Nutrient Requirements of Nonhuman Primates
Second Revised Edition, 2003
THE NATIONAL ACADEMIES PRESS
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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
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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
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*
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
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.
Tables and Figures
TABLES
1-1 |
Prosimian feeding ecology, |
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1-2 |
Callithrix feeding ecology, |
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1-3 |
Cebid feeding ecology, |
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1-4 |
Colobine feeding ecology, |
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1-5 |
Non-colobine cercopithecine feeding ecology, |
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1-6 |
Ape feeding ecology, |
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1-7 |
Form of foregut in genera of subfamily Colobinae, |
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1-8 |
Examples of food consumed by primates in zoos and in the wild, |
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2-1 |
Estimated daily metabolizable energy (ME) requirements (as multiples of BMR) for adult captive animals, |
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2-2 |
Biologic and metabolic parameters of species fed dry diets, |
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2-3 |
Biologic and metabolic parameters for the young of various species fed liquid or dry diets, |
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3-1 |
Common dietary carbohydrates and their digestion, |
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3-2 |
Fiber concentrations in wild-primate diets (% of dry matter) in studies in which over 70% of items were analyzed, |
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3-3 |
Fiber concentrations in wild-primate diets (% of dry matter) in studies in which under 70% of items were analyzed, |
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3-4 |
Fiber levels (% of dietary dry matter) fed to primates in captivity, |
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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, |
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4-1 |
Estimated protein requirements for primates using high-quality reference proteins, |
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4-2 |
Potency of common proteins measured by bioassay in primates, |
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5-1 |
Common names, scientific names, and short-form designations of fatty acids, |
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7-1 |
Survey of data used to estimate vitamin E requirements, |
7-2 |
Estimates of thiamin requirement, |
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7-3 |
Estimates of riboflavin requirement, |
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7-4 |
Estimates of vitamin B6 requirement, |
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7-5 |
Estimates of folacin requirement, |
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7-6 |
Estimates of ascorbic acid requirement, |
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9-1 |
Body weight of captive adult primates, |
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9-2 |
Body weight of captive primates at various stages of development, |
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9-3 |
Primate species identified as potentially at increased risk of obesity in captive environments, |
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9-4 |
Proximate composition of milk from several primate species, |
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9-5 |
Composition of nonhuman-primate milk, human milk, and human-infant formula, |
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9-6 |
Physical characteristics of control (ad libitum-fed) and diet-restricted (30 percent restriction) Macaca mulatta after 4.5 years, |
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9-7 |
Body fat (%) determined with three methods in Western lowland gorillas, |
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10-1 |
Plant species used in feeding captive primates, |
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11-1 |
Estimated nutrient requirements of primate model species fed purified or semipurified diets, |
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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, |
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12-1 |
Composition of important feeds: Energy values, proximate analyses, plant cell wall constituents, data expressed as-fed and dry (100% dry matter), |
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12-2 |
Composition of important feeds: Minerals, data expressed as-fed and dry (100% dry matter), |
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12-3 |
Composition of important feeds: Vitamins, data expressed as-fed and dry (100% dry matter), |
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12-4 |
Composition of important feeds: Amino acids, data expressed as-fed and dry (100% dry matter), |
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12-5 |
Mineral concentrations in macromineral sources, |
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12-6 |
Characteristics and energy values of various sources of fats and oils (data on as-fed basis), |
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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), |
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A-2 |
Weight equivalents, |
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A-3 |
Weight-unit conversion factors, |
FIGURES
1-1 |
Gastrointestinal Tract of Tarsier, |
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1-2 |
Gastrointestinal Tract of Squirrel Monkey, |
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1-3 |
Gastrointestinal Tract of Night Monkey, |
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1-4 |
Gastrointestinal Tract of Woolly Monkey, |
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1-5 |
Gastrointestinal Tract of Vervet Monkey, |
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1-6 |
Gastrointestinal Tract of Macaque, |
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1-7 |
Gastrointestinal Tract of Baboon, |
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1-8 |
Gastrointestinal Tract of Bush Baby, |
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1-9 |
Gastrointestinal Tract of Northern Douc Langur, |
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1-10 |
Gastrointestinal Tract of Colobus Monkey, |
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1-11 |
Gastrointestinal Tract of Chimpanzee, |
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1-12 |
Gastrointestinal Tract of Orangutan, |
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1-13 |
Gastrointestinal Tract of Howler Monkey, |
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1-14 |
Gastrointestinal Tract of Adult Human, |
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3-1 |
Plant Cell Components in the Analytical Fractions of the Sequential Detergent System of Robertson and Van Soest, |