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Supporting Data: Nancy A. Muckenhirn
Pages 11-90

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From page 11...
... 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.
From page 12...
... 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.
From page 13...
... . The two most important species are the squirrel monkey and the rhesus macaque, which together account for roughly 62-65 percent of all imports.
From page 14...
... 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)
From page 15...
... 15 TABLE 2 TOTAL PRIMATES IMPORTED INTO THE UNITED STATES COMPARED WITH EXPORTS FROM INDIA Total U.S. Imports, by Source*
From page 16...
... 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*
From page 17...
... , 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.
From page 18...
... 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)
From page 19...
... 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)
From page 20...
... . 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.
From page 22...
... 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
From page 23...
... regiosal primate ceste Atlasta, Georgia Wake Forest Usiversit Gray Medical School) Wisstos-Salem, Nor Harvard Usiversity Me Cester (iscludes regio: primate cester)
From page 24...
... 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.
From page 25...
... 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
From page 26...
... ) , baboons, long-tailed macaques, pigtail macaques, night monkeys, vervets, and stumptail macaques.
From page 27...
... 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.
From page 30...
... 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.
From page 31...
... 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
From page 32...
... 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.
From page 33...
... 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.
From page 34...
... 34 • Example: A laboratory maintains an inventory varying between 50 and 100 animals. Fifty animals are imported and sacrificed during each quarter.
From page 35...
... 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
From page 36...
... The most frequently ordered animal was the 4-6-pound rhesus macaque. The research interest in different species is illustrated in Table 11.
From page 37...
... 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.
From page 38...
... 38 TABLE 11 PRIMATE SPECIES IN DEMAND BY RESEARCH AREA Research Rhesus area macaque Marmoset African CrabSquirrel 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 Diseaseinfectious 1.844 614+ 46 1,440 96+ + 37 50+ Diseaseneoplasm 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 Diseaseorgan 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 + Diseaseother 119 100 85 4 Diseaseimmunology 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.
From page 39...
... 39 Stumptail Chimp, macaque Ape Tree Macaque, shrew general Galago Bonnet Pataa Spider Permacaque 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
From page 40...
... 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 .
From page 41...
... 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
From page 42...
... 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)
From page 43...
... 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.
From page 44...
... 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.
From page 45...
... 45 <,§ o o o to -4-• i -- i NO m CO " -- i -H CM rtONAL Mortality :ise Addrd Holdisg Costs ($) / rtsssr*
From page 46...
... 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.
From page 47...
... attributes many losses of vervets to the primate trade while Rowell (1968) implicates eradication programs for agricultural pests.
From page 48...
... 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
From page 49...
... 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 *
From page 50...
... 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.
From page 51...
... 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.
From page 52...
... These rates have been considered to be overly optimistic by many researchers 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.
From page 53...
... Research Colonies Species Saguinus fuscicollis 155 199 159 96 291 62 1 3 5 Saguinus nigricollis Saguinus oedipus TOTAL 449 9 SOURCE: Thorington (1972)
From page 54...
... 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.
From page 55...
... 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)
From page 56...
... , La Parguera, PR Regional Primate Centers (RPRC's) California RPRC, Davis, CA Delta RPRC, Covington, LA CDC, Atlanta, GA Gulf South Research Inst.
From page 57...
... 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
From page 58...
... 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.
From page 59...
... 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.
From page 60...
... is one of the few authors selected in such compilations 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.
From page 61...
... suggest that basic studies of husbandry are needed before self-perpetuating breeding colonies can become productive on a large scale.
From page 62...
... 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?
From page 63...
... 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.
From page 64...
... 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)
From page 65...
... Eq. Guinea Nigeria Schaller, 1963 Jones and Sabater Pi, 1971 SOURCE: Table adapted from information summarized in IUCN, 1972 for some population estimates and in Wolfheim (In preparation)
From page 66...
... apella Lagothrix lagotricha Saimiri sciureus Alouatta palliata A seniculus NOTE: Density estimates are not based on standardized field methodology.
From page 67...
... 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.
From page 68...
... 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.
From page 69...
... 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.
From page 70...
... 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.
From page 71...
... 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 .
From page 72...
... 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 reserves 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.
From page 73...
... Sri Lanka (Ceylon)
From page 74...
... l fl , 000 km 2(%) } Minimum Reserves Not Listed§ (1, 000 km2)
From page 75...
... Sierra Leone 73 Liberia 113 . Ivory Coast 322 15.7 ( 5)
From page 76...
... 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^.
From page 77...
... 77 co 5 <«4 "o T}< O H *
From page 79...
... No. named forms Number of genera are given only in total column.
From page 80...
... found for Macaca sinica in Sri Lanka, then there are fewer than 50, 000500, 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.
From page 81...
... . § Named forms follow Napier and Napier (1967)
From page 82...
... . § Named forms follow Napier and Napier (1967)
From page 83...
... . Named forms follow Napier and Napier (1967)
From page 84...
... 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.
From page 85...
... " 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.
From page 86...
... 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.
From page 87...
... . This area is one third greater than the protected area for any single primate species throughout Latin America (Table 33)
From page 88...
... 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)
From page 89...
... 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 clinical and histological picture of the disease syndrome.
From page 90...
... 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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