Second Revised Edition, 2003
National Research Council of the National Academies
The National Academies Press
PREFACE
This report is one of a series issued under the direction of the National Research Council's Committee on Animal Nutrition
(CAN) of The National Academies Board on Agriculture and Natural Resources. It was prepared by the CAN Ad Hoc Committee on
Nonhuman Primate Nutrition and is a revision of the 1978 edition of Nutrient Requirements of Nonhuman Primates. Throughout
the study process, input from others has been sought by posing specific questions in widely distributed letters, by hosting
workshops and information-gathering sessions, and by inviting sponsors and the general public to attend meetings of the
Committee. Information published before 1978 has been reevaluated, that in newer publications has been examined, and both
have been used to update this report. Greater emphasis than before has been placed on descriptions of natural dietary habits,
gastrointestinal anatomy and physiology, and the special nutrient and dietary husbandry needs of species that traditionally
have been difficult to maintain in captivity.
The order Primates is diverse and includes prosimians, New World monkeys, Old World monkeys, apes, and humans. More than 250
species and more than 600 subspecies are recognized, and new species are described nearly every year. Recently, Colin Groves
has proposed a revised taxonomic system that includes over 300 primate species (Groves, C. 2001. Primate Taxonomy.
Washington, DC: Smithsonian Institution Press). The challenge of describing the nutritional needs of primates, which range in
size from tiny mouse femurs and pygmy marmosets to the markedly larger gorillas and orangutans, is daunting, particularly
because studies of feeding ecology, gastrointestinal anatomy, and nutrient requirements have been completed for only a few of
them. Consequently, data have been sought on one or more model species in eight categories (the suborder Strepsirrhini; the
families Hominidae and Pongidae, Hylobatidae, Cercopithecidae, Cebidae, Callitrichidae, and Tarsiidae; and the subfamily
Colobinae) in the hope that such data would be representative of the Order. Little information was found on Tarsiidae and
Hylobaddae.
Over 500,000 primates live in biomedical research laboratories and conservation institutions throughout the world. Records of
the regional primate research centers provided by Leo Whitehair of the National Institutes of Health National Center for
Research Resources indicate that 16,820 nonhuman primates of 28 species were present in seven U.S. centers at the end of
1998. In 1999, an eighth U.S. center housing 3,638 animals, including about 3,200 baboons, was added. Records of the
International Species Information System (at the Minnesota Zoological Garden, Apple Valley, MN; www.worldzoo.org) indicate
that over 9,500 nonhuman primates of 145 species were in U.S. and Canadian zoos at the end of 2000. Additional nonhuman
primates can be found in U.S. and Canadian government, university, and commercial laboratories.
Many primate species serve as surrogates in studies of human physiology and disease, and their nutritional status is known to
influence susceptibility and tissue responses to infective agents. The validity of such research is open to question if the
experimental subjects have not been appropriately nourished. Likewise, the health and reproduction of primates in zoos can be
compromised to an extent that renders the maintenance or multiplication of endangered species impossible.
In preparing this report, the Committee was limited in the amount of reliable and specific information available on nutrient
requirements, deficiencies, and toxicities in primates. The authors of this publication had as their primary objective the
development of guidelines that would ensure that nutrient deficiencies or toxicities and inappropriate dietary husbandry
would not limit success in primate research colonies or zoos. We hope that this objective has been fulfilled, in light of the
limits of the information available to us, and that researchers will continue to fill the obvious information gaps so that
future editions will be more complete.
Duane E. Ullrey, Chair
Ad Hoc Committee on Nonhuman Primate Nutrition
AD HOC COMMITTEE ON NONHUMAN PRIMATE NUTRITION
Duane E. Ullrey, Chair, Michigan State University, East Lansing, Michigan
Mary E. Allen, National Zoological Park, Washington, D.C.
Lynne M. Ausman, Tufts University, Boston, Massachusetts
Nancy L. Conklin-Brittain, Harvard University, Cambridge, Massachusetts
Mark S. Edwards, Zoological Society of San Diego, San Diego, California
Joseph M. Erwin, Diagnon Corporation/Bioqual, Inc., Rockville, Maryland School of
Medicine, University of Maryland, Baltimore
Michael F. Holick, Boston University School of Medicine, Massachusetts
Daniel T. Hopkins, Purina Mills, Inc., retired, St. Charles, Missouri
Sherry M. Lewis, National Center for Toxicological Research,
The Bionetics Corporation, Jefferson, Arkansas
Bo L. G. Lonnerdal, University of California-Davis, Davis, California
Lawrence Rudel, Wake Forest School of Medicine, Winston-Salem, North Carolina
TABLE OF CONTENTS
OVERVIEW, 1
1. FEEDING ECOLOGY, DIGESTIVE STRATEGIES, AND IMPLICATIONS FOR FEEDING PROGRAMS IN CAPTIVITY, 5
Feeding Ecology, 5
Feeding-Ecology, Methods Involving Visual Observations of Behavior, 5
Observation Options, 5
Sampling Methods, 5
Alternative Feeding-Ecology Methods, 13
Analysis of Stomach Contents, 13
Fecal Analysis, 16
Food Remnants, 16
Reporting Feeding Behavior, 18
Feeding Time, 18
Mass of a Food as Percentage of Total Diet Mass, 18
Feeding-Ecology Tables, 18
Plant-Feeding Strategies, 19
Insect Foraging and Feeding, 19
Additional Considerations, 19
How to Use This Information, 20
Digestive Strategies, 20
Faunivores, 21
Frugivores, 21
Folivores, 24
Implications for Feeding Programs in Captivity, 26
References, 27
2. ENERGY, 41
Units of Measurement, 41
Classification, 41
Gross Energy, 41
Digestible Energy, 41
Metabolizable Energy, 42
Physiologic Fuel Values, 42
Requirements, 42
Basal Energy Expenditures or Basal Metabolic Rate, 43
Estimating Basal Metabolic Rate, 43
Effects of Age and Body Composition on Basal Metabolic Rate, 43
Energy Requirements for Maintenance, 43
Energy Requirements for Growth, 48
Energy Requirements for Pregnancy and Lactation, 53
References, 54
3. CARBOHYDRATES AND FIBER, 58
Carbohydrate Classification, Characteristics, Digestion, and Metabolism, 58
Monosaccharides, 58
Disaccharides, 59
Oligosaccharides, 59
Polysaccharides, 59
Starch and Starch-Like Polysaccharides, 59
Non-Starch Polysaccharides. 59
Analytical Procedures for Carbohydrate and Fiber, 61
Crude Fiber, 61
Total Dietary Fiber, 61
Neutral-Detergent Fiber and Related Fractions, 62
Carbohydrates in Wild Food Plants, 64
Significance of Fiber, 66
Proposed Fiber Intakes by Nonhuman Primates, 68
Fiber Recommendations for Other Species, 68
Fiber in Wild Food Plants as Guides for Captive-Diet Fiber
Concentrations, 68
Fiber Digestion by Nonhuman Primates as a Guide for Captive-Diet
Fiber Concentrations, 70
Proposed NDF and ADF Concentrations in Captive Nonhuman Primate
Diets, 70
References, 70
4. PROTEIN, 75
Protein Sources, 75
Assessment of Protein Requirements, 75
Methods, 75
Digestibility, 76
Requirements, 77
Protein Quality, 77
Proteins Limiting in Sulfur Amino Acids, 77
Proteins Limiting in Lysine, 78
Amino Acid Requirements, 78
Lysine and Methionine, 78
Phenylalanine, 79
Tryptophan, 79
Taurine, 79
Efficiency of Protein Use, 79
Protein Deficiency, 80
Protein for Pregnancy and Lactation, 80
Protein-Calorie Malnutrition in Young Primates, 80
Protein Excess, 83
Non-Amino-Acid Effects of Protein Sources, 83
References, 84
5. FATS AND FATTY ACIDS, 87
Fat Absorption, 88
Milk Fats, 89
Essential n-3 Fatty Acids, 89
Essential n-6 Fatty Acids, 90
Detrimental Fatty Acids, 91
Cholesterol, 91
Primates as Cardiovascular Disease Models, 92
References, 92
6. MINERALS, 94
Macrominerals, 95
Calcium and Phosphorus, 95
Magnesium, 97
Potassium, 98
Sodium, 98
Chloride, 98
Sulfur, 98
Trace Minerals, 98
Iron, 98
Copper, 100
Manganese, 101
Zinc, 102
Iodine, 104
Selenium, 104
Cobalt, 106
Chromium, 106
Fluorine, 107
References, 107
7. VITAMINS, 113
Fat-Soluble Vitamins, 113
Vitamin A and Carotenoids, 113
Measures of Biologic Activity, 113
Absorption and Circulation of Carotenoids, 114
Vitamin A and Carotenoids in Feedstuffs, 114
Absorption, Circulation, and Storage of Vitamin A, 114
Vitamin A Deficiency, 115
Vitamin A Requirements, 115
Hypervitaminosis A, 115
Vitamin D, 116
Photobiology, Metabolism, and Function of Vitamin D, 116
Measures of Vitamin D Activity, 117
Vitamin D Deficiency, 117
Discrimination Between Vitamin D2 and Vitamin D3, 118
Metabolic Resistance to Vitamin D3 in Callitrichids, 118
Animals Not Exposed to Natural Sunlight or Unable to Make Vitamin
D in Their Skin, 120
Vitamin D Requirements, 120
Hypervitaminosis D, 121
Vitamin E, 122
Chemistry and Measures of Activity, 122
Absorption, Metabolism, and Excretion, 123
Biologic Functions, 124
Vitamin E Deficiency, 124
Vitamin E Requirements, 125
Vitamin K, 126
Water-Soluble Vitamins, 128
Thiamin, 128
Riboflavin, 129
Pantothenic Acid, 130
Niacin, 131
Vitamin B6, 132
Biotin, 133
Folacin, 134
Vitamin B12, 135
Vitamin C, 137
Choline, 140
Carnitine, 141
Inositol, 141
References, 142
8. WATER, 150
Water Content of the Body, 150
Effects of Activity Restriction, 152
Effects of Cold, 152
Effects of Heat and Water Deprivation, 152
Water Sources, 153
Liquid Water Intake, 153
Preformed-Water Intake, 154
Metabolic Water, 154
Water Loss, 154
Water Quality, 155
Water Requirements, 156
References, 157
9. PATHOPHYSIOLOGIC AND LIFE-STAGE CONSIDERATIONS, 159
Body Weight, 159
Nutrition from Birth to Weaning, 159
Growth, 159
Mother-Reared Infants, 161
Artificially Reared Infants, 161
Milk Volume and Composition, 161
Volume, 161
Composition of Mother's Milk, 164
Nutrient Intakes for Milk Replacers, 164
Formulas Used for Artificially Rearing Infant Nonhuman Primates, 165
Long-Term Consequences of Different Modes of Infant Feeding, 166
Weaning Foods and Strategies, 167
Nutrition and Aging, 167
Dietary Restriction, 167
Bone, 170
Immunology' 170
Wound Healing, 170
Atherosclerosis, 171
Body Composition, 171
Obesity, 172
Regulation of Glucose Metabolism, 174
Diabetes, 174
References, 176
10. DIET FORMULATION, EFFECTS OF PROCESSING, FACTORS AFFECTING INTAKE, AND DIETARY HUSBANDRY, 182
Diet Formulation, 182
Natural Dietary Habits, 182
Digestive System Structure and Physiology' 182
Nutrient Requirements, 182
Feedstuffs, 182
Diet Formulation, 182
Effects of Processing, 183
Factors Affecting Intake, 184
Influence of Visual, Olfactory, Taste, and Tactile Clues on Food
Acceptance, 185
Regulation of Food Intake, 185
Dietary Husbandry, 186
Primary Food Source, 186
Supplements, 186
Browse, 187
References, 188
11. NUTRIENT REQUIREMENTS, 191
References, 194
12. COMPOSITION OF FOODS AND FEED INGREDIENTS, 195
References, 195
13. FOOD AS A COMPONENT OF ENVIRONMENTAL ENHANCEMENT, 259
Goal of Environmental Enhancement, 259
Role of Food and Foraging, 259
Wild Environment versus Captivity' 260
Species Differences, 261
Manipulation of Foraging Opportunities, 261
Live Prey, 262
Exudates and Gums, 262
Water, 262
Higher-Fiber Foods, 263
Epilogue, 263
References, 263
APPENDIX, 266
ABOUT THE AUTHORS, 269
INDEX, 273
WHERE TO ORDER
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NOTE: We have a second copy Of NUTRIENT REQUIREMENTS OF NONHUMAN PRIMATES available for review. If you are interested in
writing a review for this book for Primate-Science, please send your request to amask@primate.wisc.edu (Al Mask). wprc/lj
Posted Date: 04-02-03
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