Rev. sci. tech. Off. int. Epiz., 1993,12 (1), 115-135

Disease risks associated with wildlife translocation projects M.H. WOODFORD * and P.B. ROSSITER **

Summary: Translocation is defined as the movement of living organisms from one area for free release in another. Throughout the world, increasing numbers of native and exotic species are translocated every year. Most of these movements involve native mammals, birds and fish, and are made by private and national wildlife agencies to augment existing populations, usually for sporting purposes. The translocation of endangered species, often to reintroduce them into a part of the historical range from which they have been extirpated, has also become an important conservation technique. The success of potentially expensive, high-profile wildlife translocation projects depends to a large extent on the care with which wildlife biologists and their veterinary advisers evaluate the suitability of the chosen release site, and on the ability of the translocated animals to colonise the area. The veterinary aspects of reintroduction projects are proving to be of extreme importance. There are already instances of inadequate disease risk assessment resulting in expensive failures and, worse still, the introduction of destructive pathogens into naive resident wildlife populations. In this paper, some of the disease risks attending wildlife translocation projects are described and suggestions are made for the development of systematic procedures to reduce these risks both at the source of the founder animals and at the proposed release site. KEYWORDS: Conservation - Disease risks - Quarantine - Translocation Vaccination - Wild animals.

INTRODUCTION In recent years, the rate of global biotic impoverishment has greatly accelerated and is now said to be greater than at any time during the last 65 million years (51). Exponential human population growth and even greater increases in the r a t e of consumption of natural resources have led to the loss of many species and their habitats (60). Unfortunately, it is only now being realised that very few National Parks and other designated protected areas are large enough to support adequate populations of key species without the risk of slow erosion of genetic variability. This situation can be alleviated by the regular reintroduction of fresh genetic material, either in the form of

* Apt. B-709,500 23rd Street N.W., Washington D.C. 20037, United States of America. * Kenya Agricultural Research Institute, Muguga, P.O. Box 32, Kikuyu, Kenya.

116 live, individual animals from distant, unrelated sources or, indirectly, by using cryopreserved germplasm (semen and embryos). Translocation can be defined as the intentional movement of living organisms from one geographic area for free release into another, with the object of establishing, re-establishing or augmenting a population (29). The risk of disease introduction by wild animals or birds translocated from one part of the world to a n o t h e r for the pet t r a d e or to stock zoological collections is not addressed in this paper; nor is the long-distance dispersal of potentially pathogenic organisms by migratory animals and birds, unless this results from a translocation. A recent survey (1973-1986) of intentional releases of indigenous birds and mammals into the wild in Australia, Canada, New Zealand and the United States of America (USA) shows that, on average, nearly 700 translocations were conducted each year (24). Native game species, many of t h e m birds, accounted for 90% of these m o v e m e n t s . Many similar releases, usually for sporting purposes, are made each year in Europe and on a smaller scale elsewhere in the world. T h e translocation of r a r e , e n d a n g e r e d species has also b e c o m e an i m p o r t a n t conservation technique, especially for species with limited dispersal ability, since such species often find themselves confined in shrinking and fragmented habitats where early extinction can be predicted (61). Translocations of rare species can be expensive (15,35) and often attract great public attention (11). Several factors associated with the success of such projects have been discussed and evaluated by Griffith and colleagues (24) but, surprisingly, the possibility that disease might have a negative influence on the efforts of founder animals to establish themselves was not considered. However, other authors have drawn attention to the problem (7,13,16).

TYPES OF DISEASE RISK Most of the diseases likely to b e of importance in translocation projects are infectious. Whatever the objective of these projects may be, the risks involved will depend on a variety of factors. A m o n g these are the epidemiological situation at the source from which the animals derive and at the destination or release site. The source is often a zoological garden, a ranch or an extensive captive breeding establishment and is sometimes located on a distant continent. Occasionally, however, a supply of suitable wild animals for translocation can be found in another area within the country where the release is planned. The release site may be a National Park or other protected area where contact with other wild species may occur, or it may be a suitable habitat in an undesignated area where contact with domestic livestock and humans is an added hazard. Animals born and bred in a zoo or captive breeding facility in a distant country will acquire local infections and, in some cases, become symptomless carriers of disease agents. Zoo-bred stock is often exposed to exotic pathogens brought in from foreign countries and to infections transmitted by a t t e n d a n t s and visitors. F u r t h e r m o r e , captivity subjects some species to continual stress, resulting in immunodepression and increased susceptibility to infection. Tuberculosis, usually of the bovine type in ungulates and of human origin in primates, is common in zoos and unfortunately, the

117 current diagnostic tests for this disease are unreliable and difficult to interpret in the case of wild ungulates (48,21). Ranch-raised animals, usually herding ungulates, are often exposed to the common pathogens of local domestic animals. Brucellosis, bluetongue and various tick-borne haemoparasites are common examples, whereas equids are exposed to the endemic diseases of horses and donkeys in the country where they are raised.

DISEASES INTRODUCED BY TRANSLOCATED ANIMALS It is clear, therefore, that both zoo-bred and ranch-raised animals, as well as wildcaught stock, can bring new pathogens into a release area where these can cause disease among co-existing, immunologically naive wild and domestic animals. As has b e e n aptly r e m a r k e d , a translocated animal is not the representative of a single species but is r a t h e r a biological package containing a selection of viruses, bacteria, protozoa, helminths and arthropods (40). There have been many instances in which captive-bred (and sometimes wild-caught) animals have brought with them pathogens which have had a severe impact on wild and domestic stock in and around the release site (Table I). Some of these cases are well documented, such as the disastrous introduction of African horse sickness into Spain by two zebra (Equus burchelli) from Namibia in 1987 (42). Unfortunately, many reports are only anecdotal or rudimentary and unconfirmed. Capture and quarantine, in themselves, place a high level of stress on wild animals, especially those caught in the wild, and there is a great deal of variation in the response of species and age classes. Stress can lead to the clinical r e c r u d e s c e n c e of latent infectious diseases. For example, Cape buffaloes (Syncerus caffer) transported a long distance by lorry have excreted foot and mouth disease virus in sufficient quantities to infect cattle penned near the relocation site (26), and fatal cases of trypanosomosis have arisen in black r h i n o c e r o s (Diceros bicornis) c a p t u r e d and t r a n s l o c a t e d while harbouring inapparent trypanosome infections (37,19). A classic case of disease i n t r o d u c t i o n involves the o u t b r e a k of tuberculosis in Arabian oryx (Oryx leucoryx) in Saudi A r a b i a (6, 27, 36). T h e late King Khaled of Saudi Arabia was in the habit of turning loose all the herbivores which he received as gifts in a large, fenced enclosure outside Riyadh. Among these assorted animals, most of which had been zoo-bred in the country of their donors, there must have been a number which were carrying subclinical tuberculosis. Later, when it was decided to prepare a herd of these desert antelopes for release into the wild in Saudi Arabia, fifty-seven oryx were s e p a r a t e d out from the mixed herd of a n t e l o p e s and relocated by air to the National Wildlife Research Centre in Taif, some 600 miles away. Within a few weeks of translocation, some of the oryx became sick and died of acute tuberculosis, a disease apparently absent from the mixed antelope herd at Riyadh. It was considered likely that the stress of capture, crating and translocation played a part in the outbreak of clinical disease. Raccoons (Procyon lotor) t r a n s l o c a t e d in 1985 from Texas to West Virginia to augment the local raccoon stock for hunting purposes are believed to have brought with them parvoviral enteritis, a serious disease previously absent in West Virginia and now

118 TABLE I

Diseases introduced into release areas by translocated Disease/pest introduced

wildlife

Release area

Affected species

Ref.

African horse sickness

Spain

Domestic equids

42

Riyadh, Saudi Arabia (c/b)

Tuberculosis

Taif, Saudi Arabia

Translocates

Raccoon (Procyon lotor)

Texas (w/c)

Parvoviral enteritis West Virginia

Raccoon (Procyon lotor)

Florida (w/c)

Rabies

Reindeer (Rangifer tarandus)

Norway (c/b)

Translocated species

Origin

Zebra (Equus burchelli)

Namibia (w/c)

Arabian oryx (Oryx leucoryx)

27,6, 36

Local raccoons

2

West Virginia

Skunks (Mephitis mephitis), local raccoons

4

Warble flies Nostril flies

Greenland

Caribou 52,53 (Rangifer tarandus) 57

Mojave desert tortoise Pet shops in (Xerobates agassizii) California

"Respiratory disease"

Mojave desert

Wild tortoises

Bighorn sheep (Ovis canadensis)

Arizona (w/c)

"Viral pneumonia" New Mexico

Local bighorns

Plains bison (Bison bison)

Montana (c/b)

Tuberculosis Brucellosis

Canada

Wood bison 5 (B. bison athabascae)

Hares (Lepus europaeus)

Hungary and Czechoslovakia (w/c)

Brucellosis

Switzerland and Italy

Domestic animals, man

Rainbow trout (Salmo gairdneri)

USA (c/b)

"Whirling disease"

United Kingdom Trout

30

45

58

w/c = wild caught c/b = captive bred

enzootic in the local raccoon population (2). A similar case occurred when "a few thousand" raccoons were translocated from Florida to West Virginia in 1977, again for hunting purposes. This particular relocation is still blamed for the c u r r e n t rabies epizootic in raccoons and skunks (Mephitis mephitis) in Pennsylvania, Virginia and Maryland (4). Rabies is said to have been far less common in these states before the raccoon translocation from Florida. It is, of course, possible that the ongoing epizootic may be a reflection of the increase in the local raccoon population. In September 1952,225 domestic reindeer (Rangifer tarandus) were translocated by ship from n o r t h e r n Norway to western Greenland, with the aim of providing a new livelihood for the local Inuit (52). Unfortunately, t h e reindeer brought with t h e m a warble fly (Oedemagna tarandi) and a nostril fly (Cephenemyia trompe), both of which at that time did not occur in Greenland (53). In due course, these parasites began to affect the indigenous wild Greenland caribou (R. tarandus groenlandicus). Both flies severely harass the caribou throughout the relatively warm long summer days, so that the caribou are unable to feed sufficiently to build up the fat stores on which they

119 depend to survive the Arctic winter. This translocation proved a disaster for Greenland caribou which are now greatly reduced in numbers due to severe winter mortality. All caribou in western Greenland are now infested with both parasites (57). Sick specimens of the e n d a n g e r e d Mojave desert tortoise (Xerobates agassizii), unwanted by their owners, have been released back into the desert and are believed to have infected wild tortoises with a fatal upper respiratory tract infection, probably acquired on pet shop premises (30). Large numbers of hares (Lepus europaeus) are imported annually from Hungary and Czechoslovakia into Switzerland and Italy for sporting purposes. Some of these animals are infected with Brucella suis, a pathogen which can seriously affect domestic livestock (45). Plains bison (Bison bison), translocated in 1907 from Montana to Canada, brought with them tuberculosis and brucellosis; as a result, a decision was recently t a k e n to slaughter 3,200 infected animals in an attempt to eliminate the diseases from the Wood Buffalo National Park in Canada, where they t h r e a t e n the relict herd of wood bison (B. bison athabascae). However, public pressure has now caused the slaughter decision to be rescinded (5).

DISEASES ENCOUNTERED BY TRANSLOCATED ANIMALS AT THE RELEASE SITE Animals born and bred on a distant continent in a very different epidemiological environment may have encountered diseases endemic in their area of origin (and may sometimes have b e c o m e symptomless carriers of the p a t h o g e n s ) . H o w e v e r , t h e s e animals inevitably lack acquired immunity or resistance to the infections (equally exotic to them) which will challenge them at the release site. Many diseases and parasites are highly localised in distribution as a result of the specific ecological requirements of the pathogens and their vectors; even a short translocation of wild-caught animals from one eco-zone to a n o t h e r can result in exposure to unsuspected disease p r o b l e m s . Some examples are given in Table II. Approximately half of the fifty koalas (Phascolarctos cinereus) translocated from a tick-free area in Victoria, Australia to a nearby range infested with the ixodid vector of tick paralysis, rapidly succumbed (S. McOrist, personal communication). Adult Kafue Flats lechwe (Kobus leche) - a large Zambian antelope - were translocated into an area which was infested with t h e tick vector of h e a r t w a t e r and w h e r e this disease was enzootic in n e a r b y domestic stock. Within two m o n t h s , fifty-six lechwe had died. Autopsies revealed heavy tick infestations (Amblyomma variegatum) and characteristic lesions of heartwater (44). Had these species been born in the areas infested by the tick vectors, they would probably have acquired resistance to the respective diseases and the translocations would have been a success. Caribou (Rangifer tarandus) and moose (Alces americana) are seriously affected by the "meningeal w o r m " (Pneumostrongylus tenuis) of white-tailed d e e r (Odocoileus virginianus), and attempts to translocate these ungulates into the white-tailed deer range in north-eastern America have b e e n frustrated by cerebrospinal nematodosis acquired by the accidental ingestion of infected terrestrial molluscs while grazing (3). Botulism is enzootic in sheep and goats in Oman, and Arabian oryx bred in captivity under zoo conditions in the U S A have died of this disease when they were released into the desert in Oman (55).

120 TABLE I I

Diseases encountered at release sites by translocated

wildlife

Translocated species

Origin

Disease encountered

Release area

Source of pathogen

Koala (Phascolarctos cinereus)

Victoria, Australia (w/c)

Tick paralysis (vector: Ixodes spp.)

Victoria, Australia

Toxic agent in tick saliva

Lechwe (Kobus leche)

Zambia (w/c)

Heartwater (vector: Amblyomma spp.)

South Africa

Enzootic in local wild ruminants

Caribou (Rangifer tarandus)

Eastern USA (w/c)

Cerebrospinal nematodosis

Ontario

White-tailed deer 3 (Odocoileus virginianus)

Caribou (Rangifer tarandus)

Quebec (w/c)

Cerebrospinal nematodosis

Nova Scotia

White-tailed deer 3 (Odocoileus virginianus)

Arabian oryx (Oryx leucoryx)

USA (c/b)

Botulism

Oman

Enzootic in Oman

55

Muskrat (Ondatra zibethicus)

Canada (w/c)

Tularaemia

Soviet Union

Water voles (Arvicola amphibius)

46

Golden lion tamarin (Leontopithecus rosalia)

USA (c/b)

Unspecified

South-eastern Brazil

Not known

38

Hawaiian goose (Branta sandvicensis)

UK (c/b)

Avian pox (vector: mosquitoes)

Hawaii

Local birds

33,34, 9

Brush-tailed possum Tasmania (w/c) Bovine tuberculosis (Trichosurus vulpecula)

New Zealand

Deer, wild pigs, etc.

Black rhinoceros (Diceros bicornis)

Lowland Kenya Tsetse flies, local wildlife, domestic stock

Highland Kenya Trypanosomosis (w/c)

Ref.

44

28 39

w/c = wild caught c/b = captive bred

When muskrats (Ondatra zibethicus) were introduced into the former Soviet Union in the 1930s to augment the population of local fur-bearing rodents, they multiplied rapidly. At the time, tularaemia was enzootic in local water voles (Arvicola amphibius) which shared the wetlands with the translocated m u s k r a t s . M u s k r a t s are highly susceptible to tularaemia, and there ensued a massive epizootic of the disease in their expanding population. Tularaemia is a zoonosis and it was not long before the disease affected muskrat trappers as well. In this case, a disease which, previous to the muskrat translocation and p o p u l a t i o n explosion, had b e e n enzootic in the water voles and sporadic in the human population, assumed epizootic proportions and became a serious health hazard to humans and wild animals alike (46). In a n o t h e r , much-publicised translocation, captive-bred golden lion tamarins (Leontopithecus rosalia) were reintroduced into a p r o t e c t e d area in south-eastern Brazil; in the first two years, 18 of 26 "acclimatised" animals died and t h r e e were missing (38). The majority of deaths occurred shortly after release due to a variety of causes of which "disease" was said to be the main factor. After conjecture about herd

121 immunity in captivity and in the wild, it was suggested that " s o m e kind of immunological preparation, possibly including vaccination against specific infections, may come to be a significant part of reintroduction programmes" (38). Commenting on this reintroduction fiasco, Plowright (50) remarks that it is impossible to see how such an objective could be achieved without identification and culture of the " n a t u r a l " pathogens and development of the associated serological techniques. H e also noted that zoological collections provide a very unreliable guide to the diseases which may occur in the wild. Failure of the Hawaiian goose (Branta sandvicensis) to increase in n u m b e r s after reintroduction may have been due to its occupancy of only the higher altitudes of its historical range. Breeding had formerly occurred at lower, more suitable altitudes, but these became infested with introduced mosquitoes, vectors of avian poxvirus to which the goose is very susceptible (33). Black rhinoceros translocated in Kenya from tsetse-free highlands to tsetse-infested lowland areas have become infected with trypanosomosis due to Trypanosoma brucei and T. congolense (39). Many years ago, brush-tailed possums (Trichosurus vulpecula) from Tasmania were introduced into New Z e a l a n d to establish a new species of fur-bearer. T h e animals found an empty ecological niche and multiplied greatly, in spite of heavy trapping for the fur t r a d e . W h e n the d e m a n d for possum fur collapsed, t r a p p i n g ceased to b e economically attractive. There are now over 70 million possums in New Zealand and 3-30% of them are said to be infected with bovine tuberculosis, a disease which does not occur in possums in T a s m a n i a (28). T h e economic consequences for t h e livestock industry in New Zealand, including deer farming, need hardly be stressed. When translocated along with a wild animal host, an avirulent, inapparent infection can sometimes become virulent on passage through a new host in a new environment. An example of this occurred when a n u m b e r of wild rabbits (Lepus cuniculus) were translocated from E n g l a n d to South Africa. A small n u m b e r (5.7%) of rabbits in England carry an avirulent strain of toxoplasma. On reaching South Africa, t h e s e animals infected local rats (Rattus natalensis) and the passaged toxoplasma assumed a virulent form (31).

MINIMISING THE RISKS T h e success of translocation projects d e p e n d s to a large extent on the ability of wildlife biologists and their veterinary advisers to evaluate the suitability of the release site chosen, and the ability of the translocated animals to colonise the area and establish a viable breeding population. In this context, the veterinary dimensions of translocation projects are proving to be of great importance, and failure to carry out adequate preliminary investigations has already resulted in several expensive fiascos. Worse still, the introduction of destructive parasites and disease agents into often naive resident populations has had profound negative c o n s e q u e n c e s . It is t h e r e f o r e i m p o r t a n t that systematic veterinary investigations be carried out prior to the choice of the release site so that all ecological risks can be assessed in advance and, if necessary, appropriate modifications can be made to the reintroduction plans.

122 Veterinary intervention at the source of the founder stock V e t e r i n a r y involvement should begin as early as possible in the p r e p a r a t i o n of translocation plans so that the risks can be identified and avoided. The criteria for the selection of founders for a reintroduction attempt have been discussed by Stanley-Price (55). Disease risk is considered to be a major factor in assessing the wisdom of population reinforcements, and a case is cited where at least one release of rehabilitated orang-utans (Pongo pygmaeus) in Indonesia was cancelled because some were found to be infected with human tuberculosis (32). Tuberculosis and human herpesvirus B have recently been found to infect orang-utans translocated from Taiwan where they had been held captive, to Indonesia where it was planned to release them back into the wild (T. Sullivan, personal communication). These animals are now being held in isolation until an appropriate solution is found. After founders have been selected, the group should be placed in quarantine for a m i n i m u m of thirty days. T h e site of the q u a r a n t i n e station may be at the zoo, wild animal park or ranch where the animals were raised, or it can be at a separate location if animals from a number of different sources are to be combined. The main requirement is that the group should be completely isolated from its own and related species, and if possible from all species, with the necessary exception of a limited number of human attendants. The veterinary import requirements of the receiving country should be known, so as to ensure that the period of quarantine and any special screening requirements can be respected. The quarantine premises must be appropriate for the species concerned and for the epidemiological situation, e.g. n e t t e d enclosures will need to be provided where mosquito-borne diseases are to be excluded. The premises must also facilitate visual and clinical examination, as well as sampling and chemical immobilisation, if necessary. Isolation from all possible sources of infection must be absolute and human attendants must be screened for transmissible diseases, e.g. tuberculosis. Early in the quarantine period, disease screening procedures must be instituted, such as the following: a) T h e b r e e d i n g history and clinical records of the founder stock (if available) should be examined. Since founders gathered at the quarantine station may have their origins in several zoos or captive-breeding establishments, this may prove tedious. However, it is an important procedure because some zoos have a poor health status, especially for such diseases as tuberculosis, and this will influence the interpretation of subsequent tests. b) The stock should be given a thorough visual clinical examination, during which the veterinarian will look for aberrant behavioural traits as well as clinical signs. When the animals are released and exposed to the selective forces of their wild environment, any physical or behavioural abnormality will reduce their chances of survival. This is particularly important when the founders are derived from captive-bred stock. Animals accustomed to humans are only rarely suitable for reintroduction projects. c) Local and regional disease patterns in the source area must be assessed, possibly with reference to the Animal Health Yearbook published by the United Nations Food and Agriculture Organisation ( F A O ) , the Office International des Epizooties (OIE) and the World H e a l t h Organisation ( W H O ) and, for E u r o p e , to Faune sauvage d'Europe (Informations Techniques des Services vétérinaires) for details of disease

123 occurrence in the country c o n c e r n e d . T h e advice of local v e t e r i n a r i a n s , wildlife biologists and livestock farmers should also be actively sought. O n the basis of these enquiries and a k n o w l e d g e of the c o m m o n p a t h o g e n s of the founder species, the veterinarian should prepare a screening protocol which will also take into account any disease problems which may have been associated with previous translocation of the taxon, as well as any particular p a t h o g e n s stipulated for the release country by international or national veterinary authorities. d) Before u n d e r t a k i n g the screening p r o c e d u r e s , all founder animals should b e permanently marked by ear tag, tattoo and/or electronic micro-chip. e) Biological samples should be collected from the founder animals early on the day of testing so as to allow for same-day processing or rapid packaging and swift despatch to the laboratory. f) The samples should be sent to internationally recognised reference laboratories. These institutions have the requisite expertise and will use the most up-to-date tests. It may be an advantage to send replicate samples to different laboratories and obtain independent interpretations of the results. g) Laboratory procedures for the direct detection of evidence of infection should include: - clinical haematology - blood smears for h a e m o p a r a s i t e s (for t r y p a n o s o m e s the buffy coat of a micro-haematocrit tube may be examined) - bacterial cultures - viral cultures - faecal egg counts - faecal larval culture (especially for lungworm) - urinalysis (and examination of urine for kidney worm eggs) - molecular biological techniques (especially nucleic acid hybridisation with specific probes) are robust, highly sensitive and increasingly available. h) Laboratory procedures for the indirect detection of evidence of infection should include demonstration of antibodies. The presence of antibodies to a specific pathogen in a single serum sample at a determined level of dilution (titre) reveals that the animal has been exposed to infection by the pathogen concerned (either natural infection or, in the case of zoo or captive-bred stock, the possibility of prior vaccination). Serial serum samples showing an active rising antibody titre are required to determine whether an animal is incubating or recovering from an infection. D e p e n d i n g on the p a t h o g e n , further tests may be needed to determine whether specific antibodies in serum indicate that an animal is likely to be an infectious carrier of a given disease. In some cases, a total ban on the importation (e.g. into a "clean" country) of certain species may be desirable. For example, Greenwood and Cooper (23) drew attention to the likely danger represented by prairie falcons (Falco mexicanus) and great horned owls (Bubo virginianus), both of which are commonly infected with falcon herpesvirus, and suggested that the importation of these species from the U S A into Great Britain should be restricted or banned.

124 Veterinary intervention at the proposed release site W h e r e possible, the veterinarian should visit the proposed release site during the planning phase (and well in advance of translocation) to carry out the following tasks: - to consult with the D i r e c t o r s of the V e t e r i n a r y and Wildlife Services of the recipient country (this is i m p o r t a n t to avoid misunderstandings and to ascertain whether special tests or certifications are required by these directorates); - to determine which diseases of wild and domestic animals and which vectors and reservoirs are enzootic in contiguous territories. A study of local seasonal wildlife migrations and domestic livestock trade routes is also relevant; - to consult regional veterinary authorities with regard to the prevalence and incidence of local diseases; - to consult the local diagnostic laboratory on the results of recent domestic animal disease surveys; - to evaluate t h e degree of contact likely b e t w e e n t h e translocated animals and domestic stock, wildlife and humans; - to decide if the vaccination programmes of the national Veterinary Services are adequate to provide a protective immune barrier for susceptible wildlife against such diseases as rinderpest, foot and mouth disease and rabies; - to survey the proposed release site and assess the likely presence of disease vectors and disease foci (the overall suitability of the release site may be greatly influenced by these factors); - if possible, to survey and sample selected wildlife species and domestic stock at the release site and screen them for appropriate suspected pathogens; - to investigate availability of suitable vaccines to protect founder stock against local disease hazards identified during these investigations; - to determine whether any mineral or trace element deficiencies or excesses occur in the release area (if supplementary feeding is planned, foodstuffs - especially hay may have to be transported over long distances from a different eco-zone and should be checked for toxic substances, e.g. selenium, and for ticks and other parasites); - to inspect t h e release area (especially in the dry season) for the p r e s e n c e of poisonous plants which may be unfamiliar to translocated animals; - to investigate why the species to be translocated is absent from the area (have previous translocations failed? if so, was disease a reason?); - to prepare a report and send at least one copy to the Directors of the Veterinary and Wildlife Services of the recipient country. Pre-release planning T h e strategy of confining an integrated social group in a large, open enclosure near or in the release area for a considerable period before release has frequently been applied. This strategy has a number of advantages (55): - social groupings can be adjusted and become established; - the period of confinement acts as an extended quarantine during which clinical signs of infectious or contagious disease may be detected;

125 - contact with domestic stock and other wildlife can be excluded, thus reducing the chance of disease transmission; - founder stock can become acclimatised to local conditions; - handling is minimised but can also be employed with little stress, when necessary, if the enclosure is equipped with a well-designed crush. Once the founder stock is released, there will be little chance of protecting against the challenge of disease agents. Nevertheless, successful attempts have been made in the Kruger National Park to vaccinate valuable roan antelope (Hippotragus equinus) against anthrax by injecting the vaccine via darts fired from a helicopter (20), and the success of rabies vaccine baits for foxes (Vulpes vulpes) in Europe is now well known (10,45).

INTERPRETATION OF SURVEY AND SCREENING RESULTS Investigating the disease history of the source of founder animals will help in deciding if any biological tests should b e given priority. Information that zoo-bred animals have been vaccinated against a certain disease (e.g. leptospirosis) may suggest that this disease is a p r o b l e m in the zoo supplying the animals. Tuberculin tests for animals originating in a zoo where tuberculosis is enzootic (few will admit this) need to be i n t e r p r e t e d m o r e carefully t h a n w h e r e the disease is u n k n o w n . B l u e t o n g u e and epizootic haemorrhagic disease sera may cross-react, and virus isolation tests may be necessary to d e t e r m i n e w h e t h e r positive serology indicates carrier status for either virus. Zebra and wild African suids are symptomless carriers of African horse sickness and African swine fever viruses respectively, and are t h e r e f o r e subject to strict international movement regulations. Elephants (Loxodonta africana) and aardvarks (Orycteropus afer) may have antibodies to these respective disease agents, but the significance of these antibodies is unclear. So great is the variety of mammals, birds, reptiles, amphibians and even insects which may, in future, become the object of translocation projects, that specialist advice will almost certainly be required for the interpretation of results of the investigations carried out b o t h at the source of t h e founder species and at the release site. I n t e r n a t i o n a l disease m o n i t o r i n g organisations such as t h e O I E , F A O and W H O may all be consulted, as may the Veterinary G r o u p ( V G ) of the Species Survival Commission (SSC) of the World Conservation U n i o n ( W C U ) and the Veterinary Services of the countries concerned.

PROPHYLACTIC VACCINATION OF FOUNDER STOCK T h e decision to vaccinate and the choice of vaccines will d e p e n d on the interpretation of the results of the surveys and investigations described above. If there is a significant risk of founder stock being infected with serious pathogens' at the release site, it may b e advisable to carry out vaccination. T w o main types of vaccine are available: modified live vaccines which have reduced virulence for one or more species, and a r a n g e of " i n a c t i v a t e d " vaccines which c o n t a i n n o viable organisms. T h e advantages of the live vaccines are that they grow in the host after

126 inoculation and usually induce a solid immunity similar to that found in animals which h a v e r e c o v e r e d from t h e p a r t i c u l a r p a t h o g e n (if such an i m m u n i t y occurs). Consequently, vaccination with a live vaccine usually requires only one inoculation, which is a great advantage when dealing with wildlife, especially those animals which need restraint. However, while live vaccines have reduced virulence for some species, they may be pathogenic for others. For instance, live canine distemper virus vaccines have induced disease in susceptible mustelids, including the endangered black-footed ferret (Mustela nigripes). Live feline parvovirus vaccine (feline e n t e r i t i s or p a n l e u k o p a e n i a ) which is i n n o c u o u s for d o m e s t i c cats is t h o u g h t to h a v e caused disease in o t h e r felines. A l t h o u g h safe in most b r e e d s of cattle, a live r i n d e r p e s t vaccine p r e p a r e d in rabbits caused significant mortality when tested in a variety of African artiodactylids (14). Fortunately, the current cell culture-derived rinderpest vaccine has p r o v e d b o t h safe and efficacious in the wild species t e s t e d to date (including buffalo, eland and warthog, which are highly susceptible, and impala and oryx which are less so) (P.B. Rossiter, unpublished findings; 8, 49). T h e control of rabies in western E u r o p e and elsewhere has been radically improved through the use of live vaccines a d m i n i s t e r e d orally to foxes and o t h e r wildlife in baits. T h e r e is considerable variation in the susceptibility of different species to live rabies virus, and an important concern was the risk that live vaccines, although innocuous for the fox or other target species, could prove virulent for other species which might incidentally scavenge the baits. For vaccination of founder stock, live vaccines offer several advantages, provided they have been proven to be safe in the chosen species. Care should be taken to use t h e same strain of a p a r t i c u l a r vaccine which has b e e n successfully t e s t e d in the species, since different manufacturers may use different strains. Unless they have been tested with the vaccine, it is best to avoid vaccinating pregnant dams, as some live (especially viral) vaccines can cause foetal death and/or abortion. Similarly, some live vaccines may cause disease in very young animals, and t h e instructions of the m a n u f a c t u r e r should b e sought on this m a t t e r . If dams h a v e b e e n vaccinated previously, m a t e r n a l i m m u n i t y may r e d u c e the immunogenicity of live vaccines a d m i n i s t e r e d to y o u n g animals (carnivores less t h a n t h r e e to four m o n t h s old, herbivores less than six months old). Inactivated vaccines carry little risk of infecting the host, although some toxoids can still induce local reactions at the site of inoculation. H o w e v e r , since they do not replicate in the host, inactivated vaccines may require more than one application in the first instance, as well as frequent boosting. It remains to be seen whether this will prove to be the case with the inactivated canine distemper virus vaccines currently being investigated for the protection of h a r b o u r seals (Phoca vitulina) against phocid distemper (59). Inactivated vaccines are often incorporated into alum or other "adjuvants", which help to stimulate the immune response but can also cause significant local reaction at the inoculation site. A good example of the use of an inactivated viral vaccine to protect a captive-bred species prior to exposure to infection in the wild is afforded by the case of the whooping crane (Grus americana). Although never abundant in North America, the whooping crane became endangered largely because of habitat modification and destruction. To promote recovery, a captive propagation and reintroduction programme was initiated in 1966 at the Patuxent Wildlife Research Centre (PWRC) in Laurel, Maryland, USA. However, in 1984, seven of thirty-nine whooping cranes at the P W R C died as a result of

127 infection by eastern equine encephalitis ( E E E ) virus, an arbovirus which infects a wide variety of indigenous bird species, although mortality is generally restricted to introduced birds. Following identification of the causal agent, surveillance and control measures were implemented, including serological monitoring of both wild and captive birds for antibody, and assay of locally trapped mosquitoes for the virus. In addition, an inactivated E E E virus vaccine, d e v e l o p e d for use in h u m a n s , was e v a l u a t e d in t h e captive whooping cranes. Results to date suggest that the vaccine will afford protection to susceptible birds. As part of the effort to r e s t o r e whooping crane p o p u l a t i o n s in t h e wild, t h r e e geographically isolated areas in the eastern U S A are being considered as possible reintroduction sites. Since E E E viral transmission occurs annually in parts of the eastern USA, it will be important to survey for the virus and its mosquito vectors before selecting the release sites. Although the dying off of whooping cranes due to E E E virus was a setback for the captive breeding programme, it is now known that this disease must be considered in establishing wild crane populations (17). When there is an urgent need to vaccinate stock with unknown susceptibility to a live vaccine, it is preferable to employ an inactivated vaccine, if available. Failing this, the live vaccine could be tested in one or two founder stock, provided these are isolated from the rest of the group. Protective immunity may develop after a few days or several weeks. Immunisation should therefore be carried out well in advance of translocation (this provides a further quarantine period in case the animals are incubating a field infection or excreting the live vaccinal agent administered to t h e m ) . It should be r e m e m b e r e d that some live vaccines induce persistent infections, the vaccinates in effect becoming carrier animals which may pass on infection to vectors or susceptible species. Fortunately such cases are rare.

POST-RELEASE HEALTH MONITORING Regular, systematic m o n i t o r i n g of t h e health and r e p r o d u c t i v e p e r f o r m a n c e of translocated animals may provide an early warning of incipient disease problems. If the causes of disease or reduced productivity can be determined, a change in management may be indicated for current or future translocations. Provision for long-term monitoring is often included in translocation project plans but is seldom carried out once t h e released animals a p p e a r to b e surviving in the wild. Post-release monitoring of the Hawaiian goose was r e c o m m e n d e d during the project design (34), although little monitoring actually took place. After the release of 1,244 birds over sixteen years on Hawaii and a further 391 on Maui Island, the status of the reintroduced population was unknown and the reasons for the limited success (believed to be associated with avian poxvirus infection) were a m a t t e r for conjecture (9).

128

FUTURE PROBLEMS T h e veterinarian concerned with wildlife translocation should also be aware of emerging disease problems, including: - Peste des petits ruminants (PPR), a rinderpest-related disease of sheep and goats, which has not been reported to date in wild antelopes but which has caused fatal disease in captives (22), is extending its range southward in domestic stock in Sudan and Ethiopia. PPR is a disease which will have to be considered in any plans for moving wild animals into, out of, or within the East African region. - T h e accidental introduction of the New World screw-worm (Cochliomyia hominivorax) into Libya from Central America, in 1988, shows the ease with which a devastating parasite can be transferred from one hemisphere to another, albeit this time by domestic stock. The cost of the successful eradication programme carried out by the F A O was in excess of US$80 million. - Rinderpest is again expanding its range in East Africa, particularly in Sudan, Ethiopia, Uganda and Kenya, assisted by civil disorder and poorly funded Veterinary Services. - Tuberculosis, a disease which is now m o r e c o m m o n in zoos than in domestic stock, occurs in wild animals only where there has been contact with man or infected domestic animals. In Africa, tuberculosis is p r e s e n t in Cape buffalo and warthogs (Phacochoerus aethiopicus) in the Queen Elizabeth National Park, Uganda (62), in red lechwe (Kobus leche) on the Kafue Flats in Zambia (18), in Cape buffalo, greater kudu (Strepsiceros strepsiceros) and grey duiker (Sylvicapra grimmia) in South Africa (43, 45), in many wild species in New Z e a l a n d (1) and in badgers (Meles meles) in the United Kingdom (56). - Brucellosis, said to be the most economically important disease of wildlife in North America (T. Thorne, personal communication) is self-limiting in wild ungulates but is perceived as a constant threat to contiguous domestic livestock. - Sarcoptic mange is a serious and often overlooked disease of Spanish ibex (Capra ibex), Swiss chamois (Rupicapra rupicapra) and Swedish foxes. - Malignant catarrhal fever (MCF) is a killer of rare deer species, such as Père David's deer (Elaphurus davidianus) and also presents a serious threat to endangered Asian wild cattle (41). The possibility of the spread of M C F infection to these species by carrier wildebeest (Connochaetes taurinus) or domestic s h e e p should be remembered. - Foot and mouth disease (FMD) is of major economic significance in some African countries, particularly those exporting beef to E u r o p e , such as Zimbabwe, Botswana and South Africa. Although large areas of these countries have been declared free of F M D , in other areas (usually inhabited by herds of buffalo) F M D is enzootic. The intentional translocation of wild ungulates from affected to FMD-free zones is likely to be permitted (if at all) only after stringent testing and prolonged quarantine. - Vector-borne protozoa and viruses present a particularly serious risk to birds translocated long distances over land or across oceans (47). Long distance east/west translocations may introduce disease agents into north/south migratory flyways from which they were previously absent. T h e potential risk is great since five t h o u s a n d million birds are estimated to migrate southwards each autumn from the western and central Palaearctic to wintering areas in Africa (12).

129

DISEASE TRANSMISSION HAZARDS WITH CRYOPRESERVED GERMPLASM In the fairly near future, translocation of wild animal gametes and embryos may become an accepted technique for minimising the effects of inbreeding in small isolated populations. W h e n genetic resource banking p r o g r a m m e s b e c o m e established, the disease implications of these activities will have to be addressed. The diseases transmissible by semen and embryo transfer have been reviewed by Hare (25) and Singh (54). Disease transmission between different populations can be greatly r e d u c e d by e m b r y o transfer, b e c a u s e an intact e m b r y o collected from a diseased mother is often free from bacterial and viral disease agents and, therefore, does not transmit the disease to the foster mother. In addition, the surrogate mother may confer passive i m m u n i t y to t h e offspring which develops from a t r a n s f e r r e d embryo. This passive immunity may occur transplacentally or via the colostrum and can prove of value in producing offspring passively immune to local enzootic diseases. If the results of research on domestic animal embryos can be extrapolated to wild animals, it would seem that the potential of embryos to transmit infectious disease is considerably less than that of semen or live animals. In fact, it remains to be established whether, under field conditions, disease transmission ever occurs via embryo transfer. Sufficient research has been carried out with embryos from donors infected with bovine leukaemia virus and foot and mouth disease virus to determine that these viruses will not be t r a n s m i t t e d via embryos, provided the e m b r y o s are h a n d l e d properly (54). Research is u n d e r w a y at p r e s e n t to d e t e r m i n e w h e t h e r similar conclusions can be reached for other pathogens. Little research, if any, has b e e n d o n e on the disease transmission p o t e n t i a l of cryopreserved germplasm derived specifically from wild animals. Semen clearly has great potential for the spread of infectious diseases, but also provides an excellent means of disease control when collected and transferred artificially using strict aseptic techniques. Because direct animal contact is avoided, the health status of the donor can be predetermined and, if the semen is frozen, aliquots can be tested for the presence of micro-organisms. E m b r y o s have less p o t e n t i a l for disease transmission t h a n s e m e n . A t the developmental stage at which embryos are usually transferred, they are protected by a relatively thick capsule, the zona pellucida. F o r the e m b r y o to transmit infectious disease, it must either be infected with a minimum infective dose or act as a carrier through association of the disease agent with the zona pellucida. Preliminary evidence suggests that while m a n y disease agents are r e m o v e d or inactivated by washing or other t r e a t m e n t s , a small n u m b e r are not. C u r r e n t regulations to control disease transmission by embryos of domestic animals are based largely on the principle that if donors are free from specified diseases, the embryos will be similarly free. Evidence to date suggests that this a p p r o a c h may b e unnecessarily restrictive with r e g a r d to a number of diseases (25). It is expected that the principles summarised here will be applicable to cryopreserved wildlife germplasm. T h e results of current research on diseases of domestic animals transmissible by semen and embryo transfer techniques can probably be extrapolated to include cryopreserved wildlife genetic material, although care will be needed to ensure that specific wildlife diseases are not transferred.

130

DISCUSSION S o m e eighteen species have been reintroduced into the wild after captive p r o p a g a t i o n . In at least six cases - P è r e David's deer, Przewalski's horse (Equus przewalskii), red wolf (Canis rufus), A r a b i a n oryx, G u a m kingfisher (Halcyon cinnamomina) and Guam rail (Rallus owstoni) - these species were extinct in the wild at the time of the reintroduction; Père David's deer, in fact, had been extinct for 800 years! A number of other species, notably the California condor (Gymnogyps californianus) and the black-footed ferret, are likely to b e reintroduced into their native habitat as soon as captive numbers are considered adequate. In the majority of projects, systematic attempts have not been made to quantify and minimise the veterinary risks attending t h e translocation of t h e founder animals. N o t a b l e exceptions to this generalisation have b e e n the careful screening and preparation of the black-footed ferret for return to the wild, and the development of stringent veterinary protocols for the Arabian oryx destined for release in the deserts of O m a n . Protocols for the oryx h a v e now b e c o m e so strict that the captive source (a zoological collection in the USA) from which founder and reinforcement stock has been obtained is no longer able to comply. T h e "rescue", rehabilitation and return to the wild of sick and injured wild animals and birds is an activity which receives the attention and financial support of the general public. These activities are often carried out by enthusiastic amateurs and can, in some cases, be h a z a r d o u s . Animals which are sick may wander long distances from their home range, and migrating birds may alight many miles from their destination. If such specimens, when apparently restored to health, are released back into the wild, they may become serious foci of infection for local animals. Even more dangerous is the return of sick strays to their distant natural habitat after a period in captivity during which they may h a v e b e e n in contact with diseased animals of the same or related species from other sources. M e m b e r s of the veterinary profession with experience and expertise in wildlife disease should become involved in the planning of translocation projects to ensure that appropriate quarantine and screening measures are carried out. In special cases, the quarantine period may need to be extended (e.g. if tuberculosis is perceived as a special hazard). Such a variety of disease conditions affects the great range of taxa which may become the object of future translocation projects that no simple guidelines can cover all exigencies. E a c h case must be separately evaluated, taking into account all biological, ecological, geographical and epidemiological circumstances. Only then will the inherent risks in moving potential "disease packages" across the world be minimised and the chances of failing to establish a healthy new wild population significantly reduced. In the long term, the establishment of a data base on infectious agents and diseases of wildlife would be a very important support activity. T h e publication of bulletins of wildlife disease occurrence on a global scale, drawing on information from such a data base, would assist veterinarians in evaluating the disease risks which may a t t e n d a translocation proposal.

* * *

131 RISQUES SANITAIRES LIÉS A U X PROJETS D E TRANSFERT D'ANIMAUX SAUVAGES. - M.H. Woodford et P.B. Rossiter. Résumé : Un transfert peut se définir comme un déplacement d'êtres vivants d'une zone vers une autre, où ils sont relâchés. De plus en plus d'espèces autochtones et exotiques sont ainsi déplacées chaque année de par le monde. Dans la plupart des cas, il s'agit d'espèces autochtones de mammifères, d'oiseaux et de poissons, transférées par des institutions privées ou publiques aux fins de repeuplement, généralement pour favoriser le développement des activités de sport ou de loisir. Le transfert des espèces menacées, souvent réalisé dans le but de réintroduire ces animaux dans une partie de leur habitat d'origine d'où ils avaient disparu, est aussi devenu une technique importante de conservation. Le succès de projets aussi ambitieux, qui peuvent se révéler très coûteux, dépend, pour l'essentiel, non seulement du soin qu'apportent les biologistes et les vétérinaires à l'évaluation du site de destination, mais aussi de l'aptitude des animaux transférés à coloniser la région. Les aspects vétérinaires des projets de réintroduction s'avèrent extrêmement importants. Il existe déjà des exemples d'échecs coûteux imputables à une mauvaise évaluation des risques sanitaires et, pire, de cas où des agents pathogènes destructeurs ont été accidentellement introduits au sein de populations sauvages qui en étaient jusqu'alors indemnes. Les auteurs décrivent certains des risques liés aux projets de transfert d'espèces sauvages et proposent que soient développées des procédures systématiques visant à réduire ces risques, aussi bien au niveau du site d'origine qu'au niveau du site de destination prévu. MOTS-CLÉS : Conservation - Faune sauvage - Quarantaine - Risques sanitaires - Transfert - Vaccination.

* * RIESGOS SANITARIOS ASOCIADOS A LOS PROYECTOS DE TRASLADO DE LA FAUNA SALVAJE. - M.H. Woodford y P.B. Rossiter. Resumen: Un traslado se define como la captura y el desplazamiento de seres vivos de una zona a otra donde se les devuelve la libertad. Cada año se traslada en el mundo un número mayor de especies autóctonas y exóticas. La mayoría de los animales desplazados son especies autóctonas de mamíferos, aves y peces, cuyo traslado, efectuado por organismos nacionales o privados, se hace con vistas a su repoblación, generalmente para fines deportivos o recreativos. El traslado de especies amenazadas de extinción, frecuentemente con el fin de reintroducirlas en una parte del ambiente original del que habían desaparecido, constituye también ahora una importante técnica de conservación. El éxito de estos ambiciosos proyectos, que pueden resultar costosos, depende en gran medida del cuidado con el que los biólogos especialistas de la fauna salvaje y sus asesores veterinarios evalúen la adecuación del lugar seleccionado para soltar a los animales y en la capacidad de los animales trasladados de colonizar dicho lugar. Los aspectos veterinarios de los proyectos de reintroducción son sumamente importantes. Existen ya ejemplos de fracasos costosos debidos a evaluaciones

132 de riesgos incorrectas y, peor aún, de introducción de agentes destructores en poblaciones salvajes libres de ellos hasta entonces.

patógenos

Los autores describen algunos de los riesgos asociados a los proyectos de traslado de la fauna salvaje y proponen la elaboración de procedimientos sistemáticos para reducir dichos riesgos, tanto en el lugar de procedencia de los animales como en su lugar de destino. PALABRAS CLAVE: Conservación - Cuarentena - Fauna salvaje - Riesgos sanitarios - Traslado - Vacunación. *

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