Role of the Zoo Veterinarian in the Conservation of Captive and Free-Ranging Wildlife S

ZOO VETERINARIANS AND CONSERVATION 3

Int. Zoo Yb. (2007) 41: 3–11 DOI:10.1111/j.1748-1090.2007.00020.x

Role of the zoo veterinarian in the conservation of captive and free-ranging wildlife S. L. DEEM Research Veterinarian, Department of Animal Health, Smithsonian National Zoological Park, Washington, DC 20008, USA E-mail: [email protected]

The challenges to execute wildlife conservation projects for populations. Now, as zoos expand their successfully have become more complex as anthropo- role in conservation efforts and move conser- genic changes continue to stress the planet, changing wild lands. As the wild becomes less so, more species are vation outside their ‘walls’ with an increasing placed in captivity to improve their chances of long-term number of projects directed at the conservation survival, while concurrently management (and medicine) of populations in situ, the zoo veterinarian’s for free-ranging wildlife has become increasingly impor- role has also expanded. In addition to the tant. A variety of disciplines, including veterinary medi- health care provided to captive animals, zoo cine, is now recognized as key to wildlife conservation. Although veterinarians have been involved in conserva- veterinarians today have a number of roles tion for decades, it is only recently that their role has within in situ conservation projects that ensure become more appreciated in the larger conservation the maintenance of healthy and viable free- community. This realization of the contributions of ranging populations of wildlife. veterinarians has occurred at a time when disease has been recognized as significantly impacting species’ con- The commitment of zoos to conservation servation both in situ and ex situ. Today, veterinarians efforts and the development of the discipline work with captive and free-ranging animals to prevent of conservation biology are primarily and/or treat diseases that threaten species’ survival. Most responses to the current conservation crisis. of these diseases are associated with the increasing Unlike past extinctions, this ‘sixth extinction’ human footprint. In this paper, I present wildlife health in today’s world and the zoo veterinarian’s role in wild- (Leakey & Lewin, 1996), in which we are life conservation. losing species at a rate 100 to 1000 times above the ‘normal’ level (Pimm et al., 1995), Key-words: conservation; disease; health; species; is related to human activities that have wildlife; zoo veterinarian. resulted in habitat fragmentation and degradation, isolation of species and an increased INTRODUCTION contact between wild animals, domestic Veterinarians have played a key role in con- animals and humans. Zoo personnel have servation efforts carried out by zoological responded to this extinction crisis. Many of parks (zoos) for many decades. For the pur- the activities performed by zoos today are pose of this paper, ‘zoos’ refers to accredited devoted to ensuring the long-term survival of zoos, such as the more than 200 zoological wildlife. Within this directive, the role of the facilities in North America accredited by the zoo veterinarian has also expanded to address Association of Zoos and Aquariums (AZA) the health needs of wildlife populations, both and the 300 member facilities in the European in captivity and in the wild. Association of Zoos and Aquaria. Tradition- In conjunction with the current extinction ally, the zoo veterinarian’s role focused on crisis, wild places containing ‘wild’ animals, ex situ populations, ensuring animal health untouched by humans and/or human activ- and welfare for captive animals by applying ities, are now hard to find. In fact, it has been therapeutic medicine for individuals and, more noted that few species exist today that have recently, preventive and therapeutic medicine not been influenced by some form of human

Int. Zoo Yb. (2007) 41: 3–11. c 2007 The Zoological Society of London US Federal Government. 4 ANIMAL HEALTH AND CONSERVATION intervention (Redford & Richter, 1999). In this paper, I present the historical and Additionally, in the last few decades it has current roles of zoo veterinarians in conserva- become increasingly clear that the impact, and tion, and offer suggestions of how to integrate potential impact, of disease on conservation the health sciences into conservation initia- efforts must be factored into the conservation tives. Although the focus of this paper is on equation (Dobson & Hudson, 1986; May, the role of zoo veterinarians in wildlife 1988; Scott, 1988; Thorne & Williams, 1988; conservation, the distinction between the Daszak et al., 2000; Deem et al., 2001; ‘zoo’ and ‘wildlife’ veterinarian has become Cleaveland et al., 2002). Examples of diseases increasingly less clear and many veterinarians with known significant conservation implica- can be viewed as ‘zoo and wildlife’ veterinar- tions include canine distemper virus in a ians. Additionally, many ‘non-zoo or wildlife’ number of carnivore species (Deem et al., veterinarians employed in private practice, at 2000), fibropapillomatosis in sea turtles universities, in non-profit organizations and (Herbst, 1994), worldwide amphibian declines within Governments play significant roles in associated with a fungal agent (Daszak et al., conservation. 1999), Ebola in great apes (Walsh et al., 2003) and West Nile virus in free-ranging and THE CHANGING REALITY OF THE captive wild birds (Ludwig et al., 2002). WILD As reviewed by Woodroffe (1999), there are several species that have experienced near In today’s world, it is hard to define the word extinctions associated with disease, including ‘wild’ as it pertains to wildlife. Is the recently the Black-footed ferret Mustela nigripes, confiscated Jaguar Panthera onca now held Bighorn sheep Ovis canadensis, African wild at a zoo in Latin America wild? Is the African dog Lycaon pictus and the Ethiopian wolf elephant Loxodonta africana just immobi- Canis simensis, probably because small lized for telemetry collar placement in Kruger populations are particularly vulnerable to National Park, South Africa, wild? Is the external factors, including infectious dis- third-generation Western lowland gorilla eases. Additionally, the first report of an Gorilla gorilla gorilla held at a zoo in North infectious disease causing the extinction of a America wild? Or, is the Black-footed ferret species, the Land snail Partula turgida, has captive bred and identified for release to been confirmed (Cunningham & Daszak, nature, wild? If one considers the role of 1998), and there is now strong evidence of veterinarians in wildlife conservation, it is disease being the proximate and ultimate important to also consider the changing reali- cause of extinction in a species in the ties of the wildlife for which they provide wild (Sharp-snouted day frog Taudactylus care. acutirostris: Schloegel et al., 2006). The above questions exemplify the grey As part of the team to address these zone that exists for veterinary care of an disease-related challenges, veterinarians have animal we call wild and one we call captive. unique skills, training and experience that As conservation projects include the mainte- contribute to conservation programmes, both nance of some species, on the brink of ex situ and in situ. In addition to their extinction, with captive propagation for in- basic training in veterinary medicine, most tended release to the wild (e.g., Black-footed zoo veterinarians have a degree in animal ferrets and Bali mynah Leucopsar rothschildi), husbandry, biology, conservation biology the captive and wild populations effectively or zoology, and advanced training in a become one regarding health status. Simi- subspecialty of the medical profession. larly, with the growing support of ecotourism Wildlife-health-related subspecialties include projects, bringing humans in closer contact anaesthesiology, clinical medicine, epide- with free-ranging animals, as exemplified by miology, nutrition, pathology, theriogenology species such as the Mountain gorilla Gorilla and toxicology. beringei beringei (Cranfield et al., 2002), the

Int. Zoo Yb. (2007) 41: 3–11. c 2007 The Zoological Society of London US Federal Government. ZOO VETERINARIANS AND CONSERVATION 5 possibility of infectious-disease transmission environments. Zoo veterinarians applied (as and impacts on the conservation of the spe- they continue to do today) diagnostics and cies increase. therapeutics to captive animals as a means of Pressures on wildlife health from proxi- ensuring good health and long lives. Addi- mity to domestic animals have also led to tionally, veterinarians historically (as they recent epidemics among threatened species. continue to do today) were instrumental Some of the best-documented cases are in animal-welfare issues being properly studies on African carnivores and include addressed within zoos (Miller, 1992). rabies in the Ethiopian wolf (Laurenson In the past, the division between the zoo et al., 1998), rabies and canine distemper in veterinarian caring for the individual animal the African wild dog (Alexander & Appel, in captivity and the wildlife veterinarian, 1994; Kat et al., 1996), and canine distemper focusing on free-ranging wildlife popula- in Lions Panthera leo (Roelke-Parker et al., tions, was often very clear. These veterinar- 1996). Conversely, zoo animals are often ians, working in zoos or on free-ranging exposed to pathogens carried by feral domes- wildlife issues, would rarely overlap in their tic animals and/or free-ranging wildlife efforts directed at species’ conservation. Zoo including the agents that cause leptospirosis, veterinarians provided veterinary treatments rabies and canine distemper, which often for individual sick animals in cages while result in morbidity and mortality within the wildlife veterinarians focused on diseases zoological setting (Rupprecht, 1999; Deem of wildlife as they related to the health of et al., 2000; Bolin, 2003). domestic species (e.g. cows, pigs, chickens) With much of the Earth’s wild lands now in contact with wildlife, game animals (e.g. little more than very, very large zoos, zoos too deer, ducks) and/or zoonotic diseases (dis- have changed. Zoos today often have multi- eases transmissible from animals to humans), species exhibits, enclosures with more natural such as rabies, brucellosis and tuberculosis habitats and with more possible connections (Friend, 1976). Additionally, the primary role between captive and wild animals as a result of wildlife veterinarians was often only put of strategies such as captive reproduction and into action for the management (conserva- reintroduction programmes. Animals living tion) of populations experiencing disease in both these situations (captive and wild) epidemics associated with high mortality. In have been influenced by humans and may in the more recent past, we find zoo veterinar- fact now require veterinary intervention for ians providing care for animals in multi- their survival. species exhibits in captivity and directing much of their efforts towards preventive medicine on populations both in captivity THE EXPANDING ROLE OF THE ZOO and in the wild, while wildlife veterinarians VETERINARIAN may be called upon to care for an individual of a highly threatened species. Historical As a conservation tool, healthy captive ani- Present mals in zoos have been the ambassadors for their species, educating and inspiring people Zoological parks have become increasingly to care about wildlife conservation. Histori- important players in the conservation effort. cally, the zoo veterinarian’s role in conserva- No longer menageries for wild animals and tion focused on the health care of these centres strictly for public entertainment, individual captive animals. The success of zoos are now conservation centres. Many maintaining wild animals in captivity has of the activities of the ‘new’ zoo (conserva- been largely a function of our ability to tion centre) are to ensure both in situ (e.g., provide adequate nutrition and health care species’ viability and protection) and ex for these captive animals living in artificial situ (e.g., captive-reproduction programmes)

Int. Zoo Yb. (2007) 41: 3–11. c 2007 The Zoological Society of London US Federal Government. 6 ANIMAL HEALTH AND CONSERVATION conservation efforts globally. Along with this TAGs within the AZA in North America, a changing philosophy of zoos, has come an veterinary advisor is a member of approxi- expanding role for zoo veterinarians within mately three-quarters of these programmes, conservation efforts. In fact, advances in ve- providing expert opinion and input on health terinary medicine (e.g., anaesthesia, diagnos- issues (www.aza.org). Additionally, several tics and medical management) have been key SSPs also have veterinary-pathologist advi- for zoos to develop into the conservation sors and other health professionals (e.g., centres they are today. Veterinarians are one nutritionists, reproductive physiologists) component of the conservation team that who contribute to the health care of these remains instrumental for providing preventive species. and therapeutic medicine, and inspector func- It is beyond the scope of this paper to tions that help ensure the proper psychological provide a complete review of all the speciﬁc well-being, husbandry, nutrition and health diseases of captive wildlife and the role of care of the animals maintained in zoos (Miller, zoo veterinarians in the management of these 1992). However, veterinarians have moved diseases. To gain an appreciation of these beyond these traditional (and vital) roles to issues, readers are directed to have a look at include a number of other essential functions the many volumes of the Zoo and Wild for wildlife conservation in situ and ex situ. Animal Medicine textbook (e.g., Fowler & Miller, 2003) and the Journal of Zoo and Captive wildlife Veterinarians, who are inte- Wildlife Medicine, which has been published gral members of staff at many zoos, provide for 38 years (http://www.aazv.org/). A few preventive and therapeutic medicine for examples of major diseases that have hin- captive animals. Ensuring that captive zoo dered captive wildlife propagation for which animals have proper health is essential if their zoo veterinarians have directed much educational value and use as reproductive research include elephant endotheliotropic stock for species’ conservation is to be herpesviruses (Richman et al., 2000), toxo- maintained. Moving beyond the individual plasmosis in Pallas’ cats Otocolobus manul animal, zoo veterinarians now direct much (Basso et al., 2005), iron overload in a of their efforts at preventive medicine for number of birds and mammals (Lowenstine captive populations, thus minimizing the & Munson, 1999) and chytridiomycosis in need for treatment of an individual animal by amphibians (Nichols et al., 1998; Daszak decreasing the transmission of infectious and et al., 1999). parasitic agents. Preventive medicine has also As the role (to manage diseases of captive allowed species maintained at more than one animals) of zoo veterinarians expands, so too zoo to be managed as ‘one’ population. By does the contribution of zoo veterinarians to providing preventive medicine for species the signiﬁcant advances in diagnostic cap- that undergo an increasing number of abilities, anaesthesia, vaccination options, inter-zoo loans and movements, the zoo reproductive technologies and improved veterinarian helps to ensure the successful nutrition and therapeutics of these captive propagation of these populations on a scale animals. greater than any one zoo can provide. A prime example of the ‘one population’ approach in zoos today is the establishment The captive and free-ranging wildlife since the early 1980s of zoo-based Species interface As noted above, the line separating Survival Plans (SSP) and Taxon Advisory captive and wild (free-ranging) populations Groups (TAG) for wildlife conservation. is no longer distinct. Programmes such as These programmes were designed to provide wildlife rehabilitation, reintroduction and cooperative population management of a translocation all highlight the fact that the number of the most highly threatened species. health of captive and wild populations is Of the currently more than 100 SSPs and 46 often intimately linked.

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Providing rehabilitation and medical care Free-ranging wildlife Many conservation ef- to confiscated and injured free-ranging forts are now directed at maintaining the wildlife is a controversial conservation tool. population viability of wildlife in situ. However, many zoos offer this service at their This should remain a primary goal of hospitals. If one considers that the majority of conservation. As we move forward with the free-ranging animals admitted to zoo ve- in situ conservation initiatives, it has also terinary hospitals are there as a result of human become increasingly evident that disease and activities, such as confiscation from the illegal health concerns are a significant threat to animal trade, intoxication from pesticide successful conservation (Scott, 1988; Daszak application or vehicle-related injuries, many et al., 2000; Deem et al., 2001). While zoos members of zoo staff feel a responsibility to expand their in situ conservation efforts, care for these injured individuals. Beyond the and disease becomes more of an issue for individual animal, an important benefit of wild populations, the role of zoo veterinarians animals cared for in these programmes is their as integral members of these in situ role as sentinels of ecosystem health (Sleeman conservation projects has also expanded. & Clark, 2003), often alerting zoo veterinar- Decisions about the level of veterinary ians to disease issues in the free-ranging involvement in any in situ project should be wildlife around their zoo. based on: (1) the status of the species or Many conservation efforts have focused population affected or at risk; (2) the nature on captive propagation for subsequent release of the cause of the health problem, which (e.g., reintroduction) and translocation requires veterinary investigation; (3) the schemes to move animals to ‘safer’ havens. spatial distribution of the species; (4) the Zoo veterinarians are instrumental in such cost and practicality of necessary preventive efforts. There are many examples of past and treatment measures; (5) specific disease animal movements that have resulted in ser- issues of concern; (6) implications of ious wildlife disease problems owing to a intervention or lack thereof on the health lack of health concerns addressed before of other species, including humans and project implementation (e.g. see Meltzer, domestic animals (Deem et al., 2001). 1993; Woodford & Rossiter, 1993; Cleave- Above all else, veterinarians in wildlife land et al., 2002). The ability to move ani- conservation should ‘do no harm’. mals from captive-breeding programmes to In some cases, it may be appropriate to the wild and between various sites is apply therapeutic measures to an individual one conservation tool that demands that animal within its natural environment. Exam- health concerns be addressed to minimize ples of direct in situ veterinary intervention the disease threats associated with these for the individual animal have primarily programmes (Woodford, 2001). involved highly Endangered species (e.g. Zoo-based programmes, such as the SSP rabies vaccination of African wild dogs and TAG programmes mentioned above, fo- and snare removal of Mountain gorillas) cus efforts on in situ, as well as ex situ, (Gascoyne et al., 1993; Cranfield et al., conservation of wildlife. A number of veter- 2002; IUCN, 2006). These interventions are inarians within these programmes work on in response to human-induced situations, health issues of both captive and wild popula- such as rabies transmitted by domestic dogs tions of the species for which they are re- to African wild dogs and snare hunting within sponsible. One example of this dual role of a Mountain gorilla home ranges. In such cases, SSP veterinarian is the Jaguar SSP in which direct individual animal care in the wild the veterinary advisor has incorporated health is warranted as the conditions are human care for both the AZA captive population and induced, few individuals of the species Jaguars living in situ through training, hands- exist today and the extinction of the on research and publications (Deem & species is highly probable without inter- Karesh, 2002; Hope & Deem, 2006). vention.

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The fragmentation of landscapes with the these conservation strategies may facilitate the associated isolation of species onto ‘artificial transmission of diseases between humans, islands’ is another land-use change that domestic animals and wildlife by an increased often requires wildlife management (and direct, and indirect, contact between these medicine). As our continents becoming groups. Veterinary interventions to minimize increasingly divided by development, threa- disease transmission to wildlife associated tened species find themselves confined to with these strategies may include implement- small areas (artificial islands) with no routes ing preventive medicine programmes, includ- for emigration. Challenges for the long-term ing vaccination of humans (e.g., for non- conservation of these species are evident human primate conservation) and domestic when one considers the historical records of carnivores (e.g., for rabies, canine distemper species’ extinctions, many of which were and other canid pathogens) in these regions associated with disease, on geographical (Wallis & Lee, 1999; Fiorello et al., 2006). islands (Quammen, 1996). For example, Zoo veterinarians, with their knowledge of although the biological diversity of islands is animal diseases, zoonoses and species suscept- a small percentage of the world’s total, of the ibility, are instrumental in such projects. recorded number of invertebrate and verte- Thereareanumberofreviewsandpapers brate extinctions that have occurred since the on the diverse contributions of zoo veterinar- 1600s, 367 have been island species and only ians, and veterinary medicine in general, for in 124 have been continental species (Smith situ wildlife conservation. Among these con- et al., 1993). The most well known of these tributions are the acquisition of much-needed extinctions is the loss of multiple Hawaiian baseline health data, animal immobilization land birds associated with avian diseases and handling for ecologic studies, manage- (Van Riper et al., 1986). ment of wildlife diseases within park borders, Artificial islands are being developed by veterinary integration within the policy arena human activity (e.g., fencing, development to ensure that health issues are addressed in and roads) that divide and separate species park planning and conservation programmes, into smaller, isolated populations with similar rapid response to epidemics within threatened geographic and biologic constraints of popu- species’ populations, studies on domestic-ani- lations on ‘real’ islands. Modern examples of mal reservoirs, the proper research and man- the threat of disease associated with land agement approaches to zoonotic pathogens fragmentation can be found in many species associated with possible wildlife reservoirs living in National Parks throughout North and control efforts for confiscated, rehabili- America (Gillin et al., 2002), in Buffalo tated and nuisance animals (for select reviews, Syncerus caffer in Kruger National Park, see Hutchins et al., 1991; Porter, 1992; Karesh South Africa (Keet et al., 1996), as well as & Cook, 1995; Deem et al., 2001; Cranfield for a number of the most threatened species et al., 2002; Gillin et al., 2002; Deem, 2004). on the brink of extinction today, partially owing to disease (as reviewed by Woodroffe, 1999; Cleaveland et al., 2002). CONCLUSIONS A growing number of conservation projects now focus on ‘buffer zones’ around Zoo veterinarians have played a vital role in national parks and on ecotourism projects wildlife conservation for many decades, with within parks. Buffer zones often allow this role fully accepted for the health care of domestic animal grazing, and in some cases captive wildlife and increasingly accepted ensure sustainable hunting of wildlife, while within in situ wildlife conservation projects. protecting wildlife within park boundaries. As the veterinarians’ roles in ex situ and Ecotourism projects bring people into ‘pris- in situ health care are being realized, the tine’ areas, allowing close association of distinction between captive and wild animals people and wildlife. Unfortunately, both of has also become less clear.

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Wild places, containing ‘wild’ animals un- National Reserve, Kenya. Journal of Wildlife Diseases affected by human activities, are now hard to 30: 481–485. BASSO, W., EDELFOFER, R., ZENKER, W., MOESTL, K., find. In fact, few species exist today that have KUEBBER-HEISS,A.& PROSL, H. (2005): Toxoplasmosis not been influenced by some form of human in Pallas’ cats (Otocolobus manul) raised in captivity. intervention. Today, there is a place for using Parasitology 130: 293–299. wildlife health skills for the prevention and BOLIN, C. A. (2003): Leptospirosis. In Zoo and wild animal medicine: current therapy (5th edn): 699–702. treatment of disease in wild animals in situ. Fowler, M. E. & Miller, R. E. (Eds). Saint Louis, MO: Wildlife health is crucial for wildlife conserva- W. B. Saunders. tion, and the skills and knowledge that veter- CLEAVELAND, S., HESS, G. R., DOBSON, A. P., LAURENSON, inarians have, ranging from anaesthesia and M. K., MCCALLUM, H. I., ROBERTS,M.G.& WOODROFFE, clinical skills to knowledge on disease ecology R. (2002): The role of pathogens in biological conservation. In The ecology of wildlife diseases: 139–150. and epidemiology, allow them to play a vital Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, role in conservation initiatives. H. & Dobson, A. P. (Eds). New York, NY: Oxford With the current trends of human population University Press. growth, land fragmentation and degradation, CRANFIELD, M., AFFIKIN, L., SLEEMAN,J.& ROONEY,M. (2002): The mountain gorilla and conservation medicine. and increased contact between wildlife, domes- In Conservation medicine: ecological health in practice: tic species and humans, veterinarians are 282–296. Aquirre, A. A., Ostfeld, R. S., Tabor, G. M., necessary members of any multidisciplinary House, C. & Pearl, M. C. (Eds). New York, NY: Oxford approach to conservation. The efficiency and University Press. effectiveness of conservation efforts are signifi- CUNNINGHAM,A.A.& DASZAK, P. (1998): Extinction of a species of land snail due to infection with a microspor- cantly enhanced by incorporating animal health idian parasite. Conservation Biology 12: 1139–1141. considerations into the planning, implementa- DASZAK, P., BERGER, L., CUNNINGHAM, A. A., HYATT,A. tion and evaluation phases of all programmes D., GREEN,D.E.& SPEARE, R. (1999): Emerging infec- (captive and wild) involved in conserving wild- tious diseases and amphibian population declines. Emer- life. One tenet of medicine that should be ging Infectious Disease 5: 735–748. DASZAK, P., CUNNINGHAM,A.A.& HYATT, A. D. (2000): considered in the conservation equation is that Emerging infectious diseases of wildlife: threats to prevention is always better than the cure. biodiversity and human health. Science 287: 443–449. Maintaining healthy, viable populations as op- DEEM, S. L. (2004): The veterinarian’s role in conserva- posed to treating (saving) the last individual of tion. Journal of the American Veterinary Medical Asso- ciation 225: 1033–1034. a species makes the most sense. DEEM,S.L.& KARESH, W. B. (2002): The veterinarian’s It is nearly impossible to predict all the role in species-based conservation: the jaguar (Panthera future roles of zoo veterinarians (and other onca) as an example. Proceedings of the American conservationists) in tomorrow’s world, just as Association of Zoo Veterinarians 2002: 1–5. DEEM, S. L., SPELMAN, L. H., YATES,R.A.& MONTALI,R. it would have been hard to predict 50 years J. (2000): Canine distemper in terrestrial carnivores: ago the world we find ourselves in today. The a review. Journal of Zoo and Wildlife Medicine 31: world is changing too quickly and the stresses 441–451. on wildlife are too great. One thing is clear. It DEEM, S. L., KARESH,W.B.& WEISMAN, W. (2001): will take all the conservation disciplines, Putting theory into practice: wildlife health in conservation. Conservation Biology 13: 1246–1256. including veterinary medicine, to handle the DOBSON,A.P.& HUDSON, P. J. (1986): Parasites, disease current and future challenges. and the structure of ecological communities. Trends in Ecology and Evolution 1: 11–15. FIORELLO, C. V., NOSS,A.J.& DEEM, S. L. (2006): ACKNOWLEDGEMENTS Demography, hunting ecology, and pathogen exposure The author thanks Ellen Bronson, R. Eric Miller, Nicole of domestic dogs in the Isoso of Bolivia. Conservation Savageau, Patti Young and three anonymous reviewers Biology 20: 762–771. for their helpful comments on this manuscript. FOWLER,M.E.& MILLER, R. E. (Eds) (2003): Zoo and wild animal medicine: current therapy (5th edn). St REFERENCES Louis, MO: W. B. Saunders. ALEXANDER,K.& APPEL, M. (1994): African wild dogs FRIEND, M. (1976): Wildlife diseases: philosophical con- (Lycaon pictus) endangered by a canine distemper epi- siderations. In Wildlife diseases: 7–18. Page, L. A. (Ed.). zootic among domestic dogs near the Masai Mara New York, NY: Plenum Press.

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