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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003
Nutrient Requirements of Nonhuman Primates
Second Revised Edition, 2003
Committee on Animal Nutrition
Ad Hoc Committee on Nonhuman Primate Nutrition
Board on Agriculture and Natural Resources
Division on Earth and Life Studies
NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES
THE NATIONAL ACADEMIES PRESS
Washington, D.C.
www.nap.edu
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003
THE NATIONAL ACADEMIES PRESS
500 Fifth St., NW Washington, D.C. 20001
NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance.
This study was supported by the Department of Health and Human Services, the American Zoo and Aquarium Association, The Geraldine R. Dodge Foundation, Association of Primate Veterinarians, Harlan Teklad, Purina Mills, Inc., and Zupreem.
Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the organizations or agencies that provided support for this project.
Library of Congress Cataloging-in-Publication Data
Nutrient requirements of nonhuman primates.—2nd rev. ed.
p. cm.—(Nutrient requirements of animals)
Rev. ed. of: Nutrient requirements of nonhuman primates / Panel on Nonhuman Primate Nutrition, Subcommittee on Laboratory Animal Nutrition, Committee on Animal Nutrition, Board on Agriculture and Renewable Resources, National Research Council. 1978.
Includes bibliographical references (p. ).
ISBN 0-309-06989-0 (pbk.)
1. Primates—Feeding and feeds. 2. Primates—Nutrition—Requirements. 3. Primates as laboratory animals. I. National Research Council (U.S.). Committee on Animal Nutrition. II. National Research Council (U.S.). Panel on Nonhuman Primate Nutrition. Nutrient requirements of nonhuman primates. III. Series.
SF407.P7 N88 2002
636.98—dc21 2002013021
Additional copies of this report are available from the
National Academies Press,
500 Fifth St., NW, Box 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet http://www.nap.edu.
Copyright 2003 by the National Academy of Sciences. All rights reserved.
Printed in the United States of America
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003
THE NATIONAL ACADEMIES
Advisers to the Nation on Science, Engineering, and Medicine
The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Bruce M. Alberts is president of the National Academy of Sciences.
The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Wm. A. Wulf is president of the National Academy of Engineering.
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The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Bruce M. Alberts and Dr. Wm. A. Wulf are chair and vice chair, respectively, of the National Research Council
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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003
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 L. RUDEL,
Wake Forest School of Medicine, Winston-Salem, North Carolina
COMMITTEE ON ANIMAL NUTRITION
GARY L. CROMWELL, Chair,
University of Kentucky
MARY E. ALLEN,
National Zoological Park, Washington, D.C.
MICHAEL L. GALYEAN,
West Texas A&M University
RONALD W. HARDY,
University of Idaho
BRIAN W. McBRIDE,
University of Guelph, Ontario, Canada
KEITH RINEHART,
Perdue Farms, Inc., Salisbury, Maryland
L. LEE SOUTHERN,
Louisiana State University
JERRY W. SPEARS,
North Carolina State University
DONALD R. TOPLIFF,
Oklahoma State University
WILLIAM P. WEISS,
The Ohio State University
Staff
CHARLOTTE KIRK BAER, Program Director
NORMAN GROSSBLATT, Editor
STEPHANIE PADGHAM, Project Assistant
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BOARD ON AGRICULTURE AND NATURAL RESOURCES
HARLEY W. MOON, Chair,
Iowa State University
CORNELIA B. FLORA,
Iowa State University
ROBERT B. FRIDLEY,
University of California
BARBARA GLENN,
Federation of Animal Science Societies
LINDA GOLODNER,
National Consumers League
W.R. (REG) GOMES,
University of California
PERRY R. HAGENSTEIN,
Institute for Forest Analysis, Planning, and Policy, Wayland, Massachusetts
GEORGE R. HALLBERG,
The Cadmus Group, Inc.
CALESTOUS JUMA,
Harvard University
GILBERT A. LEVEILLE,
McNeil Consumer Healthcare, Denville, New Jersey
WHITNEY MACMILLAN,
Cargill, Inc., Minneapolis, Minnesota
TERRY MEDLEY,
DuPont Biosolutions Enterprise
WILLIAM L. OGREN,
U.S. Department of Agriculture
ALICE PELL,
Cornell University
NANCY J. RACHMAN,
Novigen Sciences, Inc.
G. EDWARD SCHUH,
University of Minnesota
BRIAN STASKAWICZ,
University of California, Berkeley
JOHN W. SUTTIE,
University of Wisconsin
JAMES TUMLINSON,
USDA, ARS
JAMES J. ZUICHES,
Washington State University
Staff
CHARLOTTE KIRK BAER, Director
STEPHANIE PADGHAM, Administrative Assistant
SHIRLEY B. THATCHER, Administrative Assistant*
*
through March 2000
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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 lemurs 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 Hylobatidae.
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
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Acknowledgments
The Committee wishes to thank the numerous people who provided input by letter or at public forums. In addition, we thank those who took time to meet with the Committee throughout the study process. The financial support provided by the National Center for Research Resources of the National Institutes of Health, the American Zoo and Aquarium Association, The Geraldine R. Dodge Foundation, the Association of Primate Veterinarians, Harlan Teklad, Purina Mills, Inc., and ZuPreem, is gratefully acknowledged.
This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the NRC’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of this report: David J. Baer, US Department of Agriculture Agricultural Research Service, Beltsville, Maryland; Ellen Dierenfeld, The Wildlife Conservation Society, Bronx, New York; Joseph W. Kemnitz, Wisconsin National Primate Research Center, Madison, Wisconsin; Joe Knapka, National Institutes of Health (retired); Terry L. Maple, Zoo Atlanta, Atlanta, Georgia; and Wilson G. Pond, Cornell University, Ithaca, New York. Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations nor did they see the final draft of the report before its release. The review of this report was overseen by R. Lee Baldwin, University of California, Davis. Appointed by the National Research Council, he was responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution. Finally, the Committee wishes to thank Charlotte Kirk Baer, program director, Committee on Animal Nutrition, for her encouragement and cheerful guidance of this project to completion. Her exceptional organizational skills contributed in a major way to the success of the Committee. Appreciation also is extended to Stephanie Padgham, project assistant, for her regular communications and helpful provision of supplementary materials.
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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
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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
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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
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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
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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
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Tables and Figures
TABLES
1-1
Prosimian feeding ecology,
6
1-2
Callithrix feeding ecology,
9
1-3
Cebid feeding ecology,
10
1-4
Colobine feeding ecology,
12
1-5
Non-colobine cercopithecine feeding ecology,
14
1-6
Ape feeding ecology,
17
1-7
Form of foregut in genera of subfamily Colobinae,
24
1-8
Examples of food consumed by primates in zoos and in the wild,
27
2-1
Estimated daily metabolizable energy (ME) requirements (as multiples of BMR) for adult captive animals,
45
2-2
Biologic and metabolic parameters of species fed dry diets,
49
2-3
Biologic and metabolic parameters for the young of various species fed liquid or dry diets,
51
3-1
Common dietary carbohydrates and their digestion,
61
3-2
Fiber concentrations in wild-primate diets (% of dry matter) in studies in which over 70% of items were analyzed,
65
3-3
Fiber concentrations in wild-primate diets (% of dry matter) in studies in which under 70% of items were analyzed,
67
3-4
Fiber levels (% of dietary dry matter) fed to primates in captivity,
69
3-5
Proposed fiber concentrations in total dietary dry matter of extruded diets for primate species grouped by relative ability to utilize plant cell wall,
70
4-1
Estimated protein requirements for primates using high-quality reference proteins,
76
4-2
Potency of common proteins measured by bioassay in primates,
78
5-1
Common names, scientific names, and short-form designations of fatty acids,
88
7-1
Survey of data used to estimate vitamin E requirements,
127
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7-2
Estimates of thiamin requirement,
130
7-3
Estimates of riboflavin requirement,
131
7-4
Estimates of vitamin B6 requirement,
133
7-5
Estimates of folacin requirement,
136
7-6
Estimates of ascorbic acid requirement,
139
9-1
Body weight of captive adult primates,
160
9-2
Body weight of captive primates at various stages of development,
162
9-3
Primate species identified as potentially at increased risk of obesity in captive environments,
164
9-4
Proximate composition of milk from several primate species,
165
9-5
Composition of nonhuman-primate milk, human milk, and human-infant formula,
166
9-6
Physical characteristics of control (ad libitum-fed) and diet-restricted (30 percent restriction) Macaca mulatta after 4.5 years,
171
9-7
Body fat (%) determined with three methods in Western lowland gorillas,
172
10-1
Plant species used in feeding captive primates,
187
11-1
Estimated nutrient requirements of primate model species fed purified or semipurified diets,
192
11-2
Estimated adequate nutrient concentrations in diets containing conventional feed ingredients intended for post-weaning nonhuman primates, accounting for potential differences in nutrient bioavailabilities and adverse nutrient interactions, but not accounting for potential losses in feed processing and storage,
193
12-1
Composition of important feeds: Energy values, proximate analyses, plant cell wall constituents, data expressed as-fed and dry (100% dry matter),
197
12-2
Composition of important feeds: Minerals, data expressed as-fed and dry (100% dry matter),
213
12-3
Composition of important feeds: Vitamins, data expressed as-fed and dry (100% dry matter),
228
12-4
Composition of important feeds: Amino acids, data expressed as-fed and dry (100% dry matter),
242
12-5
Mineral concentrations in macromineral sources,
256
12-6
Characteristics and energy values of various sources of fats and oils (data on as-fed basis),
258
A-1
Taxonomic relationships, genera, and partial list of species in Order Primates, based on Napier and Napier (1985), Oates et al. (1989), and Nowak (1999),
266
A-2
Weight equivalents,
268
A-3
Weight-unit conversion factors,
268
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FIGURES
1-1
Gastrointestinal Tract of Tarsier,
22
1-2
Gastrointestinal Tract of Squirrel Monkey,
22
1-3
Gastrointestinal Tract of Night Monkey,
22
1-4
Gastrointestinal Tract of Woolly Monkey,
22
1-5
Gastrointestinal Tract of Vervet Monkey,
23
1-6
Gastrointestinal Tract of Macaque,
23
1-7
Gastrointestinal Tract of Baboon,
23
1-8
Gastrointestinal Tract of Bush Baby,
23
1-9
Gastrointestinal Tract of Northern Douc Langur,
25
1-10
Gastrointestinal Tract of Colobus Monkey,
25
1-11
Gastrointestinal Tract of Chimpanzee,
25
1-12
Gastrointestinal Tract of Orangutan,
25
1-13
Gastrointestinal Tract of Howler Monkey,
26
1-14
Gastrointestinal Tract of Adult Human,
26
3-1
Plant Cell Components in the Analytical Fractions of the Sequential Detergent System of Robertson and Van Soest,
63
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Nutrient Requirements of Nonhuman Primates
Second Revised Edition, 2003
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