rhesus monkeys and humans. The toxicity of L-selenomethionine was studied in 20 female Macaca fascicularis by administering various daily doses via a nasogastric tube (Cukierski et al., 1989). The researchers concluded that the maximal dose tolerated for 30 days was 150 g·BWkg-1·d-1 on the basis of mean body weight loss, hypothermia, dermatitis, xerosis, cheilitis, dis-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 turbances in menstruation, and the need for dietary intervention to prevent death at doses of 188 µg·BWkg-1·d-1 or greater. The effects of L-selenomethionine doses of 0, 25, 150, or 300 µg·BWkg-1·d-1 via nasogastric intubation during organogenesis—gestation day [GD] 20-50— were studied in 40 pregnant Macaca fascicularis (Tarantal et al., 1991). Dose-dependent toxicity signs in the pregnant females increased with increasing duration of Se exposure and included anorexia, vomiting, and reduction in body weight. One growth-retarded fetus was recovered on GD 131 from a dam exposed to 25 µg·BWkg-1·d-1. One infant exposed to 150 µg·BWkg-1·d-1 prenatally exhibited a unilateral cortical cataract. One early embryonic death (on GD 35) and two fetal deaths (on GD 68 followed by maternal death on GD 123) occurred among dams exposed to 300 µg·BWkg-1·d-1. The Se requirement of squirrel monkeys appears to be about 0.11 mg·kg-1 of dietary DM, on the basis of the Se concentration adequate to cure deficiency signs (Muth et al, 1971). A quantitative requirement for Se for rhesus monkeys has not been established. The decrease in plasma glutathione peroxidase activity in rhesus monkeys fed a low-Se diet suggests a nutritional requirement, but it has been proposed that the higher levels of glutathione transferase (a non-Se glutathione peroxidase) in the tissues of this species accounts for its resistance to Se deficiency (Butler et al., 1988). Cobalt Cobalt (Co) is a component of vitamin B12 (cobalamin), a vitamin required by nonhuman primates. Vitamin B12 has been found only in foods of animal or microbial origin. Ruminant animals have a dietary requirement for Co, which is incorporated into vitamin B12 during bacterial synthesis in the rumen. A nutritional requirement for Co, independent of vitamin B12, for nonhuman primates has not been demonstrated. Presumably, herbivorous primates with adaptations of the stomach or hindgut that allow for microbial fermentation can synthesize vitamin B12 from Co. Vitamin B12 production has been observed in the gastrointestinal contents of baboons fed a vitamin B12-deficient diet (Uphill et al., 1977), and the presumed synthesis of this vitamin by intestinal microorganisms was offered as a partial explanation of the observation that vitamin B12 deficiency was more severe in animals fed the antibiotic ampicillin than in controls. Cobalamin absorption has been studied in normal and gastrectomized baboons (Green et al., 1982). Primates practicing coprophagy can obtain B12 from their feces (Oxnard et al., 1989). In any case, there are no data to support a quantitative requirement for Co. Excessive intakes of Co by humans have resulted in reduced thyroid activity, goiter, and cardiomyopathy (Barceloux, 1999). Chromium Chromium (Cr) appears to potentiate insulin and will reverse impaired glucose tolerance in a number of species, including humans (Stoecker, 1999). Cr presumably is involved in carbohydrate, lipid, protein, and nucleic acid metabolism, although until recently it has not been identified as a component or cofactor of any enzyme system. The oligopeptide chromodulin binds chromic ions in response to an insulin-mediated chromic ion flux, and this metal-saturated oligopeptide can bind to an insulin-stimulated insulin receptor, activating the receptor’s tyrosine kinase activity. Thus, chromodulin might play a role in the autoamplification of insulin signaling (Vincent, 2000). A contrary proposal has been made that trivalent Cr (Cr+3) can act clinically by interfering with iron absorption, decreasing the high iron stores that some have linked to diabetes and heart disease in humans and thus qualifying Cr as a pharmacologic agent rather than an essential element (Steams, 2000). Cr+3 is the form usually used in animal nutrition. Hexavalent chromium (Cr+6) should be avoided because of its higher toxicity (National Research Council, 1997). Concentrations of Cr in potable water, fruit juices, and soft drinks (Garcia et al., 1999) and in spices and aromatic herbs (Garcia et al., 2000) have been published. Chromic potassium sulfate and chromic chloride have served as sources of Cr in diets for animals, and Cr in yeast is quite bioavailable (National Research Council, 1995, 1997). Chromium picolinate is a commercial source of organic Cr but because of regulatory restraints can be added only to swine feed (American Feed Control Officials, 1997). In addition, evidence that it is absorbed and incorporated into cells in its original form suggests that the metabolism of chromium picolinate is different than of Cr occurring naturally in the diet. The picolinate ligands shift the redox potential of the chromic center in such a way that it can be reduced by biologic reducing agents, such as ascorbic acid and thiols. The resulting chromous complex can interact with oxygen catalytically, generating hydroxyl radicals, which have been shown in vitro to increase DNA cleavage substantially (Vincent, 2000). Thus, the long-term effects of chromium picolinate use need to be investigated. Davidson et al. (1967) and Davidson and Blackwell (1968) reported a high prevalence of impaired glucose tolerance in young adult female squirrel monkeys maintained on a commercial diet. The animals weighed 600-800 g. The impaired tolerance was improved by supplementation with trivalent chromium acetate at 10 mg·kg-1 in drinking water if the water was maintained at a neutral

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 pH. Supplementing with trivalent Cr in drinking water maintained at a mildly acidic pH was ineffective. Divalent Cr was not effective in improving glucose tolerance. Martin et al. (1972) reported corneal opacities in eyes of adult female squirrel monkeys (Saimiri sciureus) weighing 600-800 g that were fed a semipurified diet containing Cr at 0.093 mg·kg-1 of DMand received drinking water with Cr at less than 0.01 mg·kg-1. Total intake of Cr was about 4 µg per animal per day. The mean daily food intake was 44 g. After 6 weeks on the deficient diet, eye lesions developed, starting as haziness of the cornea. The lesions developed into superficial maculae and progressed to deeper opacities with vascularization. The lesions were not reversible by Cr supplementation or the feeding of a commercial monkey diet for up to 9 months. Similar but milder lesions developed in squirrel monkeys fed the deficient diet for 2 weeks, then supplemented with trivalent chromium at 5 mg·kg-1 in the drinking water (total intake, about 400 µg per monkey per day). The results suggest that even a short-term dietary deficiency of Cr can lead to irreversible corneal lesions. Comparable lesions were not observed in animals maintained on diets similar in composition but higher in naturally occurring Cr or on a commercial monkey diet that furnished about 150 µg of Cr per day. Other than the eye lesions, the animals remained healthy over the 34-week period without any other signs of dietary deficiency. Because of issues of biologic availability and the valence state of Cr (only trivalent and hexavalent chromium are biologically active), a quantitative requirement for Cr has not been established. The Cr content of the diet is thought to have little relationship to biologically active Cr, because of the diversity of dietary Cr forms (National Research Council, 1997). Chromium nutrition has not been studied in nonhuman primates other than squirrel monkeys. Fluorine Fluoride (F-) reduces the incidence and severity of dental caries in humans (Phipps, 1996). The caries-preventive effect of F- is attributed mainly to remineralization at the interface of teeth and oral fluids. F- in saliva shifts the balance from demineralization, that leads to caries, to remineralization, presumably because of the F--enhanced precipitation of calcium phosphates and formation of fluor-hydroxyapatite (ten Cate, 1999). It is now considered a required element in human diets because of its cariostatic effect, when it is ingested, on pre-eruptive development of teeth. F- in oral fluids also has a cariostatic effect on posteruptive teeth. The need for F- in humans is most commonly met by addition to the drinking water at 1.0 mg·L-1, which is considered an optimal concentration (Institute of Medicine, 1997). Natural ingredients used in manufactured diets for primates can contribute substantial amounts of F-. Grains, oilseeds, and their byproducts frequently contain F- at 1-2 mg·kg-1. Animal and fish byproducts containing bone can contribute to dietary F-.F- is a common contaminant in rock phosphate, the source of much of the feed-grade phosphate used as a phosphorus supplement. To qualify as feed-grade phosphate, it must be deflourinated to 1 part of F- (or less) to 100 parts of phosphorus (AAFCO, 1997). Depending on the manufacturing process, the addition of 0.25% of phosphorus from dicalcium phosphate can contribute 20 mg·kg-1 or more F- to the diet (McDowell, 1992). Thus, commercial diets for nonhuman primates, under some circumstances, can have substantially higher F- concentrations than found in human diets. F- has been shown to have a cariostatic effect in monkeys. Cynomolgus monkeys (Macaca fascicularis) 11-13 months old were given drinking water containing F- at 2 ppm for 5 years, beginning before eruption of their first permanent molars (Cohen and Bowan, 1966). The F- concentration of the diet was thought to be low but was not measured. The diet was composed of an offering of bread, bananas, canned carrots, biscuits, peanut butter, boiled eggs, jam, complan, dates, marmie, and cheese (Cohen and Bowan, 1966). Animals receiving F- had less caries than animals not receiving F-. The F- was more effective if teeth were being formed while exposed to F- than if they were exposed after mineralization (Bowen, 1973). Those results are in contrast with the observations of Ockerse and de Jager (1957), who added F- at 10 mg·kg-1 to the drinking water of African green monkeys (Cercopithecus aethiops) of unstated age that were fed a cariogenic diet; the added F- had no effect on the incidence of caries. An adequate F- intake by men was recently estimated to be 4 mg·d-1 (Institute of Medicine, 1997). Assuming that average daily intake of food is 500 g of DM, that is equivalent to F- at 8 mg·kg-1 of dietary DM. However, F- needs of people of all ages seem to be best met by its inclusion in drinking water at 1.0-2.0 mg·L-1. Some signs of mild fluorosis (mottling of the teeth) are seen when water contains F- at 2 mg·L-1. REFERENCES Alley, M.C., E.K. Killam, and G.L. Fisher. 1981. The influence of D-penicillamine treatment upon seizure activity and trace metal status in the Senegalese baboon, Papio papio. J. Pharmacol. Exp. Therap. 217:138-146. American Feed Control Officials. 1997. 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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 Golub, M.S., M.E. Gershwin, B. Lönnerdal, C.L. Keen, L.S. Hurley, and A.G. Hendrickx. 1990a. Problems associated with long-term feeding of purified diets in rhesus monkeys. Primates 31:579-588. Golub, M.S., C.L. Keen, A.G. Hendrickx, and M.E. Gershwin. 1990b. Food preferences of young rhesus monkeys fed marginally zinc-deficient diets. Primates 32:49-59. Golub, M.S., A.F. Tarantal, M.E. Gershwin, C.L. Keen, A.G. Hendrickx, and B. Lönnerdal. 1992. Ultrasound evaluation of fetuses of zinc-deprived monkeys (Macaca mulatta). Am. J. Clin. Nutr. 55:734-740. Golub, M., P.T. Takeuchi, C.L. Keen, M.E. Gershwin, A.G. Hendrickx, and B. Lönnerdal. 1994. Modulation of behavioral performance of prepubertal monkeys by moderate dietary zinc deprivation. Am. J. Clin. Nutr. 60:238-243. Golub, M., C.L. Keen, M.E. Gershwin, and A.G. Hendrickx. 1995. Developmental zinc deficiency and behavior. J. Nutr. 125:2263S-2271S. Golub, M., C.L. Keen, M.E. Gershwin, D.M. Styne, P.T. Takeuchi, F. Ontell, R.M. Walter, and A.G. Hendrickx. 1996a. Adolescent growth and maturation in zinc-deprived rhesus monkeys. Am. J. Clin. Nutr. 64:274-282. Golub, M., P.T. Takeuchi, C.L. Keen, A.G. Hendrickx, and M.E. Gershwin. 1996b. Activity and attention in zinc-deprived adolescent monkeys. Am. J. Clin. Nutr. 64:908-915. Gonzales, J., K. Benirschke, P. Saltman, J. Roberts, and P.T. Robinson. 1984. Hemosiderosis in lemurs. Zoo Biology 3:255-265. Goss, A.N., W.J. Sampson, G.C. Townsend, and G.H. McIntosh. 1988. Effect of iodine deficiency on craniofacial growth in young common marmosets (Callithrix jacchus). J. Craniofacial Genet. Devel. Biol. 8:225-233. Green, R., D.W. Jacobsen, S.V. Van Tonder, M.C. Kew, and J. Metz. 1982. Absorption of biliary cobalamin in baboons following total gastrectomy. J. Lab. Clin. Med. 100:771-777. Griffiths, H.J., R.D. Hunt, R.E. Zimmerman, H. Finberg, and J. Cuttino. 1975. 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