Session 1
Conservation and Supply, Part 1



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International Perspectives: The Future of Nonhuman Primate Resources Session 1 Conservation and Supply, Part 1

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International Perspectives: The Future of Nonhuman Primate Resources Sustainable Utilization of Kenyan Nonhuman Primates for Biomedical and Conservation Research Jason M. Mwenda, PhD The Institute of Primate Research (IPR) is a nonprofit institute that was established by the Kenyan government in 1960 to conduct biomedical and conservation research using the East African nonhuman primates. IPR is a designated World Health Organization (WHO) collaborating center for research in reproductive health and tropical diseases and a member of the European Union (EU)-supported Primate Vaccine Evaluation Network. IPR is the only multidisciplinary primate center in Africa. The Institute of Internal Scientific, Ethics, and Review Committee and Animal Care and Use Committee review all proposals and study protocols before initiation. These committees ensure that during the conduct of the biomedical research, the welfare of nonhuman primates is not compromised and the study protocols conform to the international guidelines on biomedical research using nonhuman primates (NHPs). IPR is currently involved in research in the following areas: reproductive health, tropical diseases, primate medicine (zoonotic infections, natural and experimental aging processes including Alzheimer’s disease), primate behavior, ecology, and conservation. Thus, IPR is involved in research that promotes better health for humans and animals, and especially the NHPs. In this endeavor, the Institute encourages networking with other scientists with mutual research interests and that enhances Institute of Primate Research, Nairobi, Kenya

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International Perspectives: The Future of Nonhuman Primate Resources local capacity building and promotes regional and international collaboration. Some notable achievements of the Institute include: Development of the vervet monkey model for cutaneous leishmaniasis. This model has now been accepted by WHO as an appropriate model for testing for vaccines and drugs against leishmaniasis. Identification (for the first time) of malaria-like parasites in monkeys and investigation of monkeys potentially transmitting malaria to humans. Development of the baboon as an ideal model for schistosomiasis research. This model is being used to test the efficacy of candidate vaccines. IPR scientists have shown the highest protection level in schistosomiasis Mansoni using radiation-attenuated vaccine in the baboon model (85% protection level). Development of the rotavirus diarrhea monkey model, which will be valuable for testing rotavirus vaccines to prevent severe diarrhea in children and elucidating the pathogenesis of rotavirus infection/disease. Establishment of diagnostic tests for screening pregnant baboons and women for immunological causes of infertility (caused by presence of antiphospholipid antibodies and endometriosis (characterized by severe pelvic pain). Development toward a new class of birth control methods (antifertility vaccines) for use by both men and women. Available results of testing of these vaccines show anti-CG contraceptive vaccines did not result in adverse effects in female baboons. Similarly, anti-LDH-C4 vaccine for men showed effective fertility control in baboons with no evident side effects. These immunological contraceptives offer advantages over other fertility control methods in terms of efficacy, reversibility, and safety and may be more acceptable in the African cultural setting. Development of vervet monkey and baboon models for testing AIDS drug and vaccines before clinical trials in humans. Recognition of IPR as a center of excellence for biomedical research using primates (monkeys) and specialized training (undergraduate, M.Sc., Ph.D., postdoctoral) and international scientific exchange. Development of effective strategies for conservation of endangered nonhuman primates (monkeys), including De Brazza monkeys, Tana River colobus monkey, and crested mangabey. Twelve Old World monkey species are found in Kenya. IPR has facilities for maintaining 400 monkeys, which represent nine species. In Kenya, there is an increasing demand on land for urbanization and agriculture/farming activities, mineral resources, and the establishment

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International Perspectives: The Future of Nonhuman Primate Resources of timber industries. These activities have increasingly reduced the areas available to wild primates. Thus, NHPs are commonly regarded as pests, and farmers often kill the baboons and vervets for crop-raiding. In addition, due to increased community need for forest resources and farming, land pressure on the remaining forest patches has led to the genuine concern for developing effective conservation strategies for the endangered primate species found in Kenya. IPR, in collaboration with Kenya Wildlife Service and the relevant government departments, has coordinated efforts for conservation of the following endangered and threatened NHPs: De Brazza monkey (Cercopithecus neglectus), Angolan black and white colobus monkey (Colobus angolensis), eastern black and white colobus (Colobus guereza), Tana River red colobus (Procolobus badius), and Trana River crested mangabey (Cercocebus galeritus). In Kenya, the threatened De Brazza monkeys are confined to the Kakamega Forests and the Trans Nzioa plain, which lies east of Mt. Elgon and west of the Cherangani Hills. The endangered Tana River red colobus and crested mangabey are both endemic to forest patches along the lower Tana River. In recognition of the need to conserve these two primate species and their unique habitat, the Kenyan Government gazetted 171 km2 in 1976 and established the Tana River Primate Reserve (TRPNR). Ongoing conservation studies by IPR scientists in TRPNR are focused on (1) carrying out primate census and determination of distribution of primates, (2) evaluating changes in forest sizes in relation to populations of red colobus and crested mangabey, (3) assessing human and natural impacts in forests along the lower Tana River, and (4) developing management and conservation strategies for the endangered red colobus and their habitat along the lower Tana River. Overall, the Kenyan government and IPR encourage primate conservation programs that encompass community participation, primate translocation, and conservation of biodiversity that is geared toward sustainable utilization of natural resources.

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International Perspectives: The Future of Nonhuman Primate Resources Supply and Use of Nonhuman Primates in Biomedical Research: A South African Perspective Jürgen Seier, PhD, MSc GENERAL There are six indigenous nonhuman primate (NHP) species in South Africa, of which two are used in biomedical research: the chacma baboon (Papio ursinus) and the vervet—or African green monkey (Chlorocebus aethiops). This presentation concentrates on these two species. GEOGRAPHICAL DISTRIBUTION Baboons occur in most parts of South Africa and across the entire country, with the exception of the driest areas, and they can be found near major centers such as Cape Town. Vervet monkeys are much less widespread than baboons and are mainly confined to the eastern parts of South Africa, with pockets in a few other locations. Vervet monkeys also occur in and near major centers such as Durban. Both species occur in all neighboring countries including Namibia, Botswana, Lesotho Zimbabwe, Swaziland, and Mozambique. CONSERVATION The general conservation status of chacma baboons and vervet monkeys is “low risk” (Rowe 1996), and neither species is considered threat Primate Unit, Medical Research Council, Tygerberg, South Africa

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International Perspectives: The Future of Nonhuman Primate Resources ened in South Africa, with the exception of certain local populations (e.g., Cape Peninsula baboons). Although both species are considered “common” in many areas where they occur, a lack of national census does not allow any firm conclusions. A proposal for a national census is currently being produced. Vervet monkeys and baboons are protected in conservation areas, but the protection and status outside these areas, particularly in view of agricultural problems, vary in different provinces. The controlling bodies for wild and captive populations, importing and exporting (CITES), and even moving across provincial borders are the nature conservation departments. To provide some perspective, the populations in 1981 were estimated to be approximately 20,000 to 25,000 vervet monkeys and 3,600 baboons in all protected areas of Kwa Zulu Natal (Bourquin 1981), one of nine provinces in South Africa. However, apart from being dated, such figures are misleading since many NHPs live outside protected areas, and in some provinces, baboons occur in considerably larger numbers. CONFLICTS AND THREATS As in many other countries with wild populations, in South Africa, NHPs raid agricultural crops and may vandalize gardens and homes, where human development has encroached on their territory. Farmers destroy primates that become agricultural pests, and where the territory of NHPs is close to urban areas, a number fall victim to car accidents every year. As an example, the baboons of the Cape Peninsula, which are an isolated population of about 350, are a major tourist attraction. The peninsula baboons frequently forage on the shore and supplement their diet with seafood. Residential and other human development has encroached on their territory to an extent that in certain areas, baboons have taken to raiding gardens and homes regularly. Presently the mortality rate outstrips the birth rate. In some scenic spots, visitors have been regularly feeding baboons, resulting in the baboons being habituated to people, who exacerbate the problem of large, wild primates near residential/ urban areas. USE OF NONHUMAN PRIMATES IN BIOMEDICAL RESEARCH IN SOUTH AFRICA OVER THE LAST 3 YEARS Although baboons are used mainly, both baboons and vervets are utilized in all research fields requiring primate models. Of the few primates used in biomedical research, approximately 210 baboons and 120 vervet monkeys have been utilized annually in 17 facilities nationwide. In

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International Perspectives: The Future of Nonhuman Primate Resources the last 21 years, there has been a 81% decline in the use of baboons and a 88% decline in the use of vervet monkeys. SUPPLY OF NONHUMAN PRIMATES Over the last 3 years, about 3% of baboons and 60% of vervets were captive bred, and the rest were caught from the wild. Presently only one facility systematically breeds African NHPs (vervet monkeys) for research. Local nature conservation authorities must issue permits for trapping NHPs, and proof of agricultural damage by such primates must be provided in some provinces. Only authorized trappers receive permits. Research facilities maintaining NHPs are inspected annually by nature conservation authorities and must apply every year for holding permits, even in the case of captive-bred primates. In some provinces, nature conservation authorities require an ethically approved study protocol and proof of agricultural damage before permits for capture are issued. Over the last few years, there has been an increased reluctance by the nature conservation authorities to issue capture permits. However, due to the small number of primates used locally, there are usually no major supply problems from local sources. Although there may have been sporadic transfers of small numbers, there is no provision to other countries and South Africa is not an exporter of NHPs. Moreover, it would be very difficult and costly, if not impossible, to move NHPs from South Africa since all airlines that operate transcontinentally from South Africa do not transport primates destined for biomedical research. PRIMATE FACILITIES IN SOUTH AFRICA Local facilities, which are designed for small numbers of wild-caught primates and not for breeding or long-term maintenance, concentrate on rodents. However, if funding became available, the potential of establishing breeding centers does exist, and there is generally an excellent research infrastructure and expertise. There are no national or regional centers, and the largest South Africa facility maintains 250 to 300 vervet monkeys, with the capacity to produce 100/annum. This facility has the infrastructure for long-term maintenance and has been breeding vervet monkeys for about 25 years, which has progressed to the second and third generation. Other facilities typically maintain between 20 and 60 NHPs, mainly baboons. There are no primate centers in neighboring countries and little, if any, use of primates in biomedical research.

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International Perspectives: The Future of Nonhuman Primate Resources CONCLUSIONS Vervet monkeys and chacma baboons occur in many parts of South Africa and across the entire Southern African region. Like NHPs in other source countries, vervets and baboons face a variety of threats and are in conflict with some human activities in South Africa, but these factors are unlikely to endanger the entire population. Some of these threats are highly localized (e.g., the Cape Peninsula baboons). Although mostly wild-caught primates are used in biomedical research in South Africa, the numbers are small and the effect on wild populations is minimal if any. Most research centers have no facilities for long-term maintenance and breeding of nonhuman primates, although the potential to establish such centers exists. South Africa has not been exporting NHPs with the possible exception of some sporadic transfers of small numbers. REFERENCES Bourquin 1981. Wild primates and their availability for research purposes. In: de Klerk W.A., ed. The Role and Utilization of Nonhuman Primates in Biomedical Research in South Africa. SAALAS Workshop Proc 48-54. Rowe N. 1996. The Pictorial Guide to the Living Primates. New York: Pogonia Press.

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International Perspectives: The Future of Nonhuman Primate Resources Sustainable Primate Resources Through SPF Breeding Programs in Indonesia Joko Pamungkas, DVM, MS, and Dondin Sajuthi In response to conservation concerns, both nationally and abroad, over the status of Indonesia’s naturally occurring primate populations, the Indonesia Department of Forestry enacted a regulation in 1994 that restricts the export of nonhuman primates to progeny from captive/man-aged breeding facilities. The Forestry Department also applied a law governing the quota of wild-caught primates that can be used as breeder replacements or for research to be conducted in country. Along with these government policies, the Primate Research Center at Bogor Agricultural University, in Bogor, Indonesia, in collaborations with several national and international institutions (e.g., Washington National Primate Research Center) has established two breeding facilities in Indonesia. An island natural habitat breeding facility supporting an introduced population of simian retrovirus (SRV)-free Macaca fascicularis was initiated in 1987 on Tinjil Island located off the south coast of West Java, and an SRV-free M. nemestrina captive-breeding facility in Bogor was initiated in 1992. Progeny from these two breeding facilities have been utilized in biomedical research programs in Indonesia and worldwide. Primate Research Center, Bogor Agricultural University, Bogor, Indonesia

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International Perspectives: The Future of Nonhuman Primate Resources Use of Nonhuman Primates in Biomedical Research in India: Current Status and Future Prospects A. J. Rao, PhD India is known for its floral and faunal diversity. This diversity is best represented by the nonhuman primate (NHP) population found in the country. Of the more than 30 genera and 130 species of NHPs known throughout the world, as many as eight genera having 10 species and 38 subspecies are known from India alone (Parthasarathy 1995). Of these species, seven are exclusively Indian in their distribution: Ananthana ellioti, Tupaia nicobarica, Macaca assamensis, Macaca radiata, Macaca silenus, Semnopithecus johni, and Semnopithecus geei. An additional five species are restricted to the tropical, dry, and moist deciduous evergreen forests of peninsular India: a shrew-like prosimian, a slender loris, two macaques, and a langur. Indian monkeys belong to one family, Cercopithecidae, with two subfamilies, Cercopithecinae (the macaques) and Colobinae (the langurs). None of the human-like great apes are found in India. The only tribe of apes inhabiting India is the gibbons, of which a single species, the hoolock, is found in the forests of Assam and Chittagong. The total population estimate of Hylobates hoolock is approximately 170,000 (Mackinnon and Mackinnon 1987). Macaca silenus (lion-tail macaque) is found in the evergreen forests of Western Ghats in India. This species is endangered Primate Research Laboratory and Department of Biochemistry, Indian Institute of Science, Bangalore, India

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International Perspectives: The Future of Nonhuman Primate Resources true for many sites. The very high costs quoted are the product of several factors, in addition to greed. These factors include: The wasteful use of many primates for terminal toxicological studies with no attempt to minimize numbers via rational pharmacogenomics; The use of Asian macaques with enzootic herpes virus B, which demands safety garb for personnel and insurance premiums that artificially inflate costs; The failure to select species appropriate to the question at hand or, within species, to select individuals with optimum sensitivity to the experimental intervention; and The failure to follow the dicta of the 1960s Primate Centers Program and the subsequent recommendations for the development of adequate laboratories in countries of origin so that supplies could match needs more precisely. Looking at contemporary biomedicine, both academic and industrial, there would seem to be needs for the following kinds of primate subjects: Those with spontaneous models of a human disorder (e.g., M. arctoides’ patchy alopecia, to provide the hair growth industry with a fortuitous model). Colon cancer occurs in the cottontop marmoset and human, and rarely in other primates. Hypertension occurs in C. aethiops and lagothrix and rarely in other nonhuman primates. Atherosclerosis, rare in C. aethiops, is common in Papio. Those with inducible disease models (e.g., squirrels are very sensitive to vitamin C deprivation; M. nemestrina is more responsive to laboratory SIV infection than other primates tested; and hepatitis B sensitivity apparently remains restricted to the human and the chimpanzee). Those with some particular phenotypic advantage. Baboons are large enough for a variety of surgical interventions. They also have an immune response profile close to that of the human with respect to porcine xenotransplantation. They are therefore much preferred over the Asian macaques. C. aethiops, of course, is similar in this regard. Again, for studies on reproductive technology, the straight cervix of C. aethiops is much easier to work with than the tortuous cervix of most macaque species. Animals that can be handled and/or manipulated safely (e.g., for cognitive or behavioral testing). Those with enzootic virus B are awkward for such uses. The otherwise aberrant New World marmosets and squirrels may be excellent, due to their small size and temperamental malleability.

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International Perspectives: The Future of Nonhuman Primate Resources Primates that need no qualification other than to be as close to the human as possible in regard to immune mechanisms, pharmacokinetics, physiology, and so forth. For such use as nonspecific primates, examples of the criteria should be size, convenience, safety, price, and status of endangerment. The existence of relevant normative databases is also desirable. These diverse needs are typically met by a single species the institution or investigator has chosen based usually on history, habit, chance availability, or housing space available, rather than on any of the rational criteria outlined above. The majority of animals used are the following: Asian macaques—mulatta, fascicularis, and nemestrina; African C. aethiops and Papio and New World Saimiri and Saguinus. I personally have worked with Saimiri, Saguinus, Cebus, Ateles, M. mulatta, M. arctoides, Papio, Pan, Chlorocebus (Cercopithecus), and Homo. My own favorite primate is M. arctoides, but for the past 33 years I have concentrated on C. aethiops, SK, which has several features that commend its use as a complement to the more extensively used macaca in biomedical research. The Caribbean islands of St. Kitts and Nevis are, in effect, closed breeding colonies that house approximately 40,000 to 50,000 C. aethiops sabaeus in a tropical ecology with no natural predators. It is 300 generations beyond a founding stock of approximately 1000 West African immigrants. Biochemical and molecular analyses document the genetic diversity of the population. Census data suggest that at least 5000 individuals can be harvested per annum without affecting population viability or diversity in any manner. In addition, we maintain a breeding colony of about 1000 animals, primarily for our own scientific work and that of collaborators; but this number also provides a base for developing cross-species comparative data (e.g., on pharmacokinetics and reproductive endocrinology). In addition, our breeding program can selectively target the expansion of rare naturally occurring phenotypes and the development of disease-appropriate experimental phenotypes. With 30 years of experience in establishing practical husbandry and breeding programs for 1000 to 1500 animals in addition to an ongoing research and training program with emphasis on developmental biology, the establishment of normative databases, and quantitative measures of behavior change, we can complement the abundant supply of animals with professional screening selection and advice as to handling. The St. Kitts vervet was removed from West Africa before 1700 by early French settlers to the New World. It thus escaped the major pathogens that infested contemporary African populations. In the Indies, it evolved in a predator-free environment to become the leading agricultural predator and threat to economic self-sufficiency.

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International Perspectives: The Future of Nonhuman Primate Resources This specific pathogen-free, nonendangered, readily available Old World primate has numerous immediately attractive features. It is: B virus free. This macaque enzootic pathogen is instantly fatal to the vervet as it is to the human. It has been suggested that keeping a vervet in a laboratory colony of rhesus would serve as a “canary” to detect an outbreak of immunosuppression. Nonendangered. Nowhere in its range is it endangered. It is the weed monkey of Africa, flourishing in most econiches. In the Caribbean, it is a significant crop predator and general pest. Relatively small and temperamentally tractable, unlike rhesus (e.g., adult male maximum weight = 7 kg). Also free of other pathogens. For example, there is no evidence of filovirus, SIV, or STLV, nor evidence of yellow fever, malaria, tuberculosis, yaws, or schistosomiasis. Evolutionarily closer to the human, as is the baboon, than the Asian macaques. As a consequence, examples of methods in which most human reagents can be used in C. aethiops are PCR, SNP analysis, receptor binding, and cytokine measurement. Four hours’ flight from the United States and 6 hours’ flight from Europe. A candidate for on-site facilities for scientific preparation, quarantine, sampling, pretreatment, and so forth. Highly cost effective. A candidate for several spontaneous models of human disorder that have been identified to date and several others that have been readily induced (Table 1). Relatively easy to breed in captivity, providing opportunities for genetic control, production of mother-fetus pairs for behavioral teratology, and infants for developmental studies and testing (Table 2). TABLE 1 Models of Human Conditiona Spontaneous Induced • Hypertension • Parkinson’s disease • Metabolic syndrome (X) • Multi-infarct dementia • Polycystic ovarian disease • Allotransplant GvH syndrome • Alcohol abuse and fetal alcohol syndrome • Xenotransplant GvH • Anxiety disorders including panic disorder • Estrogen-induced uterine CA • Mother-fetus dyads (e.g., for vaccine teratology)   aSee also Palmour et al. 1997. Am J Hum Genet 61:481-488.

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International Perspectives: The Future of Nonhuman Primate Resources TABLE 2 Reproductive Characteristics Sexual maturity: female, age 3; male, age 5-6 Menses: 28-day cycles during breeding season (October-March) in natural habitat. Anestrus cycles March-October, if not pregnant. Male testis in apparent regression during this period Pregnancy: 6 months. Weaning by age 6 months. Twins about 1:88 (like humans) Female fertility throughout life cycle but irregular pregnancy after age 20 Male fertility throughout life cycle The Federation of St. Kitts and Nevis is an independent nation and a member of the United Nations, the Organization of American States, the British Commonwealth, and other regional and international bodies. It is signatory to the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) agreement and other relevant international agreements pursuant to such concerns as animal health and transportation. The indigenous primate population is designated a national resource, and the export is controlled by the Ministry of Agriculture. The Behavioral Sciences Foundation is a not-for-profit research foundation, incorporated in Delaware and also established under the laws of St. Kitts and Nevis in 1968. It maintains laboratory and breeding facilities at the Estridge Estate on St. Kitts and has an affiliated institutional review board established under the principles of the Canadian Council on Animal Care. Other information about the St. Kitts vervet is available at our academic website at http://www.crcmgh.com/carib or by mail. Please contact fervin@caribsurf.com for further information.

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International Perspectives: The Future of Nonhuman Primate Resources Session 1: Panel Discussion Participants: Christian R. Abee—Session Chair, University of South Alabama, USA Mario J. Baudoin—Ministry of Sustainable Development and Planning, Bolivia Mukesh Kumar Chalise—Natural History Society of Nepal, Nepal Frank Ervin—McGill University, Canada Jason M. Mwenda—Institute of Primate Research, Kenya A. Jagannaha Rao—Indian Institute of Science, India Jurgen Seier—Medical Research Council, South Africa Mary Ann Stanley—Bioculture Mauritius Ltd., Mauritius QUESTIONS AND ANSWERS DR. ABEE (Christian R. Abee, University of South Alabama): Do you see a problem between conservation and providing animals for biomedical research? Is biomedical research likely to have an impact on indigenous populations worldwide? DR. SEIER (Jurgen Seier, Medical Research Council): It is not a problem from a South African perspective, in terms of baboons and the vervet monkeys. I think the numbers are very stable and common in many areas. There are many more animals destroyed as agricultural pests. DR. ABEE: Do you believe that each of your countries is sensitive to the issue of conservation with respect to primates?

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International Perspectives: The Future of Nonhuman Primate Resources DR. ERVIN (Frank Ervin, McGill University): Yes. We have, for example, set up sanctuaries, which are tourist attractions. Tourists love to look at monkeys; they are cute. We put the monkeys where the tourists are and took them away from where the agriculture is. We have made the monkey a stamp feature so there is a series of stamps on the St. Kitts vervet. There is a general array of procedures. We give lectures in the school system so there are ways of making this an important part of the culture. At the same time, it is one that has to be brought under control. On our island, they are like rats in Harlem. They really are not cute. DR. BAUDOIN (Mario Baudoin, Ministry of Sustainable Development and Planning): There is also a positive relationship between use and conservation that is very often forgotten. If you can give value to an ecosystem by using some of its components, you contribute not only to the conservation of those components but also to those things that will never have economic value. One major difference is between the existences of a wild population versus the use of captive breeding, which I do not think are complementary. They are not mutually exclusive. DR. VANDEBERG (John VandeBerg, Southwest Foundation for Biomedical Research): First, I would like to congratulate the panel on a superb job. You answered all of the questions that we asked you to answer, and I really appreciate the care that you invested in developing your presentations, which were all very clear and very concise. Second, I want to ask the representatives of the countries that have banned the export of primates about the rationale of their governments. That is, clearly there is a need for monkeys from some of these countries today—the baboons and vervets—and there may well be the need for the introduction of more monkeys from Africa in the future. We have heard about the animals being poisoned and shot as pests, so I would like to understand why the governments are against the exportation of these animals for research. DR. ABEE: Could I suggest that Dr. Rao speak first? DR. RAO (A. Jagannadha Rao, India Institute of Science): I think one of the major problems is that all active export will probably not be restricted, which will contribute to their decline. In India, this situation started because there was no distinction in terms of animals being pests, being poisoned, or being killed. Actually, in fact, as I quoted in one of the presentations, there are now more of them than before. Still, they are very much revered and they are not harmed. Their export in large numbers caused their number to decline, caused the rhesus to be considered only in terms of conservation, and caused the export to be banned. Actually, the current numbers are quite large and they can be used differently, with very judicious use. However, now we have more regulatory problems rather than conservation problems.

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International Perspectives: The Future of Nonhuman Primate Resources DR. MWENDA (Jason Mwenda, Institute of Primate Research, Kenya): To clarify, the Kenyan government banned the export of primates for reasons relating to the humane handling of the animals. Commercial handlers had been selling the primates under the lead of the experienced. There was an outcry of animal rights because the commercial exporters of primates were not handling the animals humanely. The second reason was to encourage research to be conducted in the country. The government believed that having research done in Kenya rather than exporting the primates would contribute more to technology transfer. DR. BAUDOIN: I was involved with drafting the 1987 disposition that banned wildlife trade. The situation was totally different from what it is now. There was very, very heavy trading in cats, for example. We had never had very strong national law enforcement because it is a huge country; however, the situation has changed now. The ban authorizes use on a species-by-species basis if enough information exists to warrant a decision. It is possible to develop the studies and study densities and then to propose the use. I think the problem now has moved to a different arena. The animal rights discussion has biologists scared to approve those studies that would say, “yes, go ahead and use.” So it has become a little more difficult, but I think it could be done. DR. MCGREAL (Shirley McGreal, International Primate Protection League): I have a question for Dr. Rao and Dr. Chalise. As you know, India banned export of monkeys because of concern over the end use in military experimentation, such as radiation and bio-warfare, which is increasing in our country now but was against the Hindu tradition. Do you believe now, Dr. Chalise, that the Hindu tradition is not strong in Nepal and that Nepal would tolerate exports? My question for Dr. Rao is whether India still maintains a concern about end use in military experimentation on monkeys? DR. CHALISE (Mukesh Kumar Chalise, Natural History Society of Nepal): Our concern is in the biomedical research, which the Natural Society has proposed and for which we are in the process of requesting approval. The proposal consists of four major points. Biomedical research is one of the components, which includes the conservation research and training program. We are specifically writing proposals that will not disturb the wild population, and we will use some of the animals to produce the offspring—only the offspring that we are utilizing. We have also assured the government that we will return the animals to the wild population. In addition, we will collect those required individuals only from the problematic areas. As far as the Hindu concern, it depends on the committee. Nepalese comprise mostly Hindus; however, there are so many different groups

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International Perspectives: The Future of Nonhuman Primate Resources (we say “class systems”), and only very traditional Hindus believe such matters are religious. I think that if we are honest in our writing and our actions, there will be no problem with the people’s religious belief. Furthermore, it will help the Nepalese people and export to develop conservation. I am hoping to collect monkeys from the problematic areas and put them in the hands of the Nepalese government school of the conservation. Currently, there is a conflict of ideas between the government, conservation enthusiasts, and the ideas and interests of the people regarding the perfect areas. People sometimes ask whether the government has a greater need for its wild animals or its people? We must think about the conservation issues because people become angry at the idea of conserving the monkey. It is very different from India. DR. SEIER: I would like to comment on the question regarding transportation and government policies. In the case of South Africa, it was not at all a government policy. It was also not an animal welfare consideration. South African Airways is a government organization in a sense, but they do make their own business decisions. Essentially, they are autonomous from the government in business. Their most lucrative routes are to Europe, where they do not wish to be targeted by animal rights people, and political people, by transferring primates. I do know and have copies of communication from UK animal rights people to South African Airways in which they were asked to state whether they are in principle willing to or currently transporting primates for biomedical research. I believe those groups write to every airline. That is the main reason they are not going to sacrifice their most lucrative business by taking a stand on transporting primates for biomedical research. We are talking not about trading but about even transfers of small numbers to other research organizations that need vervet monkeys. We have addressed this issue occasionally from Europe and the United States, that they are needed because they are free of SIV and other pathogens. This reason, not so much a government decision, formed the basis. DR. RAO: As for the question about the animal activists, if you can strike a dialogue with them, I do not think India will see a problem with the society in terms of using animals for biomedical research. Some of you might have seen recent newspaper accounts that the rhesus is very afraid of the langur. There is a need to see that the animals are removed from these areas and are repopulated elsewhere so they are not a menace. The major problem is to convince these agencies that they can relocate there and will be judiciously used. Unfortunately, under our current situation, no dialogue is possible. Otherwise, it would be possible to use enough rhesus for biomedical research or to allow other agencies from other countries to obtain them for use in separate established laboratories so that eventually the restric

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International Perspectives: The Future of Nonhuman Primate Resources tion could be lifted and they could be exported. I would like you to be aware that we are attempting to handle this major problem in our available animals. DR. ABEE: I was struck by Dr. Baudoin’s comment about creating a sense of value among the indigenous people. It seems to me that it is difficult to communicate the concept of conservation to people who are living day to day, trying to find enough food to survive. I believe this concept of creating value for the forest to conserve the fauna and flora is very important. I wonder if you have anything further you would like to say about that? DR. BAUDOIN: I think the problem is very simple. If you have a person in front of a tree, he must make a decision without considering 100% of the biodiversity in the forest. However, it is certainly much better than total replacement of the ecosystem by a much simpler system. Unless we can give value (in the sense of economic value) to some of the components of the forest, the person does not have much of a choice. PARTICIPANT: I understand there was a great amount of concern over the high price of certain kinds of tropical butterflies and that the Japanese and the Germans, in particular, who were collecting these butterflies, were suspected of depleting the national population of these butterflies. Some studies that were done to look at this found that the net effect of all this butterfly collection was actually extremely positive. It reduced the rate of deforestation. If you think about it, 9 months of hard agricultural/burn labor or a couple of weeks in the forest with a butterfly net yields the same net income for the people actually doing the catching. Obviously, insects reproduce much faster than monkeys; however, there was no detectable negative impact except in a couple of very localized areas on the populations of these animals. So I think that one way of approaching this concept of sustainable extract is that in fact, you are preserving the ecosystem by enhancing the value that exists to the people that live there. MR. BAULU (Jean Baulu, Barbados Primate Research Center and Wildlife Reserve): I would like to comment on the problems Dr. Seier described with airline transportation and so forth. We in Barbados produce at least 800 monkeys a year on average and 80% of the world’s polio vaccine through the monkeys’ kidneys that we send or the monkeys themselves. We had a problem with Air Canada, which just decided arbitrarily to ban the shipping of monkeys. We took them to court and after 3 years, we won. So when you really care about what you are doing and you have a good reason, you take them to court—it is as simple as that. I know that everybody here has problems with airlines. I believe we need to form a coalition of some kind and bring them one by one to court—because we will win.

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International Perspectives: The Future of Nonhuman Primate Resources DR. ROSENTHAL (Josh Rosenthal, NIH Fogarty Center): We have been working for several years to develop systems of sustainable use of biodiversity, in our case, plants and microorganisms for pharmaceuticals development and benefit sharing schemes to provide incentives for conservation. With success in some areas and less success in others, part of the key to those kinds of schemes is having mechanisms that relate relatively near term income to the people who are truly likely to be users of the resources. This task would be quite complicated, particularly with not very highly structured societies in a difficult regulatory environment; yet it is basically a good idea. One critical point that comes to my mind is that the situation with monkeys as an important pest in agricultural environments relates to a key information need. Very good documentation of those effects and an effort to get that message out to the public in a regular way would be one way of combating the very canalized interests of animal rights groups who then work against the airlines and other kinds of interests to promote use. MR. GRIFFITHS (Owen L. Griffiths, Bioculture Ltd.): I would like to add something to this theme about biodiversity, primates, and conservation and to clarify Dr. Stanley’s allusion. In Mauritius, for every monkey that is exported, the government of Mauritius collects $50 US. As you can see from Dr. Stanley’s figures, about 5000 monkeys are exported by our group of companies, totaling a quarter of a million US dollars every year and going straight to the national parks conservation fund that runs conservation projects in Mauritius and includes weeding native forests, getting rid of exotics, and building predator fences to keep out (so far) pigs and deer. It is a fundamental part of the conservation program in Mauritius. It is always very frustrating for us that although animal rights people, specifically from the UK, claim to be conservationists and say, “ban the use of monkeys, ban the export of monkeys from Mauritius”; yet this quarter of a million dollars a year is simply fundamental to conservation in Mauritius. Clearly there is no other equivalent source of funds available. DR. ERVIN: To reinforce Mr. Griffiths’ point, I think that nearly everyone who lives in this situation is aware of it, and it is similar on St. Kitts. For each exported monkey, a levy is paid into a special fund within the Department of Agriculture that goes to conservation, research, and education. Each farmer from whose farm a trapper collects monkeys not only has his crop protected but also receives a percentage of the trapper’s fee. So we now turn this country’s worse predator into a cash crop from which we are selling the weeds—and at a good price so that everyone at every level can understand and benefit: immediately in terms of cash, and abstractly in terms of knowing, because of work in the schools and the

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International Perspectives: The Future of Nonhuman Primate Resources newspapers that this monkey is making possible our understanding of a major brain disease or hypertension. DR. ABEE: And I think on the side of the biomedical research community, that the biomedical research community is very pleased to hear that this possibility will result from the money being generated from this. DR. LYONS (Leslie A. Lyons, California National Primate Research Center): I think Dr. Mwenda made a very important point that some of the exportations have stopped because of a desire to keep research in the countries where the animals are. Does the panel think that perhaps if the NIH or the US government invested more in training for the countries, that we could open up exportations a little bit more as a give and take to help get animals back and forth? DR. RAO: I think there is one step toward using the situation. There is a strong feeling by conservation biologists as well as animal activists that the animals are being used as a cash crop, proving that the best thing is to develop a system of centers with organizational help, such as what NCRR attempted in Bombay. Once people understand how useful they are, they will probably support the decisions, and exporting will be possible. DR. LYONS: Additionally, perhaps while we are waiting for the possible change of exportation laws, we can change the thinking of our researchers. How would we propose to have more researchers think more about vervets than macaques? DR. ERVIN: They need to be better educated. DR. ABEE: Actually I thought Dr. Ervin did a very good job of that already. I would probably buy life insurance from him also. I would like to thank all of our speakers for coming so far to share their thoughts with us. I think this session has been excellent. Thank you.