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SPECIAL CHALLENGES OF MAINTAINING WILD ANIMALS IN CAPTIVITY IN SOUTH AMERICA


*Published in Rev.sci.tech.Off.int.Epiz, 1996, 15 (1), 267-287



Zalmir Silvino Cubas
Foz Tropicana Bird Park

SUMMARY

The author summarises the occurrence of major diseases in wild animals maintained in captivity in South America. The epidemiology, impact and significance of the diseases are discussed, togheter with appropriate husbandry practices to control and prevent transmissible diseases. The following animal groups and pathologies are considered in this review:

  • Poxvirus dermatitis, gatroenteritis, pneumonia, amoebosis and coccidiosis in reptiles.
  • Management practices and diseases (including botulism, bacterial enteritis, psittacosis, aspergillosis and parasitic diseases in birds).
  • Enterocolitis, pneumonias and internal parasites in non-human primates.
  • Canine distemper, parvoviruses, babesiosis, internal and external parasites in carnivores.
  • Tuberculosis and enteritis in tapirs.
  • Haemorrhagic diseases in cervids.

KEYWORDS: Birds Carnivores Infectious diseases Non-human primates Reptiles South America Ungulates.

DIFICULDADES ESPECIALES DEL MANTENIMIENTO DE ANIMALES SALVAJES EN CAUTIVIDAD EN AMÉRICA DEL SUR.

RESUMEN

El autor resume la incidencia de las enfermedades más importantes sobre la fauna salvaje que vive en cautividad e América del Sur. Examina también la epidemiologia, impacto y significación de dichas enfermedades, así como las prácticas de cría adecuadas para el control y la prevención de enfermedades transmissibles. En este artículo se consideran las seguientes patologías y grupos de animales:

  • Dermatitis por poxvirus, gastroenteritis, neumonía, amebiasis y coccidiosis en reptiles;
  • Prácticas de manejo y enfermedades (incluidos el botulismo, enteritis bacteriana, psitacosis, aspergilosis y enfermedades parasitarias aviares).
  • Enterocolitis, nemonías y parasitismo interno en primates no humanos.
  • Moquillo canino, afecciones por parvovirus, babesiosis, parasitismo interno y externo en carnívoros.
  • Tuberculosis y enteritis en tapires.
  • Enfermedade hemorrágica en cérvidos.

PALAVRAS CLAVE: America del Sur Ave Carinvoires Enfermedades infecciosas Primates no humanos Reptiles Ungulados

OUTLINE

INTRODUCTION

South America boasts a tremendous diversity of wildlife, and a considerable amount of research on the biology of the different species remains to be done. The study of wildlife while in captivity has contributed greatly to our current biological knowledge, and zoos, wildlife breeding centers and research institutions are playing a vital role in this respect.

Projects relating to wildlife conservation and research have limited budgets in South America. Neverthless institutions have made considerable advances over the last decade. Most of the zoos in South America are maintained by municipalities or states or provincial governments, but the number of private ventures is gradually increasing. This is proving beneficial for conservation strategies and there is no doubt that the private sector and non government incentives have an important part to play in nature conservation.

Correct husbandry practices in order to prevent disease and to encourage animal reproduction is an essential aspect of the preservation of endangered species. The topic challenges of maintaining wild animals in captivity is a vast subject, and the objective of this brief review is to cover management practices and the occurrence and prevention of infectious and parasitic diseases in some animal groups.

* Foz Tropicana Bird Park, Caixa Postal 988, Foz do Iguaçu - PR

85863-000 - BRAZIL

REPTILES

Reptiles are ectothermic animals, which means that to maintain internal body temperature they need an external source of warmth. This direct dependence on environmental conditions makes reptiles very susceptible to improper husbandry practices. Metabolic processes, such as digestion of food and antibody production are dependent on adequate temperature. Sub-optimal ambient and body temperature impede the synthesis of antibodies. As a consequence opportunistic pathogens may invade tissues and cause disease.

Particular attention must be paid to basic housing conditions. Temperature is an important factor as already mentioned. Required humidity levels vary depending upon the species. Inadequate humidity can lead to impaired shedding of the old skin. Potentially hazardous pathogens can be disseminated through contaminated water. The photoperiod must be provided according to the biology of the species involved. Exposing captive reptiles to constant light results in severe stress. Newly wildcaught reptiles are particularly susceptible to diverse stress factors and may need a period of adaptation to the captive environment. Cage substrate ideally should not cause skin abrasion, nor be ingested causing obstruction and impaction; this material should preferably have good absorbancy, and not be a growing medium for bacteria. Cages should permit easy cleaning and disinfection.

Health status is also directly dependent on nutrition. Snakes, lizards, chelonians and crocodilians feed upon specific items. Scientific information on the nutritional requirements of reptiles should replace empirical feeding practices currently in use. Nutritional and metabolic diseases cause a high percentage of the losses in captivity. Nutritional disorders commonly seen are anorexia, inanition and dehydration associated with stress and maladaptation, metabolic bone disease, hypovitaminosis A in turtles, hypovitaminosis E - steatitis in crocodilians, gout and others.

Poxvirus dermatitis

An outbreak of poxvirus dermatitis was reported in a commercial caiman (Caiman crocodilus yacare) farm in Brazil. The incidence of the disease was 15% of 20,000 caymans, and affected animals 5 to 9 months old (22). The virus causes gray-white superficial skin lesions on the paws, palpebrae, maxillae and mandible. The disease is characterized by high morbidity and low mortality.

Bacterial diseases

A number of bacterial disease have been reported in this class of animals. Gram-negative bacteria are prevalent in the normal microflora of the digestive tract of reptiles, including Pseudomonas, Aeromonas, Klebsiella, Proteus. A serious disease of captive snakes is infectious stomatites, which in most cases is associated with unsuitable husbandry practices, malnutrition and decreased immune resistance.

In the Instituto Butatan, Brazil, necropsies in 805 snakes of the genus Crotalus and 301 Bothrops over a 30 months period indicated gastroenteritis and pneumonia as the most frequent causes of mortality. Restraint for constant venom extraction and maladaptation to captivity are considered to be the principal causes for the high mortality (13).

Omphalitis after birth and wounds caused by agonistic interactions are reported as serious problems on caiman farms in Brazil (15). Proper husbandry practices to prevent bacterial diseases are strict attention to the hygiene of the terraria and bedding material, providing good water quality, ensuring adequate food consumption, and removing all possible stress factors.

Parasitic diseases

The protozoan Entamoeba invadens, considered the most clinically significant parasite of snakes has produced epizootics with high mortality in several zoo collections in South America. The Boa (Boa constrictor) and the anaconda (Eunectes murinus) are species commonly infected.

Transmission of this highly infectious amebae to snakes and lizards is effected mainly by chelonians and crocodilians, considered resistant carriers for the Entamoeba sp. Amebiasis cause a severe necrotic enterohepatitis. Antemortem diagnosis is made by finding trophozoites or cysts in the stools of the affected snakes or by finding amebae in washings from the colon.

Recommended prophylatic measures to control and prevent the disease include strict quarantine for new arrivals, followed by 3 negative direct fecal examinations. Other reptiles, especially turtles and crocodilians, should never be kept with snakes, and the water supplies of these distinct groups of reptiles should also be kept separate. Affected animals must be immediately isolated and treated; contaminated cages must be disinfected. Preventive treatment with metronidazole before leaving quarantine has been suggested. An effective prophylaxis depends upon strict hygiene and water quality control.

Systemic coccidiosis were reported in caimans (Caiman latirostris) maintained in concrete tanks in Brazil. Eight adult caimans died over a 20 days period. Postmortem lesions were congestion of lungs, liver, spleen and kidneys, and hemorrhagic enteritis (3). Oocists of Isospora sp. can be found in caimans, but pathogenicity is considered low. Only stressed animals may develop the disease.

Several internal and external parasites are found in reptiles. Periodic physical examinations must be carried out to prevent diseases.

BIRDS

As they evolved, diverses groups of birds developed peculiar physiological and biological features. Providing general guidelines applicable to every group of birds is a challenging assignment, since peculiarities occur in every bird family. The primary focus of this review is to report some of the most important parasitic and infectious diseases of captive birds in South America and provide guidelines to health management.

A considerable number of avian deaths in captivity could be prevented by simply establishing basic good husbandry practices. Diseases, in general, can not be viewed as chance occurrences, but as a pathological process initiated by environmental, physiological or genetic factors detrimental to health. The more we understand the physiological necessities of animals in the captive environment, the better are the chances of achieving succesful long-term maintenance and reproduction. Good husbandry and preventive practices concerning disease must be enforced by those devoted to the conservation and reproduction of wild animals in captivity.

Management practices

Enclosures

Inappropriate aviary design favours the occurrence of accidents and diseases. It has been seen that many enclosures do not fulfil the basic needs of adequate space, shelter, privacy, security and hygiene. An aviary should provide protection against predators and adverse climatic conditions. Food and water containers should be located so that excrement contamination is reduced to a minimum. Perches should be secure and of adequate diameter for the size of the species exhibited. Nest boxes should be protected from rain and direct sunlight. Care must be taken that nesting material does not become a substrate for fungus growth. Aviary floors should always be laid with hygiene requirements in mind; a slight slope and a drainage system in the floor favour the removal of organic debris. Clean, fresh, uncontaminated water is a basic necessity for keeping birds healthy. Overcrowding may lead to agonistic interactions and deaths.

Preventive medicine program

Veterinarians should establish preventive medicine programs, which may vary according to the aviary design, the bird group involved, incidence of disease in the collection and geographic area. Quarantine procedures are mandatory to prevent the introduction of new pathogens into the collection. Preventive practices include periodic physical examinations, standard fecal examinations, periodic deworming, prophylaxis of clamidiosis, vaccination of populations at risk and control of rats and other vermin. All birds that die must be necropsied.

Hygiene and sanitation

Good hygiene is critical to the prevention and control of diseases. In the captive environment it is inevitable that there will be a concentration of organic debris and pathogenic organisms. Constant exposure of the birds to potentially pathogenic microorganisms increases the chance of infection and disease. Daily cleaning of aviaries is ideal, but in breeding colonies the constant human interference may reduce reproduction rates. Organic debris must be removed physically before using water hoses and disinfectants. When disinfection is necessary, sodium hypochlorite, quaternary ammonium and phenol are commonly used. Food and water bowls should be made of stainless steel, hard plastic or crockery to facilitate daily cleaning and disinfection.

Nutrition

An imbalanced diet represents a limiting factor in the reproduction of several species of birds in captivity. In the long-term, incorrect diet results in weaker birds more susceptible to disease and to failure to reproduce. The knowledge of scientific information on the nutritional needs of every bird species is essential to the health and maintainance of sustainable genetically viable populations in captivity. Formulated commercial diets for birds are not generally available in South America. Waterfowls and ground-dwelling birds are usually given commercial poultry food. Formulated diets for toucans, psittacines and other groups of neotropical birds seem not to be available and as a consequence, empirical feeding practices take place. Clinical conditions associated with malnutrition may be perceived only after a prolonged period of deficiency. Disorders consequent to malnutrition can affect virtually every organ or system. Birds should be fed good quality food items, which should be stored in a dry and well ventilated area, thus preventing mould. Access by rodents and insects must be prevented.

Diseases

Botulism

Avian botulism results from ingestion of a neurotoxin produced by the Clostridiumbotulinum. Outbreaks of botulism can be disastrous in a collection of aquatic birds. Favourable environment conditions are necessary for the occurrence of the disease.

Outbreaks have been reported in zoos in South America. Botulism occurrence with high mortality was reported between 1980 and 1986 in the Buenos Aires Zoo, Argentina. Larvae of flies were involved in the cycle of the disease (1). In Curitiba, Brazil, 27 ducks died in 1981 due to botulism intoxication. Beetles were found in the crop and ventriculus of the affected birds and in the mud of the ponds (26). The author studied cases of botulism type-C in south american terns (Sterna hirundinacea) in the summer of 1992, and in waterfowl in 1993. Both outbreaks occurred at the Curitiba Zoo, Brazil. Maggots were found in the ventriculus and intestines of the dead birds. Botulism in waterfowl with a high associated mortality also ocurred over the period 1993-1994 in the Sorocaba Zoo, Brazil (NUNES A.L.V., pers. comm., 1995) and recently in the São Paulo Zoological Park, Brazil (FEDULLO J.D.L., pers. comm., 1995).

Procedures to control the disease involve the management of the environment, e.g. control of water quality and level of ponds, prompt removal and disposal of carcasses, removal of healthy birds from problem areas during the botulism occurrence, and vaccination. A commercially available mink botulism vaccine was used at the Denver Zoological Gardens after 7 consecutive summer outbreaks and results suggest that the vaccine was highly efficacious (7). Mink botulism vaccines are not commercially available in the South American countries, but a bovine botulism type-C vaccine could serve as a substitute. An experimental trial using this vaccine might be indicated in collections where avian botulism is a problem.

Bacterial enteritis

Salmonella organisms can be pathogenic to birds causing septicemia and death. Subclinical carriers serve as a reservoir of the bacteria in the aviary. Free-living birds, rodents, insects and other vermin are considered vectors. Insanitary conditions favour the propagation of the bacteria. Salmonella typhimurium caused the death of a hyacinth macaw (Anodorhynchus hyacintinus) in a flock of smuggled birds confiscated at an airport in Brazil. Treatment with danofloxacin has proved to be effective (5). Practices to prevent the disease include quarantine with fecal cultures of suspected birds, hygiene and disinfection of aviaries, and rodent and insect control. Other bacteria of clinical importance are Klebsiella, E. coli, Pseudomonas, Staphylococcus and Streptococcus.

Respiratory diseases (RD)

Several etiologic agents are associated with respiratory diseases in birds. The number of clinical cases and deaths from RD is high in captivity, specially in regions of cold weather. A higher incidence of clinical cases occurs during the coldest months of the year. Enclosures that do not provide adequate protection against winds may favour the onset of an infectious process in the respiratory tract. Special attention should be given to tropical birds, which have been moved to sub-tropical areas; a period of acclimatisation before releasing is necessary. Etiologies of avian respiratory diseases can be nutritional, for instance hypovitaminosis A; toxic, such as cigarette smoke and airborne pollution or infection by viruses, bacteria, fungi or parasites.

Chamydia psittaci is an organism that may be the causative agent of respiratory diseases in psittacines. As there are few laboratories equipped to isolate the C. psittaci, the diagnosis is usually not confirmed. Preliminary results from a serological survey in 7 clinically healthy Amazons (Amazona brasiliensis) in a zoo in Brazil, revealed antibody titers in all the birds tested (FONTENELLE, J.H., pers. comm. 1995). This suggests that incidence of psitacosis may be higher in south american zoos than is usually assumed. The zoonotic potential of this disease has to be taken into consideration when handling psittacines and pigeons. Government regulations in some south american countries instigate preventive treatment prior to importation of exotic psittacines.

Aspergillus sp. is a widespread mycotic agent that frequently causes granuloma or plaques in the lower respiratory tract. All birds species can be affected, but waterfowl, penguins and psittacines are especially susceptible. Conditions conducive to stress, such as transportation, malnutrition, oil contamination insanitary conditions and overcrowding contribute to the occurrence. Preventive treatment has been advocated after circumstances of continued stress, for instance long-distance transportation. Itraconazole seems to be a safe and very effective treatment, depending on the extent of the lesion. Ketoconazole, amphoterecin-B and flucytosine can also be used to treat aspergilosis. Proper husbandry, nutrition and hygiene are essential in order to prevent the disease. Early diagnosis improves the chances of cure, and X-rays are helpful in this respect.

Parasitic diseases

Capilaria sp. is the most common cause of toucan mortality in many zoo collections in South America. Long-term maintainance and reproduction of toucans has been hindered due to the Capillaria infection among other factors. Psittacines are likewise infected. Capillaria columbae caused the death of toco-toucan (Ramphastos toco) (8). Diagnosis is confirmed by detection of bipolar eggs in fecal, flotation. Treatment with usual anthelmintics has proven to be ineffective in some instances. Anthelmintics used to control capilariosis include pyrantel pamoate, mebendazole, fembendazole and ivermectin. Birds in collections where Capillaria presents a problem, should have a minimum of one fecal flotation per month. Birds that have access to the ground and to food and water contaminated by feces tend to be subject to reinfection. Efforts should be made to destroy Capillaria eggs on the ground.

Ascarids are frequent internal parasites in psittacines and gallinaceous birds. Pathogenicity may be variable in different species. Mortality due to heavy Ascarid infection has been absorved the in purple-bellied parrot (Trichlaria malachitacea), pileated parrot (Pionopsita pileata) and conures (Aratinga sp). Regular fecal flotation and deworming are effective methods of controlling roundworms.

A fluke, Ribeiroia insignis, was described in a colony of 5 magellanic penguins (Spheniscus magellanicus) with mortality as high as 100%. (Fig. 1) Flukes were found burrowed into the wall of the ventriculus causing ulcers and hemorrhagic gastritis. (Fig. 2) Treatment with triclabendazole is effective in the early stages of the parasitism (9).

Gastrointestinal protozoans of clinical significance in captive birds in South America are coccidia and histomontisis. Coccidiosis has clinical importance in toucans and passerines. Asymptomatic birds that pass occysts in feces may develop severe clinical diasease when the symbiotic parasite-host relationship is disrupted. Histomoniasis is caused by the flagellated protozoan Histomona meleagridis, which causes ulceration and necrosis in the cecum and liver.

PRIMATES

The extensive use of nonhuman primates in biomedical research has contributed to the evolution of medical primatology and has yielded a number of publications dealing with husbandry and diseases. In recent years, emerging viral diseases of nonhuman primates either in the wild or in captivity have assumed increasing importance in biomedical investigation. The zoonotic significance of these diseases has resulted in their becoming an important subject of research. As to the prevalence of diseases in captive primates in south america, literature is relatively scarce. The pet trade in New World monkeys has continuously introduced into South American zoos an increasing number of animals which the zoos are unable to house properly. The process of transition from the wild to the captive environment exposes animals to a variety of stresses. Repeated stress and an imbalanced diet may render an animal more susceptible to infectious agents, than would normally be the case.

Diseases that most frequently cause mortality in New World primates in captivity are usually associated with inadequate nutrition and errors in management. Undernourished animals will usually offer little imunological resistance against opportunistic pathogens. Infectious diseases that frequently result in significant losses are, bacterian enterocolitis, pneumonias and parasitism. This review is concerned primarily with spontaneous infectious diseases with high incidence and mortality in New World monkeys.

Enterocolitis

Incidence and mortality due to enteritis in captive primates in South America is relatively high. Bacteria are the most frequent cause of diarrheas. Protozoans, helminths and viruses may also be causative agents of gastrointestinal disorders.

Pathogenesis of infectious diarrhea may be associated with improper diet, poor sanitation, mismanagement and other physical and psychological stressors that would be conducive to an immune suppression. The incidence is higher in younger monkies. Bacteria commonly associated with enteritis are Campylobacter, Shigella and Salmonella. Other enteric pathogens identified with less frequency in New World primates are Klebsiella, Proteus, Pseudomonas, E. coli and Yersinia. Detailed information concerning the epidemiology, pathology and pathogenesis, diagnosis and treatment of the bacterial enterocolitis can be found in specialized literature (18).

An outbreak of diarrhea due to Campylobacter jejuni in a breeding colony of tamarins (Leontopithecus chrysomelas and L. chrysopygus) was reported in the São Paulo Zoological Park, Brazil. Several individuals were identified as asymptomatic carriers (19). Campylobacter jejuni was also isolated from 10 of 15 Saguinus mystax with diarrhea in a Peruvian colony (21). Shigella infection has been reported in laboratory marmosets and tamarins. The bacteria is frequently isolated in primates taken from the forest and exposed to factors conducive to stress.

Bacterial infections usually result from human contact or from animal contact with similar or different species. Newly acquired animals should be quarantined for least 30 days. Fecal cultures for Campylobacter, Shigella and Salmonella are advisable for primates in quarantine. Sanitation of cages, feed and water containers with disinfectants is highly recommended in preventing epizootics of bacterial enterocolitis. Chronic carriers should be identified and treated or eliminated from the colony. Sources of infection need to be determined in order to control outbreaks.

Although lesions and clinical signs can vary slightly according to the organism involved, a common clinical manifestation is mild to severe diarrhea that may appear hemorrhagic or catarrhal. Nonspecific signs include depression, fever and dehydration. In the advanced stages cure is difficult and mortality can be high.

Diagnosis is based on clinical signs and laboratory findings. Since viruses and parasites are not the causative agents of the enterocolitis, bacteria need to be identified by microbiological culture. Antimicrobial susceptibility tests indicate the most effective antibiotics for treatment.

Entamoeba histolytica, a protozoan, can cause necro-ulcerative colitis. Diagnosis depends on the recognition of the causative agent in feces or invading the intestinal mucosa. Giardia and Trichomonas can be found in Cebids and Callitrichids, but pathogenicity is considered low.

Pneumonias

Bacterial pneumonia is a significant cause of mortality in captive primates . Incidence of the disease is higher during winter time. Organisms that have frequently been identified as the causative agents are Streptococcus, Staphylococcus, E. coli, Pasteurella and Klebsiella. Inadequate husbandry contributes to an increase in the incidence of the pathology. High humidity in the shelter and enclosure, poor sanitation and ventilation, and improper cage design are factors that favour the emergence of the disease. Enclosure design must take into consideration the environmental and sanitation aspects necessary to prevent pneumonias and other diseases in primates.

Internal Parasites

Internal parasites are common in New World primates. A summary of internal and external parasites is found in specialized publications (21,28). Many of the helminths occur sporadically and apper to exist in balance with the host. When this equilibrium is disrupted by diverse stress factors, clinical disease and mortality ensue.

At the Rio de Janeiro Primate Center, Brazil, Callitrichidae of several genera are commonly infected by an Acanthocephala, Prosthernorchis elegans (PISSINATI A., pers. comm. 1995). Parasites attach their proboscises to the walls of the ileum, cecum and colon with consequent inflammation, necrosis and fibrosis. Perforation of the intestine wall and peritonitis may result. Clinical signs include anorexia, depression and emaciation. Acanthocephalans have indirect life cycles and intermediate hosts are cockroaches and certain beetles. Control of the intermediate host is necessary to prevent infections in New World primate colonies. Prosthernorchis eggs are shed intermittently in small numbers. Therefore negative fecal exams do not rule out the possibility of Acanthocephalid infection. Treatments currently employed have not proved completely effective.

Strongylids, whipworms (Trichuris sp.), hookworms (Ancylostoma sp.) and roundworms (Ascarids) are treated with the usual anthelmintics, such as thiabendazole, mebendazole, fenbendazole, pyrantel pamoate and ivermectin. When handling primates one should keep in mind the zoonotic risk to humans. Protective clothing should be worn.

Strongyloides sp. was diagnosed in Cebids and Callithrichids with intestinal perforation, peritonitis and necrotizing colitis. The route of infection is oral or skin penetration by larvae. There is evidence of intra-uterine or transcolostral transmission. Infection causes a catarrhal or hemorrhagic enterocolitis. Diagnosis is by identification of larvae in the stools. Pinworm genera described in New World primates are Primasubulura sp, Subulura sp, Trypanoxyurus sp, Enterobius sp. They inhabit the colon and cecum. Trichostrongylids in the genus Molineus is known to cause hemorrhagic or ulcerative enteritis. The presence of a Spirurid, Trichospirura leptostoma was reported in the pancreas of 3 adult tamarins (Leontopithecus chrysopygus) in the Rio de Janeiro Primate Center (20). Cebids are reported to be affected by Trichuris sp. Many genera of Trematodes and Cestodes are occasionally found in New World Primates. Specific anthelmintics such as praziquantel and niclosamide are used.

Controlling internal parasites requires prophylatic measures including strict quarantine ranging from 30 to 90 days. Primates should have three consecutive negative fecal examinations before release. Fecal samples should be examined by sedimentation to detect Prosthernorchis ova.

CARNIVORES

Canine distemper

Canine distemper (CD) is an infectious disease with a worldwide distribution and of considerable importance in the Canidae, Procyonidae and Mustelidae families. In South America CD has been recognized in some zoo collections; diagnosis has been based on clinical signs and histopathological identification of CD virus inclusion bodies.

In Brazil, the higher incidence and mortality of nondomestic canids due to CD over the last 6 years has been viewed with deep concern by members of the zoological association. Up until then, zoos did not employ vaccination programs. This was possibly due to the absence of outbreaks in their zoo collections and also through not knowing the risks and immune response of available vaccines, when used in nondomestic species.

A survey to identify causes of mortality in the maned wolf (Chrysocyon brachyurus) in 20 Brazilian zoos within a 5 year period (1989 to 1993) showed that 18,5% of 108 deaths were caused by canine distemper and 1,8 % to encephalitis suggestive of CD. Six zoos reported cases of CD in maned wolves (25). In 1990 an outbreak in Sorocaba Zoo, Brazil, caused mortality in 4 crabeating foxes (Cerdocyon thous), 3 coatis (Nasua nasua), and 3 maned wolves (Chrysocyon brachyurus). A crabeating fox that had been introduced to the collection was considered the source of infection (14). Another outbreak occured in the Brasília Zoo, Brazil, during the months of November and December 1993 and caused mortality in 5 non-vaccinated maned wolves. Clinical signs included a hoarse howl, diarrhea, purulent ocular discharge, ataxia, clonic convulsions and spasm of the hind limbs. Postmortem findings were pneumonia, petecheas and ulcers of 5 to 7 mm along the intestinal mucosa. Acidophilic intracytoplasmatic inclusion bodies in leukocytes confirmed the diagnosis. Vaccinated maned wolves housed in an exhibition area of the Zoo, around 3 km distant did not present any sign of the disease (MAGALHÃES C. L., pers comm., 1995).

The emergence of outbreaks in different zoo collections made the Zoological Society of Brazil (ZSB) establish a committee of veterinarians to discuss and propose a vaccination program for south american canids. The ZSB Maned Wolf and Bush Dog SSP (Species Survival Plan) coordinators had the responsibility for including the vaccination program in the master plans. Thereafter the ZSB obtained a monovalent modified-live vaccine (MLV) of avian origin, provided by the Solvay Animal Health, USA. This has been distributed to the participating institutions. To date, commercial multivalent MLV vaccines (canine distemper MLV of avian cells origin; adenovirus type 2; parainfluenza; leptospirosis) that are produced in Brazil (Masterguard, Solvay Animal Health, Brazil) have been shown to be safe in South American Canids. The regimen recommended for the domestic dog can be appropriate for nondomestic canids. Vaccination should be given at 6 to 8 weeks of age and repeated every 2 to 3 weeks with a total of 3 inoculations. In special cases the vaccination series can be extended to 4 or 5 injections to ensure protection; annual revaccination is recommended. MLV vaccines of avian cell origin have proved to be safe and provide protection. The immunogenic response and safety of multivalent commercial vaccines need to be further investigated in South American species of the Mustelidae and Procyonidae families. Neverthless, systematic vaccination is recommended. Care should be taken to avoid canine origin vaccines in members of these families. Besides a vaccination program, strict quarantine and sanitation procedures should always be put into practice.

Enteroviruses

Nondomestic carnivores are susceptible to enteric viruses that cause disease in the dog and cat. Canine Parvovirus (CPV) has been reported in south american canids, e.g. the bush dog (Spheotos venaticus), maned wolf (Chrysocyon brachyurus ), and crabeating fox (Cerdocyon thous). Feline Panleukopenia (FPL) has been confirmed in the jaguar (Panthera onca), ocelot (Felis pardalis), and margay (Felis wiedii). Members of the Mustelidae and Procyonidae families are considered susceptible to CPV and FPL.

Gastroenteritis suggestive of enteroviruses have been reported in Carnivores maintained in captivity in South America, however conclusive laboratory diagnoses are scarce. Nonspecific gastroenteritis was responsible for 8,3% of all maned wolf deaths in 20 Brazilian zoos within the period of 1989 to 1993 (25). Although many cases were suggestive of CPV, confirmation of diagnosis by laboratory examination was not carried out.

An outbreak ot CPV confirmed by laboratory was documented in the São Paulo Zoological Park in 1989, and caused the death of 8 out of 17 adult maned wolves (Chrysocyon brachyurus) (10).

FPL in ocelots (Felis pardalis) occurred in the Curitiba Zoo, Brazil, in 1995. A young and an adult ocelot died after showing signs of diarrhea, dehydration and anorexia. Histopathological finding were suggestive of FPV. During the following weeks 4 ocelots presented identical clinical signs and one died. After this outbreak of FPV a vaccination program was initiated using killed and modified live vaccines (FISCHER DA SILVA, A.S.P., pers. comm., 1995).

Prevention of FPV and CPV depend on a program that includes strict quarantine, sanitation and vaccination procedures. The determination of causative agents would certainly help to resolve questions concerning the epizootiology of the enteroviruses. The domestic dog and cat can act as a reservoir of Parvoviruses, Coronaviruses and other viruses that cause gastroenteritis syndrome in nondomestic carnivores. Care should be taken to prevent domestic and feral animals from accessing the facilities. New animals entering the collection should never be mixed in the quarantine quarters. Sanitation practices include the disinfection of the facilities with sodium hypocholide or another virucidal agent effective against Parvovirus.

Studies indicate that immuno-competence may vary among species of the same family. This difference between species should be taken into consideration in a vaccination program. It is recommended that Caninds should be vaccinated 3 to 4 times at 2 to 3 weeks intervals from 8 weeks of age. Feline vaccination should begin at weaning and be repeated at least twice at 2 week intervals. Killed FPV vaccines have been used most frequently on exotic cats. In countries of South America where FPL killed vaccines are not commercially available, MLV vaccines have been used. So far, no adverse symptoms have been reported.

Parasitic diseases

Babesiosis

Babesiosis has been reported in maned wolves (Chrysocyon brachyurus) in South America. Babesia are intraerythrocytic sporozoan parasites that cause hemolytic anemia, weakness and death.

Two cases of babesiosis in maned wolves were reported in Sorocaba Zoo, Brazil (17). In both cases treatment was effective. Yet, within the period of 1991-1993, babesiosis caused the mortality of 4 maned wolves in two zoo collections in Brazil. (25) .A fatal case of simultaneous infection by Babesia canis and Bartonella canis was reported in a maned wolf. Only Babesia was seen in the circulating blood cells and tratment was initiated. However postmortem examination revealed high parasitism by Bartonella canis. (27). As different drugs are used in the treatment of hemoparasites, an accurate diagnosis is essential for therapy to be effective. The hemoparasites are transmitted by ticks and fleas.

Internal parasites

Exotic carnivores are susceptible to a variety of internal parasites, many of them causing clinical disease and death.

Parasitic infections may be self-limiting in adult animals, whereas in young and debilitated animals it may cause considerable losses. Ancylostoma sp. is a frequent cause of mortality of cubs and pups. The passage of larvae in the milk can result in the infection of neonates. Ascarids: Toxascaris, Toxocara and Baylisascaris are frequently found in adult and young carvivores. Whereas Toxocara canis larvae may cause prenatal infection in canids, Toxocara catti in felines do not infect fetuses in the uterus, however they do infect neonates through the mammary glands. Toxocara canis and Diphyllobotrium trinetatum were reported in south american racoons (Procyon cancrivorus) (4).

In South America Dioctophyme renale, a kidney worm, has been documented in the free-ranging maned wolf (Chrysocyon brachyurus), bush dog (Spheotos venaticus), coati (Nasua nasua), neotropical river otter (Lutra longicaudis) and gryson (Galictis vittata). It is controversial as to whether the helminth can result in the host's death.

Wild carnivores may be parasited by a number of coccidians of the Eimeria, Isospora, Toxoplasma, Sacocystis and Besnoitia genera. A wildcaught neotropical river otter while maintained in captivity died from hemorrhagic enteritis caused by a recurring Eimeria infection.

Despite advances in veterinary practice, parasites still cause significant losses among captive animals. Present-day veterinarians have access to a variety of antiparasitic drugs effective against internal parasites. However other procedures are needed to reduce mortality. Neonatal physical examination is recommended when possible, to determine health status. Standard fecal examinations should be carried out as a routine procedure in order to detect parasitic ova and protozoa. Periodic disinfection of enclosures is recommended, and one should bear in mind that some parasites are extremely resistant and reinfection can occur.

External parasites

Infestation by fleas has been frequently seen in carnivores maintained in captivity in South America. Severe infestation may cause exsanguination, anemia and death. Warmer environmental temperatures favour the insect reproduction, to the extent that a small animal can succumb in a few days from a massive flea infestation. A survey in 20 Brazilian zoos during the period 1989 to 1993, indicated that 11% of maned wolf mortalities were caused by anemia, probably due to flea infestation (25). Efforts should be made to control ectoparasites using suitable insecticides.

Sarcoptic mange has been reported in canids in captivity. Repeated treatment is required.

TAPIRS

Tuberculosis

Tapirs are particulary susceptible to tuberculosis in captivity. The causative agent is the Mycobacterium bovis or M. tuberculosis.

The author studied an outbreak of Mycobacterium infection in a group of brazilian tapirs (Tapirus terrestris). Intermittent coughing and mucous nasal discharge were thw only clinical signs observed during several months. Over a 3 year period, 3 animals died in this collection as a result of tuberculosis. The comparative- cervical intradermal skin test was conducted in 5 animals using 0,1 ml of Bovine PPD (Purifield Protein Derivate) tuberculin and 0,1 ml of Avian PPD tuberculin. A positive response was observed in 2 animals (Fig. 3). The possible sources of infection were either the public, who could have had direct contact with the animals through the wire, or vultures, that could have had access to contaminated carcasses, and served as carries of the bacilli to the zoo, or contaminated food and water resulting from wastewater discharges containing the bacteria.

Tuberculosis in tapirs was also reported in Ilha Solteira Zoo, Brazil (6) and in São Carlos, Brazil (24).

Clinical signs seen in advanced stages of the disease are coughing, nasal discharge, dyspnea and emaciation that occurs despite appetite (Fig. 4). Postmortem lesions include abcesses, and granulomas in the lungs, thoracic lymphnodes and thoracic cavity. The antemortem diagnosis of Mycobacterial infection requires a combination of tests, including the Comparative Intradermal Skin Test, Enzyme-Linked Immunoassay (ELISA) and culture of the respiratory tract. The current diagnostic tests, considered inconclusive and difficult to interpret in some instances, are however valid and necessary. The Comparative-Cervical Test is performed by injecting M. bovis and M. avium PPD tuberculin into separate intradermal sites in the skin of the neck. A delayed-type hypersensitivity response to the tuberculin indicates whether the infection is caused by a pathogenic Mycobacterium or not. Microbiological cultures are required to confirm the diagnosis and type of tuberculosis bacilli. The ELISA detects antibodies in the sera of animals infected or exposed to clinically significant Mycobacteria.

Since the treatment of tuberculosis in animals is controversial and of uncertain practical value, it is essential when considering the health of the rest of the population and of other species in the zoo, to take prophylactic measures to prevent the disease. Newly introduced animals (specially hoofstock and primates) should be subject to a tuberculin test, leaving quarantine only if returning a negative test result. The minimum period of quarantine recommended is 60 days. Tuberculin-positive animals, on which diagnosis is confirmed by intradermal tuberculin test biopsy, microbiological cultures and ELISA, should be considered for euthanasia. Enclosures for tapirs should have barriers that maintain the animals' distance from the public, and prevent direct contact. Appropriate precautions should be taken to reduce the risk of cross-infection between animals and staff and vice-versa. Food and water for drinking and bathing must be regularly inspected to assure good quality and hygiene. When tuberculosis is diagnosed in a zoo collection, facilities must be decontaminated with an effective disinfectant such as phenol type or cresylic compounds. Sodium hypochloride, quaternary ammonium and chlorhexidine are ineffective against the tuberculosis bacilli.

If treatment is attempted, a suggested protocol for hoofstock includes isoniazid in combination with rifampin or ethambutal for 9 to 12 months. A female tapir which had tuberculin-tested positive was treated with streptomicin for 30 days and isoniazid for 180 days. Thirty months after the end of treatment the female and its calf reacted tuberculin-test negative (24).

Miscellaneous conditions

Salmonella spp. cause enteritis and septicemia in both adult and neonatal tapirs. Fecal cultures are recommended in animals recently introduced into the population or individuals that present signs of gastroenteric infection. Balantidium infection of the gastrointestinal tract causing enteritis and diarrhea was reported in the postmortem of a tapir. Fasciola hepatica and Strongylids eggs have been identified in feces of healthy individuals. Other bacterial and parasitic diseases have been reported in the Tapiridae family (23).

Conditions related to inadequate husbandry and management can lead to diseases and mortality. For instance, hard and rough substrates such as cement, result in hoof lesions and lameness. Corneal opacity is usually seen in tapirs maintained in enclosures with insufficient shade. As tapirs inhabit thick forests, it is recommended that adequate areas of shade should be provided in captivity. The provision of bathing facilities is also important. Lack of such facilities can result in foot problems, constipation and rectal prolapse. However drowning is a frequent cause of calf mortality, so the female should be confined in a separate nursery area with a shallow pool just prior to parturition. The ingestion of coarse food can cause oral laceration and abcess formation, intestinal obstruction, constipation and rectal prolapse. The ingestion of large quantities of sand has been reported as the cause of colitis and colic. All these health considerations should be aken into account when designing the captive environment.

CERVIDS

Hemorrhagic disease

The term Hemorrhagic Diseasse (HD) has been used to describle a severe disease in cervids. The causative agent may be the Bluetongue virus, or Epizootic Hemorrhagic Disease virus or a related orbivirus. To date it has not been possible to isolate and identify the causative agent.

Serological studies in Chile, Paraguai, Guiana, Suriname, Colombia and Brazil have indicated the presence of antibodies against the Bluetongue-related orbivirus in livestock. Epizootic Hemorrhagic Disease has not been confirmed in South America.

The disease was first noticed in cervids in the Rio de Janeiro Zoo, Brazil in 1991. In January - February 1992, the disease was described in a herd of brown brocket (Mazama gouazoubira) in the campus of the University of São Paulo State - UNESP, Brazil. One out of 4 brockets died. Again in this institution, 6 brown brockets died in 1993. Serological studies by immunodiffusion in agar gel indicated antibodies against bluetongue (BT) or related orbivirus (11,12). In July 1992 the disease was documented in one specimen of marsh-deer (Blastocerus dichotomus) in the Ilha Solteira Zoo, Brazil (16). A serological study of 72 cervids from different regions of Brazil showed a prevalence rate of 20% (2). The disease is considered enzootic in a population of brown brocket (Mazama gouazoubira) maintained in a park close to Sorocaba city, Brazil, and has caused significant mortality over 5 years (NUNES A.L.V., pers. comm., 1995).

Incidence of HD is seasonal occuring during warm and rainy seasons when the concentration of insect vectors is higher. Biting flies of the genus Cullicoides are considered to be vectors of the disease, however other hematophagous insects are probably involved in the epizootiology of the HD. Domestic hoofstock act as reservoir of the virus. It is also likely that cervids or domestic hoofstock that survive the clinical disease become asymptomatic carriers.

Diagnosis has been based on the clinical signs, lesions and serological studies.

Necropsy findings are of widespread hemorrhage in the digestive tract, lungs, heart, liver, spleen and subcutaneous tissue. Mortality rates vary according to environmental conditions, pathogenicity of the viral strain, stress to which the animal is exposed, and secondary bacterial infections (bronchopneumonia).

To prevent and control HD, appropriate practices must be implemented. In order to avoid introducing the virus into a population free of the disease, only seronegative animals should be acquired for the collection. New arrivals should be placed in quarantine and initial screening should include serological tests. Infected animals that show clinical signs should be isolated and treated, preferably in a mosquito-proof enclosure to avoid transmission to non-infected animals. Carriers should not be kept in the colletion. Non-sterile syringes, needles and darts create a potential risk of spreading the virus among other individuals of the herd. Measures to control vectors can effectively reduce the chances of infection. Development of a vaccine using specific South American sorotypes of orbivirus is an urgent prophylatic measure. Thus, the isolation and identification of the causative agent is crucial.

The Hemorrhagic Disease represents a serious risk to the maintainance of cervids in captivity in South america. Once the disease is introduced to a population, it tends to persist causing periodic mortalities in sucessive years.

ACKNOWLEDGMENTS

The author wish to thanks the colleagues that contributed to this review, by giving information about disease occurrence in their instituions, and also Mr. John Leggatt for his revision of the english manuscripts.

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