Wildlife Health in Conservation - Wildlife Ecology and Conservation

Putting
in
Theory
into
Practice:
Wildlife
Health
Conservation
SHARON L. DEEM,* WILLIAM B. KARESH, AND WENDY WEISMAN
Field VeterinaryProgram,Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, NY 10460-1099 U.S.A.
Abstract: Infectious and noninfectious diseases are being recognized by conservation biologists as an increasing challenge to the conservation of wildlife. The amplified role of diseases as a factor limiting species'
survival can be traced to anthropogenic changes on a global scale that have direct and indirect influences on
the health of wildlife species. These changes include human population growth, habitat fragmentation and
degradation, the isolation of populations of species, and an increased proximity of humans (and their domestic animals) to wildlife. Further, some conservation projects have caused more harm than good by unwittingly introducing diseases to wildlife populations, whereas others have failed to meet their objectives because they did not take disease factors into consideration. Conservation biologists need to move quickly past
the decades-old debate on the relative importance of wildlife health to conservation and begin using all the
tools available to ensure the effectiveness of their efforts. We briefly review the literature on wildlife diseases,
place wildlife health in the context of global changes affecting wild animal populations, and offer concrete
suggestions for ways to integrate wildlife health sciences into conservation, such as including health assessment or monitoring programs and research on interspecies disease transmission in field biology projects,
training wildlife professionals in the design and implementation of wildlife studies that incorporate health
components, and encouraging interdisciplinary collaboration. Our goal is to raise awareness that conservation biologists working in disciplines ranging from field biology to policy making have an important role to
play in facilitating a transition toward a new conservation paradigm that includes wildlife health. Thisparadigm shift will take an academic understanding of the importance of wildlife disease and turn it into practical actions that will help conserve wildlife more effectively.
De la Teoria a la Piractica:la Salud de la Vida Silvestre en la Conservacion
Resumen: Los biologos de la conservaci6n reconocen que las enfermedades infecciosas y no infecciosas son
un reto cada vez mayor para la conservaci6n de vida silvestre. Elpapel de las enfermedades como unfactor
limitante de la sobrevivencia de especies se puede deber a cambios antropogenicos a escala global que tienen
influencia directa e indirecta en la salud de especies de vida silvestre. Estos cambios incluyen el crecimiento
de la poblacion, la fragmentacion y degradacion del habitat, el aislamiento de poblaciones y una mayor
proximidad de humanos (y sus animales dome'sticos) a la vida silvestre. Adicionalmente, algunos proyectos
de conservacion han causado mds danfos que beneficios al introducir, inconscientemente, enfermedades en
las poblaciones de vida silvestre, mientras que otros han fallado en alcanzar sus objetivos porque no tomaron en consideracion a factores de enfermedades. Como biologos de la conservacion, necesitamos rapidamente superar el debate que se ha dado por de6cadassobre la importancia relativa de la salud de la vida silvestre para la conservacion y comenzar a utilizar todas las herramientas disponibles para asegurar la
efectividad de nuestros esfuerzos. Brevemente examinamos la literatura sobre enfermedades de vida silvestre, colocamos la salud de la vida silvestre en un contexto de cambios globales que afectan poblaciones silvestres de animales y ofrecemos sugerencias concretas para integrar las ciencias de la salud de vida silvestre en
la conservacion, como incluir la evaluaci6n de la salud o programas de monitoreo e investigar la transmision de enfermedades entre especies en proyectos de campo, entrenar profesionales de la vida silvestre en
*email [email protected]
Paper submitted August 4, 2000; revised manuscript accepted February 21, 2001.
1224
Conservation Biology, Pages 1224-1233
Volume 15, No. 5, October 2001
Deemet al.
Healthin Conservation 1225
Wildlife
el diseno e instrumentacion de estudios de vida silvestre que incorporen componentes de salud y colaboraci6n trans-disciplinaria. Nuestra meta es crear conciencia de que los biologos de la conservacion que trabajan en disciplinas que van de la biologia de campo a definici6n de politicas juegan un papel importante en
la transici6n hacia un nuevo paradigma de conservaci6n que incluye la salud de la vida silvestre. Este cambio de paradigma tendrd el entendimiento de la academia acerca de la importancia de las enfermedades de
la vida silvestre y transformarlo en acciones prdcticas que ayudardn a conservar a la vida silvestre mds eficientemente.
Introduction
The conservation of wildlife requires an understanding
of biogeographical patterns, community structure, population dynamics, and individual behavior. A fifth factor
that should be viewed as imperative for sound conservation efforts is an understanding of health issues that affect populations. If one reads recent editorials and reviews in scientific journals, it is easy to come away with
the impression that disease and health issues have only
just been discovered as important factors in the conservation of wildlife (Meffe 1999; Daszak et al. 2000). In
fact, for many decades, disease has been recognized as a
critical issue. What is new, however, is the increasing attention the subject is receiving from the wider conservation community. This is encouraging because the attention suggests that we are poised to move beyond an
academic interest in the effect of diseases on wildlife.
Health and disease are broad terms, so it is useful to
define them in the context of our discussion. The World
Health Organization defines health as a state of complete
physical, mental, and social well being and not merely
the absence of disease or infirmity (Last 1983). While
this state can serve as a laudable goal, it does not provide us with objective criteria for determining the health
of wildlife. Wobeser (1981) defies disease in free-ranging wildlife populations as "any impairment that interferes with or modifies the performance of normal functions, including responses to environmental factors such
as nutrition, toxins, and climate; infectious agents; inherent or congenital defects, or combinations of these factors." Those impairments that negatively affect the longterm persistence of populations and the ability of healthy
populations to fulfill their ecological roles in an ecosystem are of primary concern to those of us involved in
conservation.
Impairments to the health of wildlife are being exacerbated by the human population explosion, habitat fragmentation and degradation, isolation of wildlife populations, and an increased proximity of humans (and their
domestic animals) to wildlife (Jones 1982; Scott 1988;
Daszak et al. 2000). These phenomena are occurring on
an unprecedented global scale, which in turn is creating
novel opportunities for disease to have a negative effect
on wildlife and on efforts to conserve it.
We (1) provide a historical perspective on what is
sometimes referred to as "conservation medicine" by briefly
reviewing how health and disease factors have been
seen to affect the persistence of wildlife populations; (2)
describe in more detail how global changes are expanding the role disease plays in population persistence; and
(3) make practical recommendations for prioritizing activities that workers should focus on in trying to incorporate wildlife health concerns into conservation efforts.
HistoricalPerspective
In 1933 Aldo Leopold stated that the "role of disease in
wildlife conservation has probably been radically underestimated" (Leopold 1933). Even though "conservation
medicine" has only recently reached the mainstream
conservation literature (Meffe 1999; Osofsky et al. 2000),
research began in the decades following Leopold's statement and established a large body of scientific knowledge on wildlife diseases and disease ecology. Diseases
of wildlife were first seriously addressed by the scientific
community as they related to either the health of domestic species (i.e., ruminants, pigs, chickens) with which
wildlife had contact or to that of game species (i.e.,
deer, ducks) that were important economically (Friend
1976; Pastoret et al. 1988; Plowright 1988b). Other diseases of domestic and wildlife species that were originally noted as a major concern were zoonoses (diseases
transmissible from animals to humans) such as rabies,
brucellosis, and tuberculosis (Friend 1976).
Beginning in the 1970s and 1980s, surveys that incorporated epidemiologic approaches were conducted on a
variety of free-ranging wildlife populations. Additional
interest and funding was sparked in the 1980s as a result
of the passage of the U.S. Endangered Species Act (Spalding & Forrester 1993). From the 1970s through the
1990s, relevant publications included theoretical models
describing parasite biology (Anderson & May 1979a;
1979b; Anderson & Gordon 1982; Anderson 1991), empirical examples of significant negative effects of diseases on free-ranging wildlife populations (Thorne &
Williams 1988; Heide-Jorgensen et al. 1992), and conceptual statements on the role of wildlife health in con-
Conservation Biology
Volume 15, No. 5, October 2001
1226
Healthin Conservation
Wildlife
servation (Hutchins et al. 1991; Woodford 1993; Karesh
& Cook 1995).
One issue that has received a significant amount of attention in its own right is massive die-offs associated
with disease in free-rangingwildlife populations (Young
1994). Examples include diseases such as rinderpest in
ungulate species (Plowright 1982) and botulism in waterfowl (Smith 1982), die-offs associated with oil spills
(Garrot et al. 1993), and infectious disease epidemics
such as canine distemper virus in lions (Roelke-Parkeret
al. 1996) and malariain endemic Hawaiianbirds (Warer
1968; Van Riper et al. 1986). For many years the primary
role of wildlife veterinarians was the management (conservation) of populations experiencing disease epidemics associated with high mortality.
In the recent past, naturallyoccurring infectious agents
and noninfectious etiologies (causes of disease) have
been recognized as integral in shaping many aspects of
wildlife behavior and ecology (Yuill 1987; May 1988).
Increasingly, many conservation scientists, including veterinarians, have begun to put these phenomena into the
context of the current biodiversity crisis and to examine
more explicitly the role disease can play in the loss of
species (Dobson & Hudson 1986; May 1988; Scott 1988;
McCallum & Dobson 1995; Hansen & Johnson 1999;
Daszak et al. 2000).
A review of the literature reveals decades of relevant
research, providing a foundation for efforts to integrate
concerns about wildlife health and disease into practical
conservation efforts. Workers have provided much of
the data needed to understand how the current global
changes such as increasing interactions among wildlife,
livestock, and humans affect our efforts to conserve
wildlife populations.
Global Trends AffectingWildlife Health
in Conservation
There are three broadprocesses affected by ongoing global
changes which have profound implications for wildlife
health and conservation: alterations in landscapes and
habitats, shifts in wildlife populations, and the resulting
changes in disease ecology. We recognize that to some
the distinctions between these categories may seem arbitrary;they clearly overlap and may be at work simultaneously, which complicates and compounds their effects
(Soule & Kohm 1989). Nevertheless, in the interest of
creating a simple conceptual framework for discussion of
the issues, we have chosen to categorize them in this way.
Furthermore, changes taking place at the global scale
have direct and indirect effects on the health of wildlife
species. We include examples of global changes acting
in indirect ways on wildlife health, making populations
under stress more susceptible
Conservation Biology
Volume 15, No. 5, October 2001
to disease outbreaks that
Deemet al.
otherwise would run their course without risking extinction of an entire species. Such disease outbreaks represent the way many conservation biologists traditionally
have understood how disease processes act on wildlife
populations. We also discuss certain global anthropogenic changes that have a direct effect on wildlife persistence, stressing that there are opportunities for familiar
diseases to act on wildlife populations in new ways and
situations allowing completely novel diseases to come
into play. Disease events that fall into the latter group
are not confined to an already failing population, but
rather can be a major cause of decline in themselves.
Changesin Landscapesand Habitats
Environmental changes caused by human activity have
amplified the role of diseases as regulating factors in species' survival. These changes include the conversion of
wildlife habitat for human use, resulting in habitat loss
and fragmentation, macro- and microclimate changes,
and environmental contamination.
Fragmentation of ecosystems has a variety of implications related to disease and has generated particular interest from island biogeographers and wildlife disease
researchers. Fragmentation of ecosystems can result in
human-made "island ecosystems" that have been compared to geographical islands, functioning to isolate populations of species geographically and to confine them
to smaller areas. Much has been written about island extinctions associated with human introduction of infectious and parasitic diseases (Van Riper et al. 1986; Dobson 1988; Quammen 1996).
Even though the biological diversity of islands is a
small percentage of the world's total, of the recorded
number of invertebrate and vertebrate extinctions that
have occurred since the 1600s, 367 have been island
species and only 124 continental species (Smith et al.
1993). Extinction may also be the fate of many wildlife
species located within newly created "artificialislands."
African wild dogs (Lycaon pictus) represent one wellknown example of isolated populations now teetering
on the brink of extinction, for which conservation efforts have been hampered severely by disease (Alexander & Appel 1994; Kat et al. 1996). Protected areas
that are intentionally isolated by fencing, as was true in
Kruger National Park, South Africa, or inadvertently isolated by human population growth and activities, such
as the intense agriculture one finds in Virunga National
Park, Rwanda, and south Florida, United States, are also
examples of "island"ecosystems. In all these areas diseases have a significant effect on the survival of wildlife
populations within their boundaries (Maehr et al. 1991;
Keet et al. 1996; Mudakikwaet al. 1998; Sleeman 1998).
One result of land degradation and fragmentation is
the increased opportunity for contact among humans,
domestic animals, and wildlife. This increased proximity
Healthin Conservation 1227
Wildlife
Deem et al.
may result in increased transmission of diseases between
these groups, including zoonotic and anthropozoonotic
diseases (Morell 1995; Wolfe et al. 1998; Gao et al. 1999;
Wallis & Lee 1999). The intentional practice of "multispecies land use" and buffer zones in which domestic
animals graze the same lands as wildlife may facilitate
the transmissionof disease between these two groups (Pastoret et al. 1988; Plowright 1988a; Foreyt 1990; RoelkeParkeret al. 1996; Karesh et al. 1998).
Other environmental changes related to human activity, such as climate change and pollution, have been implicated in infectious disease states in both human and
animal populations, but the long-term implications of
these findings for conservation have only begun to be
explored. For instance, we know that global climate
changes, such as warming trends and rainfall patterns,
can influence the epidemiology of various infectious diseases (Harvell et al. 1999). This realization has also occurred among conservationists concerned with long-term
species survival in reserves affected by these anthropogenic climatic changes (Peters & Darling 1985).
Air and water pollution are also linked to various noninfectious diseases. Large-scalepollution events such as
oil spills are obviously detrimental to wildlife (Garrot et
al. 1993), but long-term and low-level toxin exposure
due to pollution are now also being recognized as detrimental (Colbor et al. 1996). Two areas of toxicologic
research that have received a great deal of attention in
recent years are the negative effects of estrogenic agents
that disrupt normal endocrine function (Colbor et al.
1996; Yamamoto et al. 1996) and the negative effects of
PCBs on immunocompetence (O'Hara& Rice 1996). For
amphibians, a taxonomic group extremely sensitive to
environmental changes, there are reports of deformities
related to pesticide exposure (Ouellet et al. 1997). Light
and noise must be considered pollutants. For example,
the effect of light pollution on the survival of hatchling
sea turtles is well documented (Peters & Verhoeven
1994). Certain "new" epidemics of infectious diseases
such as fibropapillomatosis (Herbst 1994) and chytridiomycosis (Berger et al. 1998), and a number of marine
mass mortality events (Heide-J0rgensen et al. 1992), are
thought to be a direct or indirect result of environmental
pollution.
Animal translocation,
as broadly defined by The World
Conservation Union (1987), is the movement of living
organisms from one area for release in another. Thus,
translocation encompasses introduction, reintroduction,
and restocking. Many examples exist in which animal
translocations resulted in serious wildlife disease problems (Fischman et al. 1992; Jessup 1993; Meltzer 1993;
Woodford & Rossiter 1993; Davidson et al. 1996). Such
problems typically fall into the following three categories: diseases brought by a subclinical (nonsymptomatic)
host to a new region (Office International des Epizooties
1987), disease vectors introduced to new geographic locations (Curasson 1943), and diseases encountered by
translocated animals (naive to such diseases) after being
moved to a new region (Pandey et al. 1992). Examples
of species experiencing disease problems caused by the
release of captive-bred animals among free-ranging populations include golden lion tamarins (Leontopithecus
rosalia) in Brazil (May & Lyles 1987), white-tailed deer
(Odocoileus
virginianus)
in North America (Davidson
The manipulation of wildlife, whether an individual or a
population, can alter the dynamics of disease within
populations. Translocations, hunting, and live captures
for commercial trade have direct and indirect effects on
health. Alterations of host-pathogen interactions that result from these human activities affect not only the
health of targeted animals but also that of conspecifics
et al. 1996), and Arabian oryx (Oryx leucoryx) in Saudi
Arabia(Kock & Woodford 1988; Bush et al. 1993). Similar threats to wild populations have been documented
with the reintroduction of confiscated tortoises and orangutans that may have acquired an infectious disease
while in captivity from either captive animals (Jacobson
et al. 1995) or from humans (Warren et al. 1998), respectively.
Although dismissed as being insignificant and uncommonly used by many in the conservation sciences, translocations of animals have increased substantially in the
past several decades (Griffithet al. 1993), with over a million live animals moved and released as of the early 1990s
(Davidson & Nettles 1992). In practice, much of wildlife
management still depends heavily on such strategies.
Illegal and legal hunting for sport and bush meat and
capture of wild animals for the pet trade must be considered if we are to know the true scale and frequency of
animal movements that fall outside the normal geographic or behavioral scope of a given species. Removing individuals from populations and transporting their
live or dead bodies (including all the pathogens and parasites they carry) to new areas have enormous potential
for affecting the health of wild and domestic animal populations (described for infectious agents of canids in the
southeastern United States [Davidson et al. 1992] and for
rinderpest of ungulates in Africa [Plowright 1982]). In
the case of trophy hunting, there is also an effect on the
health of the source population in that the healthiest
and potentially most disease-resistant individuals often
are removed from populations already under pressure.
In developing countries, endangered species are frequently confiscated and end up in the care of foreign national biologists or rehabilitators who lack the resources
to screen for disease before release. Thus, many animals
and sympatric species.
are returned to the wild only to expose their conspecifics
WildlifePopulationDynamics
Conservation Biology
Volume 15, No. 5, October 2001
1228
Healthin Conservation
Wildlife
to novel diseases picked up during rehabilitation (Karesh
1995). In our experience, this type of "underground translocation" is common.
Disease Ecology
Ongoing anthropogenic modifications of the environment, including changes that increase interspecies contact and confine individual populations, the translocation
of susceptible hosts to regions with novel pathogens,
and the introduction of novel pathogens to susceptible
hosts in a new region, are responsible in many instances
for a change in disease ecology (Wilson 2000). One example of a shift in disease ecology is the loss of endemic
stability. An endemically stable disease is one in which the
agent, vector (in vector-borne diseases), host, and environment coexist in a manner that results in the virtual
absence of clinical disease (Norval et al. 1992). In many
regions of the world, diseases of domestic animals that
were once endemically stable, such as heartwater (Deem
et al. 1996) and theileriosis (Moll et al. 1984), are now
unstable due to anthropogenic changes. This change, to
either an endemically unstable or an epidemic state,
could happen in wildlife populations but is not as well
documented for them due to a lack of information on
those diseases historically endemically stable in wild-animal populations.
Several factors influence the spread and perpetuation
of a contagious agent once it has been introduced into a
host population: the density of susceptible hosts, the frequency of host contact, the infectiousness and pathogenicity of the disease, and the average time an infected
host is infectious (Anderson & May 1979a, 1979b). These
four factors are profoundly affected by global changes in
landscapes and wildlife dynamics.
Suggestions for Integrating Animal Health
into Conservation
Although the role of disease in species conservation has
been appreciated for years, it has only been in the recent past that health and disease issues have come to the
forefront of conservation biology as limiting factors in
wildlife conservation (Meffe 1999; Daszak et al. 2000;
Osofsky et al. 2000). Unfortunately, although many conservation biologists are interested in including questions
and concerns about disease in their study design or sampling methods, there is a misconception that the only
reason to work with veterinary wildlife professionals is
to have them immobilize study animals. Although the
veterinary profession has been instrumental in improving the safety and efficiency of animal handling procedures (Osofsky & Hirsch 2000), other pressing issues
mandate collaboration between conservation biologists
and wildlife health professionals. Thus, we present some
Conservation Biology
Volume 15, No. 5, October 2001
Deemet al.
practical steps to foster such collaboration. We base our
suggestions not only on the literature but also on a decade of experience in integrating wildlife health concerns into field biology and conservation efforts. We recommend only those approaches of highest priority and/
or those we have found most cost effective.
VeterinaryInvolvementin ConservationProjects
The use of veterinary skills in the form of either prevention or treatment is probably the most controversial issue surrounding the role of animal health in conservation efforts (Macfie 1992; Gascoyne et al. 1993; Inserro
1997). Many conservation biologists insist that "human
intervention" in the form of veterinary services should
not be provided in any way for wild animals because
such action would interfere with evolutionary processes. But there are probably few species that have not
been influenced by some form of "human intervention"
(Redford & Richter 1999). Even the simple act of conducting field research in an "untouched" area effects
change. Other people may object to veterinary involvement because of the potential risk of doing more harm
than good. This concern can easily be addressed by involving experienced, qualified health professionals in
decision making and procedures. We further recommend that the same standards be applied to the evaluation of risk of disease transmission or environmental contamination resulting from field research not related to
animal health. Rather than debate whether intervention
is good or bad, it would be more sensible to determine
the most appropriate prevention and treatment options
for wildlife populations on a case-by-case basis. Appropriate strategies for the prevention or treatment of wildlife diseases might range from public and staff healtheducation and vaccination programs to intensive disease
management. Examples of intensive management include the black-footedferret (Mustela nigripes; Thorne &
Williams 1988) and African wild dog (Gascoyne et al.
1993) conservation programs and control of waterfowl
disease epidemics (Pearson & Cassidy 1997). Aside from
ethical considerations, which vary widely among different groups of humans, decisions about the level of veterinary involvement in a project should be based on (1)
the status of the species or populations affected or at
risk; (2) the nature of the cause of the health problem,
which requires veterinary investigation; (3) the spatial
distribution of the species; (4) the costs and practicality
of necessary preventive and treatment measures; (5)
specific disease issues of concern; and (6) implications
of intervention or lack thereof on the health of other
species, including humans and domestic animals.
We stress that preventing the introduction of new
health problems, as opposed to intervening once a situation has already reached the crisis point, can and should
be a bigger part of what we do as conservation biolo-
Healthin Conservation 1229
Wildlife
Deemet al.
gists. When and whether preventive measures and crisis
intervention are needed to limit wildlife health problems
depend on so many variables in each locale that expertise in wildlife health should be aggressively cultivated
for more effective future conservation programs.
Applied Veterinary Medicine and Research in Conservation
HEALTH
ASSESSMENT
ANDMONITORING
Veterinarians perform health surveys or assessments and
long-term health monitoring that provide critically needed
baseline information on species of interest. In contrast
to our knowledge of humans and domestic animals, few
data sets exist to establish the "normal" or expected
range of values for most of the world's threatened or endangered wild species. These data sets should include
blood parameters such as complete blood count, serum
biochemistry profiles, vitamin and mineral levels, evidence of exposure to infectious agents such as antibodies or microbes, and residues of chemical contaminants.
Health assessment and monitoring programs integrated
into field biology projects have been described (Karesh
et al. 1997a; Karesh et al. 1997b; 1997c).
Baseline data on population health should be used in
population viability analysis because the viability of a
population is inseparable from its health (Karesh &
Cook 1995). These data can be used in comparisons with
the same population at a future date to determine the effects of various disturbances (i.e., ecotourism, weather
extremes, habitat loss) and for comparison with different populations. Such comparisons are valuable in determining the appropriateness of various conservation
management techniques for individual populations or
species. Just as mammal, bird, or reptile surveys allow
one to quantify population trends, documenting changes
in prevalence or exposure to infectious and toxic agents
provides objective data for management action. Changes
noted in these parameters, before and after an event (all
else being equal), would confirm that the event had an
influence on the health of the population and thus could
threaten long-term survival. Events that might be expected to influence the health status of free-ranging
wildlife include disease transmission from domestic animals in the region; exposure to industrial, agricultural,
and urban pollution; tourism; and disease transmission
between wildlife species. Identification of infectious disease threats or the presence of toxic agents would inform decisions about zoning and the use of terrestrial
and aquatic areas and could mobilize local and international support for conservation efforts.
from animals to humans; anthropozoonotic
diseases,
which are transmitted from humans to animals, and
other forms of interspecies disease transmission such as
vertebrate-to-vertebrate and vector-borne diseases. The
conservation of wildlife species is greatly complicated
by these possible disease transmission routes, and they
must be addressed to minimize potentially devastating
results for wildlife, humans, and domestic animals.
There have been many reports of disease epidemics in
both nonhuman (anthropozoonotic)
and human (zoonotic) primates (Kalema et al. 1998; Mudakikwa et al.
1998; Wolfe et al. 1998; Gao et al. 1999; Wallis & Lee
1999). These epidemics are suspected of being caused
by the direct and indirect contact of one group with another. Activities such as behavioral research or tourism,
although well intentioned, can serve to introduce new
diseases to wild populations (Wallis & Lee 1999).
As humans encroach on lands inhabited by nonhuman
primates, increase the use of nonhuman primates as a
source of protein, and continue to collect nonhuman
primates for trade as pets, the incidence of these epidemics surely will increase. An understanding of the epidemiology of these diseases through field studies is necessary to ensure that conservation projects guarantee
the survival of nonhuman primate species without risking the health of humans.
Diseases transmitted among livestock, other domestic
animals, and wildlife are also of great concern (Pastoret
et al. 1988; Roelke-Parker et al. 1996; Deem 1998; Karesh
et al. 1998). As grazing lands designated for livestock
continue to expand into regions where wildlife exist,
the opportunity for epidemics in both livestock and
wildlife populations increases. Policies to limit the use
of land for livestock are routinely unacceptable to governments and local peoples. It is therefore imperative
that we collect data to gain insight on the epidemiology
of these diseases in both livestock and wildlife hosts so
that conservation projects can be developed to ensure
the survival of wildlife species and the health of domestic livestock. The same concerns are associated with the
possible transmission of disease between wild and other
domestic animals (e.g., dogs and cats) as increased contact occurs between these two groups (Blouin et al.
1984; Kariuki 1988; Roelke-Parker et al. 1996). Researchers, protected-area managers and staff, and tour operators need to be aware that their presence, along with
that of their domestic pets and food animals, increase
the risk of introducing diseases to wildlife populations
(Karesh et al. 1997b; Wallis & Lee 1999).
TRAINING
OFZOONOTIC,
AND
HEALTH
STUDIES
ANTHROPOZOONOTIC,
OFDISEASES
INTERSPECIES
TRANSMISSION
Health assessment and monitoring programs should focus more on zoonotic diseases, which are transmitted
Worldwide, wildlife-agency workers, veterinarians, and
conservation biologists must be trained to design and
conduct wildlife studies that incorporate crucial health
considerations. Training should cover how to conduct
Conservation Biology
Volume 15, No. 5, October 2001
1230
Healthin Conservation
Wildlife
research on wildlife safely, humanely, and in a manner
consistent with conservation goals, and should provide
practical information on the ecology of diseases. We
must raise awareness among professionals in other disciplines and within local communities. Everyone, from biologists to policymakers to cattle ranchers, should be
welcome to participate in organized workshops and
other outreach programs that inform them about their
relationships to and effects on the health of wildlife. As
Osofsky (1997) says, "thinklink."
Deemet al.
serve one's special research interest. Simple guidelines
can be followed that will allow samples to be collected
for gathering a variety of health-related information simultaneously. For example, death should not represent
waste in the context of conservation-oriented studies.
Necropsies could be conducted on every animal found
dead, which could provide critically needed information
and would require only training in proper sample handling and human safety precautions.
DIAGNOSTIC
CAPABILITIES
INTERDISCIPLINARY
COLLABORATION
Interdisciplinary collaboration should be directed at studies that shed light on the effects of pathogens and toxic
chemicals on the persistence of wildlife populations.
These studies often involve the investigation of relationships among disturbed habitats and the health of wildlife, domesticated animals, and human beings. This requires collaboration between livestock and wildlife
veterinarians, physicians, and other workers in basic and
applied biomedical research, as well as epidemiologists,
conservation biologists, and ecologists. Some conservation biologists object to such collaboration, fearing that
information on the diseases of wildlife will be misconstrued by the human medical community and politicians, resulting in the persecution of wildlife as disease
carriers. This objection is based on suspicion and will
not help protect wildlife. Whether or not veterinarians
and conservation biologists choose to contribute their
opinions and professional expertise to the human medical community, research directed at public health will
continue. It is therefore imperative that veterinarians
and conservation biologists take every opportunity to
provide input to ensure that research is conducted in a
manner consistent with a conservation ethic and that
findings are interpreted with conservation goals in mind.
ANDMANAGEMENT
DATACOLLECTION
The community of people working on aspects of wildlife health as related to conservation is growing and will
continue to grow as awareness of the effects of disease
increases. It is important that we create software and databases that can make wildlife health information easy to
record, disseminate, share, and interpret. Although a variety of programs exist for experimenting with theoretical epidemiological models, only recently have a few efforts been directed at standardizing and tracking current
information collected on wildlife die-offs or at mapping
these data.
Along similar lines, biologists, ecologists, veterinarians, and medical researchers need to coordinate their efforts better to capitalize on all opportunities for gathering information. Procedures for animal handling and/or
sample collection should not be designed exclusively to
Conservation Biology
Volume 15, No. 5, October 2001
Better diagnostic capabilities are needed to identify the
wide range of pathogens that are presently and will increasingly be found in wildlife. Identification of exposure to infectious diseases is often limited by the availability of tests developed for domestic animals and humans.
For example, sensitive and specific antemortem diagnostic tests for tuberculosis are not currently available for
wildlife species. Finding antibodies to morbillivirus in
southern elephant seals (Mirounga leonine) using available tests developed for canine and phocid morbilliviruses does not identify the virus that caused the immune
response in the seals (Karesh et al. 1997d). Diagnostic
capabilities need to be developed to identify disease
agents in wildlife. Although genetic and toxicology tests
have advanced, there is still a need to refine and improve these techniques.
POLICY
The importance of integrating health issues, as one component of conservation, into policy development cannot
be overemphasized. For instance, we must recognize
threats to the health of wildlife posed by conservation
and development strategies involving ecotourism, improvements in livestock production, and wildlife harvesting programs. Tourists and the food needed to support them may transport infectious organisms (Karesh
et al. 1997c). Unvaccinated domestic animals may be
carriers of infectious diseases. In the case of wildlife harvesting, a frequently overlooked health threat is the
tracker or lure animals (e.g., dogs and parrots) used by
hunters, which may transmit diseases to free-ranging
wildlife. These situations underscore the importance of
considering health implications when establishing policies and initiating new programs. Finally, theoretically
sustainable harvesting models based on recruitment and
harvest rates must take into account the effects of health
and disease on sexual maturation, reproductive success,
and longevity. These effects may vary from year to year,
depending on factors such as host and sympatric species
densities, vector abundance, environmental conditions,
and agent pathogenicity.
We have used four policy-related strategies to prevent
wildlife disease problems: (1) to inform and educate
workers in funding agencies of the important relation-
WildlifeHealthin Conservation
Deemet al.
ships among the health of ecosystems, wildlife, domestic animals, and humans; (2) to offer input into planning
conservation or development projects that involve the
management or manipulation of wildlife or domestic animals; (3) to analyze data on wildlife health and disease
risks and integrate it into the creation of buffer zones,
multiple land-use zones, and corridors; and (4) to support stringent regulations and guidelines on wildlife rehabilitation, reintroduction, and translocation to prevent
the introduction of novel pathogens to wild populations.
Conclusion
The effects of disease on wildlife populations have been
recognized for years. It is also clear that Earth's wild places
have become smaller and more artificial in the past century, leading to a greater potential for infectious and
noninfectious diseases to adversely affect conservation
efforts. As a result, viable conservation initiatives can no
longer be designed without addressing the health issues
of wildlife. Considering that human intervention in wildlife populations occurs daily all over the world, in mostly
negative ways (i.e., human expansion into previously
uninhabited regions, poaching, and the collection and
movement of animals internationally), it is no longer
possible or ethical to justify a "hands-off" approach when
confronted with wildlife disease issues in a conservation
context. Instead, the expertise of all relevant disciplines,
including that of health specialists, should be employed
in developing better management for wildlife and ecosystems. We have presented specific suggestions for integrating wildlife health into conservation efforts, and
we have emphasized that although veterinarians and
other health professionals have an obvious role to play
in protecting the health of wildlife, conservation workers in every discipline have the ability and responsibility
to help address this issue. With minimal additional effort
and cost, conservation researchers can maximize the
data collected for monitoring wildlife health, can keep
in mind potential disease issues in their studies, and can
take a precautionary approach to preventing transmission of diseases in research, conservation, and development activities. We hope our suggestions will stimulate
innovative collaborations in the field and in the policy
arena and raise awareness of the need for a new paradigm that integrates considerations of wildlife health
and disease into mainstream conservation.
Acknowledgments
We thank K. Redford, J. Robinson, R. Cook, and the reviewers and editors of Conservation Biology for their
valuable input.
1231
LiteratureCited
Alexander, K. A., and M. J. G. Appel. 1994. African wild dogs (Lycaon
pictus) endangered by a canine distemper epizootic among domestic dogs near the Masai Mara National Reserve, Kenya. Journal of
Wildlife Disease 30:481-485.
Anderson, R. M. 1991. Populations and infectious diseases: ecology or
epidemiology? Journal of Animal Ecology 60:1-50.
Anderson, R. M., and D. M. Gordon. 1982. Processes influencing the
distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:
373-398.
Anderson, R. M., and R.M. May. 1979a. Population biology of infectious diseases: part I. Nature 280:361-367.
Anderson, R. M., and R.M. May. 1979b. Population biology of infectious diseases: part II. Nature 280:455-461.
Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L.
Goggin, R. Slocombe, M. A. Ragan,A. D. Hyatt, K. R. McDonald, H.
B. Hines, K. R. Lips, G. Marantelli,and H. Parkes. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australiaand Central America. Proceedings of the National Academy of Sciences of the United States of
America 95:9031-9036.
Blouin, E. F., A. A. Kocan, B. L. Glenn, K. M. Kocan, and J. A. Hair.
1984. Transmission of Cytauxzoon felis Kier, 1979 from bobcats,
Felis rufus (Schreber), to domestic cats by Dermacentor variabilis (Say).Journal of Wildlife Disease 20:241-242.
Bush, M., B. B. Beck, and R. J. Montali. 1993. Medical considerations of
reintroduction. Pages 24-26 in M. E. Fowler, editor. Zoo and wild
animal medicine: current therapy 3. W. B. Saunders, Philadelphia,
Pennsylvania.
Colborn, T., D. Dumanoski, andJ. Peterson Myers. 1996. Our stolen future: are we threatening our fertility, intelligence, and survival?A
scientific detective story. Penguin Books, New York.
Curasson, M. G., 1943. Trypanosoma vivax et varieties. Pages 267279 in M. G. Curasson, editor. Traite de protozoologie veterinaire
et comparee, tome I. Vigot Freres, Paris.
Daszak, P., A. A. Cunningham, and A. D. Hyatt. 2000. Emerging infectious diseases of wildlife: threats to biodiversity and human health.
Science 287:443-449.
Davidson, W. R., and V. F. Nettles. 1992. Relocation of wildlife: identifying and evaluating disease risks. Transactions of the North American Wildlife and NaturalResources Conference 57:466-473.
Davidson, W. R., M.J. Appel, G. L. Doster, 0. E. Baker, andJ. F. Brown.
1992. Diseases and parasites of red foxes, gray foxes, and coyotes
from commercial sources selling to fox-chasing enclosures. Journal
of Wildlife Diseases 28:581-589.
Davidson, W. R., G. L. Doster, and R. C. Freeman. 1996. Parelaphostrongylus tenuis on Wassaw Island, Georgia: a result of translocating white-tailed deer. Journal of Wildlife Disease 32:701-703.
Deem, S. L. 1998. A review of heartwater and the threat of introduction of Cowdria ruminantium and Amblyomma spp. ticks to
the American mainland. Journal of Zoo and Wildlife Medicine 29:
109-113.
Deem, S. L., R. A. I. Norval, T. Yonow, T. F. Peter, S. M. Mahan,and M.J.
Burridge. 1996. The epidemiology of heartwater: establishment and
maintenance of endemic stability. Parasitology Today 12:402-405.
Dobson, A. P. 1988. Restoring island ecosystems: the potential of parasites to control introduced mammals. Conservation Biology 2:31-39.
Dobson, A. P., and P. J. Hudson. 1986. Parasites, disease and the structure of ecological communities. Trends in Ecology and Evolution 1:
11-15.
Fischman, H. R., J. K. Grigor, J. T. Horman, and E. Israel. 1992. Epizootic or rabies in raccoons in Marylandfrom 1981-1987. Journal
of the American Veterinary Medical Association 201:1883-1886.
Foreyt, W. J. 1990. Pneumonia in bighorn sheep: effects of Pasteurella
hemolytica from domestic sheep and effects on survival and long
Conservation Biology
Volume 15, No. 5, October 2001
1232
WildlifeHealthin Conservation
term reproduction. Biennial Symposium of Northern Wild Sheep
and Goat Council 7:92-101.
Friend, M. 1976. Wildlife diseases: philosophical considerations. Pages
7-18 in L. A. Page, editor. Wildlife diseases. Plenum Press, New
York.
Gao, F., E. Bailes, D. L. Robertson, Y. Chen, C. M. Rodenburg, S. F.
Michael, L. B. Cummins, L. 0. Arthur,M. Peeters, G. M. Shaw, P. M.
Sharp, and B. H. Hahn. 1999. Origin of HIV-1 in the chimpanzee
Pan troglodytes troglodytes. Nature 397:436-441.
Garrot, R.A., L.L.Eberhart, and D.M. Burns. 1993. Mortality of sea otters in Prince William Sound following the Exxon Valdez oil spill.
MarineMammalScience 9:343-359.
Gascoyne, S. C., M. K. Laurenson, S. Lelo, and M. Borner. 1993. Rabies
in Africanwild dogs (Lycaon pictus) in the Serengeti region, Tanzania. Journal Wildlife Disease 29:396-402.
Griffith, B., J. M. Scott, J. W. Carpenter, and C. Reed. 1993. Animal
translocations and potential disease transmission. Journal of Zoo
and Wildlife Medicine 24:231-236.
Hansen, L. J., and M. L. Johnson. 1999. Conservation and toxicology:
integrating the disciplines. Conservation Biology 13:1225-1227.
Harvell, C. D., K. Kim,J. M. Burkholder, R. R. Colwell, P. R. Epstein, D.
J. Grimes, E. E. Hofmann, E. K. Lipp, A. D. M. E. Osterhaus, R. M.
Overstreet, J. W. Porter, G. W. Smith, and G. R. Vasta. 1999. Emerging marine diseases-climate links and anthropogenic factors. Science 285:1505-1510.
Heide-Jorgensen, M. P., T. Harkonen, R. Dietz, and P. M. Thompson.
1992. Retrospective of the 1988 European seal epizootic. Diseases
of Aquatic Organisms 13:37-62.
Herbst, L. H. 1994. Fibropapillomatosis of marine turtles. Annual Review of Fish Diseases 4:389-425.
Hutchins, M., T. Foose, and U. S. Seal. 1991. The role of veterinary
medicine in endangered species conservation. Journal of Zoo and
Wildlife Medicine 22:277-281.
Inserro, J. C. 1997. States, agencies discuss solutions for handling Yellowstone bison, brucellosis. Journal of the American Veterinary
Medical Association 210:593-595.
Jacobson, E. R., M. B. Brown, I. M. Schumacer, B. R. Collins, R. K. Harris, and P. A. Klein. 1995. Mycoplasmosis and the desert tortoise
(Gopherus agassizii) in Las Vegas Valley, Nevada. Chelonian Conservation Biology 1:279-284.
Jessup, D. A. 1993. Translocation of wildlife. Pages 493-499 in M. E.
Fowler, editor. Zoo and wild animal medicine: current therapy 3.
W. B. Saunders, Philadelphia, Pennsylvania.
Jones, D. M. 1982. Conservation in relation to animal disease in Africa
and Asia. Symposiaof the Zoological Society of London 50:271-285.
Kalema, G., R. A. Kock, and E. Macfie. 1998. An outbreak of sarcoptic
mange in free-rangingmountain gorillas (Gorilla gorilla berengei)
in Bwindi Impenetrable National Park, south western Uganda. Pages
438 in Proceedings of the American Association of Zoo Veterinarians and the American Association of Wildlife Veterinarians joint
conference. American Association of Zoo Veterinarians, Media,
Pennsylvania.
Karesh,W. B. 1995. Wildlife rehabilitation:additionalconsiderations for
developing countries. Journalof Zoo and Wildlife Medicine 26:2-9.
Karesh, W. B., and R. A. Cook. 1995. Applications of veterinary medicine to in situ conservation efforts. Oryx 29:244-252.
Karesh, W. B., K. H. Smith, F. Smith, M. Atalia, P. Morkel, A. Torres, C.
House, W. E. Braselton, and E. S. Dierenfeld. 1997a. Elephants, buffalo, kob, and rhinoceros: immobilization, telemetry and health
evaluations. Pages 296-300 in Proceedings of the American Association of Zoo Veterinarians.American Association of Zoo Veterinarians, Media, Pennsylvania
Karesh, W. B., A. Rothstein, W. Green, H. 0. Reuter, W. E. Braselton,
A. Torres, and R. A. Cook. 1997b. Health evaluation of black-faced
impala (Aepyceros melampus petersi) using blood chemistry and
serology. Journal of Zoo and Wildlife Medicine 28:361-367.
Karesh, W. B., A. del Campo, W. E. Braselton, H. Puche, and R. A.
Conservation Biology
Volume 15, No. 5, October 2001
Deemet al.
Cook. 1997c. Health evaluation of free-rangingand hand-rearedmacaws (Ara spp.) in Peru. Journal of Zoo and Wildlife Medicine 28:
368-377.
Karesh, W. B., R. A. Cook, M. Stetter, M. M. Uhart, A. Hoogesteijn,
M. N. Lewis, C. Campagna, P. Majluf, A. Torres, C. House, L. A.
Thomas, W. E. Braselton, E. S. Dierenfeld, T. S. McNamara, P.
Duignan, S. Raverty,and M. Linn. 1997d. South Americanpinnipeds:
immobilization, telemetry, and health evaluations. Pages 291-295
in Proceedings of the American Association of Zoo Veterinarian.
American Association of Zoo Veterinarians,Media, Pennsylvania.
Karesh, W. B., M. M. Uhart, E. S. Dierenfeld, W. E. Braselton, W.
Torres, C. House, H. Puche, and R. A. Cook. 1998. Health evaluation of free-rangingguanaco (Lama guanicoe). Journal of Zoo and
Wildlife Medicine 29:134-141.
Kariuki, D. P. 1988. The epidemiology and diagnosis of rabies in
Kenya. The Kenya Veterinarian 12:32-35.
Kat, P. W., K. A. Alexander, J. S. Smith, J. D. Richardson, and L. Munson. 1996. Rabies among African wild dogs (Lycaon pictus) in the
Masai Mara,Kenya. Journal of Veterinary Diagnostic Investigations
8:420-426.
Keet, D. F., N. P. J. Kriek, M. L. Penrith, A. Michel, and H. Huchzermeyer. 1996. Tuberculosis in buffaloes (Syncerus caffer) in the
Kruger National Park: spread of the disease to other species.
Onderstepoort Journal of Veterinary Research 63:239-244.
Kock, R. A., and M. H. Woodford. 1988. Reintroduction of Pere
David's deer (Elaphurus davidianus), scimitar-hornedoryx (Oryx
dammah) and the Arabian oryx (Oryx leucoryx) to their native
habitats: a veterinary perspective. Pages 143-144 in Proceedings of
the American Association of Zoo Veterinarians and the American
Association of Wildlife Veterinarians joint conference. American
Association of Zoo Veterinarians,Media, Pennsylvania.
Last, J. M. 1983. A dictionary of epidemiology. Oxford University
Press, New York.
Leopold, A. 1933. Game management. Scribner's, New York.
Macfie, E. J. 1992. An update on current medical management program for Rwanda's mountain gorillas: veterinarians as population
managers, and the effects of war. Pages 45-37 in Proceedings of the
American Association of Zoo Veterinarians and the American Association of Wildlife Veterinariansjoint conference. American Association of Zoo Veterinarians,Media, Pennsylvania.
Maehr, D. S., E. D. Land, and M. E. Roelke. 1991. Mortalitypatterns of
panthers in southwest Florida.Pages 201-207 in A. G. Eversole, editor. Proceedings of the annual conference of the southeastern fish
and wildlife agencies. Southeastern Fish and Wildlife Agencies,
White Sulphur Springs, West Virginia.
May, R. M. 1988. Conservation and disease. Conservation Biology 2:
28-30.
May, R. M., and A. M. Lyles, 1987. Living Latin binomials. Nature 326:
642-643.
McCallum, H., and A. Dobson. 1995. Detecting disease and parasite
threats to endangered species and ecosystems. Trends in Ecology
and Conservation 10:190-194.
Meffe, G. K. 1999. Conservation medicine. Conservation Biology 13:
953-954.
Meltzer, D. G. A. 1993. Historical survey of disease problems in wildlife populations: Southern Africa mammals. Journal of Zoo and
Wildlife Medicine 24:237-244.
Moll, G., A. Lohding, and A. S. Young. 1984. Epidemiology of theilerisosis in the Trans-MaraDivision, Kenya: husbandry and disease
background and preliminary observations on theileriosis in calves.
Preventive Veterinary Medicine 2:801-831.
Morell, V. 1995. Chimpanzee outbreak heats up search for ebola origin. Science 268:974-975.
Mudakikwa,A. B., J. Sleeman, J. W. Foster, L. L. Meader, and S. Patton.
1998. An indicator of human impact: gastrointestinal parasites of
mountain gorillas (Gorilla gorilla berengei) from the Virunga volcanoes region, Central Africa. Pages 436-437 in Proceedings of the
Deemet al.
American Association of Zoo Veterinariansand the American Association of Wildlife Veterinariansjoint conference. American Association of Zoo Veterinarians,Media, Pennsylvania.
Norval, R. A. I., B. D. Perry, and A. S. Young. 1992. Pages 223-234 and
285-290 in The epidemiology of theileriosis in Africa. Academic
Press, London.
Office International des Epizooties. 1987. Epizootological information,
ESP/87/1/117, ESP/87/2/119, ESP/87/3/121, ESP/4/127, ESP/87/5/
142, ESP/87/6/145. Office International des Epizooties, Paris.
O'Hara,T. M., and C. D. Rice. 1996. Polychlorinated biphenyls. Pages
71-86 in A. Fairbrother,L. N. Locke, and G. L. Hoff, editors. Noninfectious diseases of wildlife. 2nd edition. Iowa State University
Press, Ames.
Ouellet, M., J. Bonin, J. Rodrigue, J.-L.DesGranges, and S. Lair. 1997.
Hindlimb deformities (ectromelia, ectodactyly) in free-livinganurans
from agriculturalhabitats. Journal of Wildlife Disease 33:95-104.
Osofsky, S. A. 1997. Think link: critically evaluating linkages between
conservation projects and development. Journal of Zoo and Wildlife Medicine 28:141-143.
Osofsky, S. A., and K. J. Hirsch. 2000. Chemical restraint of endangered mammals for conservation purposes: a practical primer.
Oryx 34:27-33.
Osofsky, S. A., W. B. Karesh, and S. L. Deem. 2000. Conservation medicine: a veterinary perspective. Conservation Biology 14:336-337.
Pandey, G. S., D. Minyoi, F. Hasebe, and E. T. Mwase. 1992. First report of heartwater (cowdriosis) in Kafue lechwe (Kobus leche kafuensis) in Zambia. Revue d'Elevage et de Medecine Veterinaire des
Pays Tropicaux 45:23-25.
Pastoret, P. P., E. Thiry, B. Brochier, A. Schwers, I. Thomas, and J. Dubuisson. 1988. Diseases of wild animals transmissible to domestic
animals. Revue Scientifique et Technique (International Office of
Epizootics) 7:705-736.
Pearson, G. L., and D. R. Cassidy. 1997. Perspectives on the diagnosis,
epizootiology, and control of the 1973 duck plague epizootic in
wild waterfowl at Lake Andes, South Dakota. Journal of Wildlife
Diseases 33:681-705.
Peters, R. L., and J. D. S. Darling. 1985. The greenhouse effect and nature reserves. Bioscience 35:707-717.
Peters, A., and K. J. F. Verhoeven. 1994. Impact of artificiallighting on
the seaward orientation of hatchling loggerhead turtles. Journal of
Herpetology 28:112-114.
Plowright, W. 1982. The effects of rinderpest and rinderpest control
on wildlife in Africa. Symposia of the Zoological Society of London
50:1-28.
Plowright, W. 1988a. Viruses transmissible between wild and domestic animals. Symposia of the Zoological Society of London 60:
175-199.
Plowright, W., 1988b. Research on wildlife diseases: is a reappraisal
necessary? Revue Scientifique et Technique 7:783-795.
Quammen, D. 1996. The song of the dodo. Scribner's, New York.
Redford, K. H., and B. D. Richter. 1999. Conservation of biodiversity in
a world of use. Conservation Biology 13:1246-1256.
Roelke-Parker,M. E., L. Munson, C. Packer, R. Kock, S. Cleaveland, M.
Carpenter, S. J. 0 Brien, A. Pospichil, R. Hofmann-Lehmann, H.
Lutz, G. L. M. Mwamengele, M. N. Mgasa, G. A. Machange, B. A.
Summers, and M. J. G. Appel. 1996. A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379:441-445.
Scott, M. E. 1988. The impact of infection and disease on animal populations:implications for conservation. ConservationBiology 2:40-56.
WildlifeHealthin Conservation
1233
Sleeman, J. M. 1998. Preventive medicine programme for the mountain gorillas (Gorilla gorilla beringei) of Rwanda: a model for
other endangered primate populations. Pages 127-132 in Proceedings of European Association of Zoo and Wildlife Veterinariansand
British Veterinary Zoological Society. Van Setten Kwardraat,
Houten, The Netherlands.
Smith, G. R. 1982. Botulism in waterfowl. Pages 97-119 in M. A. Edwards and U. McDonnell, editors. Animal disease in relation to conservation. Academic Press, London.
Smith, F. D. M., R. M. May, R. Pellew, T. H. Johnson, and K. R. Walter.
1993. How much do we know about the current extinction rate?
Trends of Ecological Evolution 8:375-378.
Soule, M. E., and K. A. Kohm. 1989. Ecosystems: conservation and research. Pages 13-19 in M. E. Soule and K. A. Kohm, editors. Research priorities for conservation biology. Island Press, Washington, D.C.
Spalding, M. G., and D. J. Forrester. 1993. Disease monitoring of freeranging and released wildlife. Journal of Zoo and Wildlife Medicine
24:271-280.
Thorne, E. T., and E. S. Williams. 1988. Disease and endangered species: the black-footed ferret as a recent example. Conservation Biology 2:66-74.
Van Riper, C., III, S. G. Van Riper, M. L. Goff, and M. Laird. 1986. The
epizootiology and ecological significance of malaria in Hawaiian
land birds. Ecological Monographs 56:327-344.
Wallis, J., and D. R. Lee. 1999. Primate conservation: the prevention
of disease transmission. International Journal of Primatology 20:
803-826.
Warner, R. E. 1968. The role of introduced diseases in the extinction
of the endemic Hawaiian avifauna. Condor 70:101-120.
Warren, K. S., H. Niphuis, Heriyanto, E.J. Verschoor, R. A. Swan, andJ.
L. Heeney. 1998. Seroprevalence of specific viral infections in confiscated orangutans (Pongo pygmaeus). Journal of Medical Primatology 27:33-37.
Wilson, M. E. 2000. Environmental change and infectious diseases. Ecosystem Health 6:7-11.
Wobeser, G. A. 1981. Diseases of wild waterfowl. Plenum Press, New
York.
Wolfe, N. D., A. A. Escalante, W. B. Karesh, A. Kilbourn, A. Spielman,
and A. A. Lal. 1998. Wild primate populations in emerging infectious disease research: the missing link? Emerging Infectious Diseases 4:149-158.
Woodford, M. H. 1993. International disease implications for wildlife
translocation. Journal of Zoo and Wildlife Medicine 24:265-270.
Woodford, M. H., and P. B. Rossiter. 1993. Disease risks associated
with wildlife translocation projects. Revue Scientifique et Technique (International Office of Epizootics) 12:115-135.
World Conservation Union. 1987. Translocation of.living organisms:
introductions, re-introductions, and re-stocking. Position statement. Gland, Switzerland.
Yamamoto, J. T., R. M. Donohoe, R. M. Fry, M. S. Golub, and J. M.
Donald. 1996. Environmentalestrogens: implications for reproduction in wildlife. Pages 31-51 in A. Fairbrother,L. N. Locke, and G.
L. Hoff, editors. Noninfectious diseases of wildlife. 2nd edition.
Iowa State University Press, Ames.
Young, T. P. 1994. Natural die-offs of large mammals: implications for
conservation. Conservation Biology 8:410-418.
Yuill, T. M. 1987. Diseases as components of mammalian ecosystems:
mayhem and subtlety. CanadianJournal of Zoology 65:1061-1066.
Conservation
Biology
Volume15, No. 5, October2001