Rev. sci. tech. Off. int. Epiz., 1996 , 15 (1) , 251 -266

Special challenges of maintaining wild animals in captivity

in North America R.C. CAMBRE * and W.W. BUICK **

Summary: The maintenance of wild animals in captivity in North America is regulated by a number of different laws and government agencies in each country. Member institutions of zoo and aquarium associations in Canada, the United States of America and Mexico experience an extra tier of regulation in the form of industry standards, which are sometimes stricter than those imposed by government. Climate, natural disasters and harmful pest species all contribute to the challenge of keeping animals in certain locales. Vigilance against zoonotic disease transmission is maintained through industry and government-mandated sanitation standards, which are fortified by reporting regulations of local, regional and Federal health agencies. Current controversies in the keeping of particular taxa in North America include the threat to non-human primate breeding programmes precipitated by strict new import regulations, the fear of herpesvirus B infection, and commercial airline transport bans. Successive human fatalities among elephant handlers have prompted the industry and governments to re-examine the manner in which these potentially dangerous creatures are maintained in captivity.

KEYWORDS: Environmental safety - Regulation - Wildlife husbandry -Zoonoses.

CAPTIVE WILDLIFE LAWS A N D REGULATIONS

Zoos, aquariums, and other wildlife facilities that maintain, transport or deal in populations of non-domestic animal species in Canada, the United States of America (USA) and Mexico, must observe international, national, regional (provincial or state) and local laws. These regulations provide for the health of the animals in question, safeguard the well-being of domestic animal species and the human populations of these countries, and aim at protecting endangered species. Zoo administrators face several constant challenges, in seeking to comply with the voluminous legislation that regulates the transport and maintenance of animals at several administrative levels. These challenges include the following: keeping abreast of changing regulations; meeting the requirements of laws from several agencies and departments within and

* Department of Animal Health, National Zoological Park, Smithsonian Institution, 3000 Connecticut Avenue NW, Washington, D.C. , 20008-2598, Uni ted States of America .

** N O A H S (New Opportunit ies in Animal Heal th Sciences) Center, National Zoological Park, Smithsonian Institution, 3000 Connecticut Avenue NW, Washington, D.C. , 20008-2598, United States of America.

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outside their respective national, regional and local governments; and covering every eventuality when obtaining transport, holding and breeding permits. One Canadian zoo administrator has coined the phrase ' the era of total responsibility' to refer to the obligations of the shipping institution in the present climate of regulation (D.R. Banks, unpublished presentation, 1994).

The complicated process of moving an animal from one facility to another must be carefully planned and executed. The International Air Transport Association (IATA) Live Animal Regulations contain guidelines for the design of crates used in shipping. Importation of certain species is regulated by laws in the country of origin as well as in the importing country (24). Permits, usually required by several departments, can occasionally be combined into a single document.

Wildlife regulations in Canada

Federal regulations

A number of government departments in Canada have jurisdiction over the transport and maintenance of non-domestic species. Agriculture Canada, under the Health of Animals Act, sets requirements for import and export certification for land mammals. For cetaceans, this is performed by the Department of Fisheries and Oceans. Canadian Wildlife Services, a division within Environment Canada, administers the Migratory Bird Convention and the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES).

Animals not regulated by CITES which are imported into Canada from countries other than the USA require a permit from Agriculture Canada stipulating health requirements. Animals not listed in CITES which are imported into Canada from the USA do not require a permit from Agriculture Canada, but health certificate requirements must be fulfilled. This applies to all terrestrial mammals other than camelids and cervids. Transport of the latter species has been restricted by a moratorium initiated by the Canadian government in 1991, due to concern regarding the spread of tuberculosis (J. Moran, personal communication, 1995).

Agriculture Canada administers the Health of Animals Act, working closely with provincial public health departments to ensure the health of the human and wildlife populations. The Captive Ungulate Policy, under revision at present, establishes rules for transfer of animals between provinces in regard to tuberculosis and brucellosis. Although the primary contact for reporting any disease is Agriculture Canada, zoonotic diseases require attention on Federal, provincial and local levels (R. Cooper, personal communication, 1995).

Wildlife law is under comprehensive review by the Canadian Government, and a new act - the Wild Animal and Plant Protection and Regulation of International and Interprovincial Trade Act (WAPPRIITA) - will systematize and coordinate currently conflicting legislation. The Act was passed at the end of 1992 but has not yet been fully implemented.

Provincial regulations

The British North America Act of 1867 appoints control of wildlife resources to provinces, including intra-provincial management of exotic and non-domestic species. Regulation becomes complicated and sometimes conflicting, however, when animals are moved between provinces. The degree of regulation varies among the ten provinces.

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Eight of the ten provinces in Canada have licensing requirements. These eight provinces have also enacted legislation to control ownership and movement of non-indigenous and non-domestic wildlife, aimed primarily at large carnivores, primates and some species of reptiles. In Quebec, for example, zoo permits are issued which require water sampling, submission of copies of expansion plans, and yearly reports on mortality and surplus animals. Zoos in Quebec are inspected by the provincial government once a year. It is illegal in Quebec to own privately any large feline or primate, with the exception of a handful of animals, the ownership of which predates this legislation.

Each province is the sole owner of wildlife indigenous to the area within its borders. Under the WAPPRIITA Act, however, Canadian Wildlife Services will have authority to take possession of any species covered by CITES which is illegally transported between provinces; they will also regulate all imports and exports. Rehabilitation of native wildlife is regulated by the Natural Resources Ministry within each province, except in Quebec, where the responsibility is carried by the Ministry of the Environment and Fauna.

Many of the wildlife industries in Canada - e.g. ratite, venison (deer and elk), bison, llama and alpaca - are regulated on a provincial basis, rather than at the Federal level. These industries have been removed from the zoo sector and established as 'alternative agriculture' with the encouragement of the provincial governments (J. Moran, personal communication, 1995).

Any citizen of Canada may take an injured animal into care, but must report the situation to the provincial wildlife department, which will take responsibility for disposition of the animal.

Wildlife regulations in the USA

United States Department of Agriculture

The Animal and Plant Health Inspection Service (APHIS) of the United States Department of Agriculture (USDA) administers Federal regulations and laws protecting the health of animals in zoos and other captive settings. In coordination with state authorities, APHIS monitors plant and animal health, humane treatment of animals, quarantine, and the control and eradication of pests and diseases (24). The agency accomplishes this through licensing and inspection of institutions which fall under its jurisdiction. The Veterinary Services (VS) division of APHIS controls interstate transportation of mammals, importation of birds and import quarantine.

The APHIS Authorization Act includes quarantine/importation requirements to prevent contagious or infectious diseases of importance to domestic livestock industries from entering the country. In most cases, permits must be obtained to import species of concern. These regulations apply to poultry, pigeons and other bird species, swine, horses and ruminants. They also cover animal semen, embryos, blood and other tissue samples.

Under the APHIS Authorization Act, wildlife facilities and zoological institutions seeking to import and display swine and ruminants originating from countries in which rinderpest and foot and mouth disease (FMD) exist must comply with USDA restrictions by applying for Permanent Post Entry Quarantine (PPEQ) (22). The zoo in question must conform to specific instructions for waste removal, park perimeter

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fencing, and prevention of contact between these animals and domestic livestock. Only under very limited circumstances can animals potentially carrying these and other listed diseases be removed from this facility. Translocation of progeny born to PPEQ animals within the USA, however, is not restricted by the USDA (24). APHIS must also approve shipments of embryos and semen, regardless of whether or not the country of origin is free from FMD and rinderpest.

Rhinoceroses, tapirs, hippopotamuses and elephants are covered by separate APHIS regulations. A shipment containing any of these species must be accompanied by health certificates signed by a government veterinarian in the exporting country, and requires an import permit for a specific port of entry. These animals must be shown to be free of ectoparasites (e.g. ticks). Health certificates are also needed to import goats, swine, sheep, cattle and horses.

Swine from countries which are not free from FMD may be admitted to the USA only if they are to be exhibited in a PPEQ zoological park previously approved by APHIS. Special attention must also be paid to the disposal of the waste of these animals. Permits are required for importation of swine into the USA from Canada. Swine destined for exhibition in a zoological park must be accompanied by a certificate issued by a Canadian government veterinarian, stating that the animals show no evidence of communicable disease.

The Animal Welfare Act (AWA) of 1966, enforced by the Regulatory Enforcement and Animal Care division of APHIS, establishes that warm-blooded animals placed on exhibit or used in research must be treated humanely. This regulation (which includes several amendments) covers rabbits, hamsters, guinea-pigs, monkeys, cats, dogs and most other warm-blooded mammals; it does not apply to farm animals, horses, birds, fish or cold-blooded animals (22). The regulation sets minimum standards for separation of incompatible animals, adequate veterinary care, shelter from extremes of temperature, ventilation, sanitation, transportation, feeding, water supply, housing and handling (22).

Zoological facilities - including urban, roadside and private zoos which are open to the public - are regulated by the Act. Aquariums are covered by the AWA if they contain marine mammal exhibits. Other aquariums, and private wildlife collections that are closed to the public, are not regulated by the Act. The AWA also applies to shippers, carriers and other animal transport companies, public and private exhibitors (including ranches), carnivals, circuses, pet dealers and research facilities. All animal auction dealers must also be licensed and monitored by APHIS. The AWA requires that current and accurate records be kept by all regulated facilities.

APHIS also has jurisdiction over care and maintenance standards for captive marine mammals, through the Marine Mammal Protection Act of 1972, which is administered jointly with the Fish and Wildlife Service of the Department of the Interior and the National Marine Fisheries Service of the Department of Commerce. Public display and scientific research are exceptions, granted by permit, to the moratorium against taking marine mammals.

United States Department of Health and Human Services

Enforced by the Centers for Disease Control (CDC) of the United States Department of Health and Human Services, the Public Health Service Act (PHSA) regulates the importation of selected species to prevent the introduction, transmission or spread of

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communicable diseases to the USA from other countries. This Act covers the transportation of any animal that may carry an infectious disease communicable to other animals and people. This includes non-human primates, turtles, terrapins, tortoises, dogs, cats and psittacine birds. More than one rule of Federal legislation may affect transport of these species. For example, once turtles or turtle eggs have been admitted to the USA, they are governed by both the PHSA and applicable CITES regulations. Marine turtle species, however, also fall under the Endangered Species Act once they have entered the USA (22).

'Non-human primates' denotes all non-human members of the order Primates, including (but not limited to) monkeys, chimpanzees, orang-utans, gorillas, gibbons, apes, baboons, marmosets, tamarins, lemurs and lorises. Major concern exists over the potential impact of current CDC primate import regulations on present and future captive-breeding efforts (see below).

United States Department of the Interior

The United States Fish and Wildlife Service (USFWS) of the Department of the Interior regulates the transport of wildlife into, out of and within the USA. USFWS rules control inspection, declaration requirements, marking of containers or packages, and requirements for import/export licences, thus providing for transport conditions which safeguard the health and well-being of wild mammals and birds.

Wildlife import shipments must enter the USA through one of the following USFWS-approved ports: Chicago, Dallas/Fort Worth, Honolulu, Los Angeles, Miami, Boston, Baltimore, New Orleans, New York, San Francisco or Seattle. This holds true in all but special situations (e.g. scientific purposes), when a permit may be issued for the use of a non-designated port (8).

The Office of Management Authority (OMA) of USFWS processes several types of permit applications for wildlife imports to the USA. Permits issued by OMA in compliance with CITES authorize the export, re-export and import of endangered species. OMA also handles permits for species on the United States Endangered and Threatened Wildlife List. Additionally, OMA processes 'Introduction from the Sea' permits, allowing for the importation of a specimen from the high seas for research purposes (16). To ensure that potentially destructive wildlife is transported and maintained in secured enclosures, OMA may issue 'Injurious Wildlife' permits.

The USFWS administers the Migratory Bird Treaties, protecting members of species which may migrate across international borders. Adopted as a measure to reduce the reliance of the pet industry on wild-caught birds, the Exotic Bird Conservation Act became law on 23 October 1993, and is also administered by USFWS. This Act (with its accompanying regulations) establishes a moratorium on several CITES-listed species and encourages captive breeding of birds sought after by the pet bird market (9).

United States Department of Commerce

The National Marine Fisheries Service (NMFS) of the Department of Commerce controls interstate trade and importation of marine mammals, including parts of - or products generated from — these animals. This agency disperses permits concerning pinnipeds (with the exception of walrus), cetaceans, sea turtles and species of interest

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to commercial fisheries (24). Relevant areas of the Marine Mammal Protection Act, the Endangered Species Act and the Lacey Act are regulated by NMFS.

State and local laws in the USA

Each state regulates to some degree the keeping of wildlife within its borders, including the sale and possession of certain species. Some animals transported across state lines must be accompanied by a certificate of health. The shipper must always be mindful of applicable state and local laws in the areas from which, through which, and to which an animal is being transported (24).

Wildlife regulations in Mexico

A new agency has been established in Mexico, namely the Secretaría del Medio Ambiente, Recursos Naturales y Pesca (SEMARNAP), with functions similar to those of USFWS in the USA. Among the departments coordinated by SEMARNAP is the Dirección de Flora y Fauna.

The following agencies deal with disease issues:

- Secretaría de Salud, which deals with human diseases; - Secretaría de Agricultura y Recursos Hidráulicos (SARH), which deals with

diseases affecting animal production.

SARH has several commissions on specific diseases (e.g. Comisión Nacional para la Erradicación de Tuberculosis y Brucelosis and Comisión Mexico-Americana para la Prevención de Fiebre Aftosa y Enfermedades Exóticas). SARH has state offices that supervise the movement of animals between states. For example, to move a giraffe from the Africam Safari Parque in Puebla to the Zoológico de Chapultepec in Mexico City requires two permits: one from the Department of Flora and Fauna of SEMARNAP and one from SARH (A. P a r s , personal communication, 1995).

INDUSTRY SELF-REGULATION

American Zoo and Aquarium Association

The American Zoo and Aquarium Association (AZA), initially organized in 1924, is the oldest of the North American zoo industry associations. Until 1994 it was known as the American Association of Zoological Parks and Aquariums (AAZPA). In 1972 AAZPA initiated a voluntary programme of accreditation of member institutions as an in-house quality-control system, partly to pre-empt the possibility of the Federal government mandating a system that might not have included zoo and aquarium professionals in its administration. In 1985 the programme became mandatory for all members.

Organized to uphold and improve professional standards in zoo and aquarium management, the accreditation programme evaluates the membership qualifications of an institution through a combination of detailed questionnaire responses and in-depth inspection of facilities by a visiting committee. Accreditation is granted for a five-year

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period, at the end of which the institution must apply for re-accreditation and undergo the same process. AZA may call for a review of an accredited facility at any point during this five-year period (6).

Canadian Association of Zoological Parks and Aquariums

The Canadian Association of Zoological Parks and Aquariums (CAZPA) is similar in structure to AZA. CAZPA was founded in 1975 and began its accreditation programme in 1983. The Association grants accreditation on a three-year schedule. Many zoos which receive accreditation under CAZPA are also accredited by AZA, resulting in inspection by both organizations. Some of the animal welfare policies of CAZPA are more extensive than those of AZA (J. Moran, personal communication, 1995).

Asociación de Zoológicos, Criaderos y Acuarios de la República Mexicana

The Asociación de Zoológicos, Criaderos y Acuarios de la República Mexicana (Mexican Association of Zoos, Breeding Centres and Aquariums) was founded in 1990. Among the membership are zoos, aviaries, aquariums and herpetariums throughout Mexico. The Association promotes modern zoo objectives, and plans to develop formal standards for member institutions, although no accreditation programme exists at present. Information is disseminated to members through an annual congress.

E N V I R O N M E N T A L C O N C E R N S

Climate

The North American continent extends from 15°N to 80°N, from the tropics to the northern polar ice cap. In between he numerous climatic zones in the three countries of Mexico, the USA and Canada. Wild animals are maintained in captivity in all of these zones. Climate dictates many issues, including the following:

- shelter for animals, workers and visitors from extremes of temperature and weather

- employee and visitor safety - cost of construction - access to animal areas in adverse weather - transportation of animals into, within and out of a facility - animal health - parasite load - reproductive performance

- presence or absence of pests.

Temperature

Table I illustrates the wide variation in winter and summer temperatures in representative cities in the USA where zoos are present. Zoos tend to keep certain popular species, regardless of their location: giraffes and elephants, for example, can

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TABLE I

January July Location Daily minimum Daily maximum Daily minimum Daily maximum

°F °C °F °C °F °C °F °C

Anchorage, Alaska 6.0 -14.4 20.0 -6.7 51.1 10.6 65.1 18.4 Omaha, Nebraska 10.2 -12.1 30.2 -1.0 66.8 19.3 88.5 31.4 Chicago, Illinois 13.6 -10.2 29.2 -1.6 62.7 17.1 83.3 28.5 Buffalo, New York 17.0 -8.3 30.0 -1.1 61.2 16.2 80.2 26.8 Washington, D.C. 27.5 -2.5 42.9 6.1 69.9 21.1 87.9 31.1 New Orleans, Louisiana 43.0 6.1 61.8 16.6 73.5 23.1 90.7 32.6 San Diego, California 48.4 9.1 65.2 18.4 64.9 18.3 75.6 24.2 Brownsville, Texas 50.8 10.4 69.7 20.9 75.6 24.2 92.6 33.7

be found in zoos throughout the continent. This prompts seasonal strategies for keeping these animals in areas where winters are harsh, to prevent hypothermia and slippage on ice and snow. Some species are able to adapt quite well to climates other than their natural ones, while others are much less tolerant. African antelope, for example, vary widely in their flexibility to environmental temperatures, with some (e.g. nyala [Tragelaphus angasi]) being considered delicate and tolerating a narrow range of temperatures, while others are considered hardy (e.g. eland [Tragelaphus oryx]) and are able to thrive in a much broader range. This is not just a matter of humane animal keeping and basic husbandry. The Animal Welfare Act (USA), for example, dictates that animals must be protected from extremes of heat and cold, and even lists specific temperatures for a few species.

Natural disasters

Hurricanes, earthquakes, tornados, floods, drought, heat, fire, blizzards and cold have all taken their toll on zoo and captive wildlife collections in North America. Several major zoos and scores of non-zoo wildlife collections in the USA, as well as numerous zoo and wildlife facilities in Mexico, are located within the landfall zones of hurricanes. Over 800 tornados occur annually in the USA alone (14). This has prompted zoos and wildlife facilities to formulate disaster plans, including the formation of some type of emergency preparedness team, evacuation plans for visitors, and contingency plans for employees and animals (such as the installation of auxiliary electrical generators to provide ventilation, lighting and heating). Stockpiling of emergency supplies is another measure taken in disaster-prone areas.

In July 1993 widespread flooding in the midwestern USA resulted in the closure of the Blank Park Zoo in Des Moines, Iowa, due to public and animal health concerns. The supply of potable water to the city was lost due to flooding of the water treatment plant, and a state of emergency was declared. The zoo remained closed for nine days,

Average daily temperatures of various cities in the United States of America in January and July

(5)

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despite not being inundated itself. Although water service was restored after twelve days, use was severely restricted for another two weeks. Alternative sources of water were sought, including collection of rain water. The director reported that: 'Water use was prioritized according to fresh drinking water, water for washing feed pans and food preparation utensils, then for cleansing holding areas or exhibits. The water in the California sea lion and harbour seal pools and the penguin exhibit, normally cleaned and refilled twice weekly, was changed only once during the period 9-23 July.' The incident created problems with rodent control and black fly strikes. Flood-related expenses totalled US$15,000, visitor attendance declined by 47,518 and revenue for 1993 dropped by US$120,000 (1).

No animals were lost, but a ten-year-old female Siberian tiger (Panthera tigris) experienced an episode of toxic hepatitis from which she recovered. Ingestion of fungus-laden water which had accumulated in the moisture-soaked exhibit was suggested as the cause, by liver biopsy findings (23).

Hurricane Andrew devastated the Miami Metrozoo in Florida on 24 August 1992. The aviary was blown over and many of its 500 free-flight inhabitants escaped. Approximately two-thirds of these birds were recovered in subsequent weeks either alive or as carcasses. According to the zoo veterinarian, five mammals were lost, one of which was a Przewalski's horse (Equus przewalskii) that died of colic and had to be buried due to loss of electrical power to the incinerator. Three of the other four mammals that died were old or suffering with chronic health problems, and were probably unable to stand the stress of the storm. They included a crown duiker (Sylvicapra grimmia), an impala (Aepyceros melantus) and a Kirk's dik-dik (Madoqua kirki). A young gibbon (Hylobates lar) was killed outright by the storm. Stress-induced disease was still manifesting six months later, as abortions or fetal resorptions, but there was no immediate outbreak of any single disease. The veterinarian was concerned about potential tetanus and vaccinated any mammal that was handled for any reason, but a zoo-wide vaccination campaign could not be launched under the circumstances. The veterinary hospital received significant damage but was able to continue functioning (C. Miller, personal communication, 1995).

Although the zoo possessed a 'Hurricane preparation manual' (a comprehensive checklist to care for all the needs of the zoo in the event of a hurricane) since its opening in 1980, it was impossible to be prepared for a storm of this magnitude (13). Zoo staff had set aside extra food and fuel when news was received of the approaching hurricane, but these supplies were all blown away - including whole freezers - and regional zoos had to provide aid in the aftermath of the storm, with food, supplies and equipment. The zoo was closed for three months, opening again in late December, having sustained losses of more than US$15 million (13). The scars left by Hurricane Andrew will be visible for many years to come.

Harmful pest species

The imported red fire ant (Solenophisis invicta burena) has caused morbidity and mortality in zoo animals in several of the eleven south-eastern states of the USA in which it is found. Originating in Argentina, Paraguay and Brazil, this agricultural pest is believed to have been introduced into southern Alabama in the 1930s. In a 1990 survey of zoological institutions in the affected states (15), seven of thirty-seven respondents reported not having fire ants, while mortalities attributed to ants were listed by the remainder of respondents for twenty-six. zoo species, including some as

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large as Thomson's gazelle (Gazella thomsoni) and nyala. A wide variety of pesticides and biological control products were used in and around exhibits to kill ants, coupled with management changes to discourage the congregation and feeding of these pests. Management measures included hanging animal feed pans or surrounding them with water, coating their edges with petrolatum, promptly removing uneaten food, and changing the location of feeding stations. To counter ant attacks on eggs of ground-nesting birds and reptiles, eggs were artificially incubated, and the legs of hatcher and brooder boxes were placed in pans of water or oil. Zoos also reported incidents of staff and visitors being stung by fire ants.

ZOONOTIC DISEASE ISSUES

Responsible zoo managers take precautions to protect their employees and the visiting public from the threat of zoonotic diseases potentially being transmitted by animals housed in their collections. This is achieved through a combination of visitor separation from animals, veterinary preventive medicine programmes (which screen for such diseases and treat to eliminate them where possible) and education of personnel in preventive hygiene measures.

Every state in the USA issues its own list of diseases which must be reported to the state agriculture department (for animal diseases) and the state health department (for human diseases). States report weekly to the Centers for Disease Control of the United States Public Health Service, via the computerized National Electronic Telecommunications System for Surveillance (NETSS). Human exposure to zoonotic diseases of zoo animals and wildlife would be investigated first at the level of the local and state health departments, and then reported to the national database mentioned above. The situation is much the same in Canada, with all three levels of government (local, provincial and Federal) likely to be involved in the reporting of an incident.

Table II lists examples of zoonotic diseases that historically have been, or potentially could be, spread from zoo and wildlife species to humans.

Pigeons and Campylobacter spp.

Perhaps a greater threat to the visiting public and employees than the zoo animals themselves are free-ranging pigeons (rock doves [Columbia livia]), which are a common nuisance in North American zoos. Enticed by freely-accessible food in open-air exhibits, pigeons tend to nest in and overpopulate every available space. In addition to the soiling of exhibits, pigeon droppings harbour potential zoonotic pathogens. In a 1979-1980 study conducted at the Denver Zoological Gardens, 8% of 75 pigeons trapped during the winter months and 26% of 78 trapped during the summer months were positive for Campylobacter fetus subsp. jejuni on faecal culture. With one exception, the serotypes recovered from pigeons were not the same as those isolated from zoo animals. However, an isolate of a serotype commonly found in humans with enteritis caused by Campylobacter was recovered (serotype 2 in the classification scheme in use at the time) (18).

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C U R R E N T CONTROVERSIES WITH PARTICULAR TAXA Threat to breeding programmes involving non-human primates

Three problems have coalesced to threaten present and future breeding programmes for some non-human primate species in zoos in North America. These problems are described below.

New Non-human Primate Import and Quarantine Regulations in the USA

Following the importation into the USA, in 1989, of a number of crab-eating macaques (Macaca fascicularis) which were thought to be infected with the deadly zoonotic Ebola-Zaire virus (Filoviridae), strict new measures were initiated by the CDC for quarantine of incoming primates. In fact, the virus was found to be a strain which was fatal only to monkeys (subsequently named Ebola-Reston, after the Virginia city in which the infected laboratory was located). Unfortunately, the standards were so strict that many zoos were unable to retain previously-held importation permits, and even many commercial and government primate laboratories abandoned efforts to continue importing non-human primates.

The dilemma for zoos is that all primates are subject to the standards, even animals that were captive-born and have been held in responsible zoos throughout their lives. This includes New World species which have never been implicated in any Ebola outbreak. These new regulations have made it extremely difficult to continue with captive breeding programmes for certain species. Few zoos or laboratories are willing to endure the hardships of the import and quarantine regulations. The official AZA response to the proposed final CDC standards stated that (19): 'We believe that additional public health regulations should be developed in response to a careful assessment of actual public health risks associated with the importation of primates. AZA's position is that the original proposed draft technical standards do not reflect a response commensurate with that risk. AZA believes that the implementation of these draft regulations will severely limit and even halt the limited importation of primates to zoological institutions in the United States, thereby disrupting ongoing conservation programs vital to the survival of many species. While these proposed regulations consider all imported primates, regardless of origin, medical history or other factors, as presenting an equal public health risk, the AZA does not believe that this accurately reflects the true risks associated with the importation of most species of nonhuman primates. For example, a captive-born prosimian from Canada is treated as presenting ' the same risk as a wild-caught macaque from central Africa. In general, the primate populations (i.e. African green, cynomolgus, and rhesus monkeys) presumed by CDC to be a source of notable risk and that were the impetus for more stringent quarantine regulations are different from those species incorporated in most long-term conservation plans.' AZA further states that (19): 'Although cognizant of public health risks, despite a long history of primate importations into our institutions spanning several decades, we are not aware that exposure to imported nonhuman primates in zoological institutions has resulted in zoonotic disease from infectious agents classified as highly pathogenic to humans by CDC. Several areas of the proposed regulations will effectively result in a ban on primate importations.'

Fear of Herpes simiae (herpesvirus B)

Several macaque species have been found to be seropositive for herpesvirus B, an alpha herpesvirus potentially fatal in humans. Although no human fatality is known to have occurred following exposure to this virus in a zoo monkey, a level of fear has

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arisen among zoo keepers and curators about keeping these species (20). Movement of surplus animals has already been compromised, and many zoos have abandoned breeding programmes for macaque species or removed them from their collections (17). Development of 'specific pathogen free' colonies might be a way to overcome the current dilemma, but this is not being undertaken for many of these species at present.

Airline bans on primate shipments

Bowing to pressure from animal rights groups, some airlines (notably large international carriers) have recently refused to transport non-human primate shipments (21). The CDC regulations also place an extra burden on airlines which the companies are often unwilling to accept.

The dilemma of managing elephants in captivity

Of particular current concern in North America is the management of its approximately 700 captive elephants. Following the traumatic deaths of one or more elephant handlers in the zoo, wildlife park and circus communities on an almost yearly basis in recent years - 22 fatalities in the USA and Canada alone since 1975, three of whom were circus patrons (J . Lehnhardt, unpublished data, 1995) - calls have come from both industry and government sources to change the way these animals are handled.

Among proposed responses, the concept of 'protected contact' has emerged, in which the handler works from a shielded position outside the enclosure and does not enter into direct contact with the elephant. Food treats are used to form a co-operative bond with the animal. The AZA initiated debate as to whether protected contact should be mandated for all member institutions, and for a time the implementation of such standards appeared to be imminent. However, the final decision is still under debate. A survey on this topic revealed that keeper safety is the overriding issue driving the initiative, but the cost of renovations to existing facilities appears to be the major factor preventing zoos from changing to such a system quickly or at all (7).

ACKNOWLEDGEMENTS

The authors wish to thank the many persons who contributed information to this paper, including the following: K. Kenyon, J. Lehnhardt and J. Block (National Zoological Park); Dr R. Cooper and D. Banks (Calgary Zoo); J. Moran (Parc Safari Africain, Quebec); Dr A. Parás (Africam Safari Parque, Puebla, Mexico); Dr F. Guai (Zoológico de Chapultepec, Mexico City); Dr A. Perera and Dr R. Garcia (USDA, APHIS, International Services, Mexico City); Dr G. Tapia-Hervert (AZCARM, Puebla, Mexico); Dr C. Miller (Miami Metrozoo); and Dr M. McGuill and T. Broadbent (Massachusetts Department of Public Health). For technical assistance, the authors wish to thank K. Parks, E. Linnetz and S. Gill of the National Zoological Park.

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LES PROBLÈMES SPÉCIFIQUES AU MAINTIEN EN CAPTIVITÉ DES ANIMAUX SAUVAGES EN AMÉRIQUE DU NORD. - R.C. Cambre et W.W. Buick

Résumé : En Amérique du Nord, le maintien en captivité des animaux sauvages est réglementé par un certain nombre de lois et d'organismes officiels dans chaque pays. Les institutions appartenant aux associations de parcs zoologiques et d'aquariums au Canada, aux Etats-Unis d'Amérique et au Mexique sont l'objet de contraintes réglementaires accrues, notamment celles des normes professionnelles spéficiques, souvent plus strictes que celles imposées par les gouvernements. Climat, catastrophes naturelles et nuisibles sont autant de facteurs qui rendent difficile le maintien des animaux dans certains lieux. Les mesures de surveillance pour empêcher la transmission de zoonoses sont celles dictées par la profession et par les normes officielles d'hygiène; elles sont renforcées par les systèmes obligatoires de déclaration auprès des services de santé, au niveau local, régional et fédéral. Les controverses qui remettent actuellement en question le maintien de certains taxons en Amérique du Nord sont dues, entre autres, à des réglementations plus strictes sur l'importation (qui mettent en péril les programmes d'élevage de primates non humains), à la crainte de l'infection par l'herpèsvirus B, et aux interdictions des compagnies aériennes privées. Une série de décès survenus parmi les dresseurs d'éléphants ont conduit les professionnels et les gouvernements à réexaminer les conditions du maintien en captivité de ces animaux potentiellement dangereux.

MOTS-CLÉS : Elevage de la faune sauvage - Réglementation - Sécurité de l'environnement - Zoonoses.

DIFICULTADES ESPECIALES DEL MANTENIMIENTO DE ANIMALES SALVAJES EN CAUTIVIDAD EN AMÉRICA DEL NORTE. - R.C. Cambre y W.W. Buick.

Resumen: En América del Norte, el mantenimiento de animales salvajes en cautividad está reglamentado por diversas leyes y agencias gubernamentales propias de cada país. En Canadá, Estados Unidos de América y México las instituciones pertenecientes a asociaciones de acuarios y zoológicos están sometidas a un nivel adicional de reglamentación bajo la forma de normas profesionales, en ocasiones aún más estrictas que las de los propios gobiernos. Los efectos combinados del clima, de los desastres naturales y de las plagas acrecientan las dificultades de mantener a los animales en ciertos espacios. La vigilancia contra la transmisión de enfermedades zoonóticas se rige por normas sanitarias impuestas por la profesión y los gobiernos, con el refuerzo de las reglamentaciones que dictan agencias sanitarias locales, regionales y federales. La actual polémica sobre el mantenimiento de ciertos taxones en América del Norte está vinculada a la amenaza que las nuevas y estrictas normas de importación suponen para los programas de cría de primates no humanos, así como al temor que suscitan las infecciones por herpesvirus B y a la prohibición de transporte por líneas aéreas comerciales. Los repetidos fallecimientos registrados entre domadores y cuidadores de elefantes han llevado a la industria y a los gobiernos a replantearse la forma en que estas criaturas, potencialmente peligrosas, son mantenidas en cautividad.

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PALABRAS CLAVE: Gestión de la fauna salvaje - Reglamentación -Seguridad ambiental - Zoonosis.

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