2
Energy

Energy is not a nutrient in the sense of chemically identifiable substances, such as essential amino acids, fatty acids, minerals, or vitamins. Energy is an abstraction that can be measured only during its transformation from one form to another. An animal requires energy for basal metabolic functions, for muscular activity, and for tissue accretion, reproduction, or lactation. Kleiber (1975) draws an analogy between animal life and fire: As wood is a fuel supporting fire, food is a fuel supporting animal metabolism, and energy provided by either fuel can be measured in units of heat.

UNITS OF MEASUREMENT

The traditional unit of food energy in the United States is the calorie (cal), the amount of energy required at 1 atmosphere of pressure to raise the temperature of1gof water from 14.5°C to 15.5°C. The joule (J) has been adopted as the preferred unit by the Systè me International d’Unités (International System of Units, or SI) and is often used. These units can be interconverted: 1 cal = 4.184 J. Derivative units are the kilocalorie (kcal) and kilojoule (kJ), which are 103 times as great as the calorie and the joule, respectively, and the megacalorie (Mcal) and megajoule (MJ), which are 106 as times great. In much of the human food literature and on food labels, the kilocalorie is known as the large calorie or, commonly, Calorie (C).

CLASSIFICATION

Gross Energy

When organic substances are completely oxidized to carbon dioxide and water, the energy released is known as gross energy (GE) or total energy. In animal research, GE is usually determined with a bomb calorimeter. In determining the GE of food, a weighed sample in a super-oxygenated atmosphere in a heavy-walled stainless-steel cylinder called a bomb is immersed in a bucket that contains a weighed amount of water. The food sample is ignited with an electric current and burned, releasing heat that passes through the bomb into the surrounding water. The temperature of the water increases in proportion to the amount of energy released from the food. The GE of the food may be expressed in kilocalories per gram (kcal·g-1). Average GE concentrations of carbohydrates, proteins, and fats have been estimated to be 4.1, 5.6, and 9.4 kcal·g-1, respectively.

Not all the GE in food is available to the consuming animal, because of losses in digestion and metabolism. And one food can have a higher GE concentration than another but be a poorer source of available energy. A food that contains cellulose has a greater GE concentration than if cellulose is replaced with sucrose (Watt and Merrill, 1963), because combustion releases more energy from cellulose than sucrose. However, cellulose cannot be digested by endogenous mammalian enzymes, and in the absence of substantial microbial fermentation in the gastrointestinal tract, the GE in cellulose will be lost in the feces.

Digestible Energy

The GE of a food minus the GE of feces resulting from eating the food equals the apparent digestible energy (DE) of the food. It is termed apparent DE because some of the fecal energy is of nonfood origin and would be present even if no food were consumed. An estimate of true DE is attained if apparent DE is corrected for fecal metabolic energy losses, gaseous energy losses, and heat of fermentation. However, the nonfood energy losses in the feces must eventually be replaced with energy from food, and apparent DE values are most commonly used in practice.

Unlike the GE of a food, apparent DE is not a constant but is a function of food composition, the amount of food consumed per unit of time, and the ability of the consuming animal to digest it. For example, high-fiber foods usually



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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 2 Energy Energy is not a nutrient in the sense of chemically identifiable substances, such as essential amino acids, fatty acids, minerals, or vitamins. Energy is an abstraction that can be measured only during its transformation from one form to another. An animal requires energy for basal metabolic functions, for muscular activity, and for tissue accretion, reproduction, or lactation. Kleiber (1975) draws an analogy between animal life and fire: As wood is a fuel supporting fire, food is a fuel supporting animal metabolism, and energy provided by either fuel can be measured in units of heat. UNITS OF MEASUREMENT The traditional unit of food energy in the United States is the calorie (cal), the amount of energy required at 1 atmosphere of pressure to raise the temperature of1gof water from 14.5°C to 15.5°C. The joule (J) has been adopted as the preferred unit by the Systè me International d’Unités (International System of Units, or SI) and is often used. These units can be interconverted: 1 cal = 4.184 J. Derivative units are the kilocalorie (kcal) and kilojoule (kJ), which are 103 times as great as the calorie and the joule, respectively, and the megacalorie (Mcal) and megajoule (MJ), which are 106 as times great. In much of the human food literature and on food labels, the kilocalorie is known as the large calorie or, commonly, Calorie (C). CLASSIFICATION Gross Energy When organic substances are completely oxidized to carbon dioxide and water, the energy released is known as gross energy (GE) or total energy. In animal research, GE is usually determined with a bomb calorimeter. In determining the GE of food, a weighed sample in a super-oxygenated atmosphere in a heavy-walled stainless-steel cylinder called a bomb is immersed in a bucket that contains a weighed amount of water. The food sample is ignited with an electric current and burned, releasing heat that passes through the bomb into the surrounding water. The temperature of the water increases in proportion to the amount of energy released from the food. The GE of the food may be expressed in kilocalories per gram (kcal·g-1). Average GE concentrations of carbohydrates, proteins, and fats have been estimated to be 4.1, 5.6, and 9.4 kcal·g-1, respectively. Not all the GE in food is available to the consuming animal, because of losses in digestion and metabolism. And one food can have a higher GE concentration than another but be a poorer source of available energy. A food that contains cellulose has a greater GE concentration than if cellulose is replaced with sucrose (Watt and Merrill, 1963), because combustion releases more energy from cellulose than sucrose. However, cellulose cannot be digested by endogenous mammalian enzymes, and in the absence of substantial microbial fermentation in the gastrointestinal tract, the GE in cellulose will be lost in the feces. Digestible Energy The GE of a food minus the GE of feces resulting from eating the food equals the apparent digestible energy (DE) of the food. It is termed apparent DE because some of the fecal energy is of nonfood origin and would be present even if no food were consumed. An estimate of true DE is attained if apparent DE is corrected for fecal metabolic energy losses, gaseous energy losses, and heat of fermentation. However, the nonfood energy losses in the feces must eventually be replaced with energy from food, and apparent DE values are most commonly used in practice. Unlike the GE of a food, apparent DE is not a constant but is a function of food composition, the amount of food consumed per unit of time, and the ability of the consuming animal to digest it. For example, high-fiber foods usually

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 have a higher DE for animals with substantial gastrointestinal microbial fermentation than for animals that must depend exclusively on endogenous digestive enzymes. As a consequence, DE concentrations in foods are most meaningful if determined during consumption of those foods by the target species in typical amounts per day. Such determinations have seldom been made with nonhuman primates, and it is presently necessary to use DE values for foods coming from studies of other species (usually domestic) that have gastrointestinal anatomy and physiology similar to that of the target primate species. Metabolizable Energy Apparent metabolizable energy (ME) of a food is equal to food GE minus GE lost in the feces, urine, and combustible gases. Subtraction of the latter quantity is an obviously arbitrary feature of the definition of apparent ME, in that the loss of food GE in combustible gases is a consequence of digestive processes. In most cases, gaseous GE lost is largely in the form of methane from microbial fermentation in the foregut or hindgut. That loss is not accounted for in apparent DE but for some species could account for a high proportion of the food energy that is unavailable for support of metabolic processes. Analogously to the calculation of true DE, true ME is calculated by subtracting metabolic losses of nonfood origin from apparent ME. Apparent ME values are used much more commonly than true ME values. For some animal species, systems for expressing energy and nutrient requirements are based on ME intake. It is desirable to express requirements based on ME; however, research in primates has not been conducted to allow use of an ME-based system. Given the diversity of primate species and food items fed to these primates, ME values for the majority of food items have not been determined. This lack of data presently hampers development of more refined estimates of nutrient needs. Research is needed to determine ME values of particular food items for specific primate species. Obviously, not all species can be studied, due to the intensive nature of the research and the limited availability of research animals. A reasonable approach to obtaining critical information on ME would be to conduct experiments with several model primate species, from which estimates could be extrapolated for other similar species. Primate species most important to study might be those 10 model species identified in Chapter 11: (1) macaques, (2) baboons, (3) squirrel monkeys, (4) cebus, (5) howlers, (6) marmosets and tamarins, (7) colobus and langurs, (8) lemurs, (9) chimpanzees, and (10) humans. Physiologic Fuel Values Nitrogen-corrected ME, net energy, and other expressions of energy concentrations in foods are presented in NutritionalEnergetics of Domestic Animals (National Research Council, 1981b). The system that has been most widely applied to foods for primates involves calculation of physiologic fuel values (or physiologically available energy, an approximation of apparent ME); the system has been reviewed by Widdowson (1955) and is based on the German studies of Rubner in 1880-1901 and studies of Atwater (Rubner’s student) in 1895-1906 in the United States. Most tables of composition of foods for humans list physiologically available energy values (and conversion factors for carbohydrates, protein, and fat in specific foods) based on digestibility trials conducted by Atwater and others (Merrill and Watt, 1955). The general physiologically available energy conversion factors of 4 kcal·g-1 for carbohydrates and protein, and 9 kcal·g-1 for fat yield reasonable approximations of apparent ME in the typical US human diet but not in specific foods or in high-fiber diets (National Research Council, 1989). For those, specific conversion factors, such as those in US Department of Agriculture Handbook No. 8 (Watt and Merrill, 1963) should be used. Souci et al. (1994) used the general conversion factors of 4 and 9 kcal·g-1 for protein and fat, respectively, but applied the carbohydrate conversion factor of 4 kcal·g-1 only to available carbohydrate. Available carbohydrate was defined as monosaccharides, disaccharides, oligosaccharides, nonstructural polysaccharides, and the sugar alcohols sorbitol, xylitol, and glycerol. If concentrations of those compounds were unknown, available carbohydrate was defined as 100 - (water + protein + fat + minerals + total dietary fiber + available lactic, citric, and malic acids). The conversion factor used for available organic acids was 3 kcal·g-1. Total dietary fiber included primarily cellulose, hemicellulose, and lignin (or water-soluble + water-insoluble fiber) and was assigned an available energy value of 0 kcal·g-1. Ethanol was assigned a value of 7 kcal·g-1. The general conversion factors of Souci (1994) assume that there is no energy derived from dietary fiber and ignore interactions among macronutrients that may impact energy availability. A more robust approach to estimate dietary energy has been proposed by Livesey (1999, 2001). This empirical approach accounts for energy derived from all macronutrients and accounts for nutrient-nutrient interactions (Baer et al., 1997). REQUIREMENTS To conform with the first and second laws of thermodynamics, energy intake by an animal must equal energy used plus energy lost. Thus, GE in ingested food must equal

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 GE used for support of basal metabolic functions, voluntary activity, maintenance of body temperature, and product formation (for example, tissue growth, integument, conceptus, and milk) plus GE lost in feces, urine, and combustible gases and as waste heat. Basal Energy Expenditures or Basal Metabolic Rate ESTIMATING BASAL METABOLIC RATE A first measure of energy expenditure (or energy requirement) is the amount of energy required to support the basic life functions (vital cell activity, respiration, and cardiovascular distribution of blood) of an animal in repose (awake but resting and unstressed), in a postabsorptive state, and in a thermoneutral environment (no shivering or other special activity to maintain body temperature). Rubner proposed that basal energy expenditure was related to body surface area and concluded that fasting homeotherms produce 1,000 kcal of heat per square meter body surface (Kleiber, 1975). Because the surface area of a sphere is related to its volume and can be related to its weight when it has a density of 1 kg·L-1, attempts were made to relate basal energy requirements of animals to measurements of body surface area. However, animals are not spheres and do not have a density of 1, and body-surface area measurements are difficult to reproduce consistently. Thus, a search began for a relationship between basal energy requirements and body weight. Using data published by others, Kleiber (1975) explored the concept of metabolic body size as a power function of body weight (BWn) and concluded that basal metabolic rates (BMR) of fasting adult animals varying in body weight from mice (0.021 kg) to cattle (600 kg) could be expressed in kilocalories per day as 70BWkg0.75. Nonhuman-primate data included in his calculations were derived from studies of macaques (Benedict, 1938) weighing 4.2 kg, with a BMR of 207 kcal·day-1, and chimpanzees (Bruhn and Benedict, 1936) weighing 38 kg, with a BMR of 1,090 kcal·day-1. It should be noted that it is difficult to measure energy expenditure in the exact circumstances specified for determination of BMR. It is questionable whether ruminants reach a true postabsorptive state; Colobinae might not, and few animals appear to be stress-free during the measurement experience. Therefore, resting energy expenditure (REE) may be used instead. In studies with humans, BMR and REE differ by less than 10%, and the terms are used interchangeably (National Research Council, 1989). Prediction equations have been used for estimating BMR when analytic methods were not available (FAO/WHO/ UNU, 1985; National Research Council, 1989). EFFECTS OF AGE AND BODY COMPOSITION ON BASAL METABOLIC RATE Energy expenditure (EE) and therefore energy requirement generally decreases with advancing age because of a decrease in BMR, which is characterized by loss of fat-free mass (FFM). Age-related changes probably vary in rate, timing, and extent among individuals in response to differences in physical activity, disease, and other factors. Information on rates of change in BMR and FFM is limited by study design (cross-sectional rather than longitudinal) and possibly by methodology (use of imprecise or biased methods for assessment of changes in body composition) (Murray et al., 1996). The age-related decline in BMR has been partly explained by a reduction in the quantity, as well as metabolic activity, of lean-tissue components as measured by dual-energy x-ray absorptiometry (DEXA). However, even when BMR was adjusted for differences in lean-tissue and fat components, it was significantly lower in older people (50-77 years old) by 644 kJ·day-1 (Piers et al., 1998). When the BMR of similarly aged people (average, 71 years) was measured in a respiratory chamber, BMR was significantly (P < 0.01) lower after FFM, fat mass, and sex were accounted for (Vaughn et al., 1991). When REE of 40 healthy men and women (51-82 years old) was measured with indirect calorimetry, REE was highly correlated with FFM(r = 0.88; P < 0.001) and body weight (r = 0.85; P < 0.001); this supports the idea that active tissue mass determines daily EE (Fredrix et al., 1990). Total EE and activity level, measured by the doubly labeled water (DLW) method in combination with measurements of BMR, showed that EE was lower in elderly (68-71 years) than in younger (27-30 years old) subjects partly because of a significantly lower BMR (Pannemans and Westerterp, 1995). When EE (adjusted for body composition and activity) was measured in two age groups (20-30 years, n = 98; 50-65 years, n = 39), older subjects had a 4.6% lower BMR than younger subjects, independently of sex, body size, body composition, and activity (Klausen et al., 1997). An effect of sex was noted among healthy men and women (over 50 years old to control for effect of menstrual status) when 24-hour EE, BMR, and sleeping metabolic rate were measured in a respiratory chamber. Men had significantly higher 24-hour EE and sleeping metabolic rates than women after adjustment for differences in fat-free mass, fat mass, and age (Ferraro et al., 1992). Energy Requirements for Maintenance Age and body composition affected energy requirements of 101 infants, 82 girls, and 27 adults when energy expenditures were scaled for differences in body size to test the effects of age and body fatness in humans (Butte et al.,

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 1995). As humans increase in weight and fatness from infancy to adulthood, energy requirements increase as a power function (BW0.63) of body weight. The capabilities of aging people need not diminish if they maintain a healthy, active lifestyle. Energy requirements and EE of healthy, active older people (63-77 years) and younger people (average, 28 years) were reported in a study of men receiving a diet with a defined formula for 47 days under controlled conditions. Energy expenditure while they were at rest: 1.22 × BMR, and while sitting quietly: 1.30 × BMR, were the same for older and younger men (Calloway and Zanni, 1980). Moderate activity, such as walking on the level at about 2.5 mph, cost 4.51 ± 0.34 (mean ± SD) kcal·min-1 (about 1.4 × BMR). Cycling at a comfortable load (300-400 kpm) cost only slightly more energy than did walking for both age groups. Metabolizable energy intake required to maintain a constant BW for these men, who were sedentary except for 30 min of cycling per day, was 2,554 ± 222 kcal·day-1, or about 1.6 × BMR. The minimal maintenance ME requirement (ambulatory but inactive) of healthy older men was 1.5 × BMR, the same as for younger men, and similar to the averages of 1.55 × BMR for adult macaques and 1.56 × BMR for adult baboons of various ages (Table 2-1). The estimate of total daily EE, determined by multiplying energy costs of a given level of activity by the individual estimate of BMR, was 1.55 × BMR for sedentary men, as reported by Almendingen et al. (1998) in describing methods for predicting individual energy intakes. The “factorial approach” to estimating ME requirements as multiples of BMR was based on the factorial method used to determine protein requirements (Payne and Waterlow, 1971). It provides a way of partitioning the ME required for maintenance into BMR, activity, and heat increment (Lloyd et al., 1978; National Research Council, 1981b; FAO/WHO/UNU, 1985). The idea has been expanded to encompass estimates of total EE whether determined according to dietary intake, DLW, or other indirect measures of energy requirements or expenditures (Roberts, 1996; Shetty et al., 1996; Scholler, 1998; DeLany, 1998). A measure of error can be introduced into the estimate in that activity (work) is determined by mass and distance traveled in the horizontal or vertical planes and is not a function of age or gender (Mathers, 1997). When cross-sectional energy-balance measurements were made on groups of rhesus monkeys (Macaca mulatta) 6.5-7.0 years old, 8.5-10 years old, and over 24 years old, the 24-hour EE tended to decrease with age when it was expressed in absolute or BWkg 0.75 terms (Lane et al., 1995). Absolute EE (mean ± SD) declined for the juvenile, adult, and aged ad libitum-fed control groups to 1,008 ± 326, 853 ± 188, and 603 ± 148 kcal·d-1, respectively. Energy expenditures expressed in relation to BWkg 0.75 for the groups declined in a similar manner 194 ± 64, 167 ± 32, and 122 ± 46 kcal·d-1, respectively. There was no significant effect of age on either measurement. In another study of young (7-9 years), middle- (13-17 years) and older-aged (> 23 years) rhesus monkeys, energy expenditure (kJ/min) tended to decrease with age but the decrease was not significant. In this study, older animals spent less time in vertical movement and thus had the lowest energy expenditure (Ramsey et al., 2000). The ME intake required for maintenance must provide the chemical energy to meet basal metabolism, thermoregulation, and activity energy costs (Lloyd et al., 1978; McNab, 1986; Scott, 1986; Robbins, 1993a; Torun et al., 1996). In other words, ME intake must equal heat production. Such biologic factors as sex, growth, age, health, and reproductive status affect energy requirements of nonhuman primates. Evidence suggests that some nocturnal primates have lower relative basal requirements than diurnal primates (Ross, 1992). Although the maintenance energy requirement is often defined as the energy intake that sustains a constant BW, care must be taken in using weight as the sole criterion of energy balance because body composition may change, particularly with age (Robbins, 1993a). Similarly, the expression of food intake data per kilogram BW rather than per unit of metabolic body size can lead to variable conclusions, especially when small and large animals or those with different body compositions are compared (Brody, 1945; Ausman et al., 1985). In humans and rats, about 60-75% of the ME supplied by the diet is used to meet BMR requirements (Lloyd et al., 1978; Rothwell and Stock, 1981; Curtis, 1983; FAO/ WHO/UNU, 1985). About 5-10% is used to support the thermogenic effect (heat of digestion) of food (Mayes, 1996; Forsum et al., 1981). The heat increment (HI) associated with digestive and metabolic processes is energy that cannot be used for productive purposes but can be used to help to maintain body temperature in cold environments. Except for temperature extremes, the influence of environmental temperature on apparent digestibility of the energy in food is relatively small compared to that of differences in food composition (Curtis, 1983). It also is difficult to measure because climatic effects are often confounded with amounts of food consumed and the foods selected, choices that may vary seasonally among free-living mammals (National Research Council, 1981a; McNab, 1986). The ambient temperature range in which thermoregulation occurs without increasing metabolic heat production is termed the thermoneutral zone and is bounded by the upper and lower critical temperatures (Curtis, 1983; Robbins, 1993a). As ambient temperature rises above the upper critical temperature, metabolic heat production increases because of the energy-demanding processes, such as panting and sweating, required for heat dissipation. Declines in ambient temperature below the lower critical temperature require increased metabolic heat production by such activi-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 2-1 Estimated Daily Metabolizable Energy (ME) Requirements (as Multiples of BMR) for Adult Captive Animals. (Based on Studies of Estimated Ad Libitum Energy Intake and Controlled, Long-term Dietary Restriction, or Analyzed Total Energy Expenditures. Activity Levels Typical for Captivity, Environmental Conditions Measured, and Animals Maintaining Bodyweight.) n Sex BWkg Kcal ME Intakea · BMR-1 TEEb Kcal · BMR-1 TEE Kcal · BWkg1 EEc Kcal · BMR-1 BMRd MMRe Diet Typef Reference Apes (Pongidae: orangutan, gorilla)   7 M/F 76.5 2583/1811 = 1.43 100(BW0.75)   1277 3621 M King, 1978 Aye-aye     4 M/F 2.46 260/137 = 1.9 133(BW0.75) 109 275 M Sterling et al., 1994 Baboon     11 F 15.6 748/551 = 1.36 409 1099 N Wene et al., 1982 17 F 18.8 956/631 = 1.55 467 1264 N Bielert & Busse, 1983 6 F 20.0 1169/662 = 1.77 X = 1.56, 109(BW0.75) 489 1324 N Roberts et al., 1985 Colobines Langurs     7 M 7.54 629/319 = 1.97 243 637 N, ADF15 Edwards & Ullrey, 1999b 7 M 7.46 506/316 = 1.60 X = 1.78, 125(BW0.75) 241 632 N, ADF30 Edwards & Ullrey, 1999b Proboscis     5 F 9.0 1055/364 = 2.90 203(BW0.05) 276 727 M Dierenfeld et al., 1992 1 M 15.0 1758/534 = 3.29 230(BW0.75) 398 1067 M Dierenfeld et al., 1992 Howlers     7 M 7.52 430/318 = 1.35 243 636 N, ADF15 Edwards & Ullrey, 1999b 7 M 7.61 440/321 = 1.37 X = 1.36, 95(BW0.75) 245 641 N, ADF30 Edwards & Ullrey, 1999b Lemurs     13 M/F 2.5 194/139 = 1.42 110 278 M King, 1978 3 F 4.6 303/219 = 1.38 171 440 N, ADF15 Edwards & Ullrey, 1999a 2 F 4.8 286/228 = 1.25 X = 1.35, 95(BW0.75) 176 454 N, ADF15 Edwards & Ullrey, 1999a Macaca rhesus     3 M 9.0 367/364 = 1.01 276 727 SP Robbins and Gavin, 1966 14 F 6.6 277/287 = 0.97 221 576 SP Robbins and Gavin, 1966 6 M 9.0 681/364 = 1.87 1008/364 = 2.77 112.0   276 727 N Lane et al. , 1995 6 M 9.0 754/364 = 2.07 853/364 = 2.34 94.7 276 727 N Lane et al. , 1995 3 M 8.3 369/342 = 1.08 603/342 = 1.76 72.6 260 685 N Lane et al. , 1995 15 M 13.7 706/498 = 1.41   1183/498 = 2.38 373 997 P Ramsey et al. , 1997 8 M 16.5 882/573 = 1.54 884/537 = 1.54 53.5   426 1146 N DeLany et al. , 1998 M. fasicularis   16 M 5.7 627/255 = 2.46 X = 1.55, 109(BW0.75)   196 516 P Cefalu et al., 1997

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 n Sex BWkg Kcal ME Intakea · BMR-1 TEEb Kcal · BMR-1 TEE Kcal · BWkg1 EEc Kcal · BMR-1 BMRd MMRe Diet Typef Reference Macaca, diet restricted rhesus   6 M 6.0 441/268 = 1.64 903/268 = 3.36 (31%DR)g   206 537 N Lane et al., 1995 6 M 8.5 531/348 = 1.53 790/348 = 2.27 (26%DR) 265 697 N Lane et al., 1995 7 M 11.0 582/423 = 1.38   (35%DR) 318 846 N Bodkin et al., 1995 6 M 11.5 507/437 = 1.16 511/437 = 1.17 (40%DR) 329 874 N DeLany et al., 1998 M. fasicularis   16 M 5.5 432/345 = 1.25 X = 1.39, 97(BW0.75)   (30%DR)   194 328 N Cefalu et al., 1997 Marmoset   8 M/F 0.44 86.8/37.8 = 2.30   31.8 76 M King, 1978 5 M/F 0.133 26.5/15.4 = 1.72 13.5 31 P Power, 1991 8 M/F 0.355 70.8/32.2 = 2.19 X = 2.07, 145(BW0.75) 27.2 64 P Power, 1991 Squirrel monkey   11 M/F 0.79 164/59 = 2.77   48.3 117 SP Ausman et al., 1985 4 M 0.95 167/67 = 2.49 X = 2.63, 184(BW0.75) 55 135 N Weindruch et al., 1995 Squirrel monkey, diet restricted   13 M 0.80 128/59.2 = 2.16 151(BW0.75)   (28%DR)   48.8 118 N Weindruch et al., 1995 Tamarin   6 M 0.430 66.4/37.3 = 1.78   30.4 74 P Escajadillo et al., 1981 >10 M/F 0.300 42.7/28.4 = 1.50 24.2 57 N Wirth and Buselmaier, 1982 39 M/F 0.534 124/43.7 = 2.80 36.5 87 N Barnard et al., 1988 7 M/F 0.311 92.6/29.1 = 3.18 24.8 58 P Power, 1991 10 M/F 0.472 101.3/39.9 = 2.54 33.4 80 P Power, 1991 9 M/F 0.678 109.8/52.3 = 2.09 43.4 105 P Power, 1991 4 M/F 0.471 65.1/39.8 = 1.64 X = 2.22, 155(BW0.75) 33.4 80 N Kirkwood & Underwood, 1984 Chimpanzee   7 M 12.9 (26% adult weight)   893/557 = 1.60 357 953 ? Dale et al., 1967 7 F 15.9 (39% adult weight) 836/477 = 1.75 415 1115 ? Dale et al., 1967 aKilocalories of ME intake relative to estimates of basal metabolic rate (BMR, 70BW0.75) provide factors by which basal energy requirements can be multiplied to accommodate energy costs of physical activity typical of captivity. Averaged factors × 70BW0.75 provide estimates of daily energy requirements. bTotal energy expenditures (TEE) was measured with doubly labeled water method. Ratios of TEE:BMR provide factors by which basal energy requirements can be multiplied to accommodate energy costs of physical activity typical of captivity. When TEE was reported separately for males and females, there were no apparent differences between sexes in magnitude of factors (FAO/WHO/UNU, 1985). cEnergy expenditure analyzed with indirect calorimetry used as above to determine multiple of BMR. dBMR in kcal per day as function of body weight (kg) for eutherians: BMR = 57.2BWkg0.716 (McNab, 1988). eMMR (maintenance metabolic rate) in kcal of ME per day as function of body weight (kg) to meet daily maintenance energy requirements for placental mamm als: MR = 140BWkg0.75 (Scott, 1986; Robbins, 1993a). fDiet type: M = mixed, N = natural ingredient, P = purified, SP = semipurified, ADF15 = 15% acid-detergent fiber, ADF30 = 30% acid-detergent fiber. gLevel of dietary restriction below ad libitum (DR).

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 ties as shivering to maintain body temperature. Measures of heat production and heat dissipation have been made in chimpanzees at an ambient temperature of 23.9°C, presumably within the thermoneutral zone of this species (Dale et al., 1967). When heat loss was partitioned, losses were approximately equal via radiation, convection, and evaporation of moisture. Basal levels of heat production (or energy expenditure) for chimpanzees with estimated ages from 42 to 74 months and BW from 11.3 to 27.2 kg averaged 2.222 kcal·BWkg-1 hour-1, equivalent to 53 kcal·BWkg-1·day-1. BMR can be used as a baseline index of daily EE to which that of activity can be added. This basal EE is usually expressed on a metabolic body-weight basis with the equation noted previously—BMR in kcal·day-1 = 70 × BWkg0.75 (Clarke et al., 1977; Lloyd et al., 1978; King, 1978; Feldman and McMahon, 1983; McNab, 1983; Kurland and Pearson, 1986; Nagy, 1987; McNab, 1988; Mori, 1995; Tilden and Oftedal, 1995; Leonard and Robertson, 1997). The true value of the exponent has been debated, and other relative BMR scaling relationships have been described for captive and wild mammals, including primates (Stahl, 1967; Stahl and Malinow, 1967; King, 1978; Heusner, 1985; McNab, 1986; Robbins, 1993a; Stevens and Hume, 1995; Leonard and Robertson, 1997), with consideration of animal type, species, and quality of diet (Ross, 1992). In housed domestic or wild animals, energy in addition to basal requirements for ingestion and metabolism of food is required, but little is needed for thermoregulation or physical activity (Curtis, 1983; Stevens and Hume, 1995). Under these husbandry conditions, ME requirements for daily maintenance are about double the BMR of 293kJ (70 kcal) × BWkg0.75 for eutherians (Kleiber, 1961; Robbins, 1993a). Voluntary ME intakes of 120 species of zoo animals, grouped in families (including primates), were related to their predicted BMR requirements (Evans and Miller, 1968). The mean ME intake, 146 kcal × BWkg0.75 was about twice the energy required for basal metabolism, or 2.08 × BMR. The reported addition to BMR to accommodate minimal physical activity (minimal survival requirement) of humans was 1.27 × BMR (89 kcal × BWkg0.75), increasing to 1.4 × BMR (98 kcal × BWkg0.75) over 24 hours if 1.5 hours· day-1 of walking or 2 hours·day-1 of standing was included. The 1.4 value serves as a guide for estimating maintenance ME requirements of humans (FAO/WHO/UNU, 1985). A factor of 1.3 × BMR (91 kcal × BWkg0.75) has been proposed as a maintenance ME requirement for carnivores and omnivores (Scott, 1986), whereas a maintenance ME requirement of 1.5 × BMR (105 kcal × BWkg0.75) has been proposed for a range of animals when relative energy requirements were determined by a factorial approach similar to that used for estimating protein requirements (Payne and Waterlow, 1971). With increasing activity of adult omnivores (including humans) and adjustment of BMR for HI, 2 × BMR (140 kcal × BWkg0.75) has been proposed as the maintenance ME requirement for moderate activity and 3 × BMR (210 kcal × BWkg0.75) for high activity (Scott, 1986). Net costs for standing require a 20% energy increase above basal for mammals, or 1.2 × BMR (84 × BWkg0.75) (Robbins, 1993a). The energy requirement for terrestrial locomotion (TL) is an inverse function of BW, and bipeds and quadrupeds can be represented with the same regression equation, Ykcal·BWkg-1·TL·km-1 = 2.57 × BWkg-0.316 (Taylor et al., 1982). Climbing adds an average of 6 kcal·BWkg-1·per vertical kilometer climbed (Robbins, 1993a). The cost of brachiation (use of the arms to swing between objects) varies with speed, and the net cost (kcal·BWkg-1·km-1) is 1.5 times as high as for normal walking by spider monkeys (Parsons and Taylor, 1977). Hanging motionless was reported to increase resting metabolism of the spider monkey and slow loris by 65 ± 32%, which is 3 times more costly than the 20% increment for standing over resting in mammals. When energy expenditures over 24-hour periods were measured in 177 closely observed human subjects, it was demonstrated that much of the variability in daily energy expenditure, independent of differences in body size, was due to differences in spontaneous physical activity, or fidgeting. This activity accounted for energy expenditures of 100-800 kcal·d-1 in these subjects (Ravussin et al., 1986) and might apply to nonhuman primates as well. Clinical practitioners often use a simplified formula (1 kcal·BWkg-1·hour-1) to approximate average daily basal energy requirements of adult humans (Williams, 1997). Adjustments for various levels of activity may be added to this basal estimate as follows: 20%, 30%, 40%, or 50% for very sedentary, sedentary, moderately active, or very active, respectively. The normal activity of most free-living animals would be considered sedentary to moderate, requiring an energy expenditure addition of 30%-40% to the BMR. Caged animals generally would require additions of only 13%-35% to the maintenance requirement for activity (Lloyd et al., 1978; Scott, 1986). Daily total EE, the sum of all caloric costs for maintenance and activity of male and female adult wild howlers, Alouatta palliata, estimated with the DLW method, averaged 85 kcal·BWkg-1 or 135 kcal·BWkg0.75 (Nagy and Milton, 1979). By comparison, the mean total EE of adult caged M. mulatta, also determined with DLW, was 87 kcal·BWkg-1·day-1 (Stein et al., 1996). The total 24-hour EE of ad libitum-fed adult M. mulatta ranged between 112 and 73 kcal·BWkg-1 when measured with DLW (Lane et al., 1995). The 24-hour EE of prepubertal male and female chimpanzees, determined with indirect calorimetry, were about 65 and 56 kcal·BWkg-1, respectively (Dale et al., 1967). The mean daily EE of two adult male and two adult female Gelada baboons, measured with indirect calorimetry, was

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 94 kcal·BWkg0.75 or 1.34 × BMR (Iwamoto, 1979). When EE was estimated from ME intake and BMR was calculated (70 kcal·BWkg0.75) as presented in Table 2-1, the daily ME requirement for lean adult squirrel monkeys was 184 kcal·BWkg0.75 (2.63 × BMR) compared with 152 kcal·BWkg0.75 (2.17 × BMR) for obese squirrel monkeys (Ausman et al., 1985). A study comparing energy intakes and requirements among adults of three primate families found ME intakes of 137-255 kcal·BWkg0.75 by marmosets (Callitrichidae), 87.9-118 kcal·BWkg0.75 by apes (Pongidae), and 86.3-122.8 kcal·BWkg0.75 by lemurs (Lemuridae)(King, 1978). Those ME intakes were equivalent to an average of 198, 34, and 78 kcal·BWkg-1·day-1 for the three groups, respectively (Table 2-2). For marmosets, the average ME intake was 2.07 × BMR, whereas for both lemurs and apes, ME intake was about 1.4 × BMR (for BMRs shown in Table 2-1). Body weights were sustained in adult male and female rhesus monkeys (M. mulatta) when animals were fed an amount of a commercial diet (3.47 kcal ME·g-1) targeted to meet an expected daily maintenance requirement of 93 kcal·BWkg0.75 (Robbins and Gavan, 1966). Daily estimated ME intakes of 40.8 kcal·BWkg-1 for males and 42.2 kcal·BWkg-1 for females were less than those reported for M. mulatta in other studies (Table 2-2). Adult female baboons (Papio sp.), weighing an average of 15.6 kg, were fed a commercial diet (about 3.1 kcal ME·g-1) providing an average ME intake of 48 kcal·BWkg-1·d-1 (Table 2-2). That energy intake apparently met maintenance requirements on the basis of sustained body weights over a 4-week period (Wene et al., 1982). Mixed zoo diets containing an average calculated ME concentration of 3.6 kcal·g-1 and fed ad libitum to adult female proboscis monkeys (Nasalis larvatus) with an estimated mean body weight of 9 kg resulted in an estimated maintenance ME requirement of 3 × BMR, 1.5 times as great as the predicted maintenance requirement (2 × BMR) based upon body weight (Dierenfeld et al., 1992) (Table 2-1). Intakes of mixed diets by adult wild and captive aye-ayes (Daubentonia madagascariensis) were measured, and ME intakes were estimated to be 260-342 and 260 kcal· day-1 for wild and captive animals, respectively. A combined daily ME requirement was established at 280 kcal (Sterling et al., 1994). The ME intake by captive aye-ayes in relation to body weight was 106 kcal·BWkg-1·day-1 (Table 2-2). Wild adult female and male orangutans (Pongo pygmaeus) have been estimated to weigh an average of 37.8 and 83.6 kg, respectively (Rodman, 1984). For an estimated ME requirement of 40 kcal·kg-1·day-1, the daily ME requirements of the female and male orangutans would be 1,512 and 3,344 kcal, respectively. During the month of greatest fruit consumption, wild adult female and male orangutans of unknown weight consumed an estimated 7,404 and 8,422 kcal ME·day-1, respectively. During the month of lowest fruit consumption, female and male orangutans consumed only an estimated 1,793 and 3,824 kcal ME·day-1, respectively (Knott, 1998). Although energy intakes during the period of low fruit availability appear adequate, on the basis of the above estimates of body weight and ME requirements, urinary ketone concentrations indicated that the wild orangutans were not maintaining energy balance but were losing weight. Commercial diets for long-term maintenance of marmosets and tamarins, formulated to contain 3.5-4.2 kcal ME·g-1, have helped to prevent “marmoset wasting syndrome” among Callithrix jaccus, C. jaccus jaccus, C. jaccus penicillata, Saguinus oedipus oedipus, and S. fuscicollis illigeri (Wirth and Buselmaier, 1982; Clapp and Tardif, 1985). Purified diets fed to adult male cotton-top tamarins (Saguinus oedipus) and providing 160 kcal GE·BWkg-1· day-1 (154 kcal ME·BWkg-1·day-1) (Table 2-2) alleviated signs of the wasting syndrome (Escajadillo et al., 1981). An open-formula, natural-ingredient diet providing 335 kcal GE·BWkg-1·day-1 (232 kcal ME·BWkg-1·day-1) (Table 2-2) alleviated signs of the wasting syndrome in mustached tamarins (Saguinus mystax) (Barnard et al., 1988). The daily ME intake for maintenance of adult cotton-top tamarins (Saguinus oedipus oedipus) was found to decrease with age—208 kcal·BWkg-1 for a 2-year-old male and 113 kcal·BWkg-1 for an aged male (Kirkwood and Underwood, 1984). Energy Requirements for Growth Infant nonhuman primates require more energy per unit of BW for growth than do adults of their species (Stahl and Malinow, 1967; Kerr, 1972; Nicolosi and Hunt, 1979; King, 1978; Ausman, 1995). Energy requirements for growth depend on the rate and composition of gain, which can vary, particularly among wild animals influenced by seasonally variable environments (Robbins, 1993b). The mass-specific BMRs of young, rapidly growing animals are higher than those of adults because body surface area per unit of body mass is greater in the young (Scott, 1986; Robbins, 1993b); the mass-specific BMR can reach 3-4 times that of the adult (Clarke et al., 1977). Although growth of an animal is commonly described by a sigmoid curve, most of the growth occurs during a relatively linear intermediate phase. Maximal growth rates of the young of different species during this linear phase tend to increase as a power function of adult BW. The relationship between adult BW (X in g) and growth rate (Y in g·day-1) of neonates in 160 species of placental mammals has been calculated to be Y = 0.0326X0.75 (r2 = 0.94). The same relationship in 32 species of primates was calculated to be Y = 0.2165X0.35 (r2 = 0.66) (Robbins,

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 TABLE 2-2 Biologic and Metabolic Parameters of Species Fed Dry Diets Species Sex n Age (y) Body Weight (kg) DMa Intake (g·BWkg-1·d-1) MEb Intake (kcal·BWkg-1·d-1) DMc (% dig.) GEd (% dig.) Reference Aye-aye Daubentonia madagascariensis M/F 4 adult 2.46 45.9 106   Sterling et al., 1994 Baboons Papio sp. F 11 adult 15.6 15.4 48   Wene et al., 1982 P. ursinus F 17 adult 18.8 16.0 51 Bielert and Busse, 1983 P. cynocephalus and P. anubis F 6 adult 20.0 17.1 58 Roberts et al., 1985 Guerezas (values for 3): Colobus guereza kikuyuensis, Pygathrix nemaeus nemaeus, Trachypithecus f. francoisi M 7 adult 7.54 28.3 110DE 81.2 80.9 Edwards and Ullrey, 1999b Howlers (values for 3): Alouatta caraya, A. villosa palliata, A. seniculus sara M 7 adult 7.52 17.6 57.9DE 69.3 68.5 Edwards and Ullrey, 1999b Lemuridae (values for 3): Lemur fulvus mayottensis, L. mongoz mongoz, L. catta M/F 13 adult 2.5 22.0 78.0   King, 1978 F 3 adult 4.58 30.0 66.2DE 53.3 48.8 Edwards and Ullrey, 1999a F 2 adult 4.83 27.4 61.7DE 47.7 44.4 Edwards and Ullrey, 1999a Macaca Macaca mulatta M 3 adult 9.0 11.6 40.8   Robbins & Gavan, 1966 M. mulatta F 14 adult 6.6 12.0 42.2 Robbins & Gavan 1966 M. mulatta F 9 7-12 7.8 21.1 71.3 Henderson et. al., 1993 M. mulatta M 6 6.5-7 9.0 22.2 75.7   84.0 Lane et al., 1995 M. mulatta M 6 8.5-10 9.0 23.8 83.8 87.0 Lane et al., 1995 M. mulatta M 3 >24 8.3 15.2 44.5 80.0 Lane et al., 1995 M. mulatta M 15 11-17 13.8 13.0 51.4   Ramsey et al., 1997 M. mulatta M 8 >20 16.5 15.0 53.5 DeLany et al., 1998 M. mulatta M 7 21 16.4 14 54.5 Bodkin et al., 1995 M. fasicularis M 16 9-10 5.7 30.0 110.0 Cefalu et al., 1997 Marmoset Callithrix jacchus jacchus and C. argentata M/F 8 adult 0.44 52 198   King, 1978 Cebuella pygmaea M/F 5 adult 0.133 55 208DE 84.0 84.0 Power, 1991 Callithrix jacchus M/F 8 adult 0.355 63 208DE 77.0 75.0 Power, 1991 C. j. jaccus M/F >10 adult 0.300 41 142   Wirth and Buselmaier, 1982 Pongidae (values for 3): Gorilla gorilla gorilla, Pongo pongo pygmaeus, P. pongo abelii M/F 6 adult 76.5 8.8 34   King, 1978 Proboscis monkey Nasalis larvatus F 5 adult 9.0 25.7 93 88.5   Dierenfeld et. al., 1992 Squirrel monkey Saimiri sp. M 4 10-15 0.95 44.5 176   Weindruch et. al., 1995 Tamarin Saguinus oedipus linneaus M 4 adult 0.432 40.5 154 73.0   Escajadillo et. al., 1981 S. mystax M/F 39 adult 0.534 72.0 232 85.7 Barnard et. al., 1988 Leontopithecus rosalia M/F 9 adult 0.678 44.0 169DE 85.4 86.0 Power, 1991 S. fuscicollis MF 7 adult 0.311 97.0 310DE 74.3 71.0 Power, 1991 S. oedipus M/F 10 adult 0.472 61.0 224DE 83.0 82.0 Power, 1991 aDry matter intake. bMetabolizable energy unless designated as digestible energy (DE). cDry matter digestibility in percent. dGross energy digestibility in percent.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 1993b). A comparative description of growth in humans and chimpanzees has been published by Smith et al. (1975) and in chimpanzees and gorillas by Leigh and Shea (1996). However, energy requirements for growth were not reported. Because dietary energy requirements differ so widely among various animal species, generalizations about daily requirements for growth must be viewed cautiously. The composition of tissues deposited during growth and measured as weight gain significantly influences required dietary energy inputs. Each gram of protein deposited represents about 5.4 kcal of net energy; each gram of fat, about 9.1 kcal of net energy (Scott, 1986; Robbins, 1993b). However, this is far from the full story. Energy losses are associated with digestion of the gross energy in food and with metabolism of the absorbed energy as growing tissues are synthesized. In low-birth-weight human infants, it has been calculated that 10.8 kcal of dietary ME is invested for each gram of fat gain and 13.4 kcal for each gram of protein gain; this is similar to calculations for other animal species with simple stomachs (Roberts and Young, 1988). The average amount of dietary ME used for maintenance and activity in low-birth-weight infants fed different diets was 34.7 kcal·BWkg-1·day-1. Total EE data collected with DLW from low-birth-weight infants suggests that these infants have a total EE and, therefore, an energy requirement about 20% greater than that of normal-birth-weight infants (Davies, 1998). Reviews of total EE measurements of normal-weight babies indicate that energy intakes during the first year of life are considerably below current international recommendations. Those recommendations—95 and 84 kcal ME·BWkg-1·day-1 for infants from birth to 6 months and from 6 to 12 months, respectively—were based on intakes by healthy infants in developed countries (FAO/ WHO/UNU, 1985). They are based on energy expenditure plus energy storage as determined with deuterium. The estimates can be used to calculate dietary ME requirements if the ME values of foods consumed are estimated correctly. Energy stored in new tissue of growing human infants can be estimated by monitoring changes in BW over time, assuming that each gram of BW gained or lost represents 5.6 kcal (FAO/WHO/UNU, 1985; Davies, 1998). If an infant gains 40 g in a week, 224 kcal of energy would be stored as new tissue per week, assuming that that new tissue has a consistent energy density of 5.6 kcal·g-1. Dietary energy (as ME) expended each day for growth has been estimated to be 1.9 kcal·BWkg-1 at 10-15 years, 0.96 kcal·BWkg-1 at 15 years, and 0.48 kcal·BWkg-1 at 16-18 years (FAO/WHO/UNU, 1985). A similar assumption has been made for growth in other animals, in that 5.6 kcal per gram of expected BW gain is intermediate between a theoretical maximum of about 9 kcal·g-1 for fat deposition and a low of 1.5-3.5 kcal per gram of BW gain reported for white-tailed deer, field mice, and voles, animals that accumulate relatively little fat during neonatal growth (Robbins, 1993b). However, diversity in body size among nonhuman primate species creates difficulty in computation of energy needs and efficiencies. In comparing energy allocations with growth and homeothermy, McClure and Randolph (1980) found that the smaller cotton rat (Sigmodon hispidus) has a shorter gestation period, is weaned sooner, has larger litters, and reaches sexual maturation faster than the larger eastern wood rat (Neotoma floridana). Thus, it appears that young of the smaller species can allocate their energy preferentially to rapid development of physiologic functions rather than to growth. Conversely, young of the larger species can emphasize efficient growth and experience a long period of dependence on maternal investment in that growth. The authors advanced the hypothesis that, in general, large species defer onset of active thermoregulation until body masses of the young are greater (when mass-specific metabolic rates are lower) to permit more-efficient early growth. Small species sacrifice growth efficiency in favor of rapid attainment of early independence and consequently pay high energy costs to do so. If valid, that hypothesis might also apply to nonhuman primates, with species that range in adult weight from less than 100 g to more than 200 kg. When daily intakes of semipurified diets by male and female squirrel monkeys (S. sciureus) weighing 846-1,552 g were measured for a 26-week period, the estimated ME requirement (mean ± SD) for maintenance was 179 ± 19 kcal·BWkg-1·day-1. Sex, caloric density of the diet, and dietary fat content did not affect the maintenance requirement. After 24 weight gain or loss periods were measured, the cost of weight gain or loss was determined to be about 7.7 kcal·g-1 (only slightly higher than the previously discussed factor of 5.6 kcal·g-1). Body-composition changes were not determined (Ausman et al., 1981). It has been proposed that energy requirements for infant New World monkeys are 300-500 kcal GE·BWkg-1·day-1 compared with 200-300 kcal GE·BWkg-1·day-1 for infants of the larger Old World species (NRC, 1978; Nicolosi and Hunt, 1979). However, the New World data were derived only from studies of very small species, and such a generalization seems unwise. Both Old World and New World monkeys were reported to have an adult energy requirement that was lower by 30-50% on a kcal·BWkg-1·day-1 basis than requirements for growth (Nicolosi and Hunt, 1979). That is similar to the finding in humans that, although total daily EE increases between the age of 10 years and maturity (on the basis of BMR and activity estimates), daily EE per kilogram of BW decreases by about 34% and 30% for males and females, respectively (FAO/ WHO/UNU, 1985). Smaller primate species exhibit higher mass-specific energy requirements for growth than larger primate spe-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 cies. Ausman et al. (1970) reported that infant squirrel monkeys fed a commercial human infant formula consumed 450 kcal ME·BWkg-1·day-1, a caloric intake greater, relative to weight, than that of physically larger, 8-week-old cebus monkeys that consumed 300 kcal ME·BWkg-1· day-1. An average caloric intake of 200-250 kcal ME·BWkg-1·day-1 supported growth of healthy, young male squirrel monkeys (initial BW of 695 g) fed a dry commercial monkey diet (Ausman et al., 1985). When semipurified liquid and solid diets were fed to neonatal squirrel monkeys through adulthood, ME intakes approached 500 kcal·BWkg-1·day-1 during infancy and decreased to 208 kcal·BWkg-1·day-1 for lean adults (average BW, 788 g) and to 155 kcal·BWkg-1· day-1 for obese animals (average BW, 1,411 g) (Ausman et al., 1985). Growth patterns of infant squirrel monkeys fed semipurified diets (Ausman et al., 1979) are shown in Table 2-3. Both caloric intakes per kilogram BW and growth rate decreased with time and increasing body size to a final weight of 500 g. Weight gains of young male (104-156 weeks old) and young female (128-220 weeks old) squirrel monkeys (S. sciureus) fed a commercial monkey biscuit (3.1 kcal ME·g-1) were 0.88 and 0.50 g·day-1, respectively (Ausman et al., 1981). In contrast, weight gains of squirrel monkeys fed semipurified diets (21-31% of calories as coconut or corn oil, 13% as protein, and 25-35% each as sucrose and dextrin) were 2.89 and 0.89 g·day-1 for males and females, respectively. Data from those two studies suggest that the sources of energy in a diet play a role in the induction of spontaneous obesity. The markedly increased weight gain of squirrel monkeys fed the high-fat, purified diets indicates that dietary fat can be important in the regulation of body weight, as was found for rodents (Ausman et al., 1985). When the same diets were fed to Cebus albifrons, however, nutritional obesity did not develop before or during a 7-year period after sexual maturation (Ausman et al., 1981). Infant baboons (Papio spp.) were fed similar volumes of two formulas with different caloric densities (0.92 and 0.49 kcal ME·g-1) for an 18-week preweaning period (Lewis et al., 1984). Mean total ME intakes by males and females fed the high-calorie formula were 34.4 and 32.5 megacalories (Mcal), respectively. Both males and females fed the low-calorie formula consumed an average of 20.1 Mcal of ME. Males fed the high-calorie formula gained 145 g more lean mass than females, but fat-mass increases were similar in the two. When fed the low-calorie formula, males gained 150 g more lean mass than did females, but females gained 74 g more fat mass. Animals in another group fed a formula with an intermediate caloric density (0.67 kcal ME·g-1) consumed an average of 24.9 Mcal of TABLE 2-3 Biologic and Metabolic Parameters of the Young of Various Species Fed Liquid or Dry Diets Species Sex n Age (y)a Weight (kg) MEb (kcal·d-1) MEc (kcal·BWkg-1·d-1) Growth Rate (g·d-1) Diet Typed Reference Saimiri sciureus     M/F 42 N 0.150 65 433 3.4 SP Ausman et al., 1979 M/F 42 I 0.200 81 405 2.5 SP Ausman et al., 1979 M/F 42 I 0.300 112 373 1.8 SP Ausman et al., 1979 M/F 42 J 0.400 123 308 1.3 SP Ausman et al., 1979 M/F 42 J 0.500 135 270 0.6 SP Ausman et al., 1979 M/F 6 J 0.788 166 210   SP Ausman et al., 1981 M/F 13 I 0.110 49.5 450 SP Ausman et al., 1970 Cebus albifrons     M/F 9 I 0.300 97.5 325   SP Ausman et al., 1970 Macaca fascicularis     M/F 10 I 0.400 116 290   SP Ausman et al., 1970 Macaca mulatta     M/F 5 30d 0.65 178 272 6.6 SP Kerr et al., 1975 M/F 5 210d 1.71 375 219 5.1 SP Kerr et al., 1975 M/F 5 220d 1.76 386 219 5.0 SP Kerr et al., 1975 M/F 5 360d 2.37 539 226 3.8 SP Kerr et al., 1975 M/F 6 J 4.50 605 136   N Hansen and Jen, 1979 M/F 6 J 6.50 748 115 N Hansen and Jen, 1979 M/F 16 J 4.50 482 107 SP Hansen and Jen, 1979 M/F 16 J 6.50 546 84 SP Hansen and Jen, 1979 Chimpanzee     M 1 2-mo 2.94 226GE 76.8GE   — Bruhn and Benedict, 1936 aN=neonate, I=infant, J=juvenile. bDaily metabolizable energy (ME) intake unless designated as gross energy (GE). cMetabolizable energy intake·kg-1·d-1 unless designated as gross energy (GE). dDiet type: SP=semipurified, liquid, N=natural ingredient, liquid.

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 ME, an intake that resulted in total body weight gains similar to those of breast-fed baboons. A semisynthetic diet that provided 4.00 kcal ME·g-1 (high fat and sugars) sustained good weight gains (an average of 110 g·wk-1)in young male and female baboons (Papio ursinus) over a 70-week period (Du Bruyn and De Klerk, 1978). At birth, male and female cynomolgus monkeys (Macaca fascicularis) weighed an average of 402 and 362 g, respectively (Willes et al., 1977). Nursery-reared infants were fed a lactose-fortified formula providing initial intakes of 140 kcal ME·BWkg-1·day-1 to both sexes and rising at 30 days to intakes of 325 and 290 kcal ME·BWkg-1·day-1 for females and males, respectively. Caloric intake declined to 200 kcal ME·BWkg-1·day-1 for males at the age of 140 days and to 250 kcal ME·BWkg-1·day-1 for females at the age of 100 days. Kerr (1972) reported declining daily ad libitum intakes of commercial milk products by infant rhesus monkeys between the ages of 1 month and 1 year, with energy intakes declining from 270 to 190 kcal ME·BWkg-1·day-1. Starting at birth, M. mulatta weighing an average of 0.48 kg were fed a human liquid formula supplying 0.67 kcal ME·ml-1 (Kerr et al., 1975). These infant macaques exhibited decreasing caloric intakes per kilogram of BW with increasing age through 360 days and a decreasing rate of weight gain (Table 2-3). At peak lactation, the suckling young of most mammalian species consume milk energy at about 225 kcal BWkg0.83 daily from milk (Oftedal, 1984). “Milk energy” refers to the GE concentration (kcal·g-1) of the milk and does not account for the metabolic costs of milk production by the mother (Tilden and Oftedal, 1995). Diets in liquid form are essential for neonates, and commercially prepared human-infant formulas providing ME at about 0.67 kcal·ml-1 have been used as milk replacers for some nonhuman primates. However, these human milk replacers might have to be modified to meet the special nutritional requirements of some species (Ausman and Gallina, 1979; Lewis et al., 1984; Riopelle et al., 1986; Rutenburg and Coelho, 1988). Milk replacers with ME concentrations of 0.7 kcal·ml-1, mineral salts at 0.68 g per 100 kcal-1, and 38.5% of calories from lactose produced apparently normal growth in newborn squirrel monkeys (Saimiri sciureus) and cebus monkeys (Cebus albifrons and apella). Older monkeys (older than 3 months) tolerated substitutions of other carbohydrates for lactose and grew well on a liquid diet formulated to contain ME at 1 kcal ml-1, increased mineral salts per 100 kcal (68% above infant diets), and 51% of calories from a mixture of equal concentrations of sucrose and dextrin (Ausman and Gallina, 1979). Growth in clinically normal baboons (P. cynocephalus anubis) was observed during and after feeding of a control, medium-calorie (0.68 kcal ME·g-1) liquid diet, a low-calorie (0.41 kcal ME·g-1) liquid diet, or a high-calorie (0.95 kcal ME·g-1) liquid diet (Rutenberg and Coelho, 1988). After 16 weeks, when the high- and low-calorie-fed baboons were returned to ad libitum feeding of the control diet, their growth patterns returned to normal by 26 weeks. The research data suggest that in the absence of substantial dietary stressors, growth rates appear to be controlled by a genetic component. “Catch-up” and “catch-down” growth adjustments occur in the same timeframe. However, the consequences of undernutrition and the resulting growth suppression were more negative in this study than those of overnutrition. Males generally resumed normal growth patterns, and females retained the effects of neonatal dietary manipulation throughout later studies (Lewis et al., 1986; Rutenberg and Coelho, 1988; Lewis et al., 1989). Young, growing adolescent (over 4 kg) rhesus macaques (Macaca mulatta) were fed either a commercial dry diet with 4.18 kcal GE·g-1 or a highly digestible liquid diet formulated for human use with ME at 1.0-1.1 kcal·ml-1 (Hansen and Jen, 1979). Both diets provided sufficient energy. However, energy intakes on both diets decreased with increasing BW and age. Animals weighing 4-4.9 kg consumed 136 kcal ME·BWkg-1·day-1 on the dry diet versus 107 kcal ME·BWkg-1·day-1 on the liquid diet, whereas animals weighing 5-5.9 kg consumed 6.6% fewer calories from the dry diet and 13.1% fewer calories from the liquid diet per kilogram of BW. Heavier, young adult monkeys, weighing 6-8 kg, consumed the dry or liquid diet with ME at an average of 115 or 84 kcal BWkg-1·day-1, respectively (Table 2-3). Young, growing male and female pig-tailed macaques (M. nemestrina) weighing 4.5 kg initially and fed a commercial dry diet (15% protein) gained an average of 1 kg·year-1 up to the age of 4 years (Walike et al., 1977). After the fourth year, females continued to gain 1 kg·year-1, but males gained 2 kg·year-1. Energy intake and animal age are important considerations because overconsumption of calories by immature animals can result in excessive weight gain and obesity at or before normal adult weights are reached. Rate of gain of females early in life can markedly influence age and weight at sexual maturity (Steiner, 1987; Lee and Bowman, 1995). Increased calories from dietary fat, 31% versus 12%, fed to premenarchial rhesus monkeys from age 16 months to age 32 months resulted in earlier onset of perineal swelling and menarche despite lower BW. About 80% of the females consuming the high-fat diet exhibited an early first ovulation (at the age of 31-32 months), which was associated with significant differences in endocrine profiles (Schwartz et al., 1988). In a study of the diets of 30- to 70-week-old, free-living female baboons (Papio cynocephalus), energy in the diets of all the animals fell short of their optimums during a 12-month period as determined by comprehensive statistical models developed with data from these animals (Altmann, 1991). Energy limitations during developmental periods of

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 growth affect predictions of reproductive life span, survival traits of infants and juveniles, and probability of survival to adulthood. Periovulatory decreases of 10-35% in caloric intake have been reported for two baboon subspecies, Papio spp. (Wene et al., 1982) and P. ursinus (Bielert and Busse, 1983). Among macaques (Macaca mulatta), caloric intake is reduced during the preovulatory period by about 44% compared with all other phases of the estrous cycle. Increased estrogen has an apparent inhibitory influence on food intake during preovulation among both chacma baboons (Papio ursinus) (Bielert and Busse, 1983) and rhesus monkeys (Kemnitz et al., 1984, 1989). Energy Requirements for Pregnancy and Lactation Energy requirements for pregnancy and lactation remain undefined for nonhuman primates. The recommended dietary allowances for energy for healthy, active women in the first trimester are not different from those for nonpregnant women (National Research Council, 1989; Williams, 1997). However, some suggest an additional 285 or 200 kcal ME·day-1 (13% or 10% increase over 2,200 kcal·day-1) for pregnant women with full or reduced activity, respectively (FAO/WHO/UNU, 1985). Those increases sustain the increase in BMR associated with the developing mass of active tissue (fetal, placental, and maternal) plus additional energy needs for new-tissue synthesis. ME increases of 300-350 kcal·day-1 (14-16%) for the second and third tri-mesters have been recommended (FAO/WHO/UNU, 1985; NRC, 1989; Williams, 1997). The energy cost of lactation equals the energy content of the milk secreted plus the energy cost of milk production. The FAO/WHO/UNU Expert Consultation (1985) recommends that women have an additional energy allowance of 500 kcal ME·day-1 for the first 6 months of lactation on the basis of average milk production of 796 ml·day-1. The average energy concentration of human milk produced by well-nourished mothers is 0.70 kcal GE·ml-1 (FAO/WHO/UNU, 1985). The efficiency with which maternal energy is converted to milk energy in humans is about 80% (range 76-94%) compared with swine, in which conversion efficiency is about 72% (National Research Council, 1998). For humans, about 85 kcal of dietary ME are required for every 100 ml of milk produced (National Research Council, 1989). Voluntary diet consumption tends to increase during gestation, as energy demand increases, although Kemnitz et al. (1984) reported little change in food intake of rhesus monkeys during early pregnancy and suggested that food energy was used more efficiently during pregnant than nonpregnant states. Clarke et al. (1977) estimated that the requirement for energy during pregnancy was 30% above the maintenance requirement. Free-living, lactating nonhuman primates are often severely constrained by dietary energy limitations and foraging distances that increase energy costs by 50-100% above maintenance. Lactating Gelada baboons spent 30% more time in foraging than their nonlactating counterparts, and 75% more time in foraging during peak lactation (Lee and Bowman, 1995). Free-living P. cynocephalus spent 45% more time in feeding when pregnant or lactating than a “semi-provisioned” group, including nulliparous females, that had access to human food refuse. Pregnant or lactating females also consumed more energy per day, 1,084 versus 826 kcal of ME (estimated from physiologic fuel values) (Muruthi et al., 1991). Maternal energy requirements for gestation for lemurs (Eulemur fulvus and E. macaco) and bushbabies (Otolemur crassicaudatus and O. garnettii), based on litter energy (number in litter x individual GE), have been estimated to be 301 and 256 kcal·BWkg0.75 for the respective lemur species and 790 and 393 kcal·BWkg0.75 for the respective bushbaby species (Tilden and Oftedal, 1995). Over the course of gestation, those values represented modest increases (2.5-3.0% for lemurs and 3-6.5% for bushbabies) above maintenance energy requirements—estimated to be 80, 83, 88, and 89 kcal·BWkg0.75·day-1 for E. fulvus, E. macaco, O. crassicaudatus, and O. garnettii, respectively. Average litter size was 1.3 young for the two species of lemurs and 1.35 young for the two species of bushbabies. Typical increases of 23-29% in energy requirements for lactation above nulliparous requirements appear to be linked to milk volume and numbers of offspring (Oftedal and Allen, 1996; Williams, 1997). Maintenance requirements of Callitrichidae have been estimated to be roughly 2×BMR to 2.5×BMR (Kirkwood and Underwood, 1984). These researchers found that during the last 8 weeks of pregnancy, caged female cotton-top tamarins (Saguinus oedipus oedipus) gained 2 g·day-1, but the increase in energy intake above maintenance was not significant (70.0 versus 66.9 kcal ME·day-1, respectively). During lactation, however, their energy intake appeared to double (to 131 kcal·day-1), although no differences in energy intake were noted for mothers with multiple versus single neonates. Lactation is the most energetically demanding phase of reproduction for female mammals and can entail a several-fold increase in maternal food intake relative to consumption during nonreproductive periods (Tilden and Oftedal, 1995). Furthermore, both birth mass and milk output vary with body size, but not in direct proportion to maternal mass. When lactating baboons (P. cynocephalus and P. anubis) were fed 80% or 60% of ad libitum intake—1,052 vs 750 kcal ME·day-1, respectively—the 20% restricted females exhibited a 17-25% increase in efficiency of energy use (Roberts et al., 1985). At 80% of ad libitum intake, milk output and body nutrient stores were protected; but at 60%, milk output was reduced by 20% and body-nutrient mobilization increased. Average energy intake for ad libi-

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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003 tum-fed females was 1,375 kcal ME·day-1 throughout lactation. Energy intakes increased by 11% and 27% during initial and peak lactations, respectively, above the intake of 1,169 kcal ME·day-1 by nonreproductive females. Low maternal food intake clearly impairs lactation performance when severe enough to mobilize body energy stores. Energy requirements for lactation often exceed those for rapid growth. Brody (1945) calculated that average daily output of energy in the milk of mammals is about 124 kcal·BWkg0.75. Milk-energy output and milk yields are proportional to a power function of body weight (BW0.75), but milk yields exhibit a four-fold range among species (45-197 g·BWkg0.75 day-1). Primates are at the low end of this range, with typical daily milk yields of 45-70 g·BWkg0.75 (Oftedal, 1984). At peak lactation, the metabolic mass of the litter (LLM)—(number in the litter) × (average litter-mate weight0.83)—is a more reliable predictor of milk-energy yield than is maternal metabolic mass (maternal weight0.75). It has been proposed that 225 × LLMis an estimate of peak milk energy yield (kilocalores of GE) for most mammalian species (Oftedal, 1984). Primate milks are typically dilute (8.5-34.1% dry matter) with energy concentrations ranging from 0.5 to 0.85 kcal GE·g-1 for Lemuroidea and 1.1 to 1.8 kcal GE·g-1 for several prosimian species (Tilden and Oftedal, 1995; Tilden and Oftedal, 1997). Estimated GE outputs during a single lactation are 5,100-7,500 kcal·BWkg0.75 for bushbabies and 2,100-3,100 kcal·BWkg0.75 for lemurs. Thus, despite the shorter lactation in bushbabies than in lemurs, the estimated total milk-energy transfer of bushbabies is nearly twice that of lemurs relative to maternal metabolic size (Tilden and Oftedal, 1995). 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