Review

Wildl. Res., 1993, 20, 687-98

The Importance of Disease in

Reintroduction Programmes

K. L. viggersA, D. B. ~ i n d e n m a y e rand
~ D. M. sprattC
A Division of Biochemistry and Molecular Biology, The Australian
National University, Canberra, A C T . 0200, Australia.
Centre for Resource and Environmental Studies, The Australian
National University, Canberra, A.C.T. 0200, Australia.
Division of Wildlife and Ecology, CSIRO, P.O. Box 84, Lyneham,
A.C.T. 2602, Australia.

Abstract
Disease may play an important role in the decline or extinction of small, isolated animal populations.
Disease also has thwarted attempts to reintroduce some endangered captive-bred species. Despite this,
the impacts of disease rarely have been considered in the planning and design of reintroduction
programmes. A remnant wild population could be decimated by a disease cointroduced with reintro-
duced animals. Alternatively, diseases that are endemic in wild animal populations could be fatal
for those immunologically naive individuals that are reintroduced. We contend that the planning of
reintroduction programmes should include an examination of the potential impacts of disease on extant
populations and on animals targeted for release. A number of steps are outlined to reduce disease risk
and to minimise the probability of failure of reintroductions because of disease.

Introduction
Stochastic events such as the outbreak of disease have been important in the decline or
extinction of several endangered species. In the case of the heath hen, Tyrnpanchus cupido
cupido, blackhead (a disease caused by Histomonas meleagridis), lack of genetic variability
and natural catastrophes led to the extirpation of the species, after the loss of habitat and
hunting initially reduced the population (Simberloff 1986, 1988). H. meleagridis was co-
introduced with the domestic turkey, Meleagris gallopavo, to an island refuge supporting a
remnant heath hen population (Simberloff 1986). In another example, the canine distemper
virus had a substantial negative impact on the remaining wild population of the black-footed
ferret, Mustela nigripes (Thorne and Williams 1988; Clark 1989).
In an effort to counter the worldwide loss of biodiversity, there has been increasing
interest over the last few decades in mechanisms for supplementing existing small populations
or re-establishing them in parts of their former natural range (Griffith et al. 1989; Kleiman
1989). These approaches can be considered collectively as part of 'reintroduction biology'.
Although disease has contributed to the decline or extinction of small populations of some
species, its importance has been largely neglected in planning reintroduction programmes.
Here, we outline the potential impacts of parasitic and infectious disease for reintroduction
programmes as well as for captive and wild populations. We also describe a series of
simple measures that may reduce the probability of disease jeopardising the success of
reintroductions.
1035-3712/93/050687$05.00
 K. L. Viggers et al.

A Definition of Reintroduction Biology

There are three broadly defined methods of manipulating populations by transferring
animals from one location to another (after Konstant and Mittermeier 1982): translocation,
introduction and reintroduction. Translocation is the transfer of animals from one part of
their historic geographic range to another (Konstant and Mittermeier 1982; Kleiman 1989).
The removal of individuals of the common brushtail possum, Trichosurus vulpecula, from
suburban Melbourne to areas outside the city is an example of translocation (Pietsch 1993).
Introduction involves the accidental or intentional introduction of animals to previously
unoccupied areas, such as the release of the common brushtail possum in New Zealand,
where it is now a major pest (Cowan 1990). Reintroduction is the release of wild-caught or
captive-bred animals into areas where the species has declined or disappeared. There are two
types of reintroduction (after Lindburg 1992): (1) re-establishment reintroduction, which
is the utilisation of captive-bred animals to re-establish an extinct wild population (e.g.
European wisent, Bison bonasus; Pucek 1986) (this may include the transfer of wild-caught
animals to parts of the former range where the species is no longer present) and (2) re-
stocking reintroduction, which involves supplementing a declining population with captive-
bred animals [e.g. the helmeted honeyeater, Lichenostomus melanops cassidix (Menkhorst
and Middleton 1991)l. The general principles associated with the disease and health status
of wildlife populations are pertinent to all the forms of population manipulation that have
been defined above.

The Importance of Disease in Reintroduction Biology

Factors that need to be taken into account in reintroduction programmes may include:
an understanding of the processes that contribute to the demise of wild populations, habitat
suitability, behavioural biology, the density of wild populations of congeners, predators
and competitors, and the genetic composition of those individuals to be released. As a
consequence, reintroduction programmes typically require detailed planning (Menkhorst and
Middleton 1991; Lindburg 1992), considerable financial support (Kleiman 1989; Woodford
and Kock 1991), and substantial human resources for many years to implement and monitor
the programme. Despite this, reintroductions often fail. To increase the probability of
success, the risks of disease should be considered and key factors are discussed below.

Disease Considerations in Reintroduction Biology

Co-introduction of Disease
Wildlife that are reintroduced into the natural environment folIowing rehabilitation or
captive propagation may constitute a significant disease risk to wild populations of con-
specifics or other species because animals exposed to new agents of infectious disease during
captivity may act as carriers when released and may transmit disease to wild populations
(Haebler 1992). Infectious disease may also be introduced to wild populations when captive
animals with endemic disease are translocated or introduced into an area where those
diseases are not known to occur (Haebler 1992).
Pathogens present in captive-reared and released animals may infect the remnant
population. 'A major potential problem for a restocking reintroduction programme is the
cointroduction of a disease to which the extant population has not been exposed. Such a
problem arose with the proposed release of hand-raised orang-utans, Pongo pygmaeus,
infected with tuberculosis, Mycobacterium tuberculosis, into an area inhabited by unifected
conspecifics (Jones 1982). This infectious disease could have decimated resident orang-utan
populations, as well as creating a serious public health risk (Jones 1982).
New diseases that are not known to occur in wild populations may arise in captive
Disease and Reintroductions

animals. The introduction of such diseases to the wild could have a substantial negative
impact on the health and survival of wild populations. In the past decade a virulent
viral disease called callitrichid hepatitis has emerged in captive golden lion tamarins,
Leontopithecus rosalia (Montali and Bush 1992). This disease causes high mortality and has
not been detected in remnant wild populations of this species (Montali and Bush 1992).
Although the epidemiology of the disease is still not fully understood, captive golden lion
tamarins that have antibody for callitrichid hepatitis have been eliminated from the re-
introduction programme (Montali and Bush 1992). This case highlights the need for careful
assessment of the disease status of animals intended for reintroduction.
Disease problems may arise in captive-breeding programmes. Accideqtally introduced
parasitic or infectious disease may have important implications for those reintroduction
programmes that involve the use of foster parents. A number of sandhill cranes, Grus
canadensis, used to rear chicks of the endangered whooping crane, Grus americana, were
found to be infected with disseminated visceral coccidiosis (Carpenter et a/. 1980). This
disease has been a significant cause of death in whooping cranes between hatching and one
year of age and may have been transmitted by some foster parents (Langenberg 1992).
In another example, 5-10-day-old captive-bred Mauritius pink pigeon chicks, Columba
mayeri, succumbed to a Herpesvirus infection transmitted by foster domestic pigeons,
Columba livia. The Herpesvirus was present as a latent infection in the domestic pigeons
(Heuschele 1991). Apparently, pink pigeons had no natural resistance to this organism.
Hence, the introduction of the Herpesvirus to Mauritius might have decimated populations
of pink pigeon (Cooper 1989).
Pathogens in captive-reared animals may cause disease at the time of reintroduction if
the animal becomes stressed or debilitated. For example, heavy burdens of ectoparasites may
have a debilitating effect on animals already stressed by the release process. In order to
minimise these effects, treatment to reduce or eliminate ectoparasites may be carried out
prior to release. For example, reintroduced captive-bred red wolves, Canis rufus, were
regularly treated with a broad-spectrum drug to reduce impacts of endoparasites and
ectoparasites (Phillips and Scheck 1991).
Pathogens in captive-reared animals may infect other endemic species. For example,
cointroduced parasites may spread to unexposed host animals. Parasites introduced with
exotic fish have caused serious problems in some native species (Holmes 1982). In North
America, a protozoan that causes whirling disease was cointroduced with brown trout,
Salmo trutta (Hoffman 1970). This disease severely affected native rainbow trout, Salmo
gairdneri, in hatcheries and some wild populations (Hoffman 1970). In another example, when
the Caspian Sea sturgeon, Acipenser stellatus, was released into the Aral Sea, a cointroduced
gill parasite led to massive mortality in the Aral Sea sturgeon, Acipenser nudiventris (Bauer
and Hoffman 1976).
Some diseases cointroduced with released animals may affect other endemic species.
The recent decline of the endangered Hawaiian crow, Corvus hawaiiensis, has been
attributed to lack of recruitment resulting from reduced egg fertility and low survival of
young (Jenkins et a/. 1989). Avian malaria, Plasmodium relictum capistranoae, and avian
pox caused by Poxvirus avium, cointroduced with other birds, appear to have played
key roles in these reproductive dysfunctions (Jenkins et al. 1989). The abundance and
distribution of native species other than the Hawaiian crow have also been reduced by avian
malaria (van Riper et a[. 1986). This demonstrates the need to know the disease status of
the animals to be introduced, as well as the potential for disease transmission to other
species, before introducing animals into a previously unoccupied area.
Pathogens in introduced animals may increase zoonotic risk. Non-human primates
may carry several diseases that may be transmitted to other primates, including humans
(Heuschele 1991). Cointroduced diseases, such as tuberculosis, viral hepatitis, influenza and
measles, may jeopardise wild populations and also constitute an important health risk
for resident human populations (Heuschele 1991). Surveys of confiscated orang-utans in
 K. L. Viggers et al.

Indonesia (Sajuthi 1992) revealed that many animals were infected with tuberculosis and
hepatitis B, both of which are transmissible to humans and could be overlooked without
appropriate testing. This emphasises the need for a comprehensive health evaluation of
primates by an experienced veterinarian prior to reintroduction.

Endemic Disease in Wild Populations

The impact of disease on introduced animals
Diseases prevalent in other species may affect an introduced or reintroduced species.
The timing of release in relation to known transmission cycles and disease processes may
increase the likelihood of success in reintroductions (Phillips and Scheck 1991). In central
Europe, captive-bred white-tailed sea eagles, Haliaeetus albicilla, released in summer, would
soon come in contact with Clostridium botulinum, which is a major cause of mortality
in waterbirds. To avoid possible disease in sea eagles preying on carrion infected with
C. botulinum, young captive-bred birds are released in autumn and spring when natural
water-recycling reduces the prevalence of this organism (Fentzloff 1983). A C. botulinum
Type C vaccination is now available and could be used to minimise disease risk.
Diseases that occur in locally endemic species may play a role in the decline of
endangered species. An outbreak of canine distemper severely affected the black-footed
ferret captive-breeding programme and led to the extirpation of the remaining free-ranging
colony (Thorne and Williams 1988). The sources of canine distemper virus infecting black-
footed ferrets may have included unvaccinated domestic dogs and wild populations of
other animals such as red foxes, Vulpes vulpes, skunks, Mephitis mephitis, raccoons,
Procyon lotor, badgers, Taxidea taxus, and coyotes, Canis latrans (Thorne and Williams
1988; Williams et al. 1992). This highlights the susceptibility of free-ranging populations of
endangered species to diseases that may occur naturally in other species.
Parasites that are relatively non-pathogenic in one host may preclude the coexistence of
other potential host species in the same habitat. In North America, attempts to reintroduce
moose, Alces alces americana, and more recently, caribou, Rangifer tarandus, into areas
now inhabited by white-tailed deer, Odocoileus virginianus, failed partly as a result of
morbidity and mortality caused by the meningeal worm, Parelaphostrongylus tenuis
(Anderson 1972). This worm may enter the brain and spinal cord, causing severe neuro-
logical disease, and often seriously affects ungulates other than white-tailed deer (Anderson
1964, 1972). The intermediate host, a snail, which is ingested by the definitive host, is
required for the transmission of the meningeal worm (Anderson 1963). Anderson (1965)
suggested that the occurrence of neurological disease in moose may be associated with the
northern spread of white-tailed deer into regions inhabited by moose. The cointroduction
of meningeal worm with expanding herds of white-tailed deer now limits the distribution
of moose to areas where the white-tailed deer is less established.
Given that pathogenic parasites may influence the distribution of a host, translocations
of animals that may carry these parasites should be carefully planned. In the case of the
meningeal worm, some species such as elk, Cervus elaphus, may survive exposure to low
numbers of this parasite and shed infective larvae in their faeces (Samuel et al. 1992).
The range of the white-tailed deer has expanded into western North America and these
populations currently are not infected with meningeal worm. Translocation of infected elk
to game reserves in western regions could concurrently infect white-tailed deer, with reper-
cussions for other populations of ungulates (Samuel et al. 1992).
Introduced or translocated animals may be susceptible to parasites that are relatively
non-pathogenic in their primary host. The arterial worm, Elaeophora schneideri, does not
cause clinically detectable disease in mule deer, Odocoileus hemionus, the apparent primary
host (Hibler and Adcock 1971). However, this worm causes a severely debilitating and
often fatal disease in elk, Cervus canadensis, with characteristic symptoms of blindness,
neurological changes, abnormal antler growth and gangrene of the ears and muzzle (Hibler
Disease and Reintroductions

and Adcock 1971). A population of elk, translocated into mule deer habitat, did not increase
in number as anticipated, although 90% of female elk conceived and gave birth to normal
calves; however, only 1 5 2 0 % of the calves survived, and the majority of the deaths were
found to be attributable to the arterial worm, which infects calves within 2-3 weeks of birth
(Hibler et al. 1969). There is no treatment for this disease and populations of elk will be
unable to thrive in areas where the arterial worm is established in mule deer populations.
The potential negative effects on translocated or introduced animals of parasitic disease
inherent in another species cannot always be predicted and may prevent population growth
in released animals.
Animals released into previously unoccupied areas may be exposed to new ectoparasites
and other vectors of disease. Organisms carried by these intermediate hosts and vectors could
be transmitted to susceptible animals, causing fatal disease. In an effort to restore wild
populations of the whooping crane in North America, captive-bred populations were
introduced into geographically isolated areas (Carpenter et al. 1989). One-sixth of the
population died from disease induced by eastern equine encephalitis virus (EEE) (Carpenter
et al. 1989), an arbovirus that infects both indigenous and introduced birds, but causes
mortality only in the latter. Reintroduction of whooping cranes into an area that was not
part of the former range and that supported the mosquito vector of EEE led to the fatal
infection of birds. In future, sites for reintroduction of whooping cranes will be restricted
to the known former geographic range and surveyed for the presence of EEE and its
mosquito vectors (Carpenter et al. 1989). This emphasises the vulnerability of reintroduction
programmes to unexpected outbreaks of disease, and highlights the need for the careful
selection of release sites on the basis of a broad spectrum of specialist expertise.

The impact of introduced animals on the prevalence of endemic disease

Introduced or reintroduced animals may also carry or amplify diseases that primarily
affect other hosts. This may interfere with disease control, given the potential for population
increase in an introduced species outside the constraints of its natural environment. Thus,
species intended for release into new areas must be assessed for their potential to act as
reservoirs of infectious agents causing disease in endemic species. This may be particularly
important if introduced species share habitat with domestic livestock. For example, popu-
lations of the common brushtail possum in New Zealand are a reservoir for Mycobacterium
bovis, and this has thwarted attempts to eradicate bovine tuberculosis in that country, with
detrimental consequences for the beef, dairy and deer-farming industries (Davidson 1976;
Corner and Presidente 1981; Beatson 1985; Coleman 1988). The common brushtail possum
is not a reservoir of tuberculosis in its natural environment in Australia (Presidente 1984).
Animals intended for release should be tested for diseases of known biological and
economic importance that may occur in, or be transmitted to, other closely related species.
For example, bovine tuberculosis was detected in a number of Arabian oryx, Oryx leucoryx,
targeted for release into Saudi Arabia (Heuschele 1991). The introduction of bovine tuber-
culosis in this proposed translocation would have had detrimental consequences for the cattle
industry in that country. In Oman, Arabian oryx targeted for reintroduction must be tested
for bluetongue viruses, some strains of which cause disease in domestic sheep and goats, as
well as in some wild ruminants (Heuschele 1991). These cases emphasise the potential risks
of relocation or reintroduction of some animals and the need to test carefully for specific
diseases.

Lack of acquired immunity in released animals

Many natural populations of vertebrates tend to be held in long-term balance by the
interactions of prey-predator, host-pathogen, plant-herbivore and other relationships (May
1988). Typically, in host-parasite relationships, the intensity of infection is minimal in most
animals, with only a few individuals being heavily infected (Scott 1988). The acquisition of
 K. L. Viggers et al.

immunity to some diseases may require low-intensity exposure to pathogens at levels that
are insufficient to cause disease. Host susceptibility to disease is influenced by population
density (leading to nutritional and social stress), innate resistance and the ability of the host
to mount an immune response (Wakelin 1978).
The stress associated with reintroduction may increase the pathological effect of common
infectious agents and further debilitate animals already compromised by the release process.
In an attempt to overcome this problem, the release of captive-bred red wolves is timed to
coincide with low tick abundance (Phillips and Scheck 1991) to enable animals to adjust
to their environment without the immediate added impact of peak populations of
ectoparasites.

Measures to Reduce Risk of Disease

An understanding of disease processes, including identification of the causative agent,
modes of transmission, epidemiology and pathophysiology, is vital to minimise the potential
problems of disease in reintroduction programmes. A number of simple steps that may help
to minimise the risk of disease are outlined below.

Quarantine
Quarantine involves the isolation of animals for a period that is dependent on the
maximum incubation period of diseases known to affect the animal or, in the case of
parasites, the maximum prepatent period (Woodford and Kock 1991). During this time,
the development of signs of disease can be observed and treated where applicable. When
treatment is required, it is important that the selected drug is highly efficacious against the
agent of disease, so that animals that are subclinical carriers of disease agents are not
released. In the case of parasitic disease, treatment should be efficacious for all stages of
the parasite concerned. Pre-release prophylaxis against diseases known to be endemic in the
wild population may also be considered, that is, vaccination against known infectious
diseases (Woodford and Kock 1991). Prophylactic treatment may interfere with the detection
of disease and hence should be withheld until immediately prior to release. If clinical disease
or deaths occur, quarantine should be extended for those animals caged with the affected
individuals (Ashton and Cooper 1989). Quarantine is particularly important in programmes
in which captive animals are to be released into areas that support conspecifics (Fowler
1986). This applies to captive-bred animals as well as wild individuals targeted for trans-
location. As the isolation of animals with a strongly social behaviour can be highly stressful,
it may be advisable to quarantine several individuals (Fowler 1986). In addition, quarantine
allows time for clinical tests to be performed for prophylactic purposes; some of these are
outlined below.

Diagnosis of Disease
Clinical examination
All animals targeted for release in reintroduction or translocation programmes
should undergo a full clinical examination by an experienced wildlife veterinarian. Trained
veterinarians will be alert to subtle clinical signs of disease and to the appropriate tests
required to assess the disease status of the animal. A complete physical examination should
include recording of body temperature, auscultation of the heart and lungs, careful palpation
of the abdomen and lymph nodes and examination of the teeth, eyes, oral cavity and other
body systems.

Radiology
Radiology may be of assistance in the diagnosis of tuberculosis in primates. However,
calcium is not always deposited in lung tubercles in non-human primates (Fowler 1986).
Disease and Reintroductions

Hence, thoracic radiographs are often undiagnostic (Fowler 1986). Radiology should only
be used in conjunction with tuberculin skin testing for the diagnosis of tuberculosis.

Faecal examination
The examination of faeces for parasite eggs, larvae and coccidial oocysts is a simple
procedure to determine the presence or absence of gut parasites. Direct examination of
faeces is the minimum test required to detect gastrointestinal parasitic infection. Faecal
flotation is a supplementary test that may improve the sensitivity for detection of some
eggs. It is not always possible to assign eggs to parasite species, but generic groups can
usually be identified. Larval culture may aid specific identification of parasite eggs that are
retrieved from faeces. This is a specialised technique, which may be provided by veterinary
laboratories or wildlife parasitologists. Faecal egg counts may also be performed (McMaster
technique; Thienpont et al. 1979) to estimate egg burdens (eggs per gram), although the
numbers of eggs do not necessarily reflect the abundance of parasites. Faecal flotation
techniques detect the presence of adult worms only. Non-patent infections (i.e. infection with
larval stages that precede egg-laying adult worms) cannot be detected by the examination of
faeces. Treatment is elective, depending on the potential pathogenicity of the parasites
detected. However, parasites in a released animal may constitute an added stressor and
provide an unnecessary element of risk during the release process (Phillips and Scheck
1991). Other faecal tests include electron microscopy for virus particles and ELISA tests
for rotavirus.

Haematology and serum biochemistry profiles

Blood chemistry is used to aid the diagnosis of organ dysfunction and disease (Schalm
et al. 1975). Measurement of these parameters may aid in the detection of disease in animals
being prepared for release. Information on normal blood values is limited for many species;
however, knowledge of the expected variation in blood profiles from other species may
facilitate the interpretation of blood results. This may enable presumptive inferences to be
made about animal health and organ function. To establish an understanding of the normal
range of haematological and serum biochemical values, it is essential that blood samples are
collected for expert analysis whenever possible. Blood smears should be made for differential
white cell counts, platelet estimation and to determine the presence or absence of blood
parasites. Other samples should include (1) unclotted blood preserved in ethylene diamine-
tetra-acetic acid (EDTA) for haematology (0.5 mL of EDTA blood is the minimum volume
required and is generally sufficient for most automated machines), and (2) serum from
samples of clotted blood for biochemical analysis (a minimum of 1 mL of serum is obtained
from 2 mL of blood). Most current tests are relatively insensitive to subclinical levels of
disease and are therefore of dubious value in assessing subtle changes in health status.
Further research is required to develop more sensitive tests to estimate individual and
population health.

Serology
Serological testing is an important screening device for detection of infectious diseases in
animals intended for translocation or reintroduction. Serological tests are completed using
a small amount of serum to detect the presence of host antibody produced in response to
a particular disease agent. A wide range of serological tests is available for animal diseases
and these are usually carried out by an animal-pathology laboratory. The relevant tests to
be performed depend on the species and the location of the area proposed for the release
of the animal.
The importance of specific disease in endemic wild or domestic populations needs to be
determined before detailed serological tests are performed. If the disease agent is already
prevalent in local populations, the value of serological testing may be questionable. For
 K. L. Viggers et al,

example, koalas, Phascolarctos cinereus, being translocated within mainland Victoria may
not require tests for chlamydiosis, Chlamydia psittaci, if the local areas support koala
populations already infected with C. psittaci. However, testing would be essential if animals
were to be introduced to areas supporting C. psittaci-free populations, such as French Island
(Lee and Martin 1988). The importance of serological testing also depends on the potential
pathogenicity of the disease agent.

Tuberculin testing (for primates)

Tuberculosis testing of non-human primates is an essential component of preparation for
release and is vital to minimise public health risk. Primates may be infected with human,
bovine or avian tuberculosis (Fowler 1986). The tuberculosis skin-testing procedure involves
the intradermal injection of 0.1 mL of mammalian tuberculin into the edge of the upper
eyelid or into the skin of the abdomen (Fowler 1986). A positive reaction is detected within
three days of the injection and varies from slight reddening of the skin to severe oedema
with a purulent discharge and possibly some necrosis (Fowler 1986). Concurrent viral
infection may interfere with normal skin reactivity and provide false negative results. If the
result is questionable, the test should be repeated after 14 days.

Microbial culture
Microbial culture involves the isolation and identification of specific agents of infectious
disease. This is important to assist treatment decisions and to determine the potential impact
of the disease on both captive and wild populations. Special techniques are required and
these services may be provided by veterinary laboratories.
Microbial culture is appropriate for samples collected from individuals with clinical
disease, in order to identify disease agents and to ensure that they are not co-released with
the animal. Body fluids and faeces should be sampled. For birds, swabs should be taken
from the nasal cavity, pharynx, crop and cloaca (Hunter 1989; Scullion 1989). The culture
of avian faeces may reveal the presence of pathogenic bacteria such as Salmonella spp.
(Cooper 1977). Microbial culture is also an important retrospective tool for diagnosis at
necropsy (see below) and may aid the detection of potentially zoonotic diseases.

Necropsy
It is essential to determine the cause of death of any animals that die in captivity or are
found soon after death in the wild. A full post-mortem examination should be performed,
including histopathology and microbial culture (Woodford and Kock 1991). Any dead
animals discovered in the wild should be transported promptly to an experienced wildlife
pathologist or veterinarian. If this is not possible, some simple steps can be taken in the
field to obtain specimens for later assessment. If a dead animal is found (1) external changes
should be noted; (2) the ventral midline should be opened; (3) internal changes should noted;
(4) 5-mm-thick slices from the liver, kidney, adrenal, spleen, lung, heart, skeletal muscle and
brain should be taken and stored in 10% formalin, ensuring that the volume of the tissues
is less than 20% of the volume of the formalin. This will provide specimens for histo-
pathological examination.

Elimination of Pathogens
The necessity to eliminate pathogens present in animals intended for translocation or
reintroduction is dependent on the prevalence of disease in the endemic wild populations.
Indeed the treatment of animals prior to release to eliminate all pathogens may not always
be beneficial. Elimination of pathogens from the released animals may reduce levels of
immunity to disease. Problems may arise if such pathogens are present in wild populations.
Disease and Reintroductions

Given the stress of release on reintroduced animals, their survival may be compromised by
re-exposure to these pathogens at the time of release. In the case of parasites that are
present in wild populations, but to which the captive population has not received prior
exposure, it may be advisable to provide low-level exposure during captivity so that some
immunity may be developed.

Vaccination
Vaccination against some diseases may be a useful pre-release procedure. This applies
particularly to animals that may come in contact with related domesticated species. The use
of specific vaccines will depend on the host, the relative risk of disease and the efficacy of
the vaccine. In the case of canine distemper, although protection against the disease is
desirable, the safety of the vaccination is not always assured (Fowler 1986); problems arose
with initial trials of canine distemper vaccination in the black-footed ferret (Thorne and
Williams 1988) and the lesser panda, Ailurus fulgens (Fowler 1986). A safe, inactivated
canine distemper virus vaccine has since been developed for the black-footed ferret (Williams
et al. 1992). Vaccinations are also available for numerous other diseases, including rabies
(Rosatte et al. 1992), anthrax, tetanus, botulism, feline panleucopenia and canine parvovirus
(Fowler 1986).
If vaccination against specific disease agents is to be performed, it must be completed
according to the specified protocol, with booster vaccines administered when required to
achieve a satisfactory level of immunity. The levels of antibody production in response
to most vaccines can be measured by serology. Antibody titres should be measured prior to
release to ensure that protection is optimal.

Management Protocols
Management protocols should be established for any recovery and reintroduction
programme for an endangered species (Langenberg 1992). Protocol and research require-
ments will vary between species and their associated diseases (Montali and Bush 1992).
Standardised management protocols will ensure that maximum information about living
and dead animals is compiled to further expand the understanding of health and disease in
both wild and captive populations (Langenberg 1992).

Conclusions
The impacts of disease have been largely neglected in reintroduction programmes.
However, disease has contributed to the demise of several endangered species and com-
promised the success of a number of attempted reintroductions. Some of the potential
problems for reintroduction programmes created by parasitic and infectious disease may
be avoided by a number of simple steps, including quarantine with clinical assessment,
laboratory tests (haematology, biochemistry, serology, faecal examination, microbial culture)
and vaccination. Planning for such programmes should involve communication with
experienced wildlife biologists and veterinarians with a knowledge of diseases in captive
and wild populations.
Actions to minimise the impacts of disease on reintroduction programmes include
(a) assembling information from case histories where diseases have contributed to the failure
of the programme, (b) investigating diseases in captive individuals and populations, and
(c) evaluating the effectiveness of preventive and therapeutic strategies. Improved success
in reintroduction biology will also be dependent on an increased understanding of the
distribution and incidence of disease in wild populations. Further research is required on the
cointroduction of disease, the development of immunity, effective quarantine requirements,
and diseases in natural populations.
 K. L. Viggers et a[.

Acknowledgments
K. Viggers is supported by a M.Sc. scholarship at the Australian National University,
Canberra, Australia. D . Lindenmayer is funded by an Australian Research Council Post-
doctoral Award. D r P. Presidente a n d D r M. Howell offered critical comment that improved
earlier drafts of the manuscript.

References
Anderson, R. C. (1963). The incidence, development and experimental transmission of Pneumostrongylus
tenuis Dougherty (Metastrongyloidea:Protostrongylidae)of the meninges of the white-tailed deer
(Odocoileus virginianus borealis) in Ontario. Canadian Journal of Zoology 41, 775.
Anderson, R. C. (1964). Neurologic disease in moose infected experimentally with Pneumostrongylus
tenuis from white-tailed deer. Pathologica Veterinaria 1, 289-322.
Anderson, R. C. (1965). An examination of wild moose exhibiting neurologic signs, in Ontario.
Canadian Journal of Zoology 43, 635-9.
Anderson, R. C. (1972). The ecological relationships of meningeal worm and native cervids in North
America. Journal of Wildlife Diseases 8 , 304-10.
Ashton, W. L. G., and Cooper, J. E. (1989). Exclusion, elimination and control of avian pathogens.
In 'Disease and Threatened Birds'. (Ed. J. E. Cooper.) Technical Publication No. 10, pp. 31-8.
(International Council for Bird Preservation: Cambridge.)
Beatson, N. S. (1985). Tuberculosis in red deer in New Zealand. Bulletin of the Royal Society of New
Zealand 22, 147-50.
Bauer, 0. N., and Hoffman, G. L. (1976). Helminth range extension by translocation of fish. In
'Wildlife Diseases'. (Ed. L. A. Page.) pp. 163-72. (Plenum Press: New York.)
Carpenter, J. W., Spraker, T. R., and Novilla, M. N. (1980). Disseminated visceral coccidiosis in
whooping cranes. Journal of the American Veterinary Medical Association 177, 845-8.
Carpenter, J. W., Clark, G. G., and Watts, D. M. (1989). The impacts of eastern equine encephalitis
virus on efforts to recover the endangered whooping crane. In 'Disease and Threatened Birds'.
(Ed. J. E. Cooper.) Technical Publication No. 10, pp. 115-20. (International Council for Bird
Preservation: Cambridge.)
Clark, T. W. (1989). Conservation biology of the black-footed ferret. Special Scientific Report. (Wildlife
Preservation Trust: Philadelphia.)
Coleman, J. D. (1988). Distribution, prevalence and epidemiology of bovine tuberculosis in brushtail
possums, Trichosurus vulpecula, in the Hohonu Range, New Zealand. Australian Wildlife Research
15, 651-63.
Cooper, J. E. (1977). Veterinary problems of captive breeding and possible reintroduction of birds of
prey. International Zoo Yearbook 17, 32-8.
Cooper, J. E. (1989). Pathogens in threatened populations. In 'Disease and Threatened Birds'. (Ed.
J. E. Cooper.) Technical Publication No. 10, pp. 51-61. (International Council for Bird Preservation:
Cambridge.)
Corner, L. A., and Presidente, P. J. A. (1981). Mycobacterium bovis infection in the brush-tailed
possum (Trichosurus vulpecula): 11. Comparison of experimental infections with an Australian cattle
strain and a New Zealand possum strain. Veterinary Microbiology 6 , 351-66.
Cowan, P. E., (1990). Brushtail possum. In 'The Handbook of New Zealand Mammals'. (Ed. C. M.
King.) pp. 68-99. (Oxford University Press: Auckland.)
Davidson, R. M. (1976). The role of the opossum in spreading tuberculosis. New Zealand Journal of
Agriculture 133, 21-5.
Fentzloff, C. (1983). Breeding, artificial incubation and release of white-tailed sea eagles (Haliaeetus
albicilla). International Zoo Yearbook 23, 18-35.
Fowler, M. E. (1986). 'Zoo and Wild Animals Medicine.' 2nd Edn. (Saunders: Philadelphia.)
Griffith, B., Scott, J. M., Carpenter, J. W., and Reed, C. (1989). Translocation as a species con-
servation tool: status and strategy. Science 245, 477-80.
Haebler, R. (1992). Disease risk to wildlife following reintroduction. In 'Proceedings Joint Conference
of the American Association of Zoo Veterinarians and the American Association of Wildlife
Veterinarians'. (Ed. R. E. Junge.) p. 12. (Oakland: California.)
Disease and Reintroductions

Heuschele, W. P. (1991). The importance of infectious disease concerns in wildlife reintroductions.

In 'The American Association of Zoological Parks and Aquaria Annual Conference Proceedings'.
pp. 143-6.
Hibler, C. P., and Adcock, J. L. (1971). Elaeophorosis. In 'Parasitic Diseases of Wild Animals'.
(Eds J. W. Davis and R. C. Anderson.) pp. 263-78. (Iowa State University Press: Iowa.)
Hibler, C. P., Adcock, J. L., Davis, R. W., and Abdelbaki, Y. 2. (1969). Elaeophorosis in deer and
elk in the Gila Forest, New Mexico. Bulletin of the Wildlife Disease Association 5 , 27-30.
Hoffman, G. L. (1970). Intercontinental and trans-continental dissemination and transfaunation of
fish parasites with emphasis on whirling disease. In 'A Symposium on Diseases of Fishes and
Shellfishes'. (Ed. S. F. Snieszko.) pp. 69-81. (American Fisheries Society: Washington, D.C.)
Holmes, J. C. (1982). Impact of infectious disease agents on the populations growth and geographical
distribution of animals. In 'Population Biology of Infectious Diseases'. (Eds R. M. Anderson and
R. M. May.) pp. 37-51. (Springer-Verlag: Berlin.)
Hunter, D. B. (1989). Detection of pathogens: monitoring and screening programmes. In 'Disease
and Threatened Birds'. (Ed. J . E. Cooper.) Technical Publication No. 10, pp. 25-9. (International
Council for Bird Preservation: Cambridge.)
Jenkins, C. D., Temple, S. A., Riper, C. van, and Hansen, W. R. (1989). Disease-related aspects of
conserving the endangered Hawaiian crow. In 'Disease and Threatened Birds'. (Ed. J . E. Cooper.)
Technical Publication No. 10, pp. 77-87. (International Council for Bird Preservation: Cambridge.)
Jones, D. M. (1982). Conservation in relation to animal disease in Africa and Asia. Symposia for the
Zoological Society of London 50, 271-85.
Kleiman, D. G. (1989). Reintroduction of captive mammals for conservation. Bioscience 39, 152-61.
Konstant, W. R., and Mittermeier, R. A. (1982). Introduction, reintroduction and translocation of
Neotropical primates: past experiences and future possibilities. International Zoo Yearbook 22,
69-77.
Langenberg, J. (1992). Health management for the whooping crane captive propagation and re-
introduction program. In 'Proceedings Joint Conference of the American Association of Zoo
Veterinarians and the American Association of Wildlife Veterinarians'. (Ed. R. E. Junge.) pp. 2-9.
(Oakland: California.)
Lee, A., and Martin, R. (1988). 'The Koala: a Natural History.' (New South Wales University Press:
Kensington.)
Lindburg, D. G. (1992). Are wildlife reintroductions worth the cost? Zoo Biology 11, 1-2.
May, R. M. (1988). Conservation and disease. Conservation Biology 2, 28-30.
Menkhorst, P., and Middleton, D. (1991). 'The Helmeted Honeyeater Recovery Plan: 1989-1993.'
(Department of Conservation and Environment: Melbourne.)
Montali, R. J., and Bush, M. (1992). Some diseases of golden lion tamarins acquired in captivity and
their impact on reintroduction. In 'Proceedings Joint Conference of the American Association of
Zoo Veterinarians and the American Association of Wildlife Veterinarians'. (Ed. R. E. Junge.)
pp. 14-16. (Oakland: California.)
Phillips, M. K., and Scheck, J. (1991). Parasitism in captive and reintroduced red wolves. Journal of
Wildlife Diseases 27, 498-501.
Pietsch, R. (1993). The fate of urban brushtail possums translocated to sclerophyll forest. In
'Abstracts. Conference on Reintroduction Biology of Australasian Fauna'. p. 15. (Healesville
Sanctuary: Healesville.)
Presidente, P. J. A. (1984). Parasites and diseases of brushtail possums (Trichosurus spp.): occurrence
and significance. In 'Possums and Gliders'. (Eds A. P . Smith and I. D. Hume.) pp. 171-90.
(Australian Mammal Society: Sydney.)
Pucek, Z. (1986). European bison. Species 7, 9-10.
Riper, C. van 111, Riper, S. G. van, Goff, M. L., and Laird, M. (1986). The epizootiology and
ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327-44.
Rosatte, R. C., Power, M. J., MacInnes, C. D., and Campbell, J. B. (1992). Trap-vaccinate-release
and oral vaccination for rabies in urban skunks, raccoons and foxes. Journal of Wildlife Diseases
28, 562-71.
Sajuthi, D., Pamungkas, J., Iskandriati, D., Agus Lalana, R. P., Knitter, G. H., and Karesh, W. B.
(1992). The incidence of tuberculosis and hepatitis B in orangutans confiscated by the Indonesian
government in 1991. In 'Proceedings Joint Conference of the American Association of Zoo
Veterinarians and the American Association of Wildlife Veterinarians'. (Ed. R. E. Junge.) p. 17.
(Oakland: California.)
 K. L. Viggers et a[.

Samuel, W. M., Pybus, M. J., Welch, D. A., and Wilke, C. J. (1992). Elk as a potential host for
meningeal worm: implications for translocation. Journal of Wildltfe Management 56, 629-39.
Schalm, 0. W., Jain, N. C., and Carroll, E. J. (1975). 'Veterinary Haematology.' 3rd Edn. (Lea and
Febiger : Philadelphia.)
Scott, M. E. (1988). The impact of infection and disease on animal populations: implications for
conservation biology. Conservation Biology 2, 40-56.
Scullion, F. T. (1989). Microbial investigation of wild birds. In 'Disease and Threatened Birds'.
(Ed. J. E. Cooper.) Technical Publication No. 10, pp. 39-50. (International Council for Bird
Preservation: Cambridge.)
Simberloff, D. A. (1986). The proximate causes of extinction. In 'Patterns and Processes in the History
of Life'. (Eds D. M. Raup and D. Jabolinski.) pp. 259-76. (Springer-Verlag: Berlin.)
Simberloff, D. A. (1988). The contribution of population and community biology to conservation
science. Annual Review of Ecology and Systematics 19, 473-5 11.
Thienpont, D., Rochette, F., and Vanparijs, 0. F. J. (1979). 'Diagnosing Helminthiasis through
Coprological Examination.' (Janssen Research-Foundation: Beerse.)
Thorne, E. T., and Williams, E. S. (1988). Disease and endangered species: the black-footed ferret as
a recent example. Conservation Biology 2, 66-75.
Wakelin, D. (1978). Genetic control of susceptibility and resistance to parasitic infection. Advances
in Parasitology 16, 219-308.
Williams, E. S., Thorne, E. T., Kwiatkowski, D. R., and Oakleaf, B. (1992). Disease management in
the black-footed ferret (Mustelanigripes) reintroduction program in Wyoming. In 'Proceedings Joint
Conference of the American Association of Zoo Veterinarians and the American Association of
Wildlife Veterinarians'. (Ed. R. E. Junge.) pp. 10-11. (Oakland: California.)
Woodford, M. H., and Kock, R. A. (1991). Veterinary considerations in re-introduction and trans-
location projects. Symposia of the Zoological Society of London 62, 101-10.

Manuscript received 1 march 1993; revised and accepted 1 July 1993