8
Water

Water, sometimes overlooked as an essential nutrient, is critical for the health and well-being of all primates. It serves as a medium within which the chemical reactions of the body take place (Harris and Van Horn, 1992), and “life without water is impossible” (Widdowson, 1987). However, water is more than a passive solvent within which inorganic elements, gases, and organic compounds are dissolved or suspended. Water is involved in hydrolytic processes; transport of hormones, nutrients, and metabolites; lubrication of joints; transmission of light in the eyes and sound in the ears; and excretion of waste (Robinson, 1957). Water also gives form to the body and provides protective cushioning for the nervous system (Askew, 1996).

Water’s role in thermoregulation is particularly vital. Water absorbs heat at the point of generation with little temperature rise and dissipates it throughout the fluid compartments of the body. Thus, damage to enzymes and structural proteins is minimized, and heat-bearing blood plasma can be routed to the skin, where heat is transferred to the environment through conduction, radiation, convection, and evaporation. Panting also dissipates heat, and body heat is transferred to the environment via the moisture carried out by each exhalation. The vaporization of one liter of water at 20°C constitutes the loss of 585 kcal of heat (Kleiber, 1975; Askew, 1996).

WATER CONTENT OF THE BODY

Of all the molecules in the animal body, water makes up about 99% (MacFarlane and Howard, 1972). That high molecular percentage is a consequence of the size of the water molecule—which is smaller than molecules of carbohydrate, protein, and fat—and water’s high percentage of body mass. Of fat-free body mass of the adult animal, water is said to make up a relatively constant 68-72% (National Research Council, 1974). A study of the developmental body composition of squirrel monkeys (Saimiri sciureus) examined changes in water, fat, protein, and ash concentration in 51 animals from birth through the age of 156 weeks. Tissues analyzed at necropsy included the eviscerated carcass and fatty and connective tissue trimmings from the brain, thyroids, thymus, heart, lungs, liver, pancreas, spleen, kidneys, gut, and reproductive organs that were removed and not included in the analysis. It was found that fat in the carcass plus trimmings was low at birth (2.7%); on a fat-free basis, water in the carcass plus trimmings was 76.4% in the newborn and declined to 68.9% in the adult (Russo et al., 1980). When expressed as a percentage of whole-body mass, water concentrations in a wide array of species vary inversely with body fat, from 40% in the obese adult to 85% in the neonate (Robbins, 1993).

Percentage of body water differs among humans according to sex, age, and reproductive stage (Askew, 1996). Because women tend to have less muscle and more adipose tissue than men and adipose tissue has about 10% water compared with about 76% water in muscle, men usually have a higher percentage of body water (about 60%) than women (about 50-55%). A human infant has about 77% body water, whereas an elderly person can have as little as 45%. Pregnancy usually increases blood volume and alters relative water distribution between intracellular and extracellular compartments (Southgate, 1987).

About 62% of body water in humans is in cells, including erythrocytes (Askew, 1996). If the roughly 7% of total body water in joints, eyeballs, and spinal column is included in a transcellular compartment, the remaining extracellular compartment accounts for about 31% of total body water. About 75% of the extracellular fraction is found in the interstitial space and about 25% in blood plasma. Thus, blood plasma accounts for about 7% of total body water. Although it is considered outside the body, substantial water can be found in the gastrointestinal tract. In animals with foregut fermentation, such as the dairy cow, gut water may constitute 15-35% of live body mass, with lower values in late gestation and lactation (National Research Council, 2000). Bauchop and Martucci (1968) reported that the



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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 8 Water Water, sometimes overlooked as an essential nutrient, is critical for the health and well-being of all primates. It serves as a medium within which the chemical reactions of the body take place (Harris and Van Horn, 1992), and “life without water is impossible” (Widdowson, 1987). However, water is more than a passive solvent within which inorganic elements, gases, and organic compounds are dissolved or suspended. Water is involved in hydrolytic processes; transport of hormones, nutrients, and metabolites; lubrication of joints; transmission of light in the eyes and sound in the ears; and excretion of waste (Robinson, 1957). Water also gives form to the body and provides protective cushioning for the nervous system (Askew, 1996). Water’s role in thermoregulation is particularly vital. Water absorbs heat at the point of generation with little temperature rise and dissipates it throughout the fluid compartments of the body. Thus, damage to enzymes and structural proteins is minimized, and heat-bearing blood plasma can be routed to the skin, where heat is transferred to the environment through conduction, radiation, convection, and evaporation. Panting also dissipates heat, and body heat is transferred to the environment via the moisture carried out by each exhalation. The vaporization of one liter of water at 20°C constitutes the loss of 585 kcal of heat (Kleiber, 1975; Askew, 1996). WATER CONTENT OF THE BODY Of all the molecules in the animal body, water makes up about 99% (MacFarlane and Howard, 1972). That high molecular percentage is a consequence of the size of the water molecule—which is smaller than molecules of carbohydrate, protein, and fat—and water’s high percentage of body mass. Of fat-free body mass of the adult animal, water is said to make up a relatively constant 68-72% (National Research Council, 1974). A study of the developmental body composition of squirrel monkeys (Saimiri sciureus) examined changes in water, fat, protein, and ash concentration in 51 animals from birth through the age of 156 weeks. Tissues analyzed at necropsy included the eviscerated carcass and fatty and connective tissue trimmings from the brain, thyroids, thymus, heart, lungs, liver, pancreas, spleen, kidneys, gut, and reproductive organs that were removed and not included in the analysis. It was found that fat in the carcass plus trimmings was low at birth (2.7%); on a fat-free basis, water in the carcass plus trimmings was 76.4% in the newborn and declined to 68.9% in the adult (Russo et al., 1980). When expressed as a percentage of whole-body mass, water concentrations in a wide array of species vary inversely with body fat, from 40% in the obese adult to 85% in the neonate (Robbins, 1993). Percentage of body water differs among humans according to sex, age, and reproductive stage (Askew, 1996). Because women tend to have less muscle and more adipose tissue than men and adipose tissue has about 10% water compared with about 76% water in muscle, men usually have a higher percentage of body water (about 60%) than women (about 50-55%). A human infant has about 77% body water, whereas an elderly person can have as little as 45%. Pregnancy usually increases blood volume and alters relative water distribution between intracellular and extracellular compartments (Southgate, 1987). About 62% of body water in humans is in cells, including erythrocytes (Askew, 1996). If the roughly 7% of total body water in joints, eyeballs, and spinal column is included in a transcellular compartment, the remaining extracellular compartment accounts for about 31% of total body water. About 75% of the extracellular fraction is found in the interstitial space and about 25% in blood plasma. Thus, blood plasma accounts for about 7% of total body water. Although it is considered outside the body, substantial water can be found in the gastrointestinal tract. In animals with foregut fermentation, such as the dairy cow, gut water may constitute 15-35% of live body mass, with lower values in late gestation and lactation (National Research Council, 2000). Bauchop and Martucci (1968) reported that the

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 contents of the foregut of a langur accounted for 12% of live body mass, and foregut contents were 85% water. The percentage of total body water (by tritiated-water dilution) in adult chimpanzees has been found to average 67%, slightly higher than the average in adult humans because of the lower body fat in the chimpanzees studied (9%) than in the adult humans (20%) with which they were compared (Angus, 1971). On the basis of tritiated-water dilution, comparable mean concentrations of body water (64%) were found in adult female cynomolgus (Macaca fascicularis) and rhesus (M. mulatta) macaques (Azar and Shaw, 1975). In 13 normal male pigtailed macaques (Macaca nemestrina) with a mean age of 70 months, body water by tritium dilution was 72.6%. In 12 normal female pigtailed macaques with a mean age of 90 months, body water was 70.1%. In five obese female pigtailed macaques with a mean age of 130 months, body water was 52.5% (Walike et al., 1977). Nonhuman primates in captivity can differ dramatically in percentage of body water and corresponding percentage of body fat—hence their degree of obesity—just as humans do. In a study of 23 adult baboons (Papio sp.), fat in 10 males was 2.4-17.6% and in 13 females 3.7-33.0% of body mass (Lewis et al., 1986). In another study, fat in 24 adult male rhesus macaques was 5.9-49.0% of body mass (Jen et al., 1985). Kemnitz and Francken (1986) also found a wide range of adiposity in adult male rhesus macaques. Body fat ranged from 30-61% of body weight and was located most prominently in the abdomen. Glucose tolerance was normal, but blood insulin concentrations and insulin response to glucose loading increased with increasing adiposity. The authors concluded that obese monkeys, like obese humans, are at risk for diabetes mellitus and its complications. With antipyrine dilution, total body water was estimated in 16 adult nonpregnant female baboons (Papio cynocephalus) 4-14 years old and weighing 11.0-13.9 kg (Brans et al., 1985). Although mean total body water was reported to be 798 L·kg-1 of body mass, it is assumed that the authors meant 798 ml·kg-1. Thus, total body water would have been about 80% of body mass. That value is higher than expected and higher than mean values (770 and 769 ml·BWkg-1 ) reported for newborn (day 1) and 29-day-old baboons, again on the basis of the antipyrine dilution technique (Brans et al., 1986b). In a study of the effects of extracorporeal membrane oxygenation (as used in intracardiac surgery) on body water content and distribution, total body water, extracellular water, and plasma volume were measured simultaneously with antipyrine, bromide, and T-1824 (Evans blue) dilution in neonate baboons 17-28 days old and weighing 820-1,478 g (Brans et al., 1986a). Measurements were made before and after 8 hours of extracorporeal membrane oxygenation. Estimates (± SE) of antipyrine space were 843 ± 37.4 and 787 ± 80.5 ml·BWkg-1, respectively, and were not significantly different. Estimates of corrected bromide space were 361 ± 47.6 and 409 ± 47.6 ml·BWkg-1 respectively, and of plasma volume 53 ± 8.2 and 58 ± 19.2 ml·BWkg-1; and they were also not significantly different. Calculated mean volumes of intracellular water, interstitial water, and blood were 482 and 379, 308 and 350, and 84 and 95 ml·BWkg-1, respectively. When estimated with antipyrine dilution on the day of birth in newborn baboons with mean weights of 923 and 624 g, total body water volumes were 773 and 874 ml·BWkg-1 (Brans et al., 1986c). Body water content and distribution were estimated before, during, and after 32 pregnancies in baboons weighing 10-22 kg (Brans et al., 1990b). It was concluded that mean plasma volume and blood volume were higher during pregnancy than before or after. In a later study comparing H218O dilution with antipyrine dilution in neonatal baboons, Brans et al. (1990a) concluded that antipyrine dilution is of doubtful reliability for estimating total body water. Lewis et al. (1986) measured the total body water, triacylglycerol mass, and lean body mass of 13 female and 10 male 5-year-old baboons (Papio sp.) at necropsy. Total body water was calculated as the wet weight of the baboon (body weight minus contents of the gut and bladder) minus the dry weight of the tissues and organs. Male baboons were heavier than females (20.4 kg vs 15.9 kg) and had less triacylglycerol (6.1% vs 16.9%), and more total body water (67.4% vs 64.8%) per unit of body mass. Because of concern expressed by Sheng and Huggins (1979) that tritiated-water dilution overestimates total body water by 4-15% compared with determination with desiccation, a nuclear magnetic resonance (NMR) method was tested by Lewis et al. (1986a) on 21 18-week-old baboons (Papio sp.). Mean total body water concentration was 71% with NMR and 70% with desiccation. When another 19 young baboons were studied, estimates of total body water were higher in 16 and lower in three when determined with tritiated-water dilution than with desiccation. In a study of 10 adult male rhesus monkeys (Macaca mulatta), weighing 6.79-12.35 kg, Baer et al. (2000) found that body-water space with deuterium oxide dilution was overestimated by 10% as compared with direct determination by desiccation. Hydration of lean body mass was 71.2 ± 0.52% (mean ± SE) with a range of 67.9-77.3%. Chwals et al. (1992) studied the utility of magnetic resonance imaging (MRI) for determination of body water with eight Macaca fascicularis. The two measures had a correlation of 0.81 (P < 0.02), and mean total body water determined with MRI was 72.1% of body mass vs 73.8% of body mass with tritiated-water dilution. The intracellular and extracellular distribution of water and concentrations of lipid and the electrolytes sodium, potassium, and chloride in 14 tissues of six normal male

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 rhesus macaques were determined at necropsy (Liu and Griffin, 1978). The tissues examined included the cerebral cortex, cerebellum, thalamus and hypothalamus, medulla oblongata, spinal cord, heart (left ventricle), lung, liver, renal cortex, renal outer medulla, renal inner medulla, diaphragm, skeletal muscle (gastrocnemius), and hair-shaved skin. Mean total water concentrations in those tissues (on a fat-free, wet basis) ranged from 75.8% in skin to 86.8% in the medulla oblongata. The mean concentration of intracellular water as a percentage of total tissue water was lowest in the skin (33.2%) and highest in the thalamus and hypothalamus (82.0%). Pivarnik and Palmer (1994) have reported similar data on humans. Alterations in body-fluid distribution have been reported in rhesus macaques inoculated with Rickettsia rickettsii, the agent that causes Rocky Mountain spotted fever (Liu et al., 1978). There was no change in total body water concentration, but there was a shift of intracellular water to the extracellular space. The shift had little effect on the amount of interstitial fluid but mainly increased plasma volume. However, there were selective alterations in concentrations of water and electrolytes in several tissues with intracellular overhydration of the medulla oblongata. It was suggested that the localized swelling has the potential to depress the cardiovascular and respiratory centers and to lead to circulatory shock and respiratory arrest. Effects of Activity Restriction Total body water concentration, extracellular and intracellular distribution, and water intake and excretion were affected by prolonged restriction of the motor activity of rhesus macaques (Zorbas et al., 1997). Over a 90-day period of activity restriction, changes in fluid metabolism could be divided into three phases. Overall, mean total body water concentrations declined from 62.7% to 50.1% of body mass. The decline was associated with a decrease in water intake, an increase in urine excretion, and increased hematocrit and specific plasma resistance. Effects of Cold Acclimation to cold results in adjustments of body-fluid distribution (Oddershede and Elizondo, 1980a, 1982). Exposure of six adult male non-cold-acclimated rhesus macaques to a cold environment (6°C, 85% relative humidity) for 35 days resulted in a mean increase in total body water from 66.7% to 70.8% of body mass. During the pre-cold-exposure control period, intracellular, extracellular, and interstitial fluid volumes in relation to body mass were 47.2%, 19.5%, and 15.1%, respectively. Mean increases in these measures during cold exposure were 3.8%, 3.2%, and 1.0% of body mass. Prosimians generally have a low basal metabolic rate, which makes it difficult for them to deal with a cool environment (Müller, 1983). The slow loris (Nycticebus coucang) has the lowest basal metabolic rate among normothermic primates reported so far, about 40% of the mass-specific mammalian standard (Müller, 1975, 1979; Whittow et al., 1977). Although mainly an inhabitant of tropical rain forests with relatively constant high temperatures, the slow loris has morphologic features of a cold-adapted homeotherm: thick fur, short nose, small ears, stumpy tail, and short, stout limbs. Those features and vascular bundles in the extremities that function as countercurrent heat exchangers (Müller, 1979) limit loss of heat, because of the insulation of fur, the minimum surface area per unit of mass, and redirection of fluids (and the heat they carry) to the body core. Thus, core temperatures can be sustained during moderate cold exposure, even with modest basal heat production. The slender loris (Loris tardigradus) is found in tropical rainforests but also lives in deciduous forests that experience drought and heat seasonally. It has a long body, a long nose, large ears, very long, thin limbs, and a basal metabolic rate that is about 50% of the mass-specific mammalian standard. When exposed to cold, the slender loris diverts body fluids to maintain a high temperature only in a small body core; large parts of the body are allowed to cool. However, the lower limit of its thermoneutral zone was found to be only 32.5°C, and the slender loris was unable to increase heat production sufficiently to sustain vital functions at low temperatures (Müller et al., 1985). Other findings support the conclusion that this species is better adapted to high than to low temperatures—a circumstance that is consistent with its natural environment. Effects of Heat and Water Deprivation Heat acclimation of rhesus macaques from 24°C and 65% relative humidity to 35 days at 35°C and 30% relative humidity was characterized by a fluid shift from interstitial space to the cardiovascular system and the intracellular compartment. Water input via drinking increased from 95 to 118 ml·BWkg-1·d-1, and total water input via drinking, metabolic water, and moisture in food increased from 120 to 140 ml·BWkg-1·d-1. Total body water, determined by tritiated-water dilution, increased by 4.8% during heat exposure (Oddershede and Elizondo, 1980b). Hamadryas baboons (Papio hamadryas) are found in desert regions of the Horn of Africa and southern Arabia. In contrast with nondesert species, these baboons were able to maintain normal activity after 2 days of water deprivation in a warm environment by conserving blood-plasma volume at the expense of losses from other fluid compartments (Zurovsky and Shkolnik, 1982). Withholding drinking water for 48 hours during midsummer (22-32°C, 70%

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 relative humidity) induced dehydration. Total body water was determined with tritiated-water dilution, and plasma volume was determined with Evans blue dilution (before and after water deprivation). The procedure was repeated six or seven times in each of three animals over a 2-year period. After 2 days of water deprivation, 10% of body mass and 12.5% of body water, but only 4% of plasma volume, were lost. The ability to sustain plasma volume was related to an increase in plasma colloidal osmotic pressure through efficient retention of albumin and an increase in the rate of albumin synthesis (Zurovzky et al., 1984). Adolescent male baboons (Papio cynocephalus and P. anubis) weighing 11.9-16.5 kg were subjected to water deprivation for 64-68 hours, and the effects of dehydration on blood and plasma volumes, plasma constituents, and weight were measured (Ryan and Proppe, 1990). In addition, the effect of interaction of increased environmental temperature (38-42°C vs 22-24°C) and dehydration on hindlimb blood flow was explored. Plasma osmolality and concentrations of blood hemoglobin and plasma sodium and total proteins were significantly increased by dehydration. Blood volume, plasma volume, and weight were significantly decreased. Dehydration attenuated the cutaneous vasodilatory response to heat stress in the hindlimb, and studies of intravenous fluid replacement suggested that the attenuation was associated with a local mechanism in the vascular smooth muscle cell that was triggered by interstitial-fluid volume depletion. Crab-eating macaques (Macaca fascicularis) are found along the southeastern coast of the Asian continent and on Southeast Asia islands. On the Indonesian island of Bali, the species has adapted to a region of considerable rainfall (72-98 mm per month) and to a region with a dry season when there is no water in the rivers and monthly rainfall is only 7-12 mm. They were free-ranging monkeys, so it was possible to study shifts in body fluids in response to dehydration only by collecting single blood samples from each animal. Hematologic data on 85 crab-eating macaques in the two regions revealed that blood-plasma protein, creatinine, and sodium ion concentrations were increased in monkeys in the region with low water supply (Takenaka, 1986). The morphology and behavior of the slow loris equips this species better for dealing with an occasional cool environment as opposed to a hot one. It has a thermal neutral zone between 24-33°C (Müller, 1975), and exposure to an environmental temperature above 35°C usually leads to a rapid rise in rectal temperature (Müller, 1979). Although respiration rate increased to 140 breaths·min-1 at an ambient temperature of 40°C, evaporative cooling at 35°C was sufficient only to dissipate about 50-60% of metabolic heat production (Müller, 1983). The potto (Perodicticus potto) exhibits similar limitations (Hildwein and Goffart, 1975). In contrast, the respiration rate of the slender loris at an environmental temperature of 35°C increased to 200-300 breaths·min-1, and about 80% of metabolic heat production was dissipated by evaporation (Müller et al., 1985). When the water content of surrounding air (75% relative humidity) and ambient temperatures (35°C) were high, the efficiency of evaporative cooling was reduced. However, evaporative cooling was supported by a cardiovascular response that increased transport of body heat from the core to the surface. As a consequence, deep-rectal temperatures rose only slightly above ambient temperature, even after prolonged heat exposure. WATER SOURCES Water to meet requirements comes from three sources: free or liquid water, as in dew, rain, snow, terrestrial and arboreal pools, streams, and lakes; preformed water in food; and metabolic water from oxidation of organic compounds in body tissues. Liquid-Water Intake What it eats, ambient temperatures and humidity, activity, and other factors influence the amount of water that a primate drinks. Maintenance of body water balance is the ultimate homeostatic objective. Diets low in moisture or high in fiber, salt, sodium bicarbonate, or protein will increase water consumption (Harris and Van Horn, 1992). Increased air temperatures and aridity will increase water loss and the amount of water consumed for replacement. Some conditions can induce abnormal water intake. A deficiency of n-3 fatty acids in rhesus macques was shown to result in polydipsia, even though the kidneys retained their ability to concentrate urine and there was no evidence of diabetes insipidus (Reisbick et al, 1990, 1991). Although water, consumed as such, is the major water source for humans in large areas of the world, much of the human water intake in the United States comes from consumption of beverages, such as soft drinks, juices, milk, tea, and coffee (Askew, 1996). Nonhuman primates in the wild drink from running and standing water sources, either by crouching and sipping, by dipping their hand in the water and drinking from their hand or fingers, or by using chewed leaves as sponges to soak up and direct water into the mouth (Angus, 1971). They also have been observed licking moist rocks and plants moist with dew or rain (Nishida, 1980). In a study of free-ranging New World monkeys, mantled howlers (Alouatta palliata) were never seen drinking from terrestrial water sources but rather drank from arboreal cisterns (such as depressions at junctures of tree limbs and trunk) during the wet season. During the dry season, when arboreal cisterns were empty, the howlers

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 maintained their water balance by selecting a diet comprising largely succulent new leaves (Glander, 1978). Quantitative data on liquid-water consumption are available for few species of nonhuman primates. Pace et al. (1964) reported that three adult pig-tailed macaques (Macaca nemestrina) fed a dry commercial diet consumed gross energy (GE) at 70 kcal·kg-1 of body weight and water at 1 ml·kcal-1 of GE. Kerr (1972) concluded that consumption of water at 1 ml·kcal-1 of GE was a reasonable estimate of liquid-water intake. Schroederus et al. (1999) measured baseline water intakes in adult rhesus monkeys of both sexes. Older monkeys (20-36 years) drank 380 ± 63 ml·d-1, significantly less (P < 0.05) than the 679 ± 92 ml·d-1 consumed by middle-aged (13-17 years) monkeys or the 750 ± 128 ml·d-1 consumed by young adults (7-9 years). Patterns of eating and drinking were studied in five adult male rhesus macaques housed in individual cages and provided food and water ad libitum. Animal weights and ambient temperatures and relative humidity were not given, but the light:dark cycle was 12:12. Purina Monkey Chow 5040® providing metabolizable energy (ME) at an estimated 4 kcal·g-1 (air-dry) was fed. Mean daily food consumption was 126.8 g and mean daily liquid-water consumption was 440 ml. Thus, daily liquid-water consumption was 3.5 ml·g-1 of air-dry diet or 0.87 ml·kcal-1 of ME consumed (Natelson and Bonbright, Jr., 1978). Six rhesus macaques were housed in individual cages at an ambient temperature of 24-29°C, a relative humidity of 75-80%, and a light:dark cycle of 12:12 (Zorbas et al., 1997). They were 3-4 years old and had a mean body weight of 5.58 kg. They had ad libitum access to a commercial dry diet and liquid water. Food intake was not reported, but mean water intake was 679 ml·d-1 or 122 ml·BWkg-1·d-1. Daily food and water intakes of 253 wild-origin cynomolgus macaques (Macaca fascicularis) kept in individual cages were determined (Suzuki et al., 1989). Mean (± SD) body weight of 61 males was 6.5 ± 1.3 kg and of 192 females 3.4 ± 0.9 kg. They were fed a dry commercial primate diet plus apples and oranges. Mean (± SD) drinking-water intake by males was 50 ± 33 ml·BWkg-1·d-1 and by females 49 ± 48 ml·BWkg-1·d-1. Mean (± SD) total water intake from drinking water and food by males was 76 ± 35 ml· BWkg-1·d-1 and by females 100 ± 51 ml·BWkg-1·d-1. Preformed-Water Intake Preformed-water concentration in ingested food varies greatly with the diet but accounts for about one-third of water intake by humans (Askew, 1996). Most foods contain some water, and water in the edible portions of cultivated fruits and vegetables generally makes up 80-95% of their mass (National Research Council, 1989; Holland et al., 1991). Preformed water in the foods of free-ranging nonhuman primates can be as little as about 2-3% of air-dried seeds in hot deserts or over 70% of the fresh weight of succulent plant parts in a tropical rainforest (Baranga, 1982; Calvert, 1985; Rogers et al., 1990; Barton et al., 1993; Robbins, 1993; Edwards, 1995). Metabolic Water The gross yield of metabolic water from oxidation of 100 g of carbohydrate, protein, and fat is about 60, 41, and 107 g, respectively (Askew, 1996). However, excretion of the urea produced during protein oxidation requires nearly all the metabolic water released. Thus, there is no net water yield from oxidation of protein. Metabolic water furnishes about 8-10% of the water needs of humans (Askew, 1996). If 100 g of a nonhuman-primate diet contained 16% digestible protein, 10% digestible fat, and 50% digestible carbohydrate, complete oxidation of these three fractions would have a net yield of about 40 ml of metabolic water, or about 1 ml per 8.8 kcal of ME. Metabolic water is also generated during muscular activity through catabolism of stored glycogen and fat. However, the anaerobic metabolism of glucose to lactate (associated with intense effort) yields only one-third as much water as does complete glucose oxidation, and the metabolic-water contribution from either anaerobic or aerobic effort is still a small proportion of total body water (Askew, 1996). WATER LOSS Water is lost from the body mainly via the lungs, skin, intestine, and kidneys, although losses also occur via menstruation and lactation (Widdowson, 1987; Harris and Van Horn, 1992; Askew, 1996). In the absence of sweating, about 44% of total water loss from the human body is insensible water vapor from the lungs or from diffusion through the skin (National Research Council, 1989). These insensible losses increase under conditions of high ambient temperature, high altitude, and low relative humidity. Perspiration increases human water loss further, but there is little information on the presence of sweat glands and sweating in nonhuman primates. Water concentration of feces varies with diet but in healthy adult humans is about 70% (Askew, 1996). In the absence of sweating, water in the normal human stool makes up about 3-4% of total daily water loss; diarrhea can greatly increase this figure (National Research Council, 1989). Cotton-top tamarins (Saguinus oedipus) frequently exhibit colitis in a laboratory environment, and daily fecal output of tamarins with mild, moderate, or severe colitis was 6.0, 7.6, or 8.1 g·BWkg-1, respectively. Water concentrations were 49.4% or 55.0% in the feces of tamarins with mild or moderate colitis (Stonebrook et al., 1996). Suzuki

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 et al. (1989) reported that mean daily fecal outputs of captive cynomolgus macaques were 3.0 and 3.9 g·BWkg-1 for males and females, respectively, but they did not report fecal moisture concentrations. Mean daily total water intakes (drinking water plus water in food) by males and females were 76 and 100 g·BWkg-1, respectively. If these primates were in water balance, water intakes plus metabolic water would be equaled by water loss. Assuming fecal water concentrations of 50-70%, fecal water loss would be equivalent to 2-3% of total water intake. If it were possible to account for the contribution of metabolic water to water balance, fecal water loss presumably would be a still lower percentage of total water loss. The majority of total water loss in nonsweating humans, about 53%, is lost as urine (National Research Council, 1989). Because the concentrating ability of the adult human kidney is limited to about 1,400 mOsm·L-1, the amount of waste that must be excreted by the kidneys dictates the minimal volume of water required for urine formation. Much of the waste comes from products of protein catabolism, such as urea, sulfates, phosphates, and other electrolytes. Several studies have found that rhesus macaques fed a dry commercial diet excreted urine at about 20-50 ml·BWkg-1·d-1 (National Research Council, 1978). Male and female cynomolgus macaques fed a dry commercial diet plus apples and oranges excreted urine at 21 and 27 ml· BWkg-1·d-1, respectively, or about 27% of the total water intake from drinking water and food (Suzuki et al., 1989). Common marmosets (Callithrix jacchus) were placed in metabolism cages for 24 hours without food but with ad libitum access to water. Mean water intakes during 161 observations were 11.7 ml, whereas mean urine volumes were 12.6 ml (Lunn, 1989). In controlled laboratory studies with adult male lesser mouse lemurs (Microcebus murinus), it has been demonstrated that photoperiod and diurnal variations in activity can influence water loss (Perret et al., 1998). This lemur is a small, arboreal, nocturnal prosimian found near the south coast of Madagascar. Its winter environment is dry and up to 20°C cooler (considering both diurnal and seasonal differences), and more limited in resources than the rainy summer environment. Daylength at the winter solstice is 10 hours 50 minutes and at the summer solstice is 13 hours 20 minutes. As days shorten and preparation for winter begins, the animals fatten and decrease their locomotor activity, whereas reproduction occurs during the lengthening days of late spring and early summer. Lesser mouse lemurs were subjected in the laboratory to a constant temperature (24-26°C), 55% relative humidity, and short days (light:dark ratio, 8:16) for 14 weeks, followed by long days (L:D, 14:10) for 22 weeks. Initial mean (± SEM) body mass was 97 ± 3 g; it increased to a maximum of 125 ± 4 g after exposure to short days. After exposure to long days, mean body mass declined to 77 ± 3 g. Total water loss declined during short-day exposure to 38 ± 0.3 mg·BWg-1·day-1 after 3 months and increased during long-day exposure to 87 ± 7 mg·BWg-1·day-1 after 2 months. When measured in a post absorptive state (no food or water during 24 hours), water in feces accounted for less than 0.5% of total water loss and water in urine about 37%, and the remainder was presumably evaporative water loss. Urine was voided only at the beginning of the nocturnal active period, and total water loss at night was always greater than during the daily sleeping period. Dehydration is a common cause of fluid and electrolyte imbalance in elderly humans and, if not properly managed, can lead to central nervous system dysfunction, convulsions, coma, and death (Miller, 1987). It has been suggested that this susceptibility to dehydration resides in impaired regulation of thirst, impaired urine-concentrating ability, or both. The issue has been studied in monkeys by Schroederus et al. (1999). Although elderly rhesus macaques (20-36 years old) drank less during a baseline period than did younger macaques (7-17 years old), the elderly macaques responded to 24-hour water deprivation by eating less and concentrating their urine to the same degree as the younger macaques. During a postdeprivation compensation period, water intakes of elderly and younger macaques returned to predeprivation levels. According to Harris and Van Horn (1992), animals can lose nearly all the fat and about half the protein of the body and still survive, but a loss of about one-tenth of total body water results in death. Even moderate restriction of water sources will generally diminish food consumption (National Research Council, 1981, 1986). WATER QUALITY Analyses of surface water and groundwater by geologic, agricultural, and public-health agencies have established the presence of variable concentrations of essential and nonessential mineral elements (National Research Council, 1974). In some cases, concentrations of essential minerals can be high enough to contribute substantially to meeting total nutrient needs (National Research Council, 1974, 1980). In others, mineral concentrations can be infinitesimal or excessive and potentially toxic. Because streams, lakes, and private wells are widely used by agricultural interests, these issues are of particular importance to farm families and their livestock. Water-quality guidelines for livestock and poultry were developed (National Research Council, 1974); they are commonly updated in publications in the National Research Council Nutrient Requirements series as they are revised. In contrast with agricultural animals, captive nonhuman primates usually get their water from municipal water systems just as do most humans in the United States. Although

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 the composition of water can vary among municipal systems, all such systems are required, at a minimum, to meet national primary drinking-water standards (National Primary Drinking Water Regulations [NPDWR]) established by the US Environmental Protection Agency (EPA). These primary standards protect drinking-water quality by setting limits on levels of specific contaminants that can adversely affect public health and that are known to occur or can be expected to occur in public water systems. The contaminants are divided into inorganic chemicals, organic chemicals, radionuclides, and microorganisms. EPA has included two levels in the NPDWR for each contaminant. The first is the Maximum Contaminant Level Goal (MCLG), defined as the maximal level of a contaminant in drinking water at which no known or expected adverse effect on human health would occur; MCLGs are nonenforceable public-health goals. The second is the Maximum Contaminant Level (MCL), defined as the maximal per-missible level of a contaminant in water delivered to any user of a public water system; MCLs are enforceable standards. MCLGs are equal to or lower than MCLs, with margins of safety that ensure that slightly exceeding the MCL does not pose a substantial risk to public health. EPA also has established secondary drinking-water standards (National Secondary Drinking Water Regulations) that are nonenforceable guidelines related to contaminants of drinking water that might cause cosmetic effects (such as skin or tooth discoloration) or aesthetic effects (such as taste, odor, or color). Although the EPA does not require compliance with these secondary regulations, some states comply. It is not experimentally verified, but water-quality standards established for humans would probably be satisfactory for nonhuman primates. Detailed information on the EPA drinking-water standards for US public water systems can be obtained at http://www.epa.gov/safewater/mcl.html. Composition of the water from specific municipal water supplies can usually be obtained from public-works departments or state departments of health. WATER REQUIREMENTS Requirements for liquid-water intake are dictated by the need to balance total water intake and water loss when metabolic water and water from food are inadequate for that purpose. Thus, liquid-water requirements will vary with food composition, intake, and metabolism and with activity and the need to dissipate body heat. The efficiency of the latter process varies with environmental circumstances, particularly ambient temperature and relative humidity, which in turn affect food intake. Thirst is the body’s clue that something is amiss with water balance, and it encourages the thirsty subject to seek and consume water. Little has been reported on the physiology of thirst in various species of nonhuman primates, and the issue is complicated by observations that the mechanisms involved can be different in different non-primate species (Wood et al., 1982). Homeostatic regulation of body fluid volumes has received major attention in humans because of its importance for normal subjects and for clinical patients (Oh and Uribarri, 1999). Body fluid is an aqueous solution containing many electrolytes in intracellular and extracellular compartments. Intracellular fluid occupies not a single large compartment but myriad cell compartments, which have their characteristic environments and communicate with each other via interstitial fluid and plasma. Although cells in different tissues can vary in the solutes present and in solute concentrations, osmotic equilibrium is maintained so that the same number of water molecules surrounds each particle of solute throughout the body. Cell membranes are so permeable to water that osmolality is normally the same throughout the body fluid. Most of the metabolic reactions of the body take place in cells. For normal operation of these reactions, optimal ionic strengths must be maintained in the cellular compartment, and the homeostatic mechanisms of the body are constantly at work to provide such an environment. Extracellular fluids (ECFs), in contrast, are not sites of major metabolic activity. Therefore, there can be substantial alterations in ionic strength of ECFs without adverse effects. The primary function of ECFs is to serve as a conduit between cells and between organs. The interstitial fluid surrounds cells and allows for slow but efficient intercellular solute exchange. Plasma is a conduit for rapid solute exchange between organs. ECFs thus regulate intracellular volume and ionic strength. The kidneys and central nervous system are jointly responsible for maintaining the homeostasis of body fluids. When water loss exceeds water intake, increases in extracellular fluid osmolality shrink the hypothalamic osmoreceptor cells, which then signal the thirst center in the cerebral cortex and the antidiuretic hormone (ADH) releasing center in the supraoptic and paraventricular nuclei. ADH release is also regulated by nonosmotic factors, such as low effective arterial volume. ADH is released from the posterior pituitary, is carried in the plasma to the kidneys, and stimulates tubular resorption of water from the renal glomerular filtrate. At the same time or shortly thereafter, the thirst center responds by increasing the thirst drive and consequently promotes water intake (Askew, 1996; Oh and Uribarri, 1999). Because of the complexity and interrelationships of factors affecting water requirements and the dearth of information from studies of nonhuman primates, water needs can be most safely met by providing ad libitum access. It should be noted that in group-housing situations, competi-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 tion for the water supply can require special measures to ensure that access (Weisbard and Goy, 1976). When research protocols make ad libitum access to water impossible, preliminary studies should be conducted under similar environmental circumstances and conditions of management to ensure that a limited water supply will not alter research findings or adversely affect animal health. A starting point for an estimate of the daily water needs of adult primates might be 1 ml·kcal-1 of ME expenditure, on the basis of studies with humans (National Research Council, 1989), adult pig-tailed macaques (Pace et al., 1964), and adult rhesus macaques (Natelson and Bonbright, Jr., 1978). Small species of nonhuman primates might have higher water requirements, on the basis of 161 observations of adult common marmosets (Callithrix jacchus) that consumed a mean of 11.7 ml of water per day (Lunn, 1989). 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