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Nonhuman Primates: Usage and Availability for Biomedical Programs (1975)

Chapter: Supporting Data: Nancy A. Muckenhirn

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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Page 24
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Page 27
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 28
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 29
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 30
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 31
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 32
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 33
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 34
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 35
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 36
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 37
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 38
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 39
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 40
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 41
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 42
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 43
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 44
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 45
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 46
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 47
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 48
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 49
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 50
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 51
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 52
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 53
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 54
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 55
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 56
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 57
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 58
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
×
Page 59
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Page 60
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Page 61
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Page 62
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Page 63
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Page 65
Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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Suggested Citation:"Supporting Data: Nancy A. Muckenhirn." National Research Council. 1975. Nonhuman Primates: Usage and Availability for Biomedical Programs. Washington, DC: The National Academies Press. doi: 10.17226/18765.
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SUPPORTING DATA Attitudes and Historical Trends in Primate Usage Impressive contributions to public health have been made possible through the application of information derived from the use of laboratory animals in studies of basic biomedical problems and diseases. The most striking example of the benefit derived from the use of primates in research was the development of polio vaccine. The close phylogenetic relationship between monkeys and man has been cited repeatedly as a justification for using primates in research. Two recent statements by researchers crystallize the variance of scientific viewpoints that have developed on this topic. Typical of those investigators who specialize in the study of human medicine and look for an experimental substitute in the primate is E.I. Goldsmith, M. D. , chairman of the utilization committee for the Laboratory for Experi- mental Medicine and Surgery in Primates, who stated: Our attitude is that when the fundamental research reaches a point where it needs to be translated toward human use, then it is logical to interpose the primate as an approximate of the human condition. (Zucker, 1974) In general, scientists who have a medical orientation, a professional af- filiation with a primate facility, or are in applied research with vaccine and drug testing will promote the use of primates. These scientists usually estimate that increasing demand will always exceed supply. In contrast, scientists specializing in basic biological research have generally taken a more comparative stand, such as W. G. Hoag (1974): The ultimate test of any product for human usage must be made in man himself. The pretesting of such products in animal models is an important step leading to this final test. It is important that the animal model selected provides the test system which simulates the one in the human biological system. This similarity does not necessarily relate to the phylogenetic proximity of the animal species to the human species. It is important for investigators in planning animal experiments to look first for the model biological system. Such researchers are generally affiliated with institutions having facilities for handling many species, including the larger domestic animals, and fre- quently recommend that the expected high costs of captive-bred primates will result in reduced demand for them as scientists are forced to shift to other species. They point out that the low cost and ready availability of primates in the past has resulted in a high rate of usage that has been op- 11

12 portunistic rather than scientifically based. The fact that the U.S.S.R. successfully launched and returned man from outer space based upon extrap- olation from experiments using dogs instead of primates, as was practiced by the United States, is a case in point. The problem of estimating future needs is compounded by a widely felt prestige factor associated with studying primates, which has followed the development of polio vaccine in one species of monkey. This has encouraged the widespread use of primates rather than the limited use of them in studies that are needed to expand the results derived from experiments on more rapidly bred species, including rodents, dogs and cats. As monkeys become more expensive, a greater selectivity in the choice of animal model and multiple use of primates on experiments will become necessary. Institutions that could not afford to hold animals between experiments, or to ship an animal at rates that exceeded the purchase price of a replacement will find that these actions may become economically feasible as relative costs change. Such developments should act to reduce the numbers of animals euthanized for obtaining single organs and consequently the total number of primates needed. Hence, some scientists predict decreasing needs for primates. This range in predictions from greatly increasing needs to stable or decreasing needs creates a major dilemma for those charged with the responsibility of anticipating and planning supplies. The association of value judgments with professional background, affiliation, and research specialty should not be overstressed. However, because economics, prestige, and research specialties continue to color recommendations, it is necessary to identify and separate these factors from the question of needs based upon scientific criteria. For the purposes of this report, it is recognized that primates have a significant role to play in certain areas of reproductive endocrinology, immunology, virology, and certain neurological studies. However, metabolic pathways may or may not be similar between primates and man. In certain areas of metabolism, physiology, and biochemistry, nonprimate species would appear to be as useful or more so as disease models. The advantages of dogs for many toxicological studies has been reasserted by the Committee on Toxicology (1974). Primates will always be of limited use in studies of genetics because of their slow reproduction. Shifting needs for numbers and species have occurred. For example, exports of rhesus macaques to the United States alone at the rate of more than 200, 000 individuals in the late 1950's (during the development of polio vaccine), were limited a decade later by the Indian government to around 50, 000 for the entire world (Hartley, 1972). While the needs of monkeys for polio research have decreased, demand for other species-- most noticeably, New World monkeys--has been created in the past few years due to developments in such research areas as viruses, hepatitis, and malaria. Numerically, the most important species for medical research and drug testing has been the rhesus macaque, followed by other macaques, baboons, and vervet monkeys. The obvious reasons for the early popularity of these species was their greater survival rate under early captive conditions when little was known about nutritional needs. The extensive accumulation of baseline data, especially on the rhesus macaque, has increased its value for continued use. In one respect it is fortunate that these semiterrestrial

13 species became popular in a commercial trade that depended upon wild caught animals. Their large geographical distributions and adaptability to many habitats protected them from decimation. They are favored in areas of mixed forests and open land and even increase in areas of subsistence agriculture as commensals of man. However, their continued survival demands that plans for their captive breeding and their management as a second crop on agricultural land be examined, as changing attitudes and more intensive, technological agriculture and forestry reduce cultural tolerance for agricultural pests. Current Volume of the Primate Trade Species Commonly Imported to the United States Of the 82 species of primates imported into the United States over the past 3 years, 13 species comprise 96-98 percent of the total volume (Table 1). The two most important species are the squirrel monkey and the rhesus macaque, which together account for roughly 62-65 percent of all imports. Import statistics for the United States are published in three forms. Overall volumes of wildlife imports have been published by the Fish and Wildlife Service of the U.S. Department of the Interior (USDI, 1968-1 970a, 1971-1973). The mammals imported between 1968 and 1972 are also itemized by species in several reports by the same agency (Jones, 1970; Jones and Paradiso, 1970; Paradiso and Fisher, 1971; Clapp and Paradiso, 1973; and USDI, In preparation). It is unclear why the volumes of the latter reports are generally 10 percent lower than the former. Additional statistics are published by the U.S. Department of Commerce (USDC, 1965-1974). The statistics for rhesus macaques and for totals are compared in Table 2. The records maintained by the Indian government concerning monkeys exported to the United States are generally 10-percent higher than those for monkeys received by the United States. Trends in the Export of Primates to the United States The numbers of primates exported from the major supply countries are presented in Table 3. India, Peru, and Colombia are the only countries that have exported more than 20, 000 primates during any year within the past decade. These three countries are responsible for 78 percent of the 1973 primate trade. Another 6 countries, Pakistan-Bangladesh, Thailand, Malaysia, the Philippines, Ethiopia, and the Somali Republic have exported over 2, 500 primates during one or more years since 1964. These account for an additional 13 percent of the primate trade. The total numbers exported to the United States from all countries decreased by 32 percent from 1964 to 1973. Most of the major source countries except Malaysia, which has fluctu- ating export numbers, have exported decreasing numbers of primates over the past decade. The steady 6-year decline in numbers from Peru and

14 TABLE 1 SPECIES COMMONLY IMPORTED INTO THE UNITED STATES* No. Imported Species 1970 1971 1972 Saimiri sciureus Macaca mulatta Cebus sp. Saguinus sp. Aotus trivirgatus Cercopithecus aethiops and C-. pygerythrus Lagothrix lagotricha A teles geoffroyi Macaca arctoides Macaca fascicularis Papio sp. Macaca nemestrina Pan troglodytes TOTAL IMPORTS 26, 124 23,302 5,935 4,189 4,209 106 244 ,870 070 609 753 662 185 29,877 22,097 5,619 5,333 3,728 2,817 2,226 1, 617 1,207 1,727 1,092 436 205 25,295 23,210 6,063 5, 545 3, 533 3,272 2, 125 1,841 1,676 1,397 1, 328 581 234 78,375 79,691 77,636 SOURCE: Data from Paradiso and Fisher (1971); Clapp and Paradise (1973). *See Appendix I for a comparison of common and scientific names

15 TABLE 2 TOTAL PRIMATES IMPORTED INTO THE UNITED STATES COMPARED WITH EXPORTS FROM INDIA Total U.S. Imports, by Source* and Type Exports from Rhesus Imports India ** Year A B C Macaques § from India? U.S. Worldwide 1964 102,080 31,640 35,159 1965 96,112 27,121 30,559 1966 103,859 26,268 28,557 1967 104,346 62,526 30,849 34,937 48,617 1968 126,857 124,440 113,714 30,933 30,315 34,791 48,162 1969 105,719 99,668 108,974 27,462 29,734 33,930 49,428 1970 90,743 85,151 78,375 23,302 26,056 28,791 41,959 1971 79,846 86,535 79,691 22,097 21,152 23,883 35,296 1972 75,784 90,559 77,632 23,210 21,330 1973 69,548 25,413 *A11 primates, source A=USDC (1965-1974); source B=USDI (1968-1970a, 1971-1973); source C=Jones (1970), Jones and Paradiso (1970), Paradiso and Fisher (1971), Clapp and Paradiso (1973), and USDI (In preparation). §Rhesus data from same sources as C above. JU.S. -India import data from USDC (1965-1974). **Exports from India data from Kawanishi (1972) cited from Monthly Statistics of the Foreign Trade of India.

16 ^ o> ^ DO O a «> « CO Pn ^ .M t^" [TI CJ H w^ 0 f\j CO _j 00 CO + t— co i^ r- o Ov oovo'oo' tN- ro 0 F^ ro ^t* oo in co r^ r^^oor-^ooi— 1 co1 QX CO CO CO *-> CL. 1 1 1 • I-H O^ 1 1 1 H;- 1 1 1 ff) 1 1 W c X ^ H 0) w <} U q Ov H 0) M rM CO FH m in ^H o m oro^fr^mo cr^Tf1oo1 o^ oo CO m CO r-H O ,—! N o co •.* <o t-^ Ov ON P-H ro s^ T^ 0 ^ ^* Q o^ ^ in co ro -H roo^mvor-Hco vo^ NO -H m W ^ in ro" N r-H I-H I-H ro NO ro ro O N vO H ro § o m , o r- o o Tj<O^vQ[--,-Hco oo^1-Hin ^ ^ H CM r*j o m -^ oo mro-Hinoor^ ooro ^ro xO CO a> CO ^f CO vo ro r^ o^ co I-H ^H ro • — i 07v m ^ r*~ X V O^ - • • • - » I-H in H •i-H i— H CM " ro -H !H r- O "c CH ,-•" C * o vO 00 [ -^ o vO o in ^^ vO I ^^ CO 0 O^ vO oo tN- Ov r-H CO CO U O m o CO o --H 1n oom mr-Hin CMCMor^oo ro ^ H i— i o r- t^ -H O r-H co LO 0v r— i r-n r** oo ^-H ^ vO r-H r- H n) — i vO~ ^ ^ i—i co CM ^0 CM oo" o" <1 • H ro CO ^H rt *J a i—j o 2 H m in o in ov 1 m co r- CO CO 0v ^ O^ CO CO LO O Ov I Tt< m A S" 00 CO 00 CM o CO o^cMcocoif1r*-- r^or*-^ co NO ^ vO co t^ ^H co I-H oo oo tu ^ o* IS *i *l •* « - 0 o - CO CM -~t 1-1 r-H m co •* m ro ro vo CM H «H i—t 2" ^ W CO " O [r] •£ oo vO in m CO 1 1 in r-H oo oo ^ vO "xf I-H ^* i 1 -H 0 O N CH H O — NO CM 1n o* ro • — i oo "xt* vX3 co oo 0v m -H m 1—1 X r t D. X -0 ro O 't o N o^comco co^r-i m oo m H ^ W ov vD CM N m N ^ ^ pj- ^ r- O^ m co vO H 5 ro CO o 0v £o — i [H r } o in T^ ^* in vo 1 o^ONDLn-HvO t^- •— 1 oo ro co oo o Q 1, ^ 00 [„ f-- v£> ro o^ ^^ co ov co rt ^^ ^^ t**- ro ^o -H CO ^ i— 1 •S vO o\ 00 r-HTfmminco oo oo r- •— i ^^ ^^ CO »-H j 0v « . „ « » . ^ . . •i •• p .«. ^ ^^ — H CO N r—i m co ro vo vi> co ro py CO CO o 6 ^ Qj r-H o w o y N l rH 3 H H r- A ^ r * >s "M o^ to ^ C .S Q -H 0) t0 ~ O 1* TABLE 3 ' Thailasd Pakistas ( Basglad Philippinr Malaysia rtsdosrsia Sisgaporr cd T H ™ ^ 3 cdflj-r-i-"-'. ^ *Q rt tiO LLj I fl) <U 1^ t^ Othrr TOTAL SOUrtCE: o rt u^.S^S^a! cgo^^rt •cS•^SSS1* 3 S "S 2 S ° M C r <1) T) o "i -In "-1 'tJiUO^inJ-rH

17 Colombia, which currently export approximately half and a fourth, respec- tively, of their 1968 numbers, has been attributed to decreasing availability rather than demand and is in part responsible for the limitations imposed by these countries in 1973. The 10-year trend in exports of rhesus macaques from India has shown a steady overall decline of 24 percent. Kawanishi (1972) summarized the monthly statistics of the Foreign Trade of India, which showed a 27-percent decline in exports worldwide from 48,617 to 35,296 over the 5-year period between 1967 and 1971. This overall decline included a 33. 5-percent decrease in exports to the United States and a 16. 6-percent decrease to all other nations. There have been sizeable declines of 50-80 percent in exports originating in Sierra Leone, Kenya, and the Philippines. Only in such countries as Tanzania and Nigeria having export volumes less than 1,000 annually did the numbers change less than 20 percent. The striking increases of 80-90 percent in the newly developing export trade from Paraguay and Indonesia have not yet reached annual volumes exceeding 1,000. Primates have not been exported to the United States from South Vietnam since 1965 or from Cambodia since 1966 due to the Indochinese war. Expor- tation was stopped from Pakistan during 1972 and re-established from Bangladesh in 1973. In 1974, however, Bangladesh instituted a 5-year moratorium against all primate export. Uganda has not exported primates to the United States since 1967, presumably for political reasons, and no trade with the Republic of China has been developed. Exportation of primates, opposed in Nepal for religious reasons, has never been allowed commercially from Burma (Southwick e-t aJL. , 1970), and was stopped temporarily several years ago by the Indian government in response to religious criticism of the large losses in the commercial trade. Sample Export and Import Volumes for Other Nations The monthly statistics of the foreign trade of India as cited by Kawanishi (1972) illustrate that the worldwide trade in rhesus is only two-thirds of the 60, 000 per year that has been the volume generally quoted within the United States. Of the 35,300 primates exported from India in 1971, the United States received 23, 900 or 68 percent of the total. The United Kingdom and the U.S.S.R. each received approximately 10 percent or 3,400-3, 500 animals. Another 4 percent was exported to Yugoslavia, which has rapidly increased its usage of Indian primates from 350 in 1967 to 1,360 in 1971. The remaining 8 percent of the Indian monkeys were shipped to several other countries: The Netherlands, Italy, West Germany, Thailand, Czecho- slovakia, Japan, and Canada received 100-800 each. Although the United Kingdom cut its total demand in half between 1967 and .1971 (Department of Education and Science, 1969a, b, c, 1972), several other countries are rapidly increasing their demands for primates. Japan doubled its volume of imports from 4, 000 to 7, 700 in the 7-year period 1962-1969. The demand nearly doubled again during the following 2 years, 1969-1971, to a current total volume of 14, 300 (Kawanishi, 1972). Although the overall volume imported into the United Kingdom and Japan is low relative to that imported into the United States, the species compo- sition is very different. The volume of long-tailed macaques, the most

18 important species in those 2 countries, is approximately 10-times the 1, 500 imported into the United States (Table 4). Differences with other consuming nations also exist in the sources of primates used, because some countries that do not export primates to the United States are shipping to other countries. For example, North Vietnam ships several Asian species, including Macaca nemestrina, M. arctoides , M. assamensis, and M. mulatta to the Sukhumi Primate Center in the U.S. S.R. (Lapin et al. , 1965, cited by Wolfheim, In preparation). Statistics of the volume of primates re-exported from various countries are scanty. The re-exportation volume from the United Kingdom typically exceeds a fourth of the total volume imported (Hartley, 1972). Neglect of the re-exportation volume in summing the import statistics for several countries could lead to a sizeable overestimate of the worldwide traffic in wild-caught primates. Accuracy of Estimating Primates Needed for Research In 1955, under an agreement between the governments of India and the United States, the Animal Resources Branch of the National Institutes of Health began to act as a central agency for forwarding certificates of need for rhesus macaques. During the past 3 years the number imported has ranged between 52 and 81 percent of the number requested (Table 5). By comparison, the numbers imported into the United Kindgom have been less variable, averaging between 71 and 79 percent of the numbers licensed. Whether the less variable estimates of needs in the United Kindgom result from the smaller total volume to be estimated or from the stricter procedure of licensing is not apparent. The accuracy of estimating the future needs for primates in the United States must rely upon extrapolation from previous import data. It is, therefore, worthwhile to examine the proportion of the primate trade entering biomedical uses. Estimates of Current Usage Volume U.S. Department of Agriculture Estimates Totals Since 1964, when the Animal Welfare Act, PL, 89-544, was enacted, institutions that are involved with the research, exhibition or supply of animals have been inspected by the U.S. Department of Agriculture (USDA). Research facilities have been registered, and exhibitors and dealers have been licensed under this act. An amendment in 1970, PL 91-579, expanded the coverage of the inspection authority from facilities handling dogs and cats to those handling most species of mammals. An interesting account of the enactment of this law from a humane society's point of view has been published by the Animal Welfare Institute (Leavitt, 1968). The first annual report prepared by USDA gives the rates of usage of the major laboratory animals by state for 1972 (USDA, 1972). The total research use of 1, 662, 026 mammals published by USDA is somewhat greater than

19 TABLE 4 PRIMATES IMPORTED INTO THE UNITED KINGDOM AND JAPAN United Kingdom Japan, 1971 Source Species 1967 1971 Asia All primates — M 11,033 Long-tailed macaque 7, 513 4,582 - India and Pakistan All primates - - 247 Rhesus macaque 4,719 3,435 - Africa All primates - - 271 Baboon 1,811 2,184 - Vervet monkey 3,139 184 - Patas monkey 2,533 737 - Americas All primates - - 2,623 Squirrel monkey 2,282 610 - Europe All primates - - 95 TOTAL (all species) 24, 895 12, 150 14,269 SOURCE: Kawanishi (1972). TABLE 5 ACCURACY OF ESTIMATING PRIMATE NEEDS Country and No. of Primates Type of Primate 1970 1971 1972 United States--rhesus Imports 23,302 22,097 23,210 Number requested 36,965 27,307 44,377 Percent of requests actually imported 63 81 52 United Kingdom--all primates Imports 11,695 12,962 13,087 Number licensed 15,765 16,344 18,426 Percent of licensed primates actually imported 74 79 7J- SOURCE: Data from McPherson (pers. comm. , 1974); Department of Education and Science (1972).

20 the arithmetic sum of 1, 571, 963 obtained by adding the totals by species. The 732 research facilities that were registered and that met the February 1972 filing date reported the following overall usage rates for mammals other than mice and rats: Animal No. Percent Rodents (guinea pigs and hamsters only) 851,295 54 Rabbits 379,375 24 Dogs 185,788 12 Cats 79,397 5 Primates 42,658 3 Other (animals from the wild and hoofed stock) 33,450 2 TOTAL 1,571,963 100 Although the number of registered research facilities increased to 871 in 1973, the reported animal usage remained static at 1, 653,132 mammals (USDA, 1974). Since data from individual reports for 1972 were released by the Congress of the United States for public use, it was possible to inspect the reports filed with the Animal and Plant Health Inspection Service of USDA for specific information relating to primate usage. Inspection of the individ- ual reports revealed that 38 percent (276) of the registered research facili- ties outside of the federal government laboratories were using a total of 55, 057 primates. It is difficult to account for the increase of 12, 400 pri- mates found during an examination of the same individual records that were the basis for the estimate of 42, 658 submitted by USDA. Nearly 2,000 of the 12,400 increase results from research facilities that were known to use primates but were not located in the USDA file and presumably were not yet registered. Much of the discrepancy may be due to including in the 55, 000 estimate individual reports that were filed after the February 1972 dead- line. A small source of variation is the result of combining all prosimians and tree shrews with primates in the larger estimate of usage instead of following the example of USDA and summing them with other wild animals. Size Classes of- Research Facilities Using Primates The concentration of primates in a few institutions is emphasized in Table 6. Only 13 percent of the 276 research facilities use 40, 000 or 72 percent of the total number of primates. Each of the 37 largest research facilities using 300 or more primates is identified in Table 7. Care should be taken in interpreting these tables since most facilities are combinations of several smaller units and, therefore, do not represent the holding capacity of any single laboratory or even geographically contiguous laboratories. A research facility (RF) as defined by USDA is that administrative unit that is legally responsible for the conduct and reporting of the various laboratories within its jurisdiction. This method of measuring size accentuates the size of research facilities for which the parent institution reports for all sites relative to those for which each site reports separately. Likewise, those states in which a university such as the University of California files one

21 TABLE 6 PRIMATES USED BY SIZE CLASS OF RESEARCH FACILITY (USDA, 1972) No. Primates Used/Research Facility Facilities Using Primates Primates Used Per Year Total No. Percent Total No. Percent 1-99 189 69 6,776 13 100-299 50 18 8,381 15 >-300 37 13 39,900 72 TOTAL 276 100 55,057 100

22 8 H S rt tM r- 3 ffl o in o o CO O o CO o * CO 00 vO CM o •0 A 6 u ^ <*H Usiversity of Texas Syste (isclsdes 7 campuses asd hospital) Austis, Texas 0) 1nternatiosal Research & Developmest Corp. Mattawas, Michigas rtterlisg Drug, Isc. Rensselaer, New York Retisa Fousdatios Bostos, Massachusetts G. D. Searle asd Compas Chicago, Illisois Esdocrise Laboratories o Madisos, Isc. Madisos, Wiscossis Usiversity of Califorsia (8 campuses asd regiosal Usiversity of Washisgtos (isclsdes regiosal primat Usiversity of Wiscossis ( regiosal primate cester) Madisos, Wiscossis T he Populatios Cosscil New York, New York B. Usiversities primate cester) Berkeley, California cester) rteattle, Washisgtos ~H ^ 00 f- 0 0 o 0 00 *•• 00 ^ vO r*~ in qfi CO tM tM 00 0 Qs 00 o ^* c O- 0 0 vD tM iH 0 00 00 m ^ n ) Tf CO <M" cJ J" -H" -. — C0 r CL v u m « I o 5 in • B- « 3 H* CL u C0 Research 1sstitutes, Pharmaceutical Com [erck & Co. (2 cities) Rahway, New Jersey ittos Biosetics, Isc. Bethesda, Marylasd azletos Laboratories, Is Falls Church, Virgisia he Dow Chemical Compa ; cities) low Laboratories, Isc. Rockville, Marylasd authers Research Institsi Birmisgham, Alabama regos Regiosal Primate esearch Cester Beavertos, Oregos eter Best Brigham Hospi Bostos, Massachssetts suthwest Fousdation for esearch asd Educatios Sas Astosio, Texas mericas Cyasamid Comp Pearl River, New York bbott Laboratories North Chicago, Illisois licrobiological Associate Bethesda, Maryland Q w Midlasd, Michigas 0 H < 2 J K r-S k W Octf (X cotf < < 2

23 f> 1 n) £ c a £ a o ffi I tM o in <0 V r 31 C CL ft) a x U 0 4) •r-i c >-i O o ^J vO -H o fl U *! ft) w g ' O 4-i U c v Usivers w Haves 21 n) S 4) C V U «S Ss u £ £•• CO o r- ^ rt 5 .S O ^ HCX m m CM T!^ T tM *& O O ill -H rt ^J CO 00 --- r~ j <u rj en 3 S 0 -H — 1 O ft) R) H ai In V "rt tj u *J O U) cl w .3 ft> 4*> ^ "^ 0) u "« £ M ^ ^ 3 4j n) ni ^ H ft) > « 0) .rt o H ft) C Cd D O o in oo * O in oo f» o tu fc o 13 e n) -H 4.> 4-1 •rH r-H a ni 0O CO £ >* C £ O is it in 4) O tt r-H 01 (|J OS 1 s CQ U t4 4> r i-> 1 (J "O -T~ c J rt n.3 >r J 51 1 •S u T3 * •s rH •— 1 • +j *» I r O 3 7T ? g > - C — — ' ^ .r4 Emory Usiversity (isc! regiosal primate ceste Atlasta, Georgia Wake Forest Usiversit Gray Medical School) Wisstos-Salem, Nor Harvard Usiversity Me Cester (iscludes regio: primate cester) Bostos, Massachsse Tulase Usiversity (isc! medical school, hospit regiosal primate ceste New Orleass, Louis rttate Usiversity of Nev Rssh-Presbyterias-St. Medical Cester Chicago, 1llisois Usiversity of Michigan Ass Arbor, Michiga Usiversity Health Cest Pittsburgh (iscludes si asd hospital) Pittsburgh, Pesssyl Usiversity of Chicago Chicago, Illisois Usiversity of Hawaii a usiversity hospital Hosolslu, Hawaii Baylor College of Med Houstos, Texas ^Figures from Dr. Mo (7 campsses) Albasy, New York c o ••H 4-i rt u - ^ c I o u .-H I 0 01 M 4) a

24 report for all campuses appear to have much larger facilities than do states in which each campus registers as an independent facility and reports separately to USDA. Many hospitals and research foundations that are affiliated with medical schools or universities and may share staff on joint appointments also register independently with USDA. A similar latitude in meaning exists for the term "site" as listed on the USDA questionnaires. A site within a RF may be a university department that holds animals in several buildings, a building that houses primates administered by several departments, an entire campus, or a complex of buildings at a geographical site such as a primate center or a research institution. Estimates from Institute of Laboratory Animal Resources Surveys Composition of ILAR Surveys The mailing list from previous surveys was augmented through the cooperation of the Washington Primate Center's announcement of the survey. Of 354 questionnaires sent to users, 255 (72 percent) responded for approximately 306 sites as active, 52 (15 per- cent) indicated they did not use or had discontinued using primates, and 47 (13 percent) did not respond to either a questionnaire or a telephone call. Six suppliers indicated they were out of business leaving 8, or a third of the remaining 24 suppliers on the active mailing list and half of the 15 known suppliers that reported their sales volumes. The respondents to the ILAR 1973 survey are identified in Table 8 by type of institution and compared with those of earlier surveys. Phar- maceutical companies and the Regional Primate Centers are not specifically identified in Table 8 but maintain large inventories. The Pharmaceutical Manufacturers Association (PMA) surveyed its 35 member companies in 1973 and reported inventories of 6,300 primates and an import volume of 9,200 for that year. By contrast, PMA reported that its member institutions used 17,400 primates in 1967. At that time all commercial facilities reported using 20,000 primates (ILAR, 1970). Relatively few of the PMA member institutions participated individually in the ILAR 1971 survey (Thorington, 1971a), explaining the low number of institutions listed as research institutes for that year in Table 8. If the participating membership was approximately the same in both 1967 and 1973, the decrease in use by these companies was nearly 50 percent. If the 104, 000 estimate of imports for 1967 is considered to be correct (Table 2), and the intermediate value between the 1972 and 1973 import numbers of 73, 000 is accepted as representative of the survey period, then the decline in imports between 1967 and 1973 was roughly 30 percent. Of the 264 sites in the private sector that reported inventories of 36,000 primates, 7 of these sites were Regional Primate Research Centers that reported a composite inventory of 8, 165 and an import volume of 1, 800. The'NIH inventory of 6, 100 in 1971 is greater than the 4, 100 inventories recorded for NIH and the Caribbean Primate Research Center in 1973. The 1973 import volume for NIH was reported as 3,000 for the quarantine facility with a few hundred additional animals coming onto the campus from quarantine at other facilities. The average number of imported primates moving through the intramural quarantine during the past 15 years has been 3, 800 with an annual volume ranging from 3, 100 to 5, 500.

25 ^ n l 0 i CO 00 c^i ^ ON —in NO ON CM in o o 01 — - o l CO O 00 CO CO 00 O O CM CO 00 — in o 0 c r~ c Q nl rf NO o —• r- NO rf ^r oo °^ w o E NO CM _ tM tM Ov r^ T)* ^ CM ON GO *•* i- NO NO 3 - iTJ X cu *• c "5 r 'n H 01 1-1 0) ^ c — •£ c 7 ° o g S Q U 01 -H — 1 _ fO NO ^ in oo CO ON oo in rN- 01 - f tt! W H O 4-J CO — . •* CM CO Z"-I t/3 a* £ J?l C/3 " F. oi o ^ 0) ^ > .2 U u -- CO l CO _ m _ co — i CO — I CO r--i CO U r C — OS a r~ r~ r^ r*- IN- r** 1** r- r- r- r^ r- r- r- " fll ~ *r5 o ON O- a- o ov Os o O- ON ON ON ON ON O- ™ B,a u W ^ 5? I? Co ^ 01 01 O ft) O M **^ H M r r f 2 22 1 3 h f t ) •2 -H oS C •PH r-i SJ •^1 ! u 01 • 3 h r a 3 id c Q °* o* 01 3 n I 01 ^ o u +i " u C ° c • 4 ^ — o ^ o 3 ^ ^ I •p a r M CM •" *D *• rij c iS EARC u c « 0) aj d u S "° •O j c V a i I > CO —i CO ^ ?3 > » • oS • CM aj 5 r- M "5 ON a i-l 01 i NO" o =00 c o H ci5 ~.Q -l fll *^ •O TOTAL REr t 4-» acilities Not R Federal Goveri CH Q V s H! TOTAL rtA djusted Total 1 s£ « 3 ^2 ss jf Agriculture i urvey values n es reported to 3 c *• - Q „ 5 i, * ° V « 3 S) 2 ss i* 01 1- d -o rt1H "C "c "c c S > to < 01 1 <; ui V nj a) v O 3 U U O U S <O r~ a 10 r- t-i H h 4£ ON ON 01 ' Q M £< ° OS s3 s S 0) V iss ?N! --, •* in NO t« r"* ^ 5 I-H 4-) U73 ^ ^^ u« ^~ ^^ wjn 101 . ( aC- u O. IS 2 oo in CO O CM — 1 ON ^* ON CO CO ON r- in — ^ ON m (J o I [- 00 NO in co ON NO NO NO ON O CM CO in — i r- r- m r- -Nf Q r-^ ^ JS £ NO CO o CM T)* r* CM o CM r- oo — 0- -. •* CM r- O NO NO "J| .5 W 01 J •* in NO m o^ CO — i in oo NO ^ CM CM l l j> CM CO — i — . in in PJ CO u B 3 io .j -— * -~ 2• O -IH D^ l pg B' -^ ^^ io ~ *^ P n f m c oo •* in r- O NO ~" T3 r-H °S N^N— O CO NO CO T)• •V in NO ON in NO oo y m r- CM NO O Tjr CO N— CN- NO 00 in oo ^* CM ^* oo NO N— DC U U OS NO - 00 -. •* — NO r- NO — -. [N- 00 NO IS j3 wS 3 CM CM -. — r -i u * •* -1 CM S"« -^< M m •H SJ r•o° 2; 8-2 r-^ ON ^ 4-i in -Nf CM in" I^TN^ Jr 0 ) 3 C/5 H V 4_» :£.:£. o CO NO NO r- in NO al "2 Q U) mf* CM r- 0) CJN ON ON in CO|oo m NO ~o NOko CM ^* f) 3 01 o j " [Z i M , CO T)< 00 01 NO — 1 r- CO oo W *J *3 qj • fi, o -H id M CM CM - - 2 1 f t ) •S « P E 2 S 01 3 to J° • g 01 M L^ *j Ol U O. 01 O ry-, h g| •" 01 u . V W 2 ^ 5 u " >* ^ 0) o a 01 tt •S 01 n •" • TABLE 8 1rtrtT1TUT1' rt Research Facilities rtample: 1971 rtAR* 1973 rtAR* esearch institutes, hog 1972 rtrt Facilities omitted ,ocal, state government 1972 rtrt Facilities omitted rtUBTOTAL (private 1972 rtrt Facilities omitted Connposite rtrt rtample: 1971 rtAR 1973 rtA TE: rtumbers in par en 5rt values for primate lorington, 1 971a) and 1 ( rimates for all composi ictly comparable to use c o niversities* 1972 rtrt Facilities omitted Composite rtrt Composite rtrt rtample: 1971 rtAR 1973 rtAR Composite rtrt rtample: 1971 rtAR 1973 rtAR .ij 01 •c VV4 O <u Q W O OJ ^ Q ,-. ** A M H Z * EHi^ n

26 The advent of required registration by the USDA for all users made it possible for the first time to estimate the proportion of users responding to ILAR surveys. As Table 8 illustrates, approximately 50 percent of the research facilities outside of the federal government that use primates did not participate in ILAR surveys during any specific year. Although the labo- ratories or units maintaining primate inventories reporting to ILAR and to USDA are not strictly comparable sites, a similar proportion of these smaller units was overlooked. Those sites that were not identified or did not return questionnaires were not limited to the small users. A com- parison of the ILAR questionnaires returned in 1971 and 1973 prior to telephone inquiries indicated that a fourth of the institutions in the larger size class using 300 or more primates did not respond. None of the seven facilities omitted from the 1971 ILAR survey was a university. If use in 1972 is accepted as a measure of size, more than 5, 000 monkeys were overlooked in these laboratories of the largest size class. Inventories by Species The numbers of each species in the 1973 inven- tories of survey respondents are presented in Appendix I. Rhesus macaques outrank all other species with 20,400. More than 1,000 individuals of 9 other species are maintained. In descending order of abundance they are squirrel monkeys, marmosets (Saguinus sp. ), baboons, long-tailed macaques, pigtail macaques, night monkeys, vervets, and stumptail macaques. Research facilities maintain between 500 and 1, 000 capuchins and chimpanzees. Another 6 species with inventories between 100 and 500 include bonnet macaques, greater galagos, marmosets (Callithrix), Japanese macaques, and brown lemurs, v The inventories maintained in 1973 are compared to those of 1971 in Appendix I. Since the sample of laboratories differs slightly between the two surveys, the gross differences between 1971 and 1973 inventories are not strictly indicative of changes in species use. At first glance, it appears that 10 species have been deleted from inventories between 1971 and 1973 and another 10 species have been acquired. Many of the species that do not appear on inventories of both years were probably reported as "other" species, and were not itemized. The 11 Cebus capuchinus and 45 Presbytis entellus may represent actual deletions; the 5 species of callitrichids probably represent real additions. Increases in inventories of individual species include twofold increases in Lemur fulvus and Cebus apella. A fivefold increase in Ateles sp. may result from the increased use of this species in studies of malaria. It is not clear whether the 30-percent increase in inventories of Papio sp. or the 30-50-percent declines in Erythrocebus patas, Macaca cyclopsis , and M. fascicularis result from actual changes in usage rates or from a difference in the number and identities of laboratories sampled. Apparent decreases of 30-50 percent in the inventories of Galago erassicaudatus and Cercopithecus aethiops are probably real, with the latter decrease resulting from the Marburg virus scare. Ihe most striking change appears to be the 20-percent increase in inven- tories of callitrichids. The apparent shifts in inventories of Saguinus fuscicollis and ^. nigricollis probably represent re-identifications rather than real changes. The reason for the tendency to hybridize tamarins, producing 114 hybrids, is probably due to lack of early identification.

27 Total acquisitions The numbers of imports and total acquisitions during 1973, including animals from other laboratories and from colony births, are presented by species in Appendix II. At least 61 percent of the 33, 520 primates imported during 1973 were used in terminal studies within a year. When the reported value for the number of deaths of 1973 imports resulting from terminal studies was lower than the difference between the number of imports and the inventory on October 1, 1973, then the latter value was accepted as an estimate of imports sacrificed within a year. Since the subtraction method could only be used for those laboratories having small inventories, the estimate of numbers of animals imported that are dead within a year must be viewed as a considerable underestimate. The discrepancy between reported and probable deaths was large only for tree shrews and night monkeys. The size of the range of values for these species may be attributed in part to under-reporting of the numbers "used up" within a year, but it was also a result of interpretation of the unfortunately ambiguous term terminal studies used on the questionnaire. Several respondents apparently did not consider use in drug production or safety testing as research use. Some investigators exempted from the category of terminal use certain procedures, such as experimental surgery, that may result in the loss of animals, since the sacrifice of animals is not required by the experimental design. Although the ambiguity of the question did not always allow needs for new imports to be distinguished from planned usage of primates already on inventory, the anticipated needs for 1974 exceed 1973 imports by 20 percent. Proportion of the Trade Entering Biomedical Uses Approximately three-fourths of the primate trade entering the United States is consumed for biomedical uses annually. The other fourth of the trade supports exhibitors, a large pet industry, and includes the losses absorbed in dealers' compounds. Neither the sum for sales nor the sum of purchased imports in Table 9 can be considered complete. Although only half of the 15 dealers that supply primates for research responded to the 1973 survey, these suppliers reported selling more primates of 1 5 species to research institutions than users reported purchasing. On the other hand, users reported buying more of 6 species during the same interval than suppliers reported selling. Ihe proportion of each species that was used in research is only a rough guide to relative usage since the numbers of primates used and imported were not available by species for identical 12-month periods. The estimates exceeding 100 percent of purchases over imports for 7 species result from the attempt to compare purchases for 1973 with import volumes for 1972 rather than inaccuracies in reporting. The larger estimate of sales to research institutions, whether provided by the users or suppliers, was accepted as an indication of the percentage of imports used in biomedical programs for each species. The sum of the larger estimates of each species gives a minimum of 49, 000 sales. Due to incomplete reporting, total sales probably reach 55,000 primates. As outlined previously (Table 2), the best estimate for total imports lies within the range of 70, 000-80, 000 primates for 1972 and 1973. The best minimal estimate for annual sales to researchers lies between 70 and 80 percent of total imports.

28 £ » o g „ a> '" rZ! -S 2 o o co "~f CO o O 1 oo CO CO _4 CM oo oo o ON O O 00 O O 00 J * 1 s •" 0 O ^ r-H ^ o m r-H CM r-H ON r— •MOO in o 0 ON H £ ~ s 2 k r-H I-H r-H r-H r-H r-H O PH H CJ u O O 00 oo ^ ON CO -* i CO 0 CO m .-. r-H CM r-H • .O r— O r-H r-H o oo I-H HH 1 1 -""1 rH CM CO in m --H r-H CO NO CO r- NO CM ON r-H t^ CM f~- ON •— i OO r-H CM W Q .2 o t~- r-H r-H ON o o o CM CM CM • -o co CM m CO L.^ CO O Qi ON CM* - •,•,•, ^ i-) i—i d —i r-* -H CO CM NO CM in co '-H •— 1 CO r-H Q r-J M fc I—) CM CM 5 CO "£ H o C Q ^j Iv- IN- CM CO CO I*- ON CM o 00 CM -HH 0 CM CO m — H CO CM r^ NO -H m Tt< m CM vO ON CO a "LJ I-C ^ ^ m co ^ NO t*- m CO NO m r-H CM oo oo in o CM co m ON [D o Q QO'H — 1 r-H co NO in o •^ CO f^ ^ CM CM CO ON J PH 9• o ^ 4J — CM" CM r-H* r- ^ M C CQ O O r-H CM r-H U 0) CO - O O r— I [3 Q 1 W rn CM CO 1 ici .M r r- r- O CM m 1 -^ NO m O in ,—, r-H NO f«- r- 1 o m ^ ^^ ON ON f^ O 1 00 f-i CO nj ON ON O r-H ^j CO jr-- in t>- f^ co NO NO 00 o m ON CM CO CO CO r-H ON o o a> oj -H --H CM r-H r- CM 00 r- m CM r-H rf in r-H r-H CM CM r-H ^rt3 I^> . . * to" co" ^ oo PH H ry-) -(-i••-) r-H r-H m .— 1 fl O O O ^ OO CM CM O CO ^ 4 CO r CO W O H O- V 0) <J 0 ^ CM -i CM 1 r-H CM CO CM r-H co r-H in CM in 1 CM CM PO CM NO CO r-H r-H CM 5 co Z Q a w M 1-) H H 0) CO • r-i CO <J r-H 2 a r S a r*, C . co f-Lrj - v co o ^r^ o ? co 0 _, V* ON O CO 1 1 | CM r-H r-H 0 r-H CO oo 0 ON i o m O O r-H ON 1 CM CO ^ -M -W NO NO NO CM NO ^ 0 *^ r-H in -rtf OO - — i ^•S 1-lJ M C r-H r-H ON CM -H CM vO in O f-N O 0) 4-> CO u a > u CM" < ^ i — i & O CO H a .paia sp. .lago crassicasdal 5 -i 0 °S •cticrbss coscasg ircocrbss torqsati or C. atys ircopithecss arthi & C. pygrrythrss ythrocrbss patas us Sprcirs srsrgalrssis ibsrlla pygrara gsinss ordipss sigricoiiis & S. fsscicollis itss trivirgatss icaca arctoidrs fascicslaris rslatta srrrstrisa sigra H d m ry s tax irrosrts d Co iriri sp. . radiata .pio sp. d .a u H CO CO CO ro V r-H 3 ,0 0 be p ro 6 r>- 0. rt *v o 0) fi A ni CO V UJ H Sfft HO 2 U CO C 0| W % < U U U W

29 r-^ *> B1 C U rn «J . c •e £ •" J2 o ** —« *o J3 •Nf O O CO 5 1 s 1 * pq CO O NO to ^ 00 ^ CO 1 — ' .w ^H CNj on co co Q 2 o c^- oo oo NO co o aO N i3 r^ CO 1 •J M oo on u o CO ^ f~- t*~ r^ m 1 0 O. "» c^ O"^ O^ IX^ 0) o oo^ ^ 0 PS 5. 2» . CO "^ oo j• g £ O O OJ co CO to en 00 on o - 1 *j r r- r~ 0 1 I « 4) m m -H M CO flj ON ON oo .« 4,l en *« r-H -H CO 0 V u) ^ -r • |H 0) •lH co on o Scd H-) • • ^wotit; a o M nj "S - - » ^oo 0) O . — i 4) !H •^ OO ON CO ifl -r" (H r CO * *•* 0 a a; i5 °* -S. CO 1 1 CO 2i Q NO ON 00 ON 00 ^* rH oo oo o in r>- . • iH W .* ** CO i— 1 -4-1 CO M 0. pj o Cco *-^ ' u a w o ^r- u CD CO | CQ O _. ^* 1 1 "-""- <n -*-* •rH C\J -»-i 4J -* O 1) *j* .i 1 a - <H S 5| ^ ^ T3 0) c a o n M iJ-1 o • rH a > u •r-i u M o g « * o J2 M » s rH rH 2 M rt n) U CU 4J in U 0 S PH i C -H i 0) • |H • iH C CO 3 ^^ \^ •— i NO O "^ !J i— i ^* NO co M 9 CO 0) •H CO Co £,"" isclsdrs £ iD >> 4) rrt -rH Cd llicrbss w ° ^T JJ O -4-i -, 0 4 "* 0) % % I— 1 ^ cTl msr o 2 -•H JS m a"u C ^ o^cu .5 ^ ^ ^2 a w M a 2 o w 5 M n . •— ' nl U <D J ^1 -"H n) (—, rM O i— i rt *J hr ^ <r< U P.U o I c4 H H.S e ^^^ -4-i O nl 0 ±! H Pn PH O

30 Research consumes nearly all of the individuals of several species imported in large numbers. These include rhesus monkeys, mystax mar- mosets, vervets, baboons, and probably both night monkeys and white- lipped marmosets. The continuing dependence of zoological parks and other exhibitors on wild-caught primates is illustrated by the annual importation of nearly 1,000 animals belonging to 14 genera, all of which represent exotic species that were not imported for biomedical research. There is a minimal discrepancy of 41 percent between imports and re- search use for those New World species that are the most popular as pets. This discrepancy includes 19, 700 squirrel monkeys, 3, 100 marmosets, 5,200 capuchins, 2,000 woolly monkeys, and 2,000 spider monkeys. A total of 32,000 monkeys of these 5 or 6 species are unaccounted for and it has been assumed that most of them enter the pet trade. Plausible estimates of the maximum conservation of primates that could be realized by eliminating the pet trade range from 20,000 (75,000 imports less 55,000 research use) to the 32, 000 identifiable South American monkeys. These estimates represent half to two-thirds of the savings anticipated from earlier estimates of 46,000 (Thorington, 1972) to 50,000. However, the magnitude of the earlier estimates is based upon incomplete surveys of research users. These figures suggest that the number of primates that would be saved by eliminating the pet trade has been overestimated. Records for the intramural facility at NIH show that the average losses during quarantine have been 11-12 percent over the past 15 years. The majority of primates handled by the facility have been rhesus macaques which have been shipped directly from India. For certain South American species, especially the delicate night monkeys and marmosets, the NIH quarantine losses have reached 50 percent. Assuming that this loss rate is typical nationwide, then as many as 10, 000 primates (13 percent of 75, 000) may be lost annually by importers during conditioning and quarantining. Such estimates suggest that nearly half of the 20, 000-40, 000 imported primates that have been attributed to the pet trade may in fact be losses inherent in the present system of commercial collecting. Trends in acquisitions Between 1 959 and 1973, 65, 537 primates were processed through the quarantine facility at NIH and may be considered representative of trends in acquisitions within the scientific community. During the last 15 years, the volume averaged 3, 500 rhesus and 300 primates of other species yearly. Ninety-one percent of the primates acquired were rhesus macaques in a ratio of three 4-6-pound juveniles to one adult. Twenty-two species comprised the remaining 9 percent of the volume. Only chimpanzees, vervets, and squirrel monkeys were imported every year along with rhesus macaques. Long-tailed macaques and marmosets were imported in all but 3 of the 15 years. Since 1970, night monkeys, capuchins, baboons, and patas monkeys have been added to the list of species consistently imported. An increasing demand for New World primates is also indicated by the Certificates of Need for 1974 that have been placed by researchers with a single supplier. These requests represent increases over the total 1973 sales to research identified for all of the participating suppliers as follows (Table 9): cotton-top marmosets, a fourfold increase; white-lipped marmo- sets, a threefold increase; mystax marmosets, night monkeys, capuchins,

31 and woolly monkeys, each a twofold increase. These estimates of need, if filled, would increase the imports of mystax marmosets and night monkeys over the total volume for these species imported during 1972. Composition and Turnover of Rhesus Macaque Inventories Users reported that 83 percent (14, 287 of 17, 224) of the rhesus macaques imported are sacrificed within a year (Appendix II). The 8, 693 surviving monkeys from 1973 imports represent 38 percent of the total inventory of 22, 980 reported by users. Another 22 percent (5, 096) of inventories were identi- fied as long-term holding of animals maintained for 3 or more years. The final 40 percent (9, 191) of inventories is expected to be carry-over from acquisitions of 1-2 years. Due to the fact that the deaths from other acqui- sitions and from the carry-over held on inventory from previous years were not determined, the total percentage turnover for the inventory cannot be calculated. The percent annual turnover due to imports alone is 72 percent of inventory [1/2(17,224 imports + 14,287 deaths)/average inventory]. Like- wise, the percent annual turnover of imports represents 50 percent of the total volume of rhesus macaques assigned to biomedical programs. The total volume of 33, 182 includes total acquisitions and the carry-over from previous years held on inventory. The percentage composition of total inventories provided in the sample of users may be used to extrapolate to the nationwide holdings of rhesus macaques It is generally accepted that nearly all of the 23, 000 rhesus macaques imported are used for the purposes of research, and the produc- tion and safety testing of vaccines. The sales volume estimated by suppliers was slightly greater than the total import volume although only three-fourths of total imports were identified by the users sampled (Table 9). The inventories reported by users are probably two-thirds of the total (Table 8). Extrapolating from these values, it is estimated that the nationwide inventories may reach 34, 800 rhesus macaques. The projected values suggest an inventory composition differing slightly from that of the above sample, with 11 percent (3,900) surviving imports of the previous year, 22 percent (7,700) rhesus on long-term holding, and 67 percent (23,200) as carry-over from 1-2 years. Discussion of Usage Volume Apparent Trends in Acquisitions Since factors influence apparent trends in the primate trade, considerable care must be used in interpreting changes in export levels. Many of the declines, bans, or interruptions in primate exports have been politically motivated or have resulted from wartime conflicts or social reasons. Declines in the primate trade can also result from purely economic reasons, such as when an exporter retires or goes out of business. A decrease or shift in demand can account for reduced exports. The fact that the number of rhesus macaques exported from India during the past several years has declined steadily below the 50, 000 annual quota established by the Indian government supports a real decreasing trend in the worldwide demand for

32 this species. The final cause for reductions is a decline in supplies re- sulting from overexploitation and habitat destruction. Declines in overall exports from 127, 000 to 70, 000 between 1968 and 1973, despite a high trapping pressure in many countries, and the trend to expand into several additional countries for primates during the last half of the decade, support the reports that wild populations are declining and traditional trapping areas are being overexploited. 1 he difference in rank orders of species in use in various countries is of particular significance for the choice of alternative species that could be substituted if the species currently used in the United States become less available. Both long-tailed macaques and baboons have been suggested frequently as appropriate substitutes for the rhesus macaque. However, other countries already import these species in greater numbers than does the United States. Comparability between ILAR and USDA Censuses Because of the academic autonomy of biomedical researchers, surveying by questionnaire provides an incomplete census. The importance of the data collecting function of a government department, such as USDA, in identifying users and in assessing the volume of use of animals in research is highlighted by a comparison of their files with those of ILAR that are based upon voluntary cooperation. One problem with interpreting the results of questionnaires has been to recognize duplication of inventories. This problem arose when research staff had joint appointments and experiments in progress at more than one laboratory, or when animals held in one facility but on contract with another laboratory were included in the inventories of both facilities. Omissions represent the reciprocal problem and occurred frequently when an investigator or administrator responded for only the colonies under his restricted jurisdiction but neglected to specify that he was not reporting for all departments of the medical school or all sites of the research institute or university. It is unlikely that any duplications exist for the 1971 and 1973 ILAR surveys. There is no reason to believe that the comprehensiveness of the 1971 ILAR survey differed from that of earlier surveys. Since approx- imately 50 percent of the RF's and 50 percent of the primates used in the private sector were not reported to the ILAR surveys for a particular year, the previous estimate of primate inventories in biomedical research that were based upon these surveys should be increased by roughly 60 per- cent of the given value. Primate usage in surveys prior to 1971 refers to total acquisitions rather than inventories. Estimates of imports acquired by users were provided by suppliers, not users. Dealers' estimates of sales volumes in 1973 were illustrated in the section, "Proportion of the Trade Entering Biomedical Uses. " These values underestimated sales volumes by 6 percent (46, 000 vs. 49, 000) to 20 percent (46, 000 vs. 55, 000). Previous ILAR surveys should be increased by at least this volume.

33 Interpretation of Usage The difficulty in the interpretation of the term usage is exemplified by the following situation Pharmaceutical companies showed a decrease in impor- tation rates that was greater than the national average. This suggests that there has been a proportional shift in usage patterns of monkeys from drug production and safety testing to research, a change in the composition of the PMA sample between the 2 years, or a shift in the use of primates from in-house to outside contractors by these companies. However, the potential difference in reporting between the words "use" in 1967 and "imports" in 1973 raises the question of whether reported use in 1967 included both imports and inventory. If so, the reduction between years would be 11 rather than 50 percent. Obviously, if half of the companies reported their use by each method, the overall decrease of approximately 30 percent is in line with the national average. Most estimates of the volume of laboratory animals have been based upon reports of numbers "used" in research. This applies equally to early ILAR surveys and current USDA estimates. Unfortunately, the term "usage" has not been defined in these surveys and no consistent reporting from institutions can, therefore, be expected. Three hypothet- ical examples given below may illustrate the potential variance in the legitimate interpretations of the word "use." The number reported presumably will depend upon whether the institution wishes to minimize its apparent consumption of animals. Type A Laboratories with Stable Facilites A few research laboratories are involved in long-term experiments that last from several years to the lifetime of the experimental animal. These laboratories generally have large inventories relative to their acquisitions. Examples of research areas include ethological studies, breeding colonies, learning or addiction studies, and basic physiological studies relating to metabolism, aging, debilitating diseases, and genetics. • Example: A laboratory maintains approximately 100 animals on inventory and may import 10 per year to augment 10 births or acquisitions from other sources and to offset 20 deaths per year. Use may be reported as any of the following values: As imports = 10 As acquisitions = 20 As mean inventory =100 As total volume, i. e. , all animals held over from the previous year plus acquisitions. The total volume covers all animals that were assigned to experimental studies during the year. =120 Type B. Laboratories with Stable Facilitie s. The majority of laboratories using primates in biomedical research appear to be involved in short-term procedures such as experimental surgery, characterization of pathogens, tissue culture work, or the development and safety testing of drugs and vaccines. These facilities generally have animal importation volumes considerably larger than their inventories.

34 • Example: A laboratory maintains an inventory varying between 50 and 100 animals. Fifty animals are imported and sacrificed during each quarter. Another 40 are obtained from other laboratories. Quarterly changes in this sample laboratory are summarized in Table 10. Use may be reported as any of the following values: As inventory at start of year = 60 at end of year = 50 average for 4 quarters = 64 As imports =200 As total acquisitions (includes 40 from other labs) =240 As deaths experimental =225 all deaths =250 As number "used up" =190 While this example may be stretching the point slightly, if a laboratory wished to minimize the number of animals used up during a calendar year by deleting the number in quarantine and the number of carry-overs from the imports of the previous year, then the reported value for use may be considerably lower than actual use. In this example, the 50-60 animals deleted would represent a fourth of the number imported or a fifth of the total number of deaths. Type C. Laboratories with Fluctuating Inventories or with Changing Facilities The hypothetical situations of laboratories with inventories that fluctuate on a time scale longer than 1 year or those with expanding facilities or decreasing usage rates create additional inconsistencies in interpreting previous estimates of the volume of animals used annually in research. • Example: A laboratory adds 100 imports to an inventory of 100 animals. Ten animals die during the first year; another 90 die during the second year. Conceivably, such a laboratory may report use in any of the following ways: Usage during year 1 As imports 100 As inventory at start of year 100 at end of year 190 average 145 As deaths 10 Usage during year 2 As imports 0 As inventory initial 190 final 100 average 145 As deaths 90

35 TABLE 10 QUARTERLY CHANGES IN A HYPOTHETICAL TYPE B LABORATORY No. Primates Quarter 1 Quarter 2 Quarter 3 Quarter 4 Initial inventory Imports Other additions 60 50 90 65 + 50 + 50 + 40 + 50 + 50 Number sacrificed - 60 - 50 - 50 - 65 Natural deaths - 25 Final on inventory 50 90 65 50

36 Note that in this example if the deaths were considered for a 2-year period, they would include all 100 animals and average 50 per year instead of the apparent 10, or 90 per year, derived from reporting on an annual basis. Comparison of a Sample of Institutions Reporting Both USDA Usages and ILAR Inventories As illustrated above, a major problem in interpreting usage volumes has been determining when the usage reported included both acquisitions and inventory and when usage implied acquisitions only. In the former case, there would be a considerable amount of redundancy in reporting the same inventory or holding capacity in successive surveys. The presence of both types of reporting was apparent from examination of a sample of 184 laboratories that reported to both ILAR and USDA. The laboratories were divided roughly into thirds, with each third of the laboratories reporting inventories that were greater than (36 percent), less than (25 percent), and equal to (39 percent) their usage rates. Clearly, a laboratory that reported an inventory differing by no more than 10 monkeys from its annual usage rate had a redundancy in reporting of 0 or 100 percent, or had under-reported its annual volume. Since the laboratories reporting similar volumes for usage and inventory were generally small sites (x = 54 monkeys), it is probable that many of them had negligible turnover and had nearly complete redundancy in reporting usage rates between years. The group of institutions reporting usage rates lower than inventories cannot be easily explained except by under-reporting or by a very small replacement volume relative to inventory. Neither of the first two groups accounted for a significant proportion of the primates used. Nearly 71 percent of the primates used (25, 500 of 35, 000) were held in institutions that reported usage rates that were 41 percent greater than their inventories. Substitution of the terms "acquisitions" and "inventories" for "usage" in future questionnaires under the Animal Welfare Act would increase the accuracy of the surveys. Research Areas Using Primates Indications from the Survey With the exception of studies in reproductive physiology, the designated research topics were grouped in Tables 11 and 12 into areas by diseases, when these were specified. Reproductive studies were grouped together whether disease related or not since few studies outside of these require animals of a specific sex. If behavioral studies are combined with repro- ductive studies, only 8 percent of the total research can justify a need for female monkeys. Most investigators did not designate the sex of animals in their orders for imports. The most frequently ordered animal was the 4-6-pound rhesus macaque. The research interest in different species is illustrated in Table 11. The import volume or inventory was accepted as the number used in the

37 research area for which the respondent listed a species and study but not the number of monkeys needed for that study. If the volume of animals is considered, there are 7 important species, each used at an annual rate over 1,000. Sixty percent of the use is focused on rhesus macaques. Rhesus together with marmosets, squirrel monkeys, night monkeys, vervets, long-tailed macaques, and baboons represent 96 percent of the use. Eight species are used in two-thirds of the 16 research areas (Table 11). The large-bodied pigtail and stumptail macaques need to be substituted for night monkeys to obtain a list of the most widely used species from the list of those used in the largest volume. There is an apparent concentration of species used in particular areas. Pharmacology and toxicology account for the first 38 percent of all primates. The largest numbers of rhesus macaques and vervets are used in polio vaccine production and testing; these species are also used along with long- tailed macaques and squirrel monkeys in a variety of toxicological tests. Studies of various diseases, including experimental surgery, account for the second largest demand, or 36 percent of the total primates. Cancer studies consume marmosets over all other species, including rhesus. Both marmosets and night monkeys are used in proportionately high numbers along with rhesus in studies of infectious diseases. This probably reflects the use of marmosets for work in hepatitis and night monkeys in malaria. Nearly as many baboons as rhesus are used in experimental surgery, which is striking when one considers their relative total numbers in use. Neurophysiological studies account for 16 percent and represent the second largest use for each of 3 species: the traditionally available rhesus macaque, the relatively large-brained squirrel monkey, and the night monkey, which is favored for its large eyes and nocturnally adapted retinas. The final 10 percent of total primates are used in physiological and behavioral studies. The research topics that were grouped together into research areas are identified in Table 12. The groupings of research areas are somewhat arbitrary due to overlap in both emphasis and techniques used. Obviously, physiological parameters are measured to describe the clinical signs of a disease, and developments in pharmacology and toxicology are specific to a particular disease syndrome. Psychobiology, which is mistakenly equated with behavior by biomedical researchers, is listed separately in Tables 11 and 12. Behavior is limited to those studies in which an animal could interact with conspecifics. In order to differentiate studies of social behavior and husbandry from studies of the reinforcement characteristics of an animal's button-pushing behavior, about 100 primates were shifted from studies in behavior to studies in psychobiology. The latter category includes studies in learning and addiction, which are typical of the studies undertaken at that facility. Since the facility was designed for single- caging except for mating purposes and infants are removed for hand- rearing, social behavior is severely restricted. The numbers of animals mentioned were more dispersed over the re- search areas than were the numbers of animals used. This pattern under- scores the concentration of use in a few research specialties and institu- tions. Sixty percent of the investigators studying infectious diseases (including hepatitis, malaria, and viruses) felt that another taxon could not be substituted for primates. By contrast, fewer than a third of respon- dents in other research areas indicated that it would not be acceptable

38 TABLE 11 PRIMATE SPECIES IN DEMAND BY RESEARCH AREA Research Rhesus area macaque Marmoset African Crab- Squirrel Night green eating Pigtail monkey monkey monkey macaque Baboon Capuchin macaque Pharmacology, toxicology 7, 370 36 838 1,147 810 81 165+ 10 Safety testing and vaccine production 4. 352 250 200 40 52 Disease- infectious 1.844 614+ 46 1,440 96+ + 37 50+ Disease- neoplasm 505+ 2, 347 350 162 180 200 Neurophysiology 2,084 10 526 7 12 154 45 15 Sensory 1, 556 146 367 26 20 133 Other 1,230 37 15 304 112 100 226 Reproductive physiology 1.328 57 6 143 219 58 Behavior 952 328 63 228 3 53 Disease- organ systems 742 234 75 78 103 25 24+ 27 Psychobiology 744 32 127 10 64 3 Experimental surgery 439 35 6 20 60 367+ 10 Physiology 358+ 20 179 24 10 152 74 18 Dental 341 120 50 124 Environmental 441 180 + Disease- other 119 100 85 4 Disease- immunology 182 40 6 14 TOTAL 24, 587+ 3, 604+ 3,310 2,086 1,960+ 1.629+ 1,326+ 578+ 571 Percent 60 9 85 5431 1 SOURCE: 1973 ILAR survey.

39 Stumptail Chimp, macaque Ape Tree Macaque, shrew general Galago Bonnet Pataa Spider Per- macaque monkey monkey Other Total cent 20 15 10,499 25 50 4.944 12 70+ 150 12 30+ 4,389 10 151 84 45 5 55 50 17 13 9 2 3,744 9 4 2 3, 118 8 2 2, 339 6 2 2,041 5 + 1, 869 4 5 1,682 4 30 17 20 20 1,464 4 6 1, 142 3 1,030 864 648 621 150 , 164+ 106 29 78 13 105 IS 5 12 463 1 254 1 531 1 251 + 1 225 I 72+ 67 57 56+ 37+, 41,111 100

40 TABLE 12 RESEARCH TOPICS INCLUDED IN RESEARCH AREAS AS IDENTIFIED BY SURVEY RESPONDENTS No. Mentions Research Area and Topic Topic Total Area Total Neurophysiology 93 Neurophysiology 59 Central nervous system, neuropharmacology 14 Neurosurgery 11 Neuropsychology, implant studies 9 Pharmacology-Toxicology 75 Toxicology 38 Pharmacology 16 Vaccine production, testing, tissue culture 12 Blood studies 9 Sensory 53 Ophthalmology 40 Otolaryngology, vestibular, auditory 13 Reproductive Physiology 52 Obstetrics-gynecology 22 Reproductive endocrinology, birth control 10 Fetal development, birth defects, teratology 11 Perinatal studies 9 Psychobiology 51 Addiction studies, psychopharmacology 26 Learning 13 Psychology 12 Behavior 51 Unspecified 33 Social 18 Disease--Organ Systems 47 Cardiovascular, atherosclerosis 29 Musculo skeletal-injury 5 Respiratory-pulmonary, TB 5 Endocrine-diabetes 3 Nervous-epilepsy, multiple sclerosis 3 Sensory-glaucoma, uveitis 2 Infectious Disease 46 Virus 22 Malaria, tropical diseases 12 Parasitology 8 Hepatitis 4 Physiology 42 Metabolism, nutrition 16 Physiology, anatomy 12 Endocrinology 7 Urology . 7 Other 31 Unspecified biology, microbiology Experimental Surgery 30 Dental ~~2~8

41 No. Mentions Research Area and Topic Topic Total Area Total Disease-Immunology 19 Environmental 20 Radiobiology, heavy metal toxicity, hyperbaric medicine Disease-Neoplasms, carcinogenesis 17 Other Diseases--pathology, pediatrics, dermatology 9 TOTAL MENTIONS 664

42 to substitute different taxa for primates. Pharmacologists and respondents generally mentioned that macaques were acceptable as alternate primates. Long-tailed macaques and capuchins were the most frequently mentioned specific alternatives. Indications from Representative Literature General The volume of scientific papers written in the field described as primatology is large enough to support three journals devoted specifi- cally to primate studies: Primates (Japan Monkey Centre), Folia Primatologica, and Journal of Medical Primatology (S. Karger, Basel). In addition, a computerized weekly bibliographic service (Current Primate References) from the University of Washington Regional Primate Center covers approximately 200 papers per week, and these represent a small selected sample of the total. A quarterly newsletter, Laboratory Primate Newsletter (Brown University) disseminates current information to aid investigators in exchanging surplus breeders and research animals. The Primate Zoonoses Surveillance (Center for Disease Control, Public Health Service) is another quarterly bulletin that summarizes pathological findings in several large colonies. Ihe literature in primatology expands yearly with the publication of two monograph series: Contributions to Primatology, the successor to Bibliotheca Primatologica (S. Karger, Basel); and Primates in Medicine. The research areas in the latter series range from immunology (Kratochvil, 1968, 1972) to comparative studies and husbandry (Beveridge, 1969a, b) and conservation (Harrisson, 1971). Symposium volumes resulting from Conferences on Experimental Medicine and Surgery in Primates are published in a series entitled Medical Primatology (Goldsmith and Moor- Jankowski, 1969, 1971, 1972a, b, c) Papers from a variety of fields in primatology have been collected in volumes of the International Primatological Society since 1966. Topics discussed at recent conferences include the utilization of primates in toxicology (Miller, 1966) and virology (Gerone e^t al. , 1973). Disease hazards associated with laboratory primates have been considered (Perkins and Donoghue, 1969), as well as the health problems of concern in inter- national shipments of wild primates (PAHO, 1972). Guidelines and handbooks on the care of monkeys, with speciesl emphasis on macaques, have been developed (Committee on Standards, 1973; Whitney et. al.. , 1973; Valerio e-t al. . 1969). Aspects of the utilization and supply have been examined for Asian primates (ICLA, 1973), South American primates (Thorington and Heltne, In press), and for a variety of species (Bermant and Lindburg, 1975). These discussions follow by two decades the conference on rhesus monkey supply that examined the need for large scale breeding in captivity (ILAR, 1955). Finally, special symposia have directed increasing attention to the maintenance and breeding of primates (Harris, 1970; Beveridge, 1972; and Diszfalusy and Standley, 1972). The growth of a body of literature on specific species is shown by col- lections of contributed papers on chimpanzees (Bourne, 1971; Reynolds, 1969) and books of bibliographic citations (Rohles, 1962). Many gaps exist in species covered by published bibliographies over the range from

43 chimpanzees to tree shrews (Elliot, 1971). The traditionally used baboon (Vagtborg, 1965) and rhesus macaques are subjects of several volumes, although works on the more recently used species like the squirrel monkey (Rosenblum and Cooper, 1968) are gradually being compiled. Reviews Surprisingly few reviews of species selection for appropriate laboratory animal models for particular medical uses were located in the literature. In publications that do evaluate a species choice, primates are often dismissed because they are too costly and the supply too unpredict- able (McKelvie et a•L , 1971) or they are considered necessary and a comparison with nonprimate species is then ignored. At present the reviews that do exist compare only a few of the total number of species that have been used in the study of a particular disease. The valuable compilations that are surveys of a wide variety of species, are typically not accompanied by a critical review of the advantages and limitations of the particular species listed (Cornelius, 1969; Jones, 1969). Two areas for which recent reviews are available are atherosclerosis and cholesterol metabolism (Strong, 1974; Taylor et al. , 1973) and leukemia (Dutcher, 1973). The taxonomic spread of species that have been used in this research is very broad, suggesting that there are several primates and several nonprimates that can serve as appropriate models. Bibliographies have also been compiled on such diverse topics as spontaneous neoplasia in primates (Caminiti, 1974), deprivation and separation (Agar and Mitcher, 1973), and reproduction and breeding in primates (Morrow and Terry, 1974). Characteristics of the Primate Trade Costs For the purpose of levying an import duty of 3. 5 percent the U. S. Depart- ment of Commerce (USDC) places a value on each imported item that reflects its sales value in the country of origin. In 1973 the assessed value per monkey from most Asian countries was $15-17; from Colombia and Peru, $10-11; and from Sierra Leone, $223 (USDC, 1968-1973). The higher value from the latter nation reflects the numbers of chimpanzees that were imported with other species from that country. Prices quoted in early 1971 for an infant chimpanzee showed a mark up from a trapper's price of $20 to an exporter's price of $260 to an importer's price of $650 (Goldsmith and Moor - Jankowski, 1972d). Ihe issue cost of rhesus macaques to investigators at NIH varied from $53 in fiscal year (FY) 1969 to $70 in FY 1974. These low values were possible because little of the expense of quarantining primates was passed on to the individual investigator. During the first half of FY 1974 the price of an unconditioned import (established by contract for large quantities) varied between $28 and $38 depending upon the size class. During this period the issue rate for a primate was 50-55 percent of the cost of a kennel-raised dog, such as a foxhound. Per diem charges for primates were less than those for all types of hoofed stock.

44 During fiscal 1974 and 1975 the Veterinary Resources Branch revised the issue rates each 6 months and finally ended the indirect subsidizing of primates by incorporating both the quarantine costs and a mortality factor into the price schedules. The method is summarized in Table 13. This economically realistic step increased the issue costs over 100 percent within a year to $110 for the small rhesus macque of 4-6 Ib, $160 for the large rhesus of 10-14 Ib, and $250 for the extra large macaque of over 14 Ib. Even at these prices, the smaller size class of monkeys is cheaper to use than dogs. If the rate setting manual for an animal facility of a sample medical school is representative (Division of Research Resources, 1973), the cost of a conditioned rhesus macaque to an investigator at a university was approximately $162 in 1973. The procurement expense of a partially conditioned rhesus macaque is estimated at $80, with indirect university costs and a facility service fee raising the unit cost of a monkey to $108. The addition of a $54 cost for quarantine, based upon a per diem holding charge of $1.25 for 44 days, gave a total cost of $162. Seasonality of the Primate Trade Both the seasonal availability and a seasonal demand influence the peak months of primate shipments. Apparently, the trapping season in Indonesia and Malaysia lasts between March and August or September because both Japan and the United States import 80-84 percent of their total numbers from these countries during this half of the year (Kawanishi, 1972; USDC, 1968-1973). A comparable proportion of the numbers are imported into Japan during these same 6 months (Table 14). This overall peak period probably reflects both the fact that half of the total number of primates imported into Japan are from Indonesia and the fact that the fiscal and academic year in Japan begins in April after a holiday period. Total imports into the United States fall to three-fourths of the average monthly numbers during the vacation months of July and August. The United States imports the largest number of primates from Malaysia in September. Both October and December, which are peak months of primate importation for the United States, fall outside of the apparent peak of availability from the country of origin. Isalickis (1972) started a breeding colony of squirrel monkeys in Peru by releasing animals onto an island between 1967 and 1970. The months between July and December when he released 90 percent of the animals presumably reflect the period when his supplies exceeded the export demand and, therefore, also the main trapping season. The drop in imports from Peru during July and August to less than a third of the average monthly rate again reflects the decreased demand during the holiday months in the United States. Losses in the Primate Trade Heavy losses in collecting and shipping freshly trapped monkeys have been recognized for several years. Roth (1965) considered that losses of 35

45 <,§ o o o to -4-• i— i NO m CO " — i -H CM rtONAL Mortality :ise Addrd Holdisg Costs ($)/ rtsssr* rH O U CM vO 00 H - -i -^ c 2 n « V — «2 ^ 09 o 15 " • — • " j rt J3 H fn ^y O -rl w M Tt* Tt* NO rH N is rH /T CO CO H £ H co ••" 1-1 •? -51 1 CO W rH "S CO « » 0 PH O M 00 NO vO W W^ rH rH «* 0 O O ^^ fT, H-) " O CM NO S CO -^ j . * - •4 (H m NO oo ^ J « <u [T[ | 0) c ^-i ^C e J^ •rH ( 1 1 r i • H Cj CO H-) r t ffi -4-) C 00 00 00 c «) rt PH Q w NO NO NO rH pT ft, rH M Q • • (j H° rd 3 O S a c* co W *5" <+H °s « T O U H c -HO m o o r*-* Ov* oo • H 0 £p H » * "~ pi CO g •rH 1— 1 I— 1 ftS 0 Q a n) CO 0) fH , T3^ ri «> T' CO CO rH CO 0) s -o " ° 0 « c -^ G o NO in m r- co n rH .rH «| rH 00 fS 0, PH n) fH bo bo V rS<! r^ J) ^ TJH or, MM n 55 CO •HH vO CO 1 , rH m srr rH oo "m r • v*J 13 M rH ^ CO Cu Lj , " CO SrH ^T nl X co M W 1 r i •M-

46 TABLE 14 SEASONALITY IN THE PRIMATE TRADE Imports into Japan 1971* Imports into US 19705 Estimated Trap Imports From Indonesia Total From Rate in Peru Malaysia Total 1967-1970J Into US, 1970JT January 20 205 85 6,473 227 1,885 February 130 428 92 7, 017 20 2, 530 March 515 1,384 169 9,060 35 2,970 April 970 1,851 225 8,392 74 4,299 May 1, 076 2,146 177 8,825 0 3, 657 June 1,030 2,020 132 9,212 265 3,426 July 1, 142 2, 180 335 5, 593 658 846 August 1, 001 1,956 57 4, 113 1, 190 855 September 490 990 484 6, 706 588 1,986 October 215 646 50 7, 538 495 2,319 November 105 270 50 6,950 1,202 2,897 December TOTAL 120 193 50 10,864 938 5,059 6, 814 14,269 1,906 90, 743 5,690 32,729 x/mo. 568 1,189 159 7, 562 474 2,727 6 Peak Mos. (Percent Total) 84 81 80 59 89 68 *Kawanishi, 1972 §USDC, 1970 JTTsalickis, 1972

47 percent of the total number captured was a conservative estimate. Lewis (1973) described the importation of rhesus macaques and long-tailed macaques into Australia. By estimating from his graphs, only a half of the 47,216 primates imported between 1955 and 1961 survived a 12-week quarantine period. These losses were cut nearly in half when the consign- ments were shipped in small groups averaging 216 rather than in large groups averaging 1,089. The quarantine losses from shipping freshly trapped animals were reduced to less than 10 percent by transporting imports that were acclimatized for 12 weeks prior to shipment. Unfortu- nately the losses in the country of origin were not added to the losses in the receiving country to obtain a comparison of total losses from an acclimatizing program. This report is comparable to a 1973 estimate that 60 percent of the long-tailed macaques imported into Canada from Malaysia die within a month of arrival (M. Walcroft of Connaught Labs, personal communication to J. Vickers, 1974). Considerable controversy exists over the causes for losses in primate populations. S. M Richards (personal communication, 1974) attributes many losses of vervets to the primate trade while Rowell (1968) implicates eradication programs for agricultural pests. Richards describes an unpub- lished report by P. Pegg submitted in 1967 to the Kenyan government. Pegg estimated that 62 percent of the vervets died within country from a variety of factors including dead animals at the collecting station, deaths in unattended traps, young released without their mothers, and the culling rate by dealers who accept only animals of a specific size. The culled animals are sold for dog food in Kenya and account for an estimated difference between 62-percent and 25-percent losses within country. The situation differs in Uganda where Rowell reports that approximately 6, 000 vervets were killed as agricultural pests in 1964. Specifically organized expeditions have proven to reduce losses. For example, baboons have been collected for the Southwest Foundation for Research and Education by special collecting trips to Kenya. The Wilsons have recently collected long-tailed macaques in Indonesia for the U. S. Primate Centers. Rhesus macaques have been shipped from Kashmir with minimal losses when monitored from trap to their U.S. destination at Charles River Breeding Laboratories, Inc. (Kaufmann, personal com- munication, 1974). The cost of 150 rhesus macaques acquired by this method was $152 per monkey, or about $50 higher than the 1974 purchase price from commercial dealers. The greater cost included higher shipment charges resulting from the use of crates with individual compartments, special handling during trapping, isolation from other shipments during truck transport and holding within India and during air shipment, and the travel expenses for two persons from the United States to the capture site. The special procedures included limiting contacts of the monkeys to handlers wearing protective face masks and gloves, provisioning with commerical pelleted feed and treated water, and screening for several diseases at the trapping site. The animals were tuberculin tested and vaccinated against measles. Serum and stool samples were obtained and later analyzed, especially for shigella, salmonella, and Herpesvirus simiae. These pro- cedures reduced mortality from the typical 10-20 percent to less than 1 percent, and minimized the need for clinical treatments during quarantine. The reduction in quarantine losses decreased the difference between monkeys

48 SI Si « 1 3 1 S Si e s £ a 3 g :2 £ '; 3 m ., Gt 4Ji 3 • j -i- 3 ^ ^-ri ^ 03 ^ § rql £ |"-E s | K s|" "S ~r § c oa<o3~cu,3 — i IT) . Dd^ j| I|i|- ^lUlSl^i <|oi| Jl u|u . i - ^ g Cj >>oso;tt:>>-. >« r- cr- g T> _ « 4) "* ^ A 0. "5 Z ^ a .2 si s- "i -5"- n ^03 ^ •2 ro ^iS^ * - i HI M -^ - .- .g .^ " £*a u 0 ^H 21 ® « 3 C u . nl I-H^ ".; .. .T* u » ; " 1 « M -* -2 ^ i 1 | ? S[S 5ZE Jl j| „• oil JMI u"lu|u| 111 u u u u "" ""." if l ^ 13 Ul Tl io — M = T) £•? T) -2 •?* "•c "c c« c •• « —. » Where Found K^ b* « «< otfl •g o-g o „ „ „ 5^ Si 2 9 T) - o.•25"i.«K.y-;';i.i So \o a c-3 —u S 3•3 e-J c01 £ £ ^ ^ — •8 C "Sg T) 33 «« rt.3CcCmnl«mm« CO ) ^ rt rto ** "^o3 £t- t-cyu4)4i-4)./:0330O^ 2cj 2U ^ to w ww •sjm r- r ..j O 2 3 ) u ' J J J ?? i *<J - + + + + + ++2:Z++So"1""1" o r- 3 £c ••* « Ml Ml . CL- u OT OT . <KI H 3 io c M J 3 u w 2 - S c 0, E « u u O "^ "^ M. ^ Q ift * T) °* D S co ~ 5 h -S r « .2 « 2 •» u g -. Z tt rt „ u « »" "0.2 "S u 3 "^ ^ u -° Z £ • o" " o > » Q V flj J Z H i 5 -a U Q r-H 00 u £ " in Z C **" OC **H 'JT " gg Q o 0) u "^ ,22 ^. -0 S • «i c ^ B 01 C io r-^ C H M JJ h r Og--o£ E 15 PROTEC H C •9 V M * M-i^mX £ J3 <fl J .^ r "Sf*1 — w E i - s : 2 ^"H i5 5 34i£:"P«'« MC Q) uo r^ifl*-.£uj "ifl Sm" 3 .2 * S0rr in » S"o"14> i I c|a-s x c 1 2 "s •« 2 -- -« lu£ IslljgoSs^af** S | 1 •• I -j « s -1 SSio^S"iJ u!H= ^io u « o « g •; J W*EaS°Vuifl^t-rO«3 io^J •o-^u .5*u J* m 6jH5|5u2£5l<ol|Q 5 •J " | u'3 < ^< <lffl H J £ Q U U

49 « m £ II ., :- - ° £p ' M T fll 1 1C j,| 01 oteicuidi U73 A> A XOS oi »» I i i i i 1 g§ 2™ • 5 -1 N S 00 S 3 j3 •o c WW W W W W U U *1 Where Found * Is i . i-i i .5 I :1 IJ.llljl ^Sl -H-iSs 5- C « - - & A I.S| .S|.i^i i< 1 I §rg! illlil- ^ •a o a .•o5«>,o2•oc"'Oo-o"!5i3i5a> "2^35 "Ssm1u^1- "2 z£^<Sw5->«ffl£^i--NC« £Sin^ a^^o^H o^ m 5 u r S S-2 £ c **• ^ 4JJJ J J JJ "^ 2|"SJJ : J J 1.«o Z++ZZZZ Z+Z+ZZ+ . ..Z •• Z Z + 0| X|X| ^ 4; "* v A| . D. V d ui w + 1 H D ^ 2 m 0 g s e ^ *O « 1 « 1 S M 3£ i >• 01 " S! "O 1 c 1 51 -i jc > « .2 ^ .. -g .*; 01 .2 c "3 •o .5 n co r- * •S 1 j?i S £ 3 rsJ I |5 ? U a i ifl X O . rt b" S 2 P*| 2 uu iX & a H Co A 1 "C « V o J i ! a a I N <) * M C •5 s V T 33 "q Q 1 ** C 3 i " ^ rt CJ (/, ** >- rtL=not listed E=endangered; V "ABJ•E 15 (contin c i „?! •,. ill 1 3 q S, I V I o 8 M-S IP -g^S 1 1 J S ] || a < a 58S li •§35 ': s. 1 s 1 s ^ s D. mum 'SI S AI8..3 J3J3» S •O°'Qj O i, 0) " - M in c ', Jn - ." C ii u -.«1... >-«.S • • "S i F OOO. O ^ 2|o 0. MO.I O.Z(n OO•^::w5 § s O X Ci •::- u^,

50 TABLE 16 CURRENT BREEDING OF MOST COMMON SPECIES IN BIOMEDICAL RESEARCH LABORATORIES Females in Breeding Colony Rank by Births by Species Total Inventory 1973 Species Births Macaca mulatta 22,980 4, 358 3,129 2,318 1,836 1,439 1,390 1, 316 1, 083 673 511 419 295 261 186 2,732 499+ 414 480 304 462 118 23 260 145 21 159 94 65 48 991 185 316 120 94 241 33 2 68 46 7 66 64 30 43 1 Saimiri sciureus 4 3, 10, 13 5 6 2 14 Saguinus sp. Papio sp. Macaca fascicularis Macaca nemestrina Cercopithecus aethiops Aotus trivirgatus Macaca arctoides 7 11 Pan troglodytes Cebus apella Macaca radiata 8 9 16 12 Galago crassicaudatus Cebus albifrons Callithrix jacchus TABLE 17 PRIMATES THAT SHOULD BE BRED IN LARGE NUMBERS Species No. Citings Rhesus macaque Squirrel monkey Baboon Marmoset Stumptail macaque Pigtail macaque Vervet monkey Night monkey Chimpanzee Long-tailed macaque Capuchin Spider monkey Others TOTAL 148 90 46 36 35 23 23 16 15 14 12 4 15 477 SOURCE: ILAR 1973 questionnaire data from biomedical researchers.

51 acquired by expeditions and those imported commercially to $28 per monkey ($214 vs $186 issue cost from a $0. 68 per diem-90 day quarantine). The anticipated benefits from decreased death losses in the breeding colony resulting from reduced incidence of pathogens will further offset and justify the greater initial expenditures (Kaufmann, personal communication, 1974). Regulations The Convention in International Trade and Endangered Species of Wild Fauna and Flora that was signed by several nations in 1973 could become law in 1975 if a total of 10 countries ratifies the Convention. If so, the animals listed in Appendixes A and B will become regulated internationally. Table 15 compares the species protected by the International Convention, those protected by the import restrictions of the U.S. Endangered Species Act of 1969, and those species listed in the International Union for the Conser- vation of Nature and Natural Resources (IUCN) Red Data Book (IUCN, 1972). Captive Breeding of Primates Species Currently Bred in Research Laboratories Survey Totals No major changes in the numbers of births, the numbers of breeding females, or the species bred during the last 4 years are apparent from a comparison of the ILAR surveys for 1970 (Thorington, 1971a) and 1973 (Appendix III). Efforts to breed certain species are evident from the increase in births of Galago crassicaudatus from 34 to 64 and of Cebus species from 1 0 to 37. The most commonly bred species in research facilities are ranked by order of numbers held on inventory in Table 16. Generally, the species used most frequently are not those currently being bred in the largest numbers. Aotus trivirgatus and Cebus apella both rank among the top 1 5 species used but are not among the top 15 species bred. The lack of emphasis on breeding is further illustrated by the small number of females assigned to breeding colonies and by the low number of live births occurring in 1973. Biomedical researchers were requested to list the species they thought should be bred in large numbers for research. Predictably, most listed the species they were studying. The order of the preferred species listed in Table 17 reflects the relative usage rates of these species more closely than does the rank order of the species currently being bred (Table 16). A second generation of a variety of species has been bred in captivity (Appendix III). These primates represent a valuable breeding resource and current inventories of laboratory reared stock are increased from 700 F i and F£ females to nearly 1, 000 when primates of several generations at the Caribbean Primate Center are included. Rhesus Macaques A sample of the usage of the reproductive output of breeding colonies exemplifies the priorities of current programs (Table 18). At first sight the apparent productivity of 41 percent of the adult

52 females seems particularly small. This proportion underestimates considerably the reproductive success because the value for births applies to 1972 and the number of adult females assigned to breeding colonies applies to October, 1973. Since it could be expected that several females have been added to colonies during this interval, some females would not have been in residence in the colony long enough to complete a gestation period. Of particular interest is the fact that 29 percent of the total productivity is used as experimental fetuses. Of those pregnancies that complete term, 57 percent are reared to 6 months of age. A fairly large proportion of these infants are also used experimentally. A breeding colony as defined in this report is one that is self perpetu- ating. Under such a definition, only one research institution could realis- tically be classified as a breeding colony for rhesus. The California Regional Primate Research Center holds the majority of the 100 captive- raised breeding females that could be traced through the 1973 survey. These F]• females have produced only 50 second generation offspring. Estimates of gross yield for breeding macaques frequently assume an 80 percent reproductive rate and 10 reproductive years for each female. These rates have been considered to be overly optimistic by many research- ers and rates of 50 percent for 5 years may be more realistic, especially for species other than rhesus. Net yield per 100 breeding females could reach 57 yearlings if the sex ratio of breeders were 10 females : 1 male; the reproductive rate was 80 percent per female; 10 percent of the breeders were replaced annually; and infant losses were 15 percent. Fifty-seven yearlings could be produced for $640 each for a colony with these character- istics if the holding costs were $0. 50/day for each of the 212 breeders and maturing young necessary to perpetuate a colony of 100 females. Marmosets Since marmosets can produce twins annually, and occasion- ally twice per year, they can theoretically maintain a level of 200 percent productivity annually. The few research facilities that have bred mar- mosets have demonstrated that this level of reproduction can be achieved (Table 19). However, most of these laboratories remove the infants at birth for the expensive procedures of hand rearing. Such reproduction would not come under the definition of a breeding colony in the strict sense since the colonies depend upon a continuous supply of wild-caught adults. Saguinus sp. are most frequently bred in the United States while Callithrix sp. , especially (3. jacchus, are typically bred in the United Kingdom. Production of marmosets in the United States was 350 in 1972 by breeding colonies that maintained 450 females. Hobbs (personal communication, 1974) has reported 532 marmoset births in the United Kingdom for 1972. Taking the lead in the United Kingdom was the Imperial Chemical Industries with 350 births and Fisons Pharmaceuticals, Ltd. , with 112 births. An examination of reproduction in zoos shows that only 46-68 percent of the infants survive when they are raised by their mothers (Table 20). This range spans the survivorship of 61 percent achieved under intensive laboratory management of individually caged pairs. Based upon observed losses in the marmoset colony at Rush-Presbyterian-St. Luke's Medical Center, the 39-percent infant loss includes 21 percent stillbirths, 16-20

53 TABLE 18 RHESUS MACAQUE BREEDING COLONIES IN 1972 No. Percent Use Primates of Neonates Adult females (on inventory, October, 1973) 2,532 Experimental fetuses 286 Live births - 1972 817 Use of Neonates - Sample N = 632 Experimental deaths 217 34 Nonexperimental deaths 57 9 Reared to 6 months 358 57 TABLE 19 REPRODUCTIVE RATE OF CALLITRICHIDAE BRED IN UNITED STATES RESEARCH INSTITUTIONS DURING 1970 Live Births/Female (Percent) No. Births U.S. Research Colonies Species Saguinus fuscicollis 155 199 159 96 291 62 1 3 5 Saguinus nigricollis Saguinus oedipus TOTAL 449 9 SOURCE: Thorington (1972). TABLE 20 SURVIVAL RATE OF CALLITRICHIDAE BORN IN WORLD ZOOS DURING 1970 AND 1971 Infant Survival (Percent) No. Zoos Maximum No. Births No. with Surviving at Births Births 1 Zoo in 1 Year Species Leontopithecus rosalia 46 151 76 106 441 20 17 20 5 6 4 San Diego, U.S.A. Rio de Janeiro, Brazil London, ZSL G.B. Inuyama, Japan (Cebuella pygmaea) Callithrix jacchus 58 68 Saguinus oedipus 1 5 species of Callitrichidae 60 55 6 SOURCE: Data from Lucas and Duplaix-Hall (1972); Duplaix-Hall (1973).

54 percent loss during the first 30 days for hand-reared or mother-reared infants, and an annual holding loss of 8 percent (L. G. Wolfe, personal communication, 1974). The differences between observed and expected production are compared in Table 21. The net yield from the idealized production centers of wild- caught breeders have overestimated the obtainable yield by 46 percent (160 vs. 86) based upon present management methods. Under the same sets of assumptions the food costs per yearling produced are somewhat higher for rhesus macaques ($640) than for marmosets ($560, Table 21). Additional savings in breeding marmosets should be realized from lower costs for equipment and space. The calculations for Table 21 are based upon 200 established breeders. The Rush-Presbyterian facility has experienced a 20-percent loss during 3 months of quarantine. If there were no harvesting, it would take 4 years at observed survival rates to produce 1 6 F£ progeny and to double the in- ventory of 148 imports surviving quarantine. It would take at least 5 years to double the colony size above the original 200 imported animals. Planned and Proposed Production Centers A number of primate breeding colonies have been established in recent years, but most have been funded to provide animals for the internal needs of the funding organization, specifically intramural NIH and the primate centers. Table 22 summarizes the large production centers that are currently funded. Current inventories of adult breeders are projected to increase over the next 5 years from 5, 800 to 9, 500. The nuclear breeding stock at primate centers and several other institutions have been described by Goodwin (1 972) and Neurauter and Goodwin (1972). The need for continued expansion of breeding efforts has been stressed by Goodwin (1974). One commercial free-ranging colony has been started for breeding rhesus macaques on an island in the Florida Keys by Charles River Breeding Labs, Inc. Commer- cial production centers for compound breeding are being planned by Earth Science Products, Inc. in Hawaii and South American Primates in Brazil and Peru, in addition to the commercial centers already funded in the United States (Table 22). The development of a primate center in Israel has also been proposed, although the original projections were based upon the assumption that the center could serve as a conditioning facility for continuously available wild primates, rather than as a production center (Goldsmith and Moor-Jankowski, 1972d). Cost estimates made in 1971 (excluding profits) for production centers have been summarized by Hobbs (1974) for colonies in the United Kingdom. He suggests that a yearling macaque could be bred for $225-$260, a young marmoset for $85-$90, and a squirrel monkey for $170. Estimates derived from 1971 costs at the National Primate Centre at Tigoni, Kenya, suggest a 6-month old vervet would not exceed $68. Elliott (1972) estimated that a macaque could be raised in outdoor compounds in Singapore for $66 each in 1971. However, the difficulties in controlling insect and avian-borne

55 TABLE 21 OBSERVED PRODUCTION OF MARMOSETS IN BREEDING COLONIES Observed rates include: 90% birth rate (assumed for 10 yr/female) 1. 92 infants/birth 39% infant loss until one year of age equal birth and death rates for each sex Colony Composition Observed Category Female Male Inventory No breeders 100 100 200 Gross annual production 86. 5 86. 5 - Infants surviving to 1 yr Replacement holding for 2 yrs Net yield (held for sale at 1 yr) 53 10 43 53 10 43 40 86 TOTAL 326 No. Cost ($)/ Annual Net Yield Produced Yearling* Observed annual net yield/100 females (inventory 326) 86 692 Expected annual net yield/100 females in idealized production colony of wild-caught breeders assuming 80% reproductive rate, 100% twinning, negligible infant losses (inventory 360) 160 Expected annual net yield/100 females in self-sustaining colony with 80% reproduction, 10% breeder replacement, and 15% infant loss (inventory 356) 116 411 560 SOURCE: Data based on colony at Rush-Presbyterian-St. Luke's Medical Center, Chicago, Illinois; L. G. Wolfe, personal communication, 1974. *Based on $. 50/day/animal x 365 days x inventory/yearlings produced.

56 TABLE 22 PUBLIC HEALTH SERVICE SUPPORTED DOMESTIC PRODUCTION OF PRIMATES Contractor and Location Funding Agencv Current Status Adult Inventory, Mid-1974 Proposed No. Breeders by 1979 Rhesus Macaques Timed Pregnancy VRB, Bethesda, MD VRB-NINDS, Bethesda, MD Gulf South Research Inst. , New Iberia, LA NICHD, Bethesda, MD Production Colonies VRB Center, Perrine, FL U. Puerto Rico (CPRC), La Parguera, PR U. Puerto Rico (CPRC), La Parguera, PR Regional Primate Centers (RPRC's) California RPRC, Davis, CA Delta RPRC, Covington, LA CDC, Atlanta, GA Gulf South Research Inst. , New Iberia, LA Hazelton Corp. , Herndon, VA Hazelton Corp. , Edinburgh, TN Bionetics Corp. , Yamassee, SC Charles River Corp. , Key Lois, FL Research Funding Proposal NIH-DRS 160 NIH-DRS 40 NIH-DRS 100 NIH-NICHD 50 NIH-DRS 350 NIH-NINDS 160 FDA-BOB 600 RHESUS SUBTOTALS NIH institute contracts Other agencies (BOB,C Regional Primate Centers NIH-DRR 1, 150 NIH- NICHD 250 FDA-BOB 100 CDC 150 NIH-DRS 100 NIH-DRS 225 NIH-DRR 140 NIH-DRR 110 NIH-DRR 600 NIH-NIDR 0 cts 2,285 3, CDC) 850 enters 1, 150 4,285 Other Macaques Washington RPRC, Seattle, WA RPRC's RPRC's California RPRC, Davis, CA Wisconsin RPRC, Laredo, TX site Baboons RPRC's Washington RPRC, Seattle, WA Southwest Fdn. Research and Education, San Antonio, TX LEMSIP, Sterling Forest, NY NIH-DRR NIH-DRR NIH-DRR NIH-DRR NIH-DRR 650 pigtail 120 long-tailed 1 60 stumptail 115 bonnet 86 Japanese NIH-DRR 15 NIH-VRB 9 (for NICHD) NIH-VRB 20 (for NICHD) NIH-VRB 10 (for NICHD) 350 160 40 100 50 6, 860 700 160 1,000 1, 150 300 1,000 300 350 350 500 400 600 50 3,760 2,300 1, 150 7,210 1, 131 650 120 160 115 86 38 9 31 10 88

57 TABLE 22 (continued) Contractor and Location Funding Agency Current Status Adult Inventory, Mid-1974 Proposed No. Breeders by 1979 Patas Monkeys Meloy Labs, Springfield, VA Chimpanzees Yerkes & Delta RPRC's LEMSIP, Sterling Forest, NY Albany Medical Center, Hollomon AFB facility, Alamogardo, NM New World Monkeys VRB Center, Perrine, FL NIMH, Bethesda, MD Delta RPRC, Covington, LA Delta RPRC, Covington, LA Prosimians Oregon RPRC, Beaverton, OR Oregon RPRC, Beaverton, OR Oregon RPRC, Beaverton, OR NIH-NCI, 0 120 NINDS NIH-NHLI 10 27 NIH-NHLI 0 100 NIH-NIAID, 40 50 FDA-BOB, CDC NIH-VRB 50 squirrel 100 HEW-NIMH 100 squirrel 10 NIH-DRR 60 squirrel 155 NIH-NIAID, 30 (Saguinus 300 FDA-BOB, CDC mystax NIH-DRR 74 (Galago 74 crassicaudatus) NIH-DRR 38 Lemur fulvus 38 NIH-DRR 20 L. catta " 20 OTHER SPECIES NIH institute contracts 30 SUBTOTALS Other agencies (BOB, CDC, 100 HEW) Regional Primate Centers 1, 387 1,517 TOTAL 5, 844 9,465 120 177 565 132 CDC - Center for Disease Control CPRC - Caribbean Primate Research Center FDA-BOB - Food and Drug Administration, Bureau of Biologies LEMSIP - Laboratory of Experimental Medicine and Surgery in Primates NIH - National Institutes of Health DRR - Division of Research Resources DRS - Division of Research Services NCI - National Cancer Institute NHLI - National Heart and Lung Institute NIAID - National Institute of Allergy and Infectious Diseases NICHD - National Institute for Child Health and Human Development NIDR - National Institute of Dental Research NINDS - National Institute for Neurological Diseases and Stroke VRB - Veterinary Resources Branch NIMH - National Institute of Mental Health, Department of Health, Education, and Welfare RPRC - Regional Primate Research Center

58 diseases is cited as one disadvantage of outdoor compounds (Hobbs, 1974). These 1971 estimates are considerably lower than the current estimates between $250 and $500 for primates raised at the proposed Hawaiian facility of Earth Sciences Products, Inc. , and more than $500 in most U.S. facilities. Most facilities in the United States assume a holding charge of at least one dollar per day for each animal. Porter (personal communication, 1974) of South American Primates has estimated a production volume of 4, 000-5, 000 platyrrhines per year in facilities to be built in Peru and Manaus, Brazil, with costs for captive- bred animals to be in the range of $100-$! 50 as are current for wild- trapped animals. During the initial phases of development of these facilities and selecting breeding stock, he expects to condition and provide about 400 per month for research. After 5 years Peru has indicated that all exported primates will have to be captive bred. Plans for Manaus include breeding monkeys in cages rather than on islands. The monkeys are expected to cost twice as much but also be free of tropical diseases. Considerable skepticism has been voiced concerning the sincerity of breeding efforts since there are examples of discontinued or poorly managed colonies. Carpenter (1972) has documented the sporadic history of the free-ranging rhesus macaque colony released on Cayo Santiago Island in Puerto Rico. This colony has been managed since its establishment in 1939 for several different purposes ranging from studies on social behavior to production of experimental animals. The colony was not continuously provisioned for nearly 10 years after the second World War, and the population declined from around 600 to 150 in 1956, although half of the initial number were probably trapped and sold. A second example is a free-ranging colony of squirrel monkeys estab- lished on Isla de Santa Sofia II, in Leticia, Colombia, and has been described by Tsalickis (1972). Tsalickis released 5,690 monkeys onto the 400-hectare island between 1967 and 1970 and estimated that the population should reach 20, 698 by 1971 if there were an 80-percent birth rate and no mortality. After censusing the island in 1972, Bailey e-t al. (1974) esti- mated that the population was under 1, 000 animals. Despite historical problems with the transplanted macaques on Puerto Rico, the populations have provided information useful for management. The net annual increase at Cayo Santiago Island has been 16 percent; that at La Parguera, 13 percent (Drickamer, 1974). Because the data from these colonies have been accumulated on known animals for over 10 years, they are more accurate than estimates of the potential harvest of vervets on St. Kitts (McGuire, 1974). A harvest of 10-40 percent may be derived from McGuire's estimate of 2, 000 animals killed for bounties from a population estimated to be between 5, 000 and 20, 000. The life tables obtained for provisioned populations differ from those obtained from natural populations. In the toque macaque, higher death rates offset birth rates and lead to stable populations (Dittus, 1974). Discussion of Primate Trade and Breeding Research Use of Primates One way of differentiating research demand for species is presented in Table 11. Both marmosets and night monkeys may be considered as

59 "special use" species at the present time because more than 80 percent of the animals of these species are used in a single research category--that related to specific diseases. This pattern contrasts to the "general use" species such as the rhesus macaque and the squirrel monkey , which are utilized in each of the research categories. The relevance of this sepa- ration for the selection of species to be bred in captivity is the trend in use that the pattern reflects. Demand for a species that is found to be useful in basic research into a particular disease increases from several disci- plines as baseline data on the species accumulate over several years. As drugs or vaccines are developed for a disease, the proportional demand for that species shifts to the area of pharmacology and toxicology. If the level of demand for marmosets and night monkeys to test the safety of cancer drugs and malarial vaccines parallels the demand for rhesus macaques and vervet monkeys in the earlier work with polio, then the demand for these New World species will increase substantially. Other species are so poorly known and so unavailable that no demand currently exists for them; however, the number of citings for capuchins, tree shrews, and patas monkeys that were noted for work in infectious diseases and neoplasms is indicative of potential demand. Even though each of these species comprises less than 1 percent of the listed demand, it maybe assumed that their usage would rise with availability. The belief that supply creates demand has been shared by many investigators, the impor- tant factor being the reliability of a captive-bred supply that is sufficiently large to respond to research demands (Hobbs, 1974). Recent editions of Bowker's Medical Books in Print confirm the recent explosion of work in neurophysiology and the diversification in species examined. Prior to 1968 the rhesus macaque, squirrel monkey, and chim- panzee were subjects of brain-mapping studies. By 1970, stereotaxic atlases had been published on seven more species of primates--the baboon, capuchin, long-tailed macaque, pigtail macaque, Japanese macaque, common marmoset (Callithrix jacchus), and tree shrew. With a description of 10 primate species and 10 other laboratory animals (dog, cat, rat, Citellus sp. , mouse, guinea pig, hamster, rabbit, pigeon, and mallard) to choose from, this research area exemplifies the need for evaluation and review before species lists are magnified without direction. The expanding volume of publications that describe studies using monkeys has frequently been considered an indication of the increasing need for primates in research. However, there are serious shortcomings in much of the medical literature that result from a lack of attention to defining experimental variables. Several studies lack a statement onthe number of animals used, sex, or weight class (as an estimate of age), and do not describe diet and housing conditions. This lack of sophistication in describing the animal model contrasts greatly with the awareness and control of environmental variables in work with other species (Magalhaes, 1974). St. Clair et al. (1967) conducted one of the few studies that correlated a physiological variable in monkeys, blood cholesterol levels, with the type of caging and the time since capture. Many original papers still refer to "the monkey" or "the marmoset" without giving an accurate identification of the species used (Hershkovitz, 1965a, 1965b). Thorington (1971b) has also stressed the need for proper identification and voucher specimens of primates used in viral research. Medical journals are far

60 behind journals of primatology in using scientific nomenclature for experi- mental primates as can be seen by a perusal of the titles cited in the Washington Primate Center's "Current Primate References." The addition of specific identifications in titles would reduce costs and time in biblio- graphic indexing and could be implemented easily by revised editorial policies and conscientious peer reviews. A second noticeable shortcoming is the magnification in the literature citations of single-occurrence or rare observations. This practice is par- ticularly unfortunate when the observation is made in an endangered species with a limited normal gene pool. Examples include observations of mon- golism (McClure, 1972) and kuru in chimpanzees (Gajdusek and Alpers, 1970, cited in Moor-Jankowski and Goldsmith, 1972). These citations have been added to the compilation of animal models of human diseases prepared by the Armed Forces Institute of Pathology. The importance of the first demonstration of a slow neurotropic virus of human origin (kuru) in primates is widely recognized. However, through the process of repetition and extraction of citations covering a single species choice, certain animal models become overemphasized to the neglect of potentially more appro- priate ones. Marsh (1972) is one of the few authors selected in such compi- lations who compares a class of related diseases and susceptible animal models. If kuru resembles transmissible mink encephalopathy, scrapie, and Creutzfeldt-Jakob disease, the range of potential animal models for at least one of these diseases that could be substituted for chimpanzees and gibbons in studies of slow viruses includes squirrel monkeys, stumptail and rhesus macaques, hamsters, mice, mink, raccoons, striped skunks, and goats. The Primate Trade The amount of primate use has been influenced by the relative costs of other experimental animals, maintenance, and acquisition costs. The lower charges noted at NIH for primates relative to laboratory-bred dogs have undoubtedly encouraged the research use of primates over the past several years for economic reasons alone. Because quarantine nearly doubles the initial price of primates, some investigators have questioned the need for a long quarantine period. Pressures from professional organizations and government regulations have converged in attempting to correct abuses of the past commercial trade in primates. The Joint Primate Specialist Group of the International Union for the Conservation of Nature and Natural Resources and the Inter- national Primatological Society stated in a 1973 resolution that primates have been undervalued as a national resource by most countries. The organization recommends that governments in the source countries should not only restrict exports of wild primates but should also tax exports if necessary to conserve natural populations of laboratory primates and to encourage the development of self-sustaining breeding colonies. One of the services of commercial suppliers appears to have been that of absorbing the holding costs of several months between the period of dry season trapping and peak demand. For example, only 2 of the 6 high import

61 months for primates from Peru correspond to the high months of avail- ability in that country. It seems probable that the large primate trade volume in the past several years, contributed to, in part, by the pet trade, has buffered researchers from the seasonal effects of availability of wild- caught animals. As the volume of exports is restricted by any particular country, researchers will have to absorb these holding costs or experience several months of unavailability annually for these species. Whenever animals are captured through special trapping expeditions, there is the added advantage that they are obtained from known localities. Special collections permit comparative studies into the variability within species and the extrapolation of results that previously has been impossible. A smaller sample size needed for statistical significance of results can also be expected from the use of more homogeneous groups of experi- mental animals. Conservation objectives have been gained through the reduction in losses during capture and shipping of semi-terrestrial species. It is important that a similar effort be directed toward the capture of arboreal species. Additional innovations are necessary to curtail losses presently occuring in marginal and underfinanced holding facilities which compound the problems of infectious diseases, nutritional deficiency, and crowding stresses. Losses resulting from unsystematic collecting methods have been estimated by some to be as high as 50 percent of the numbers captured. If the purchase prices of primates must cover a loss rate of 50 percent, the economic advantages resulting from reducing losses and the numbers of treatments during quarantine should offset the increased costs of specific expeditions. Biomedical researchers have been generally so specialized that they have not informed themselves about the degree of poaching and illicit trade they have supported inadvertently through providing a demand for research animals. Government officials in the exporting countries could be expected to be cooperative towards an expedition method of trapping since the legitimacy of the research user, the acceptability of the trapping sites, and adherence to the trapping and export regulations could be monitored more readily. Permit quotas and certificates of need channeled through commercial exporters represent an indirect approxi- mation of the expedition method financed directly by the users. Captive Breeding It is clear from the data presented that breeding was funded in the past primarily for research on facets of reproduction and most of the repro- duction served experimental purposes rather than replacement. These priorities for restrictions on breeding were justified economically in the past while imports were available and inexpensive, but they have main- tained the dependency of researchers upon wild-caught monkeys up to the present time. The feasibility of multigenerational breeding for many species has been shown by the determination of several investigators who have bred primates in spite of negligible funding for this purpose. However, the results of captive breeding (illustrated by marmosets) suggest that basic studies of husbandry are needed before self-perpetuating breeding colonies can become productive on a large scale.

62 Cadigan and Lim (1975) have recommended managing multiple species under natural conditions since sympatric forms maintain spatial stratification and different activity patterns. Free-ranging colonies may offer sizable savings in labor and maintenance costs while providing a net annual growth varying between 13 and 16 percent. However, since animals in free-ranging colonies require continuous provisioning and monitoring, the planning and financing of additional colonies will have to be large enough in scope to carry them from their inception to self-supporting levels of production. Without long-term financing for future colonies, the question of whether production colonies could become a screen for exporting primates will continue to be raised. Ecological Considerations of Primate Populations Relatively little information is available on the status of wild primate popu- lations because biomedical funds have been primarily directed to research on health problems of national concern, and have not been so readily avail- able for studies related to population dynamics of wild-caught research animals. Thus, the acquisition of large numbers of primates for biomed- ical programs has not coincided with a program of monitoring the impact of the commercial trade on trapped populations. The recent curtailment of primate exports by countries having a commercial trade and a developing interest in a sustained harvest of primate populations raises several ques- tions: (1) What is the population size of different primate species in the wild, (2) what are the trends within these populations, (3) what does the area of national reserves indicate about the size and diversity of primate populations that will receive long-term protection, and (4) what are the prospects for wild populations? Population Densities Estimates of populations were located for only 16 named forms. The majority of these estimates can be found in the Red Data Book of threatened and endangered forms (IUCN, 1972) (see Table 23). Except for threatened species with very restricted distributions, only two regional or national population estimates are available that have been extrapolated from study populations by authors familiar with local habitats. These studies illustrate the value of applying demographic methods in estimating populations over 100,000. Southwick £t al. (1970) estimated that rhesus macaques number a half million in Uttar Pradesh; Chivers £t al. (In press) estimated that there may be a quarter million gibbons on the Malayan peninsula. Wolfheim (In preparation) has itemized field studies and identified trends for many primates based upon a recent survey of the literature and field inves- tigations. Most current estimates must be regarded as ecological density estimates (estimates based upon usable habitat) but a few are more properly considered as crude density estimates (overall or geographical estimates). Density estimates are of limited value when authors do not report the total area and number of animals from which the estimates were derived. This prevents the reader from identifying the type of density estimate when com- paring species and study sites.

63 Selected population densities for several species are given in Table 24 and 25 for New World and Old World species, respectively. These estimates provide examples of population densities which might be considered common in representative habitats under normal ecological circumstances. Average population densities are almost impossible to calculate since they vary consid- erably in different habitats and regions. Maximum densities have the advantage of indicating potential populations in areas of most favorable habitat. However, maximum densities are often exceptional cases since estimates of several authors cluster at much lower values. The higher density estimates noted for provisioned macaques in city parks (Southwick, 196la; Neville, 1968; Southwick and Cadigan, 1972) and temple areas and for howlers in remnant forests in expanding agricultural areas (Baldwin and Baldwin, 1972) have not been in- cluded although it is recognized that managed primates can be maintained at much higher densities than occur naturally. Differences in authors' census techniques, actual carrying capacities, and protection from exploitation that have contributed to the high density estimate for squirrel monkeys have not been evaluated. Those primates with the lowest maximum densities include the large-bodied apes and savanna species, such as patas monkeys. Trends Declining trends in rhesus macaques and vervets are well documented. These include a 75-percent decline in unprotected populations of rhesus macaques in the Aligarh district of India over the last 15 years and an esti- mated 90-percent decline over the last 20 years (Southwick and Siddiqi, In press). A 33-percent decline in vervet populations within six years between 1964 and 1969 occurred in Masai-Amboseli Game Reserve (Struhsaker, 1973). The decline in vervet numbers may have resulted from changes in the water table or the loss of food trees destroyed by competing elephants or livestock. Recent surveys have shown that market hunting for meat is a serious drain on primate populations in Colombia and Peru. This exploi- tation has reduced primates by 90 percent in some areas and the problem of hunting for local consumption has been exaggerated by the practice of supplying petroleum survey teams with wild meat (Neville and Castro, In preparation). Less quantitative estimates are available for describing trends in other species. General population trends for 10 types of primates used in large numbers in biomedical work are summarized below. Marmoset, Saguinus species Saguinus mystax occurs in parts of Peru and Brazil, while £i. nigricollis occurs in adjacent areas of Colombia and Peru from the Ecuadorian border to the Brazilian border. The more wide- spread S-. fuscicollis with 13 named races extends through parts of Colombia, Ecuador, Bolivia, Peru, and Brazil. £>. fuscicollis occurs up to nearly 1,400 meters in Peru, a higher elevation than has been noted for several other species (Grimwood, 1968). Hernandez and Cooper (In press) noted that these white-lipped marmosets occupy secondary forests and some primary rainforests in lowland areas of Colombia and survive around areas of moderate human activity. Marmosets generally appear to do well in forests with thick tangles of vines and understory vegetation that increases in luxuriousness around forest edges, treefalls, and streams.

64 TABLE 23 POPULATION ESTIMATES FOR PRIMATE SPECIES Species Population Estimates Country Reference Latin America Leontopithecus rosalia 700 - 1,600 L. r. rosalia 400 200 100 600 500 500 L. r. chysomelas L. r. chrysopygus Brachyteles arachnoides 3,000 Asia Presbytis geei 550 1,000 - 12,200 Macaca silenus Pongo pygmaeus 4, 450 1,000 - 4, 500 1,000 - 4,000 2,000 - 3, 000 450 - 700 Hylobates syndactylus 30, 000 +• 5,000 Macaca fuscata " 22,000-34,000 Hylobates lar Macaca mulatta 205,000-255, 500 500,000 Present, no population estimates Africa Col"obus badius kirkii 144 - Propithecus diadema perrieri Gorilla gorilla beringei Cercocebus galeritus galeritus 1,500 - Colobus badius rufomitratus Brazil Brazil A s sam -Bhutan border, 1964 India IUCN, 1972; Coimbra-Filho and Mittermeier, 1973 IUCN, 1972 IUCN, 1972 Sugiyama, 1968a Basjarudin, 1971; Indonesia-Sumatra Mackinnon, 1971; -Kalimantan (Borneo) Reynolds, 1967; Malay sia-Sabah Rijskin, 1974; -Sarawak Schaller, 1961 Malayan peninsula Japan Malayan peninsula India-Uttar Pradesh (earlier estimate 1 million) Bhutan Afghanistan 196lb Burma Bangladesh China Cent. India Laos Pakistan Nepal Thailand Sikkim Vietnam Chivers, In press Takeshita, 1964 cited by Itani, 1975 Chivers, In press Southwick jit al. , 1970 Southwick et al. , 200 Tanzania-Zanzibar 500 Madagascar 1,000 Rwanda, Uganda, Zaire 2,700 Kenya 1,900 Kenya IUCN, 1972 IUCN. 1972 IUCN, 1972 IUCN, 1972 IUCN, 1972

65 TABLE 23 (continued) Species Population Estimates Country Reference Pan troglodytes Gorilla gorilla 14, 550 - 15,750 Present, no estimates; generally reported as declining 50 12, 500 1,000 200 1,000- 2,000 Continued presence questionable 5,000 - 15,000 400 - Present, reported declining Few hundred Continued presence questionable 500 200 Total estimates of stud ied or surveyed popu- lations in 5 of 1 8 countries CAR Cameroon Congo Guinea Gabon Ivory Coast Mali Liberia Togo Rwanda Sudan Sierra Leone Tanzania Senegal- Niokolo Koba NP Guinea (90,000 km ) Ghana, total Studied in Zaire -70-80 Beni -97 eastern Zaire Uganda -Budongo Forest Burundi Nigeria Dahomey Upper Volta Dupuy, 1970 Bournonville, 1967 Booth, 1956 Kortlandt, 1962, cited by Bournon- ville, 1967; Rahm, 1967 Reynolds and Reynolds, 1965 Rwanda, Uganda, Zaire Virunga volcanoes Kayonza Forest CAR Cameroon Gabon Congo-Br. Eq. Guinea Nigeria Schaller, 1963 Jones and Sabater Pi, 1971 SOURCE: Table adapted from information summarized in IUCN, 1972 for some popu- lation estimates and in Wolfheim (In preparation) for species presence in several countries.

66 TABLE 24 SELECTED POPULATION DENSITIES REPORTED FOR NEW WORLD PRIMATES No. Individ- Species uals/km ty Country Reference CALLITRICHIDS Saguinus fuscicollis 8-16 12 5 60 Peru Peru Peru Panama Freese, In prep. Neville and Castro, In prep. Freese, In prep. Dawson, Pers. comm. , 1975 S. imperator S. oedipus geoffroyi CEBIDS Ateles paniscus 12-15 2-14 2-24 6-10 2-36 15-46 7 12-46 19-31 16-84 151-528 50 72-102 12-29 15 61-108 Colombia Peru Peru Colombia Peru Peru Peru Peru Colombia Peru Peru Canal Zone Canal Zone Colombia Peru Venezuela Klein and Klein, In press Freese, In prep. Freese, In prep. Klein and Klein, In press Freese, In prep. Neville and Castro, In prep. Freese, In prep. Neville and Castro, In prep. Klein and Klein, In press Freese, In prep. Neville and Castro, In prep. Carpenter, 1934* Chivers, 1969* Klein and Klein, In press Neville and Castro, In prep. Neville, 1972 Callicebus moloch Cebus albifrons C. apella Lagothrix lagotricha Saimiri sciureus Alouatta palliata A. seniculus NOTE: Density estimates are not based on standardized field methodology. There is no intention to imply that these densities prevail throughout the range of the species. *Estimates as calculated by Baldwin and Baldwin, 1972.

67 TABLE 25 SELECTED POPULATION DENSITIES REPORTED FOR OLD WORLD PRIMATES Species No. Individ- f\ uals/km Country Reference PROSIMIANS Galago alleni Perodicticus potto Galago demidovii CERCOPITHECINES Cercopithecus aethiops Erythrocebus patas Macaca fascicularis M. mulatta (forest) M. nemestrina M. sinica Papio cynocephalus P-. hamadryas COLOBINES Presbytis cristatus P. entellus P-. melalophos ANTHROPOIDS Gorilla gorilla Hylobates agilis H. lar H-. syndactylus Pan troglodytes Pongo pygmaeus 14-25 5-28 32-117 89 17-153 0.6-1. 2 11 33-143 39 20-57 1. 5 4-28 100 4-10 11 2 22-120 3-6 85-135 97-104 9-51 20 0.5-2.6 6-18 0.9-1. 1 3 0.05-0. 5 0.3-1. 5 0.2 1 3 Gabon Gabon Gabon Uganda Kenya Uganda Malaya Sumatra India India Malaya Sumatra Sri Lanka Kenya Uganda Ethiopia Sumatra India India India Sumatra Malaya Zaire, Uganda Sumatra Malaya Malaya Guinea Equatorial Guinea Sarawak Sumatra Kalimantan Charles-Dominique, 1971 Charles-Dominique, 1971 Charles-Dominique, 1971 Gartlan and Brain, 1968 Struhsaker, 1967b Hall, 1965a, b Medway and Wells, 1971 Wilson and Wilson, In prep. Southwick et aL , 196lb Neville, 1 9~6~8 Medway and Wells, 1971 Wilson and Wilson, In prep. Dittus, 1974 DeVore and Hall, 1965 Rowell, 1966 Rummer, 1968 Wilson and Wilson, In prep. Yoshiba, 1968 Sugiyama, 1964; Sugiyama et al. , 1965 Vogel, 1971 Wilson and Wilson, In prep. Medway and WeUs, 1971 Schaller, 1963 Wilson and Wilson, In prep. Southwick and Cadigan, 1972 Chivers, 1971 Bournonville, 1967 Jones and Sabater Pi, 1971 Schaller, 1961 MacKinnon, 1974 Rodman, 1973 NOTE: Density estimates are not based on standardized field methodology. There is no intention to imply that these densities prevail throughout the range of the species. Most estimates are based on small samples, e.g. , the density of 0. 6 patas/km was determined from the home range of a single troop (Hall, 1965a). Hall noted the crude density for his study area based upon 5 troops with 110 patas was 0. 04 individuals/km^ .

68 Marmosets are found in family groups frequently reported as varying between 3 and 10 members. Recent estimates of less than one individual per 2 hectares are lower than previously assumed based on the animal's size (Table 24). Both Dawson's recent study of the Panamanian marmoset and Neyman-Warner1 s data on the Colombian form of Saguinus oedipus indicate that the membership of groups is not stable. This variability increases the difficulties of determining accurate population densities. Cotton-top marmosets have the most restricted distribution of marmosets of biomedical importance and have declined seriously due to the habitat loss within their limited range and the heavy trapping pressure for export (Hernandez and Cooper, In press; Struhsaker £t al. , In preparation; Green, In press). Except for the cotton-top marmoset of northern Colombia, estimates of population trends for the marmosets most in demand for research are not available. Night monkey, Aotus trivirgatus Night monkeys occur from Panama south to central Brazil, Paraguay, and Argentina. Brumback (1973) demonstrated karyotype differences in night monkeys from opposite sides of the Andes. Despite this large distribution, the biomedical usage of night monkeys has been concentrated on animals of Colombian origin as the preferred model for malarial research. Most of the 4, 000 night monkeys imported into the United States annually have been from Colombia prior to the export limitations imposed by that nation in an effort to protect the species until the effects of trapping can be determined (Hernandez and Cooper, In press). These nocturnal monkeys generally live in family groups consisting of a pair with their young. Night monkeys have a wide habitat and altitudinal tolerance in Colombia, extending up to 3, 200 meters. No density estimates for this species are available in the literature. Squirrel monkey, Saimiri sciureus Although the squirrel monkey is reported to be common in parts of Peru (Grimwood, 1968), its status in most countries from its northern limit in Costa Rica to its southern limit in Paraguay is not well documented. Deforestation is responsible for declining squirrel monkey populations in Panama (Baldwin and Baldwin, In press) and is largely res- ponsible for the inclusion of the Central American subspecies on the U.S. endangered species list. This widespread and adaptable species tends to be relatively more abundant than other neotropical forms (Grimwood, 1968). This contention has been supported by recent field data from those habitats that support several primate species (Freese, In preparation; Neville and Castro, In preparation; Klein and Klein, In press) but is not true in all cases (Baldwin and Baldwin, In press). Thorington (1968) cautioned against acceptance of the frequently repeated large group sizes for squirrel monkeys. He noted that estimates reported to him for his study area were 2-5 times greater than the number he determined from age and sex class identifications. Field studies that have included home range or density estimates have not verified the concen- trations of 200-300 animals that have been noted away from human habitation in Amazonia (Baldwin and Baldwin, 1971). Instead, group counts from acces- sible study areas generally range from 10-50 animals (Baldwin and Baldwin, 1971; Neville and Castro, In preparation; Freese, In preparation) with esti- mates frequently being in the twenties and thirties (Baldwin and Baldwin, In press; Klein and Klein, In press). More than a tenfold difference exists bet- ween available density estimates of 20-30 animals/km 2 (Klein and Klein, In press) and 150-500/km (Neville and Castro, In preparation). This reflects

69 differences in sampling methods in addition to population differences between two forests in southern Colombia and Peru. This variance in estimates of troop size and densities illustrates the lack of our current understanding of the population status and dynamics of a species that has been imported into the United States at the rate of 25, 000 annually. Vervet monkey, Cercopithecus aethiops The vervet monkey is generally abundant in relation to other monkeys within its distribution, which encom- passes most of subsaharan Africa. This species is one of the few for which estimates of both crude and ecological densities are available. Struhsaker (I967b) found 4 troops in Masai-Amboseli Game Reserve living at crude densities of 17-153 monkeys/km.2 . The ecological densities for these troops were 126-31 9/krn2. The vervet populations supported within these home ranges declined by 33. 3 percent within 7 years (Struhsaker, 1973). Initially troops averaged 24 individuals in the reserve (Struhsaker, 1967b). Vervets have been studied in a number of countries and do well in a variety of habitats as long as some moisture, sleeping trees, and an adequate density of food species are available. Vervets are controlled in some areas of Sierra Leone, Uganda, Ethiopia, northern Rhodesia, and Cameroon, where they are considered as agricultural pests. They are shot for bounties in agricul- tural areas of St. Kitts, a Caribbean island to which they were transplanted. Long-tailed macaque, Macaca fascicularis This widespread species occurs throughout Southeast Asia from Burma to the Philippine and Indonesian islands. No recent information was located with respect to its status in China, Burma, or most of Indochina. It is reported to be decreasing in Thailand, South Vietnam, the Philippines and parts of Indonesia. Recent field studies have shown this species to be more common in some areas of Indonesia and Malaysia than previously known. The species has been reported as common on the Malaya Peninsula, (Medway, 1969), Sumatra, and the island of Borneo (Wilson and Wilson, In preparation). The long-tailed macaque is an adaptable "edge" species showing greater abundance in riverine, disturbed and secondary forests than in primary rain-forest. Types of disturbed forests include those seasonally flooded, coastal mangroves, lumbered areas, urban parks, and those around Buddhist temples and plantations (Wilson and Wilson, In preparation). Long-tailed macaques are dependent on man for much of their food in many cultivated areas of Malaysia, Sumatra, Java, and Thailand, and are killed as agricultural pests. They are hunted for food in both Thailand and Malaya. The export trade from the Philippines has practically ceased due to the depletion of these macaques (Rabor, 1968). Nearly 70, 000 Macaca fascicularis were exported annually from West Malaysia in the early 1 960's (Southwick and Cadigan, 1972) but this number had dropped to a seventh of this volume by the end of the decade. The 2, 000 imported into the United States was about 20 percent of these exports. Greatly reduced populations have been reported for Thailand (Lekagul, 1968), the third country that has exported large numbers. The export trade from Indonesia has been increasing with a Japanese company exporting large numbers from Java. Wilson and Wilson (In preparation) have considered long-tailed macaque populations to be large enough in Sumatra to support a managed export trade for several years. This is a primate resource which could be utilized more fully if cropped animals were supported by more reliable feeding, handling, and transportation.

70 Rhesus macaque, Macaca mulatta This species is abundant in some parts of northern and central India with scattered populations stretching from eastern Afghanistan to the Kowloon peninsula of Hong Kong. It has been eliminated from much of its former range in Thailand, and probably parts of Indochina. Its status in Pakistan, Nepal, Sikkim, Bhutan, Bangladesh, and China is not known. Data on population trends are available only from Uttar Pradesh where more than half of all rhesus macaques are found in villages and towns (Southwick e-t al. , 196la, b, 1965; Southwick and Siddiqi, 1966, 1968, 1970, In press; Southwick et al. , 1970). These surveys estab- lished an estimate of a half million rhesus macaques for this North Indian province--a major decrease from previous reports of 10-20 million. By recensusing the same populations, the Aligarh district studies have demon- strated the effect of commercial trapping on the age structure of troops. During the years of intensive trapping in the 1950's and early 1960's, the percent of immatures dropped to 30 percent from 50 percent, which was found in stable populations. Juveniles were particularly reduced from a normal population representation of 25-30 percent to a low of 5. 9 percent. After a decade of reduced trapping pressure, the effect of the modified age structure was still evident because most troops had only 44. 6 percent immatures. Southwick £t al. (1970) calculated a potential renewable harvest from Uttar Pradesh of~~6~0, 000 rhesus monkeys annually based upon the assump- tion that a population of 500, 000 produced 176, 000 infants annually and 35 percent of these could be cropped. The feasibility of sustained-yield har- vesting from agricultural areas has been noted by Bermant and Chand- rasekhar (1971) and Southwick (1971). The need for such management is evident in the light of increasingly urban and concentrated populations, a shift that results from a combination of three factors. Both commercial trapping of woodland macaques and human efforts to exterminate agricultural pests are contributing factors. The most important factor may be the shifting land use patterns with the proportion of the province under culti- vation, in fallow, or uncultivatable increasing above 86 percent, while the area of natural forest is decreasing from 14 percent at the rate of 2 percent annually in some places. A recent report byMukherjee and Mukherjee (1972) indicates densities of a different order of magnitude from those of other investigators. An estimates of . 008-. 05/km^ for rhesus along roadsides around Delhi contrasts strikingly to estimates of 5-57/km from longer studies in other areas. Since no other indications of such population decimation are available, an evaluation of census tech- niques and studies of larger scope would be appropriate before export restrictions are modified in the light of this report. Pigtail macaque, Macaca nemestrina Pigtail macaques occur in a variety of lowland and hill forests in Thailand, Malaya and Sumatra (Wilson and Wilson, In preparation). Pigtails appear to have lower natural densities and wider ranging habits than other species of macaques. The status of pig- tail macaques is unknown through its range from Assam eastward to Indo- china, Malaysia and Indonesia, except for Thailand, Sumatra, and West Malaysia where it is seriously declining. Considerable hunting pressures are exerted on this species due to its destructiveness to crops in Thailand (Lekagul, 1968), Malaysia (Bernstein, 1967) and Sumatra (Wilson and Wilson, In preparation), its value for use as a trained coconut picker (Bertrand, 1967), for meat, and for the biomedical export trade.

71 Stumptail macaque, Macaca arctoides No field studies of the stumptail macaque have been conducted that would provide estimates of population density or home range size although Bertrand (1969) was unable to find groups outside of protected forests in southern Thailand that had not been trapped or shot. This species, which has been imported into the United States from Thailand and Assam at the rate of 200-300/year, is becoming scarce in these countries and in Malaya. Its present status in Burma, China, and Indochina is not known. Factors responsible for decreasing numbers include deforestation or military activity throughout most of its range. Trapping for export to the United States with the killing of animals too old to export and hunting for meat have been detrimental factors in Thailand and Assam. Baboon, Papio cynocephalus Altmann and Altmann (1970) have considered baboons to be the most abundant and widespread African primates. Baboons utilize a wide range of forested savanna and altered habitats. They are more dependent upon a water source than patas monkeys (Hall, 1965a, b) but toler- ate droughts better than some ungulates due to a varied diet that includes tubers (DeVore, 1965). Yellow and olive baboons generally occur at low den- sities of 4-10 individuals per km? in two Kenyan reserves (DeVore, 1965; Devore and Hall, 1965) and Il/km2in Uganda (Rowell, 1966). Troop size averages from the twenties to eighties with groups infrequently topping 100 individuals (Altmann and Altmann, 1970; DeVore and Hall, 1965; Rowell, 1966). Divergent views exist regarding the effects on baboon numbers of pest control programs, localized trapping for export (which totals less than 1, 000 annually to the United States), and various agricultural practices. For example, Kingdon (1971) felt pest control programs in Uganda had not greatly reduced baboon populations, but Hall (1965a) noted that baboons were rare in some farming areas. The existence of pest control programs in some subsaharan countries from Uganda (Rowell, 1968; Kingdon, 1971) to South Africa (Keith and Stoltz, 1971) attests to the abundance of baboons but also to the erosion of their habitat and numbers with the spread of agriculture. Chimpanzee, Pan troglodytes Density estimates ranging from . 05-6.7/krrr are available from studies conducted in Guinea (Bournonville, 1967), Equa- torial Guinea (Jones and Sabater Pi, 1971), Tanzania (Lawick-Goodall, 1968), and Uganda (Sugiyama, 1968b). The species is reported as declining in those countries for which information regarding their status is available. Habitat destruction, and hunting chimpanzees for meat and to reduce their damage to crops are factors contributing to declining populations, but the effect of shooting females to obtain young for export is considered to be a sufficient factor by itself to account for the decimation of populations of these slowly reproducing apes. For example, if 4-6 mothers are killed in Africa for each young chimpanzee that survives international shipment, then 3, 000- 4, 000 chimpanzee mothers would have been lost from Guinean populations in order to sustain 1 supplier's average export rate of 1 6 young chimpanzees annually between 1917 and I960. Kortlandt (1966) estimates further thatthis loss would be equivalent to all mothers in a population of approximately 15,000 chimpanzees. By extrapolation, Sierra Leone and Liberia cannot be expected to maintain their current rates of export without exterminating their populations within a few years.

72 Forested and Reserved Areas For many species, the rapid development of natural areas means that only those populations afforded long-term governmental protection will continue to survive. For planners whose primary interest is the number of primates available for consumption, it is necessary to know the minimum size of future populations. A first approximation of this figure may be obtained by combining estimates of population densities with figures for areas set aside as national parks and reserves in tropical countries. The areas of wildlife re- serves currently set aside within the estimated distributions of primate species are compared in Table 26-28 with the total areas and forested areas in Latin America, Asia, and Africa. Only those reserves such as the Galapagos Islands and waterfowl marshes that provide no primate habitat were eliminated from the list. An additional refinement of this list would exclude certain arid areas in Botswana and areas outside primate distributions in Argentina and other countries. Even though area estimates were not obtained for all countries and the areas vary greatly in habitat quality for primates, the available statistics provide a perspective for comparing countries. The importance of the tourist trade and the conservational organization in each country is indicated by the proportion of the total land mass set aside in reserves that meets the criteria of the United Nations (UN) list (ICNP, IUCN, 1971; Harroy, 1972). There are four countries each in Latin America and Asia with at least 1 percent of their total geographical areas in reserves. Those in South America are Surinam, Venezuela, Colombia, and Peru; those in Asia include Japan, Sri Lanka, Cambodia, and Malaysia. By comparison, 29 of the 42 African countries listed have 1 percent or more of their total areas in reserves. Currently, the rank of a country by total size does not correspond to its rank in listed national reserves. For example, Brazil is the largest Latin American country but ranks third after Argentina and Peru in the size of reserved areas. India ranks second to China in size but follows Japan and Indonesia in the area of sanctuaries. Sudan is the largest African country with endemic primates but is ninth in listed reserves. The criteria for inclusion of reserves in the UN list of national parks and equivalent reserves require legal protection under a central govern- ment, a minimum size of 5-20 km , a supervisory commitment of one person per 40-100 km , and an expenditure in U.S. dollars of from $5 to $10, 000 per km . The large ranges of minimum values depend upon the human population density of the area surrounding the reserve. The pattern of development of reserves is illustrated by the maps accompanying the UN list (ICNP, IUCN, 1971). Reserves are generally established as develop- ment intensifies around urban centers. Few reserves have been demarcated specifically through land use planning to protect large gene pools of endemic species within their natural distributions. The large number of additions and exclusions from sequential editions of the UN list demonstrates that the protection afforded the wildlife populations is continually changing. Primate Diversity The distributions of primates have become important to planners whether they are interested in ranching primates, in assessing populations that cannot withstand the added stress of trapping, in epidemiologic and

73 TABLE 26 ASIAN FORESTLANDS AND NATIONAL PARKS Listed Geographical Forested National Parks Area* Area* and Reserves § Country (1,000km2) fl, 000 km 2 (%)] [i, 000 km 2(%)] Minimum Reserves Not Listed§ (1,000 km2) Sri Lanka (Ceylon) 65 44 (68) 2. 1 (3. 2) 1. 3 India 3,270 605 (19) 5. 2 (0. 1) NI-72 parks Afghanistan 658 NI - - W. Pakistan 801 26 ( 3) 0. 04 0. 3 Nepal 141 45 (32) 1. 0 (0. 7) 0. 8 Bhutan 47 NI - 0. 4 Bangladesh 143 22 (15) - 1. 1 Burma 678 91 (13) 1. 2 (0. 2) 4. 2 "Reserved forests" Laos 236 NI NL 1. 5 Vietnam (N) 159 NI NI NI Vietnam (S) 172 NI - 9. 3 Cambodia 181 82 (45) 2. 1 (1. 2) 78. 0 Thailand 514 308 (60) 3. 8 (0. 7) 8. 7 Malaysia 5. 1 (1. 5) 1. 4 W. Malaysia 132 55 (42)1 4. 4 0. 5 Sabah 80 NI 0. 7 Sarawak 121 NI 0. 02 0. 9 Indonesia 1,900 903 (48) 11. 3 (0. 6) 13. 0 Java 1. 8 - Sumatra 8. 5 4. 7 Kalimantan (Borneo) 0. 07 5. 1 Sulawesi (Celebes) 0. 06 West Bali 0. 2 - Sunda Archipelago 0. 6 - West Irian l 3. 2 Philippines 300 159 (53)** 1. 9 (0. 6) 2. 6 Taiwan 36 23 (64) NL China 9,597 120 ( 1) NI 84. 0 Korea (N) 122 ca. 98 (80) NI NI "Non-cultivatible" Korea (S) 98 NI 0. 4 (0. 4) 1. 9 Japan 370 250 (68) 20. 0 (5. 4) - (Includes grassland) NOTE: NI = no information; NL = none listed. *Paxton (1973). §ICNP,IUCN (1971); Harroy (1972). !FReserved forests 33 (25); productive forests 22 (17). **Commercial forests 87 (29); non-commercial forests 72 (24).

74 TABLE 27 LATIN AMERICAN FORESTLANDS AND NATIONAL PARKS Listed Geographical Forested National Parks Area* Area* and Reserves § Country (1 , 000 km2) f 1 , 000 km2(%)l fl , 000 km 2(%)} Minimum Reserves Not Listed§ (1, 000 km2) Mexico 1,967 385 (20) 1 .6 (0. 1) 5. 6 Guatemala 109 72 (66) 0 .9 (0. 8) - British Honduras 23 8 (35) - 5 Honduras 112 50 (45) - - Salvador 21 8 (38) - - (non-agricultural) Nicaragua 139 40 (29) - - Costa Rica 51 40 (78) 0 . 3 (0. 6) - Panama 76 58 (76) 0 .03 9 (undeveloped) French Guyana 91 80 (88) - - Surinam 163 NI 4 .8 (3. 0) 1 Guyana 210 183 (87) 0 .1 (0. 1) - Brazil 8, 512 NI 13 .4 (0. 2) 25. 6 Venezuela 912 NI 14 .6 (1. 6) 22 Colombia 1,139 599 (52) 11 .0 (1. 0) 2 Ecuador 456 233 (51) - - Peru 1,285 NI 19 .0 (1. 5) 42 Bolivia 1,098 926 (84) 2 .2 (0. 4) 20 Paraguay 407 NI - - Argentina 2,778 889 (32) 26 .5 (0. 9) - Trinidad 5 2 (30) - 1. 7 NOTE: NI = no information. *Paxton (1973). §ICNP, IUCN (1971); Harroy (1972).

75 TABLE 28 AFRICAN FORESTLANDS AND NATIONAL PARKS Listed Geographical Forested National Parks Area* Area* and Reserves? Country (1,000km) (1,000km2) fl, 000 km2 (%)] Minimum Reserves Not Listed§ (1,000 km2 ) Mauritania 1,031 . 3. 1 Senegal 198 8.3 ( 4) - Gambia 0.08 - - Mali 1,204 3. 5 (0.5) 5.4 Niger 1, 187 3.0 (0.5) 45.3 Chad 1,284 4. 1 (0.5) 26.6 Sudan 2, 500 347; 691 savanna 24. 5 ( 1) 14.3 Ethiopia 1,000 .2 4.4 French Somaliland 23 . 1.0 Somalia 700 6.2 ( 1) - Portuguese Guinea 36 - - Guinea 246 13.0 ( 5) - Sierra Leone 73 - - Liberia 113 . - Ivory Coast 322 15.7 ( 5) 1.9 Upper Volta 274 5.4 ( 2) 5.4 Ghana 238 82; 156 savanna? 8. 0 ( 3) . Togo 56 .6 ( 1) - Dahomey 113 7.8 ( 7) 23.9 Nigeria 924 5.3 ( 1) - Cameroun 474 9. 1 ( 2) 10.7 Cent. African Repub. 625 14.2 ( 2) 38.6 Equatorial Guinea 28 . 3 ( 1) 1.0 Gabon 267 4. 2 ( 2) 1. 5 Congo -Brazzaville 342 1. 1 (0.5) 11.3 Zaire 2,345 52.6 ( 2) - Uganda 236 8.4 ( 4) 40.9 Kenya 569 16. 8 reserves 25.7 ( 4) 4.8 Rwanda 26 2. 7 (10) - Burundi 28 - - Tanzania 886 10. 4 tropical 36.9 ( 4) 56.9 forest** 349. 6 savanna forest Angola 1,247 21.2 ( 2) 41.3 Zambia 752 59.0 ( 8) - Malawi 94 3. 1 ( 3) 2.0 Mozambique 785 5. 7 ( 4) 19.3 Rhodesia 391 28.5 ( 7) - Southwest Africa 823 65.0 ( 8) 26.9 Botswana 575 100. 1 (18) - South Africa 1,221 12.5§§ 31.8 ( 3) 6.1 Swaziland 17 .03 (0.5) — Lesotho 30 .06 ( 4) - Madagascar 594 10. 5 ( 2) - *Paxton (1973). §ICNP, IUCN (1971); Harroy (1972). 5Of totals, 1 5, 000 km of forest and 6, 000 km of savanna are reserved. =.-*Forest reserves covered 117,700 km2, 1961. §§Exotic trees cover 10,000 km2; indigenous trees 2,500 km2.

76 zoogeographic studies, or in selecting experimental species that might be imported from harvested wild populations for several years. For planning to be effective the number of alternative countries that could export a particular species must be known, as well as the number and size of countries that could provide alternative species. The identi- fication of those countries that, geographically or politically, represent sole suppliers for a particular species is equally relevant. The questions of alternative experimental species and the relative protection provided and needed by various species require that the examination of primate populations not be limited to the species traditionally used. If management is limited to a single species, then any country in which the species does not represent an exotic introduction is a potential candidate for establishing protection or ranching. However, if efforts are to be cost effective for the greatest number of species, then a knowledge of species diversity would allow better decisions to be made in land management--decisions that would perpetuate the ecological complexity of habitats within those countries with the greatest species diversities. Six Latin American, 3 Asian, and 12 African countries have 14 or more primate species. Brazil and Colombia, Indonesia and Malaysia, and Zaire and Cameroon rank highest in diversity for each of the 3 continents, respectively (Tables 29-31). The widespread distributions of primate families and selected genera suggest considerable flexibility in obtaining related primates from alter- native countries. This flexibility would lessen the effectiveness of export restrictions imposed for political considerations. However, the geographic and genetic variability within these taxa indicated by the number of named forms (subspecies) would preclude their interchangeability for many bio- medical uses. For example, although a representative macaque occurs in many Asian countries, the genus Macaca includes 12 species and 49 distinct races (Napier and Napier, 1967). Each primate form can be expected to differ in its disease susceptibilities and immunities as the examples of macaques and night monkeys have demonstrated. Areas Protecting Primates Any assessment as to how well a given species or species group is pro- tected by the establishment of reserves within its geographic range depends at least in part on one's opinion as to taxonomic relationships. If species are broadly defined, protection seems to be more complete than if fine taxonomic distinctions are made. In the latter case, some populations are likely to be found outside of any protected areas. The protected areas within the estimated distributions of primate species are given in Tables 32-34. The pattern of simultaneous increase in the total protected area, the number of named forms within a listed taxon, and the number of countries protecting a species, is evident for all three continents. While no Asian species occurs in more than 30, 000 km of protected area, a few Latin American species receive protection in reserves totaling up to 80, 000 km^. The development of reserves in Africa is of a different order of magnitude with the protection afforded widespread taxa reaching 450, 000 km . The greater governmental protection offered many African forms is shown by the fact that nearly 40 percent of the African forms (as grouped in Table 34) have more protection than any Latin American species (Table 33) and nearly 60 percent have more protection than any

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79 TABLE 31 DIVERSITY OF PRIMATE TAXA IN AFRICAN COUNTRIES Cerco- Cerco- Cercopithecids Lorisids Galagids cebus pithecus Papio Colobus Pong 1ds Total Genera (species) named forms 2(2)7 3(6)31 1(4)11 2§(23)78 1(7)25 1(10)31 2(3)8 13(56)193? No. countries 20 35 14 38 38 23 22 38 Country* Mauritania - - - (1) (2) - - 2(3) Senegal (1) (2) - (2) (l) (2) (1) 8(9) Gambia - (1) - (2) (1) (2) . 4(6) Mali - (1) . (1)2 (2) - (1) 4(5)6 Niger - (1) . (1)2 (1) - - 3(3)4 Chad - (1) . (1) (1) - - 3(3) Sudan • (1) . (3) (2)4 (2) (1) 6(9)11 Ethiopia - (1)3 - (5)8 (2) (1)2 - 6(10)175 Somalia - (2) - (3)5 (3) - - 4(8)10 Port. Guinea (1) (2) . (1) (1) . (1) 6(6) Guinea (1) (2) (1) (6) (2) (3)4 (1) 9(16)17 Sierre Leone (1) (2) (1) (6) (2) (2) (1) 9(15) Liberia (1) (2) (1) (5) (1) (2) (1) 8(13) Ivory Coast (1) (2) (1) (5)8 (1) (3)1 - 9(14)19 Upper Volta - (2) - (2) (0 - - 5(5) Ghana O) (2) - (5) (i) (2) (1) 9(12) Togo (I) (2) - (5) (1) (1) (1) 8(11) Dahomey (1) (2) - (5) (1) (1) (1) 8(11) Nigeria (2) (4) . (8)9 (3) U) (2) 10(20)21 Cameroon (2)3 (4) (1) (9)11 (3)5 (3) (2)3 11(24)30 CAR (2) (2) (1) (3) (1) (1) (2) 11(12) Eq. Guinea (2) (3) (1) (5)6 (2) (2) (2) 11(17)18 Gabon (2) (3) (2) (5)T (2) (1) (2) 11(17) Congo-Br. (2) (2) (2) (6) (2) (2) (2)3 10(18)19 Zaire (2)3 (4)5 (2)4 (10)21 (2) (4)8 (3)4 11(27)47 Uganda (1) (4) (1) (7)8 (1)2 (3) (2) 11(19)21 Kenya (1) (3)8 (2) (6)9 (2)4 (3)1 - 8(17)29 Rwanda (1) - . (4)~ (I) - (2) 5(8) •" Burundi (1) - . (3) (i) (i) (1) 5(7) Tanzania - (3)10 (1) (3)11 (2) (4)5 (1) 8(14)30 Angola - (3) (1) (5)7 (2) (O - 6(12)14 Zambia - (2) - (4) (2)3 - - 4(8)9 Malawi . (3) - (2)4 (2) . - 4(7)9 Mozambique . (2)3 . (2)£ (2)3 . . 3(6)12 Rhodesia - (2)3 - (2) (2) - - 3(6)7 SWA - (2) - (1) (1)2 - - 3(4)5 Botswana - (2) - CD (2) . - 3(5) S. Africa • (2)1 - (2)4 (1)4 - • 3(5)U- >•=Numbers in columns indicate No. genera (No. species) No. named forms Number of genera are given only in total column. Nomenclature is adapted from Hill and Meester (1971), Dandelot (1 971), and Napier and Napier (i 967). Distributions were estimated from above sources and Wolfheim (In preparation). A few countries were excluded from the table: Fr. Somaliland, Swaziland, and Lesotho were not specified regularly in described distributions; Tunisia, Libya, and Egypt lack primates; Morocco and Algeria include the range of Macaca sylvanus only; Madagascar includes Lemurids only. §Erythrocebus is totaled as a separate genus, although it is included as a subgenus of Cercopithecus by Dandelot (1971). yTheropithecus gelada occurs in Ethiopia and Saudi Arabia; the two subspecies were included only in the totals.

80 Asian form (Table 32). This pattern of protection is inversely related to the current biomedical demand for species by continent. The rank order of safe areas provided the more studied African species appears to agree with their relative abundance. For example, the drill, Papio leucophaeus, has been considered to be among the most threatened of African primates while vervets and baboons are regarded as being among the most abundant species on the continent (Struhsaker, 1967a, b; Altmann and Altmann, 1970). Gartlan (1974 personal communication to Wolfheim, In preparation) has found that the drill is restricted to 78, 000 km ^ or half its total previous range in Cameroon. If the drill remains only in the Korup Reserve in Cameroon and not in the reserves of neighboring coun- tries, then the estimate of the protected area must be reduced from 15, 000 km to 1,250 km . Upward adjustments may be needed for other species as additional reserves become more closely administered. For example, the woolly spider monkey, Brachyteles arachnoides, is protected within eight state and private reserves set aside for its safety (Aguirre, 1971, cited in IUCN, 1972). These reserves double the protected area for this species from the 593 km2 for the 5 listed national parks to 1, 165 km . It should be emphasized that while the rank order of primates may be representative, many reserves do not provide adequate habitat for many species and the protected areas listed are therefore considerable over- estimates. Distributional limitations imposed by altitude, amounts of forested habitat, and rainfall need to be considered to increase the accuracy of the tables. In addition, certain species occur in different regions of the same country but not sympatrically. Because these cases were not always possible to discriminate, and due to the larger relative sizes of African re- serves, the largest overestimates may be expected for Africa. The listing needs to be refined based upon actual faunal lists of reserves to avoid assigning a primate to a sanctuary in which it does not occur. There are several species in Latin America and Asia that do not appear to reside in any areas qualifying for the UN list. Additional species occur in a single country or are protected in only one of the countries in which they are found. Except for the callitrichids, the 10 species traditionally used in biomedical studies are protected in a least 1 reserve in 4 or more countries (Tables 32-34). With more than 100,000 krr? of listed reserves, the protection afforded the 5 African species of medical importance contrasts sharply with that offered Asian species. In the New World, the 3 frequently exported cebids are protected within at least 40, 000 km but the protection marmosets receive is limited. Saguinus oedipus is variously considered as one or two species. The Colombian form, which has been employed in medical work, currently receives no protection. The protected status of populations of Saguinus nigricollis, which is restricted to Colombia and Peru, is only slightly less critical. The further biomedical use of species that are not protected in countries of origin, such as Saguinus oedipus, will be wholly dependent upon captive-bred individuals. If one assumes that the density of many forest species lies between the 10 macaques per km that Medway and Wells (1971) found for Macaca fascicularis in Malaysia and the 100 macaques per km that Dittus (1974) found for Macaca sinica in Sri Lanka, then there are fewer than 50, 000- 500, 000 animals of at least 23 Latin American species, 29 Asian species, and 3 African species that are protected. At these density estimates of 10-100 rhesus macaques per km^ there maybe only 60,000-600,000 rhesus macaques in its 6, 000 km ^ of protected range.

81 TABLE 32 PROTECTED AREAS WITHIN THE ESTIMATED DISTRIBUTIONS OF ASIAN PRIMATE SPECIES Protected Area* 1,000 km Species (No. named forms )§ No. Countries Within Distribution or Protecting Species No known Hylobates klossi (1) protection Macaca cyclopis (1) Nycticebus pygmaeus (1) Presbytis francoisi (4) P-. potenziani (2) Simias concolor (2) Rhinopithecus avunculus (1) R. roxellanae (3) Metawi Isl. , Indonesia Taiwan Laos, Vietnam China, Laos, Vietnam Metawi Isl. , Indonesia Metawi Isl. , Indonesia N. Vietnam China 0-0. 7 0-0.7 0-2. 0 0.06 0.06 0.08 0.1 0.2-0. 5 0.3 0.8 0.8 1-9 1.1 1. 1 1.2-7.7 1.4 1.8 2. 1 2.8 3.7 4.1 4. 5 6.2 7 0 7.1 8. 3 10-19 Presbytis geei-P. pileatus (6) 1 Assam 2 1 Cambodia 1 Sulawesi, Indonesia 1 Sulawesi, Indonesia 2 2 2 1 Thailand 1 India 1 Philippines P. rubicunda (5) Pygathrix nemaeus (2) Macaca nigra (4) Tarsius spectrum (5) Presbytis frontata ( 2) Nasalis larvatus (1) Presbytis phayrei (4) Hylobates concolor (6) Presbytis johni (1) Tarsius syrichta (3) Macaca silenus (1) 1 India 1 India 3-4 1 Sri Lanka 2 1 Sri Lanka 2 2 2 2 4 2 4 4 5M. arctoides (4) M. radiata (2) Presbytis senex (5) Hylobates hoolock (1) Macaca sinica (3) Tarsius bancanus (4) Loris tardigradus (6) tfMacaca mulatta (4) Hylobates pileatus (1 ) Presbytis obscura (7) Pongo pygmaeus (2) Macaca assamensis (2) Presbytis entellus (15) 12.9 13.3-15.3 18.0 20-29 Hylobates syndactylus (2) Presbytis cristata (8) 2 Hylobates lar (9) 1-2 3 20.0 20.4 21.0 23.6 25.2 Macaca fuscata (2) 1 Japan 4 5 7 6 JMacaca nemestrina (4) Presbytis aygula-melalophos (27) Nycticebus coucang (9) ifMacaca fascicularis (21) -Protected areas listed in ICNP, IUCN (1971); Harroy (1972). § Named forms follow Napier and Napier (1967); species are grouped according to Wolfheim (In preparation); occurrence in reserve was estimated from above sources. J Traditional species of biomedical importance.

82 TABLE 33 PROTECTED AREAS WITHIN THE ESTIMATED DISTRIBUTIONS OF LATIN AMERICAN PRIMATE SPECIES Protected Area*, 1 , 000 km2 Species (No. Named Forms)§ No. Countries Within Distribution or Protecting Species No known Alouatta pigra (1) Mexico, Guatemala, Br. Honduras Colombia, Peru, Brazil Venezuela, Colombia, Brazil Colombia, Peru, Bolivia Brazil Colombia, Brazil Peru Brazil Colombia, Brazil Colombia? , Brazil Colombia protection Cacajao calvus (3) C. melanocephalus (1) Callimico goeldi (1) Callithrix humeralifer (2) Cebuella pygmaea (2) Lagothrix flavicauda (1) Saguinus bicolor (2) S. inustus (1) S. labiatus (2) <1 0-0.7 0-0.7 0.03 0.03 0.6 1-9 0-4.0 0-4.7 0-10.0 2.6 2.7 4.0 4. 5 5.0 11.0 10-19 S. leucopus (1) Callithrix argentata (4) 2 Chiropotes albinasa (1) 1 Brazil 1 Panama 1 Brazil 1 Brazil JSaguinus oedipus (2) Leontopithecus rosalia (3) Brachyteles arachnoides (1) Saguinus mystax (3) Callicebus torquatus (3) 1 Peru 1 Peru 1 Venezuela 1 Brazil 1 Brazil 1 Peru 3 2 1 Brazil Alouatta belzebul (5) Callicebus personatus (4) Alouatta fusca (3) ?Saguinus nigricollis (2) Cebus capucinus (5) Saguinus midas (2) Callithrix jacchus (7) 14.0 14.0 14.0-20.0 15.0 15.0 20-39 Alouatta caraya (1) 2 Saguinus imperator (2) 1 Peru 2 IS. fuscicollis (7) Pithecia pithecia (1) 3 Chiropotes satanus (2) 3 20.0 31.0 31.7 31.7 32. 5 40-59 40.4 44.0-58.6 51.4 51.1-56.1 60-79 Cebus nigrivittatus (5) 3 C. albifrons (12) 3 4 4 6 Lagothrix lagotricha (4) Callicebus moloch (7) Alouatta palliata (7) Pithecia monachus (2) 5 ?Sairniri sciureus (8) 6-7 6 Alouatta seniculus (5) ITAotus trivirgatus (9) 9 67.4 T Cebus apella (11) Ateles paniscus (16) 8 11 67.4 * Protected areas listed in ICNP. IUCN (1971); Harroy (1972). § Named forms follow Napier and Napier (1967); species are grouped according to Wolfheim (In preparation); occurrence in reserves was estimated from above sources, Hernandez and Cooper (In press), and Thorington (1974). f Traditional species of biomedical importance.

83 TABLE 34 PROTECTED AREAS WITHIN THE ESTIMATED DISTRIBUTIONS OF AFRICAN PRIMATE SPECIES Protected Area* 1. 000 km2 Species (No. named forms)§ No. Countries Protecting Species 1-19 20-59 60-79 80-99 0.06 0.3 15 15 22 24 28 34 63 70 72 79 85 96 100-199 110 118 119 152 165 186 200-299 214 243 273 300-399 396 400-499 446 450 Theropithecus gelada (2) Papio hamadryas (1) Papio leucophaeus (2-3) P. sphinx (1-3) Pan paniscus (1) Colobus verus (1) Euoticus spp. -E-. elegantulus and E. inustus (3) C-. talapoin (4-1) C-. 1hoesti (2) Cercocebus torquatus and C-. galeritus - supersp. torquatus (6) Galago alleni (1 ) Gorilla gorilla (3) Arctocebus calabarensis (2) Subgenus Piliocolobus-including 5 spp. : C-. badius, C-. kirki, C-. pennantii, C-. rufomitratus, C-. tholloni (20-14) ?Erythrocebus patas (4) Perodicticus potto (5) yPan troglodytes (3-4) Cercopithecus ascanius (5) Cercocebus albigena and C-. aterrimus - supersp. albigena (4-5) Subgenus Colobus - including 4 spp.: C-. angolensis, C-. guereza, C-. polykomos, C-. satanas (22-16) Galagoides demidovii (7) Cercopithecus mitis and C. albogularis (20-19) UGalago crassicaudatus (10-11) G. senegalensis (9) 1 Ethiopia 2 4 5 1 Zaire 3 6 3 5 5 8 10 17 13 14 8 8 17 18 12 10 27 ? Cercopithecus aethiops group including 4 spp. : C, aethiops, C-. pygerythrus, jC. sabaeus, C-. tantalus (21) 28 yPapio cynocephalus group including 4 spp. : P-. anubis, P-. cynocephalus, P. papio, P-. ursinus (12-18) 31 * Protected areas listed in ICNP, IUCN (1971); Harroy (1972). § Nomenclature is adapted from Hill and Meester (1971), Dandelot (1971), and Napier and Napier (1967). Named forms follow Napier and Napier (1967); second values indicate differences in Hill and Meester (1971), and Dandelot (1971). Occurrence in reserve was estimated from above sources, Williams (1968), Smithers (1971), ICNP, IUCN (1971), Curry-Lindahl and Harroy (1972), and Wolfheim (In preparation). Thirteen forest Cercopithecus sp. that were each protected in less than 60 km2 of area were not itemized in the table due to their lack of use in biomedical work and lack of field data on them. 5 Traditional species of biomedical importance.

84 Prospects for Wild Primates Several factors complicate the evaluation of the lists of protected areas and general population trends for different species. These include 1) the habitat quality within the reserves, 2) the purpose for which the reserves and forestlands are managed, 3) whether the habitat is fragmented or reaches a minimum area required to sustain a heterogeneous gene pool, 4) the rate of deforestation, and 5) the relative size of species populations inside and outside of the reserves. Habitat Quality in Reserves The number of primates supported by an area of a particular size varies with the quality of that habitat. Most field studies have been conducted at study sites selected for high quality and correspond- ingly high primate densities because this maximizes the productivity of visual observations. This factor indicates why current estimates of many primate densities may be higher than those in many reserves. Re- serves are frequently established in areas that are minimally productive agriculturally. These areas also represent marginal habitat for many wildlife species. The size of such areas may give an inflated impression of the actual protection offered native wildlife. For example, in Sri Lanka, nearly 85 percent of the area of listed reserves lies in the arid and dry zones of the country. The carrying capacity of the habitat in one of the dry zone reserves was much less for all primates than the carrying capacity estimated at a wetter study site outside of the reserve, but still within the dry zone. The reserve supported less than 1 kg/krr£of macaque (Macaca sinica) or purplefaced langur (Presbytis senex) while the wetter site supported 190 kg/km2 and 1,000 kg/km 2,respectively (Eisenberg et al. , 1972). The reserve also supported 38 times less biomass of gray langurs (Presbytis entellus). Therefore, it is not possible to use the size of reserves, independent of habitat evaluation, as a measure of the size of protected populations. Management Purposes After the absolute size and the habitat quality of re- serves, the third factor that influences the size of primate populations is the purpose for which the area is managed. Some reserves may receive government protection only as long as specific endangered species survive in them; others may be managed to the detriment of primate populations. A reading of the UN list illustrates the focus, with primates and species smaller than ungulates and carnivores rarely itemized. This emphasis raises doubts concerning whether many reserves will be continued if the conspicuous species, such as the Asiatic lion in the Gir forest, are eliminated. The dry Gir forest is currently the largest Indian sanctuary within the distribution of rhesus macaques. In other instances, primate populations may be cropped for competing with species of primary concern. An example of this situation occurred at Lake Manyara National Park, Tanzania, where 700 baboons were killed in 1962 for their alleged destruction of bird populations (Altmann and Altmann, 1970). Struhsaker (1967a, b) found elephants to be the major competitors of vervets in East African savanna, where elephants knock down the refuge and food trees of primates. Areas managed to protect elephants may show corresponding reductions in primate populations. The opposite policy also has negative long-term effects as elephants and other species

85 play important roles in the dispersal of seed plants which in turn form part of the diet of primates. When forestry departments reduce elephants as destructive to growing timber, or spray herbicides, they may be upsetting poorly understood equilibria. Such influences may reduce the quality and diversity of the forest for many wildlife species by producing long-term changes in its botanical composition (Struhsaker, 1972). Critical Population Size The assumptions and methods for managing wild populations must be re-evaluated to allow for the biological differences in recruitment rates between species identified as "r-strategists" and "K- strategists. " The minimum population size necessary to maintain a diverse gene pool in wild populations will differ considerably for these two groups of species. Life tables for wild, unprovisioned primates are needed to supplement the data collected on other species before adequate estimates of minimum population size can be made. The organisms most frequently found as domestic stock, as pets, or as research animals share several biological characteristics not shared with primates. These characteristics that allow intensive utilization and manage- ment include annual or more frequent reproduction, multiple births, and rapid maturation. These species have been labeled as "r-strategists" by population ecologists due to their high rates of natural increase. These species can recover rapidly from low population densities and colonize new environments that are only temporarily suitable for their survival. Histori- cally, the administrative familiarity with only this type of species in agri- culture and wildlife management has resulted in management practices for wildlife that have been based on the implicit assumption that harvesting will remove surplus animal production rather than decimate the breeding population. Only recently have data been collected on life tables for species that have the opposite reproductive strategy. These species have been referred to as "K-selected" species after a term for the saturation density for the species in the logistics equation that describes the growth of populations. K-strategists are species that tend to have longer life spans, slower matur- ation rates, and fewer offspring. However, since each offspring receives more parental investment, it has a higher probability of survival. Because K-selected species have lower rates of increase and mortality and have a closer adjustment to the long range carrying capacity of the environment, they tend to be found in habitats that have traditionally been very stable. Lumbering, slash and burn agriculture, and irrigation have tended to supplant stable ecosystems with transient ones. Gradual habitat changes and selective pressures for hunting and trapping have resulted in a propor- tionately high representation of K-selected species on the lists of species that are either threatened or in danger of extinction. The large-bodied primates with a 3-4 year maturation time and a single offspring born at 1-2 year intervals are prime examples of K-selected species. Unfortunately, life tables for primates under natural conditions are not available. However, a recent publication based upon another species with similar population characteristics has demonstrated how extremely slow recovery is for these species. Miller and Botkin (1974) calculated the population dynamics of sandhill cranes, a species with a 25-year life span and a 4-year age at puberty. They showed that a popu- lation that has been reduced to approximately 200, 000 birds would be forced

86 to extinction within 25-30 years if only 5 percent of the population were harvested annually. A computer simulation of the long-range effect of an annual harvest of 6,000 individuals indicated that 30 years of harvesting at this rate would reduce the population to 50 percent of its former level. Even if a moratorium were introduced at the end of 30 years, it would take another 70 years for the population to return to its former equilibrium level. Although the values of the constants, the annual recruitment rate, and the age-specific survivorship would differ somewhat for each species of primate, the general magnitude of the slow recovery rate can be extrap- olated directly. For a species of bird with known wintering grounds and migratory routes, one would expect that census data would be rather accurate relative to data on tropical forest species, and that it could be used to monitor population fluctuations. To the contrary, the authors state that the data cannot be used in this way since sampling errors were probably the cause of a 35-percent discrepancy between censuses taken 2 years apart. Since harvests of only 2, 000 individuals annually would reduce the equilibrium value for the popu- lation, the authors concluded that the discrepancies "emphasize that current census methods are too crude to detect significant population decreases in fluctuations. To the contracy, the authors state that the data cannot be used in this way since sampling errors were probably the cause of a 35-percent discrepancy between censuses taken 2 years apart. Since harvests of only 2, 000 individuals annually would reduce the equilibrium value for the popu- lation, the authors concluded that the discrepancies "emphasize that current census methods are too crude to detect significant population decreases in time to take the necessary remedial action." Further, their model demon- strated that population events cannot be predicted accurately with a simple annual census of total numbers. The authors' conclusion that too little is known to manage this species properly also describes the situation for all primates. The above theoretical example illustrated one method for making long- term projections about populations; it also illustrated how short a time wild populations have been censused. The earlier discussion of the pro- tected area provided by reserves ignored the amount of fragmentation of populations and the minimum size of reserves necessary to protect hetero- geneous populations. Medway and Wells (1971) have accepted a population of 5, 000 individuals as a minimum number that should be provided contin- uous protection. This is a good heuristic figure for which we need more data. If this is a good estimate, then the 2 langur species would require areas of 250 km2 (98 mi2) and 500 km , respectively, for populations of 5,000 individuals in Malaysian forests. A long-tailed macaque population would require 500 km , while the gibbons and siamang would need areas of nearly 2, 000 km2. The wider ranging pigtail macaque (Macaca nemestrina) would require over 3, 300 km2 of continuous habitat to provide safety for a heterogeneous gene pool of this size. A minimum population is necessary to maintain diversity in wild popu- lations but few estimates are available. Studies of the heterozygosity of 22 vertebrate species have shown the proportion of polymorphic loci to vary between 10 and 20 percent. Recently, Bonnell and Selander (1974) have been unable to identify any polymorphisms in the blood proteins of surviving wild populations of elephant seals. This species was reduced to fewer than 100 individuals and 1 or 2 harem-breeding males at the turn of the century.

87 These authors suggested that the lack of variability with which to adapt to changing conditions increases the vulnerability of this species to environ- mental modifications. A similar situation, but without the breeding bias, is greatly reducing polymorphisms and increasing the vulnerability of several species of primates. Primates (are typically forest species that) represent a small portion of the mammalian fauna in tropical forests even before they are exposed to hunting and trapping pressures. The only available estimates for balanced ecosystems are those of Eisenberg and Thorington (1973) who calculated that primates represent from 6 percent to 10 percent of the total mam- malian biomass in Surinam and on Barro Colorado Island, respectively. The primate portion of the fauna is further characterized by slow recruit- ment--typically, one young per year or every other year--and slow maturation--typically, 3-5 years. The combination of factors, including habitat destruction by deforestation, slow population recruitment, and selective hunting and trapping of species that initially represent a small proportion of the mammalian biomass, creates a bleak picture for the future of unprotected primate populations in the wild. The increasing number of reports of population declines throughout the tropics arise from this combination of circumstances. Rate of Deforestation Forest habitats of many primate species are being depleted as a result of logging and clearing for other purposes. The changing pattern of land use in South America is indicative of trends throughout the tropical forests. Estimates of the actual area of tropical forest that has been cleared in South America range from 50, 000-100, 000 km^nnually, although the proportion of this area that may be second growth is not indicated (Nelson, 1973). Estimates of new cropland are 10,000 km2 annually. In Brazil, 84 percent of the increased crop output between 1948 and 1962 has been attributed to the incorporation of additional area. In the 17 years between 1950 and 1967, an area of 90, 000 km2 in the humid tropical regions of South America was converted to agriculture (Nelson, 1973). This area is one third greater than the protected area for any single primate species throughout Latin America (Table 33). Deforestation in tropical countries has concerned several authors. For example, the loss of habitat resulting from deforestation in Equatorial Guinea (Sabater Pi and Jones, 1967), in Thailand (Lekagul, 1968), in northern Colombia (Struhsaker et a-l. , In preparation), and in Malaysia (Southwick and Cadigan, 1972) is reducing the ranges of some primate species. Lumbering has progressed at a rate of 223 km2 annually in Malaysia. Finally, Richards (1973) has pre- dicted that all major blocks of tropical forest will be gone by the year 2000. Relative Numbers £f Primates Inside and Outside Reserves Primates have been trapped from undeveloped areas in past years--ones neither managed intensively nor set aside as reserves. While the size of reserves provides an estimate of minimum future populations and indirectly of government attitudes towards the development of natural areas, the reserves will not supply the primate trade. Indeed, most are managed to prevent exploitation of animals. The following discussion compares the chimapnzee, a species that probably will occcur only inside reserves within a few years, and other species that adapt to moderate agricultural development and should continue to occur in larger numbers outside of reserves.

88 The diversity and widespread nature of the pressures exerted on primate habitats is illustrated by chimpanzees because the species has a wide geographical distribution and large home ranges (Wolfheim, In preparation). The most severe land exploitation within the distribution of chimpanzees has occurred in such areas as western Guinea where 40 percent of the land is under intensive nomadism and agriculture (Bournonville, 1967). The range of chimpanzees is being reduced in Equatorial Guinea through the degeneration of soil conditions after forests are cleared (Sabater Pi and Jones, 1967). Less diverse vegetation frequently replaces rain forests where timber concessions are granted, where plantations replace natural forests, or where natural forests are being managed for single objectives with little ecological consideration. Struhsaker (1972) stated that timber concessions threaten the Tai Reserve, which is the last forested area where chimps occur in the Ivory Coast. A program using arboricides to weed out noncommerical species of trees after logging is a method of forestry management presently practiced in Uganda that alters the habitat for chimps (Reynolds and Reynolds, 1965). Suzuki (1971) reported that a fourth of the Budongo Forest had been treated with herbicides and future plans included spraying the entire area. The program kills primate food sources, such as fig trees, and it promotes growth of secondary brush. The ability of chimpanzees to survive in agricultural areas has been documented by Dunnett e-t al. (1970), but the hunting and trapping pressures summarized by Wolfheim (In preparation) have had a devastating effect on populations outside of reserves. The prospects for the continuation of much larger populations outside than inside reserves are more favorable for the species numerically more important in biomedical work than they are for the rarer and larger species. Semi-terrestrial species such as rhesus macaques, baboons, and vervet monkeys and arboreal species such as squirrel monkeys have in common the ability to utilize a variety of habitats (Eisenberg et aL , 1972; Southwick etal. , 1965; Altmann and Altmann, 1 970; Gartlan and Brain, 1968; Rosenblum and Cooper, 1968). The baboons can exploit the drier savannas as well as the mixed, regenerating, and riverine forests utilized by the other species. These species are not specialists but consume a wide variety of natural foods including fruits, flowers, buds, insects, and small vertebrates. They are well adapted to live at the ecotone, or the interface between habitats, where food supply increases with botanical diversity. Because the medically important species, rhesus macaques, baboons, and vervet monkeys, are both opportunistic feeders and semi-terrestrial, they have frequently shown population increases in areas where the mature forest is degraded to mixed and successional growth and also where patches of forest are interspersed with cultivated crops. Such increases have been observed during the early stages of agricultural expansion where there is a slash and burn subsistence pattern of planting and fallow. Such increases continue until the human settlements become more densely populated and the forest patches that serve as retreats for monkeys are removed. As agriculture shifts to a cash crop basis and becomes increasingly technological, monkeys become labelled as crop raiders and may be exter- minated through systematic hunting, trapping, or poisoning. Baboons are considered to be sufficiently damaging as agricultural pests in South Africa to warrant governmental publication of a brochure for farmers that

89 explains how to capture and dispose of troops systematically (Keith and Stoltz, 1971). McGuire (1974) estimated that 2,000 vervets were killed annually for bounties on the Caribbean island of St. Kitts. Small numbers of vervets were introduced onto the island decades ago and current population esti- mates range between 5, 000 and 20, 000. Rowell (1968) estimated that 6,000 vervets were killed as agricultural pests in Uganda in 1964. Such animals represent untapped sources of primates that could potentially be harvested on a sustained-yield basis through purchases from farmers who allow the depredations of these animals on their crops during the year. If the eradication programs succeed, the population increases of these opportunistic primate species may turn out to be only temporary increases lasting for a few years in actively developing agricultural regions. Although certain monkeys may continue to exist in large numbers outside of reserves, urban monkeys that co-exist with humans become less useful for medical research because they may carry antibodies to the disease under study and may have various pathologies that confuse the clin- ical and histological picture of the disease syndrome. They also require increasingly expensive quarantine procedures to cure them prior to use. Southwick and his colleagues have documented a general increase in scaven- ging urban populations and a corresponding decline in the numbers of rural and woodland monkeys because these are trapped more intensively for bio- medical use and are also trapped or shot as agricultural pests. Although problems of continually changing disease status can be minimized by obtaining experimental animals consistently from known localities, this trend in the relative abundance of urban and agricultural monkeys is reducing the potential biomedical usefulness of many monkey populations found outside of reserves. Few populations of primates have been sampled repeatedly in a fashion that has provided data for understanding population trends. Only a fifth of the 146 field studies conducted during the last few years have been sup- ported to any extent by the National Institutes of Health (Chivers and Chivers, 1974). An awareness of the trends in wild populations that in- fluence the quality of animals has become increasingly important for users because there will be a continuing need to procure breeding stock and to obtain animals for comparative studies. Programs that develop captive colonies cannot afford to ignore the need for protecting wild populations that can serve as insurance against colony loss. Risks inherent in captive colonies include the loss of genetic diversity, selection for detrimental genes, and nutritional problems, as well as the risk of colony loss from an epidemic. Unless breeding colonies are established on a large scale, it will be necessary to supple- ment breeding stock from the wild. If breeding colonies are too small, genetic drift or decreasing fertility may occur. Fertility has been found to decline with inbreeding by the sixth to eighth generation in several species of nonprimates. At 5 years per generation of macaques, such a reduction could be expected in as little as 30-40 years of captive breeding in closed colonies where turnover is maximized in order to study the influence of inheritance on disease susceptibility and resistance. There are examples of unanticipated selection in the literature, e.g. , progres- sive deafness appearing in strains of mice susceptible to audiogenic seizures (Ralls, 1967). Captive breeding generally promotes rapid growth and maturation. Few reproductive studies based upon small

90 captive gene pools are available. Recent observations on exotic birds indicate that growth rate is as finely tuned as any physiological parameter and that increasing the growth rate for tropical species may result in physical deformities when bone, muscle, and tendon growth do not keep pace with each other (Kear, 1973). Both the intrinsic population ecology of primates and current environ- mental changes in the tropics have increased concern for the future of wild primates. More accurate data on the status and trends of closely monitored wild populations must be accumulated in order to manage harvestable populations both in the wild and in captivity.

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