Putting Theory into Practice: Wildlife Health in Conservation

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Conservation Biology, Pages 1224–1233Volume 15, No. 5, October 2001

Putting Theory into Practice: Wildlife Healthin Conservation

SHARON L. DEEM,* WILLIAM B. KARESH, AND WENDY WEISMAN

Field Veterinary Program, 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 in-creasing 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 onthe health of wildlife species. These changes include human population growth, habitat fragmentation anddegradation, the isolation of populations of species, and an increased proximity of humans (and their domes-tic animals) to wildlife. Further, some conservation projects have caused more harm than good by unwit-tingly introducing diseases to wildlife populations, whereas others have failed to meet their objectives be-cause they did not take disease factors into consideration. Conservation biologists need to move quickly pastthe decades-old debate on the relative importance of wildlife health to conservation and begin using all thetools 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 concretesuggestions for ways to integrate wildlife health sciences into conservation, such as including health assess-ment 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 healthcomponents, and encouraging interdisciplinary collaboration. Our goal is to raise awareness that conserva-tion biologists working in disciplines ranging from field biology to policy making have an important role toplay in facilitating a transition toward a new conservation paradigm that includes wildlife health. This para-digm shift will take an academic understanding of the importance of wildlife disease and turn it into practi-cal actions that will help conserve wildlife more effectively.

De la Teoría a la Práctica: la Salud de la Vida Silvestre en la Conservación

Resumen:

Los biólogos de la conservación reconocen que las enfermedades infecciosas y no infecciosas sonun reto cada vez mayor para la conservación de vida silvestre. El papel de las enfermedades como un factorlimitante de la sobrevivencia de especies se puede deber a cambios antropogénicos a escala global que tieneninfluencia directa e indirecta en la salud de especies de vida silvestre. Estos cambios incluyen el crecimientode la población, la fragmentación y degradación del hábitat, el aislamiento de poblaciones y una mayorproximidad de humanos (y sus animales domésticos) a la vida silvestre. Adicionalmente, algunos proyectosde conservación han causado más daños que beneficios al introducir, inconscientemente, enfermedades enlas poblaciones de vida silvestre, mientras que otros han fallado en alcanzar sus objetivos porque no toma-ron en consideración a factores de enfermedades. Como biólogos de la conservación, necesitamos rápida-mente superar el debate que se ha dado por décadas sobre la importancia relativa de la salud de la vida sil-vestre para la conservación y comenzar a utilizar todas las herramientas disponibles para asegurar laefectividad de nuestros esfuerzos. Brevemente examinamos la literatura sobre enfermedades de vida silves-tre, colocamos la salud de la vida silvestre en un contexto de cambios globales que afectan poblaciones silves-tres de animales y ofrecemos sugerencias concretas para integrar las ciencias de la salud de vida silvestre enla conservación, como incluir la evaluación de la salud o programas de monitoreo e investigar la trans-misión de enfermedades entre especies en proyectos de campo, entrenar profesionales de la vida silvestre en

*

email [email protected] submitted August 4, 2000; revised manuscript accepted February 21, 2001.

Conservation BiologyVolume 15, No. 5, October 2001

Deem et al. Wildlife Health in Conservation

1225

Introduction

The conservation of wildlife requires an understandingof biogeographical patterns, community structure, pop-ulation dynamics, and individual behavior. A fifth factorthat should be viewed as imperative for sound conserva-tion efforts is an understanding of health issues that af-fect populations. If one reads recent editorials and re-views in scientific journals, it is easy to come away withthe impression that disease and health issues have onlyjust been discovered as important factors in the conser-vation of wildlife (Meffe 1999; Daszak et al. 2000). Infact, for many decades, disease has been recognized as acritical issue. What is new, however, is the increasing at-tention the subject is receiving from the wider conserva-tion community. This is encouraging because the atten-tion suggests that we are poised to move beyond anacademic interest in the effect of diseases on wildlife.

Health

and

disease

are broad terms, so it is useful todefine them in the context of our discussion. The WorldHealth Organization defines health as a state of completephysical, mental, and social well being and not merelythe absence of disease or infirmity (Last 1983). Whilethis state can serve as a laudable goal, it does not pro-vide us with objective criteria for determining the healthof wildlife. Wobeser (1981) defines

disease

in free-rang-ing wildlife populations as “any impairment that inter-feres with or modifies the performance of normal func-tions, including responses to environmental factors suchas nutrition, toxins, and climate; infectious agents; inher-ent or congenital defects, or combinations of these fac-tors.” Those impairments that negatively affect the long-term persistence of populations and the ability of healthypopulations to fulfill their ecological roles in an ecosys-tem are of primary concern to those of us involved inconservation.

Impairments to the health of wildlife are being exacer-bated by the human population explosion, habitat frag-mentation and degradation, isolation of wildlife popula-tions, and an increased proximity of humans (and theirdomestic animals) to wildlife ( Jones 1982; Scott 1988;Daszak et al. 2000). These phenomena are occurring onan unprecedented global scale, which in turn is creatingnovel opportunities for disease to have a negative effecton wildlife and on efforts to conserve it.

We (1) provide a historical perspective on what issometimes referred to as “conservation medicine” by brieflyreviewing how health and disease factors have beenseen to affect the persistence of wildlife populations; (2)describe in more detail how global changes are expand-ing the role disease plays in population persistence; and(3) make practical recommendations for prioritizing ac-tivities that workers should focus on in trying to incor-porate wildlife health concerns into conservation efforts.

Historical Perspective

In 1933 Aldo Leopold stated that the “role of disease inwildlife conservation has probably been radically under-estimated” (Leopold 1933). Even though “conservationmedicine” has only recently reached the mainstreamconservation literature (Meffe 1999; Osofsky et al. 2000),research began in the decades following Leopold’s state-ment and established a large body of scientific knowl-edge on wildlife diseases and disease ecology. Diseasesof wildlife were first seriously addressed by the scientificcommunity as they related to either the health of domes-tic species (i.e., ruminants, pigs, chickens) with whichwildlife had contact or to that of game species (i.e.,deer, ducks) that were important economically (Friend1976; Pastoret et al. 1988; Plowright 1988

b

). Other dis-eases of domestic and wildlife species that were origi-nally noted as a major concern were zoonoses (diseasestransmissible from animals to humans) such as rabies,brucellosis, and tuberculosis (Friend 1976).

Beginning in the 1970s and 1980s, surveys that incor-porated epidemiologic approaches were conducted on avariety of free-ranging wildlife populations. Additionalinterest and funding was sparked in the 1980s as a resultof the passage of the U.S. Endangered Species Act (Spal-ding & Forrester 1993). From the 1970s through the1990s, relevant publications included theoretical modelsdescribing parasite biology (Anderson & May 1979

a

;1979

b

; Anderson & Gordon 1982; Anderson 1991), em-pirical examples of significant negative effects of dis-eases on free-ranging wildlife populations (Thorne &Williams 1988; Heide-Jørgensen et al. 1992), and con-ceptual statements on the role of wildlife health in con-

el diseño e instrumentación de estudios de vida silvestre que incorporen componentes de salud y colabo-ración trans-disciplinaria. Nuestra meta es crear conciencia de que los biólogos de la conservación que traba-jan en disciplinas que van de la biología de campo a definición de políticas juegan un papel importante enla transición hacia un nuevo paradigma de conservación que incluye la salud de la vida silvestre. Este cam-bio de paradigma tendrá el entendimiento de la academia acerca de la importancia de las enfermedades dela vida silvestre y transformarlo en acciones prácticas que ayudarán a conservar a la vida silvestre más efi-

cientemente.

1226

Wildlife Health in Conservation Deem et al.


servation (Hutchins et al. 1991; Woodford 1993; Karesh& Cook 1995).

One issue that has received a significant amount of at-tention in its own right is massive die-offs associatedwith disease in free-ranging wildlife populations (Young1994). Examples include diseases such as rinderpest inungulate species (Plowright 1982) and botulism in wa-terfowl (Smith 1982), die-offs associated with oil spills(Garrot et al. 1993), and infectious disease epidemicssuch as canine distemper virus in lions (Roelke-Parker etal. 1996) and malaria in endemic Hawaiian birds (Warner1968; Van Riper et al. 1986). For many years the primaryrole of wildlife veterinarians was the management (con-servation) of populations experiencing disease epidem-ics associated with high mortality.

In the recent past, naturally occurring infectious agentsand noninfectious etiologies (causes of disease) havebeen recognized as integral in shaping many aspects ofwildlife behavior and ecology (Yuill 1987; May 1988).Increasingly, many conservation scientists, including vet-erinarians, have begun to put these phenomena into thecontext of the current biodiversity crisis and to examinemore explicitly the role disease can play in the loss ofspecies (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 relevantresearch, providing a foundation for efforts to integrateconcerns about wildlife health and disease into practicalconservation efforts. Workers have provided much ofthe data needed to understand how the current globalchanges such as increasing interactions among wildlife,livestock, and humans affect our efforts to conservewildlife populations.

Global Trends Affecting Wildlife Healthin Conservation

There are three broad processes affected by ongoing globalchanges which have profound implications for wildlifehealth and conservation: alterations in landscapes andhabitats, shifts in wildlife populations, and the resultingchanges in disease ecology. We recognize that to somethe distinctions between these categories may seem ar-bitrary; they clearly overlap and may be at work simulta-neously, which complicates and compounds their effects(Soulé & Kohm 1989). Nevertheless, in the interest ofcreating a simple conceptual framework for discussion ofthe issues, we have chosen to categorize them in this way.

Furthermore, changes taking place at the global scalehave direct and indirect effects on the health of wildlifespecies. We include examples of global changes actingin indirect ways on wildlife health, making populationsunder stress more susceptible to disease outbreaks that

otherwise would run their course without risking ex-tinction of an entire species. Such disease outbreaks rep-resent the way many conservation biologists traditionallyhave understood how disease processes act on wildlifepopulations. We also discuss certain global anthropo-genic changes that have a direct effect on wildlife persis-tence, stressing that there are opportunities for familiardiseases to act on wildlife populations in new ways andsituations allowing completely novel diseases to comeinto play. Disease events that fall into the latter groupare not confined to an already failing population, butrather can be a major cause of decline in themselves.

Changes in Landscapes and Habitats

Environmental changes caused by human activity haveamplified the role of diseases as regulating factors in spe-cies’ survival. These changes include the conversion ofwildlife habitat for human use, resulting in habitat lossand fragmentation, macro- and microclimate changes,and environmental contamination.

Fragmentation of ecosystems has a variety of implica-tions related to disease and has generated particular in-terest from island biogeographers and wildlife diseaseresearchers. Fragmentation of ecosystems can result inhuman-made “island ecosystems” that have been com-pared to geographical islands, functioning to isolate pop-ulations of species geographically and to confine themto smaller areas. Much has been written about island ex-tinctions associated with human introduction of infec-tious and parasitic diseases (Van Riper et al. 1986; Dob-son 1988; Quammen 1996).

Even though the biological diversity of islands is asmall percentage of the world’s total, of the recordednumber of invertebrate and vertebrate extinctions thathave occurred since the 1600s, 367 have been islandspecies and only 124 continental species (Smith et al.1993). Extinction may also be the fate of many wildlifespecies located within newly created “artificial islands.”African wild dogs (

Lycaon pictus

) represent one well-known example of isolated populations now teeteringon the brink of extinction, for which conservation ef-forts have been hampered severely by disease (Alex-ander & Appel 1994; Kat et al. 1996). Protected areasthat are intentionally isolated by fencing, as was true inKruger National Park, South Africa, or inadvertently iso-lated by human population growth and activities, suchas the intense agriculture one finds in Virunga NationalPark, Rwanda, and south Florida, United States, are alsoexamples of “island” ecosystems. In all these areas dis-eases have a significant effect on the survival of wildlifepopulations within their boundaries (Maehr et al. 1991;Keet et al. 1996; Mudakikwa et al. 1998; Sleeman 1998).

One result of land degradation and fragmentation isthe increased opportunity for contact among humans,domestic animals, and wildlife. This increased proximity



1227

may result in increased transmission of diseases betweenthese groups, including zoonotic and anthropozoonoticdiseases (Morell 1995; Wolfe et al. 1998; Gao et al. 1999;Wallis & Lee 1999). The intentional practice of “multi-species land use” and buffer zones in which domesticanimals graze the same lands as wildlife may facilitatethe transmission of disease between these two groups (Pas-toret et al. 1988; Plowright 1988

a

; Foreyt 1990; Roelke-Parker et al. 1996; Karesh et al. 1998).

Other environmental changes related to human activ-ity, such as climate change and pollution, have been im-plicated in infectious disease states in both human andanimal populations, but the long-term implications ofthese findings for conservation have only begun to beexplored. For instance, we know that global climatechanges, such as warming trends and rainfall patterns,can influence the epidemiology of various infectious dis-eases (Harvell et al. 1999). This realization has also oc-curred among conservationists concerned with long-termspecies survival in reserves affected by these anthropo-genic climatic changes (Peters & Darling 1985).

Air and water pollution are also linked to various non-infectious diseases. Large-scale pollution events such asoil spills are obviously detrimental to wildlife (Garrot etal. 1993), but long-term and low-level toxin exposuredue to pollution are now also being recognized as detri-mental (Colborn et al. 1996). Two areas of toxicologicresearch that have received a great deal of attention inrecent years are the negative effects of estrogenic agentsthat disrupt normal endocrine function (Colborn et al.1996; Yamamoto et al. 1996) and the negative effects ofPCBs on immunocompetence (O’Hara & Rice 1996). Foramphibians, a taxonomic group extremely sensitive toenvironmental changes, there are reports of deformitiesrelated to pesticide exposure (Ouellet et al. 1997 ). Lightand noise must be considered pollutants. For example,the effect of light pollution on the survival of hatchlingsea turtles is well documented (Peters & Verhoeven1994). Certain “new” epidemics of infectious diseasessuch as fibropapillomatosis (Herbst 1994) and chytridio-mycosis (Berger et al. 1998), and a number of marinemass mortality events (Heide-Jørgensen et al. 1992), arethought to be a direct or indirect result of environmentalpollution.

Wildlife Population Dynamics

The manipulation of wildlife, whether an individual or apopulation, can alter the dynamics of disease withinpopulations. Translocations, hunting, and live capturesfor commercial trade have direct and indirect effects onhealth. Alterations of host-pathogen interactions that re-sult from these human activities affect not only thehealth of targeted animals but also that of conspecificsand sympatric species.

Animal translocation

, as broadly defined by The WorldConservation Union (1987), is the movement of livingorganisms from one area for release in another. Thus,translocation encompasses introduction, reintroduction,and restocking. Many examples exist in which animaltranslocations resulted in serious wildlife disease prob-lems (Fischman et al. 1992; Jessup 1993; Meltzer 1993;Woodford & Rossiter 1993; Davidson et al. 1996). Suchproblems typically fall into the following three catego-ries: diseases brought by a subclinical (nonsymptomatic)host to a new region (Office International des Epizooties1987), disease vectors introduced to new geographic lo-cations (Curasson 1943), and diseases encountered bytranslocated animals (naïve to such diseases) after beingmoved to a new region (Pandey et al. 1992). Examplesof species experiencing disease problems caused by therelease of captive-bred animals among free-ranging pop-ulations include golden lion tamarins (

Leontopithecusrosalia

) in Brazil (May & Lyles 1987), white-tailed deer(

Odocoileus

virginianus

) in North America (Davidsonet al. 1996), and Arabian oryx (

Oryx leucoryx

) in SaudiArabia (Kock & Woodford 1988; Bush et al. 1993). Simi-lar threats to wild populations have been documentedwith the reintroduction of confiscated tortoises and or-angutans that may have acquired an infectious diseasewhile in captivity from either captive animals ( Jacobsonet al. 1995) or from humans (Warren et al. 1998), re-spectively.

Although dismissed as being insignificant and uncom-monly used by many in the conservation sciences, translo-cations of animals have increased substantially in thepast several decades (Griffith et al. 1993), with over a mil-lion live animals moved and released as of the early 1990s(Davidson & Nettles 1992). In practice, much of wildlifemanagement still depends heavily on such strategies.

Illegal and legal hunting for sport and bush meat andcapture of wild animals for the pet trade must be consid-ered if we are to know the true scale and frequency ofanimal movements that fall outside the normal geo-graphic or behavioral scope of a given species. Remov-ing individuals from populations and transporting theirlive or dead bodies (including all the pathogens and par-asites they carry) to new areas have enormous potentialfor affecting the health of wild and domestic animal pop-ulations (described for infectious agents of canids in thesoutheastern United States [Davidson et al. 1992] and forrinderpest of ungulates in Africa [Plowright 1982]). Inthe case of trophy hunting, there is also an effect on thehealth of the source population in that the healthiestand potentially most disease-resistant individuals oftenare removed from populations already under pressure.In developing countries, endangered species are fre-quently confiscated and end up in the care of foreign na-tional biologists or rehabilitators who lack the resourcesto screen for disease before release. Thus, many animalsare returned to the wild only to expose their conspecifics

1228



to novel diseases picked up during rehabilitation (Karesh1995). In our experience, this type of “underground trans-location” is common.

Disease Ecology

Ongoing anthropogenic modifications of the environ-ment, including changes that increase interspecies con-tact and confine individual populations, the translocationof susceptible hosts to regions with novel pathogens,and the introduction of novel pathogens to susceptiblehosts in a new region, are responsible in many instancesfor a change in disease ecology (Wilson 2000). One ex-ample of a shift in disease ecology is the loss of endemicstability. An endemically stable disease is one in which theagent, vector (in vector-borne diseases), host, and envi-ronment coexist in a manner that results in the virtualabsence of clinical disease (Norval et al. 1992). In manyregions of the world, diseases of domestic animals thatwere once endemically stable, such as heartwater (Deemet al. 1996) and theileriosis (Moll et al. 1984), are nowunstable due to anthropogenic changes. This change, toeither an endemically unstable or an epidemic state,could happen in wildlife populations but is not as welldocumented for them due to a lack of information onthose diseases historically endemically stable in wild-ani-mal populations.

Several factors influence the spread and perpetuationof a contagious agent once it has been introduced into ahost population: the density of susceptible hosts, the fre-quency of host contact, the infectiousness and pathoge-nicity of the disease, and the average time an infectedhost is infectious (Anderson & May 1979

a

, 1979

b

). Thesefour factors are profoundly affected by global changes inlandscapes and wildlife dynamics.

Suggestions for Integrating Animal Healthinto Conservation

Although the role of disease in species conservation hasbeen appreciated for years, it has only been in the re-cent past that health and disease issues have come to theforefront of conservation biology as limiting factors inwildlife conservation (Meffe 1999; Daszak et al. 2000;Osofsky et al. 2000). Unfortunately, although many con-servation biologists are interested in including questionsand concerns about disease in their study design or sam-pling methods, there is a misconception that the onlyreason to work with veterinary wildlife professionals isto have them immobilize study animals. Although theveterinary profession has been instrumental in improv-ing the safety and efficiency of animal handling proce-dures (Osofsky & Hirsch 2000), other pressing issuesmandate collaboration between conservation biologistsand wildlife health professionals. Thus, we present some

practical steps to foster such collaboration. We base oursuggestions not only on the literature but also on a de-cade of experience in integrating wildlife health con-cerns into field biology and conservation efforts. We rec-ommend only those approaches of highest priority and/or those we have found most cost effective.

Veterinary Involvement in Conservation Projects

The use of veterinary skills in the form of either preven-tion or treatment is probably the most controversial is-sue surrounding the role of animal health in conserva-tion efforts (Macfie 1992; Gascoyne et al. 1993; Inserro1997). Many conservation biologists insist that “humanintervention” in the form of veterinary services shouldnot be provided in any way for wild animals becausesuch action would interfere with evolutionary pro-cesses. But there are probably few species that have notbeen influenced by some form of “human intervention”(Redford & Richter 1999). Even the simple act of con-ducting field research in an “untouched” area effectschange. Other people may object to veterinary involve-ment because of the potential risk of doing more harmthan good. This concern can easily be addressed by in-volving experienced, qualified health professionals indecision making and procedures. We further recom-mend that the same standards be applied to the evalua-tion of risk of disease transmission or environmental con-tamination resulting from field research not related toanimal health. Rather than debate whether interventionis good or bad, it would be more sensible to determinethe most appropriate prevention and treatment optionsfor wildlife populations on a case-by-case basis. Appro-priate strategies for the prevention or treatment of wild-life diseases might range from public and staff health-education and vaccination programs to intensive diseasemanagement. Examples of intensive management in-clude the black-footed ferret (

Mustela nigripes

; Thorne &Williams 1988) and African wild dog (Gascoyne et al.1993) conservation programs and control of waterfowldisease epidemics (Pearson & Cassidy 1997). Aside fromethical considerations, which vary widely among differ-ent groups of humans, decisions about the level of veter-inary involvement in a project should be based on (1)the status of the species or populations affected or atrisk; (2) the nature of the cause of the health problem,which requires veterinary investigation; (3) the spatialdistribution of the species; (4) the costs and practicalityof necessary preventive and treatment measures; (5)specific disease issues of concern; and (6) implicationsof intervention or lack thereof on the health of otherspecies, including humans and domestic animals.

We stress that preventing the introduction of newhealth problems, as opposed to intervening once a situa-tion has already reached the crisis point, can and shouldbe a bigger part of what we do as conservation biolo-



1229

gists. When and whether preventive measures and crisisintervention are needed to limit wildlife health problemsdepend on so many variables in each locale that exper-tise in wildlife health should be aggressively cultivatedfor more effective future conservation programs.

Applied Veterinary Medicine and Research in Conservation

HEALTH

ASSESSMENT

AND

MONITORING

Veterinarians perform health surveys or assessments andlong-term health monitoring that provide critically neededbaseline information on species of interest. In contrastto our knowledge of humans and domestic animals, fewdata sets exist to establish the “normal” or expectedrange of values for most of the world’s threatened or en-dangered wild species. These data sets should includeblood parameters such as complete blood count, serumbiochemistry profiles, vitamin and mineral levels, evi-dence of exposure to infectious agents such as antibod-ies or microbes, and residues of chemical contaminants.Health assessment and monitoring programs integratedinto field biology projects have been described (Kareshet al. 1997

a

; Karesh et al. 1997

b

; 1997

c

).Baseline data on population health should be used in

population viability analysis because the viability of apopulation is inseparable from its health (Karesh &Cook 1995). These data can be used in comparisons withthe same population at a future date to determine the ef-fects of various disturbances (i.e., ecotourism, weatherextremes, habitat loss) and for comparison with differ-ent populations. Such comparisons are valuable in deter-mining the appropriateness of various conservationmanagement techniques for individual populations orspecies. Just as mammal, bird, or reptile surveys allowone to quantify population trends, documenting changesin prevalence or exposure to infectious and toxic agentsprovides objective data for management action. Changesnoted in these parameters, before and after an event (allelse being equal), would confirm that the event had aninfluence on the health of the population and thus couldthreaten long-term survival. Events that might be ex-pected to influence the health status of free-rangingwildlife include disease transmission from domestic ani-mals in the region; exposure to industrial, agricultural,and urban pollution; tourism; and disease transmissionbetween wildlife species. Identification of infectious dis-ease threats or the presence of toxic agents would in-form decisions about zoning and the use of terrestrialand aquatic areas and could mobilize local and interna-tional support for conservation efforts.

HEALTH

STUDIES

OF

ZOONOTIC

,

ANTHROPOZOONOTIC

,

AND

INTERSPECIES

TRANSMISSION

OF

DISEASES

Health assessment and monitoring programs should fo-cus more on zoonotic diseases, which are transmitted

from animals to humans; anthropozoonotic diseases,which are transmitted from humans to animals, andother forms of interspecies disease transmission such asvertebrate-to-vertebrate and vector-borne diseases. Theconservation of wildlife species is greatly complicatedby these possible disease transmission routes, and theymust be addressed to minimize potentially devastatingresults for wildlife, humans, and domestic animals.

There have been many reports of disease epidemics inboth nonhuman (anthropozoonotic) and human (zoo-notic) primates (Kalema et al. 1998; Mudakikwa et al.1998; Wolfe et al. 1998; Gao et al. 1999; Wallis & Lee1999). These epidemics are suspected of being causedby the direct and indirect contact of one group with an-other. Activities such as behavioral research or tourism,although well intentioned, can serve to introduce newdiseases to wild populations (Wallis & Lee 1999).

As humans encroach on lands inhabited by nonhumanprimates, increase the use of nonhuman primates as asource of protein, and continue to collect nonhumanprimates for trade as pets, the incidence of these epi-demics surely will increase. An understanding of the epi-demiology of these diseases through field studies is nec-essary to ensure that conservation projects guaranteethe survival of nonhuman primate species without risk-ing the health of humans.

Diseases transmitted among livestock, other domesticanimals, and wildlife are also of great concern (Pastoretet al. 1988; Roelke-Parker et al. 1996; Deem 1998; Kareshet al. 1998). As grazing lands designated for livestockcontinue to expand into regions where wildlife exist,the opportunity for epidemics in both livestock andwildlife populations increases. Policies to limit the useof land for livestock are routinely unacceptable to gov-ernments and local peoples. It is therefore imperativethat we collect data to gain insight on the epidemiologyof these diseases in both livestock and wildlife hosts sothat conservation projects can be developed to ensurethe survival of wildlife species and the health of domes-tic livestock. The same concerns are associated with thepossible transmission of disease between wild and otherdomestic animals (e.g., dogs and cats) as increased con-tact occurs between these two groups (Blouin et al.1984; Kariuki 1988; Roelke-Parker et al. 1996). Research-ers, protected-area managers and staff, and tour opera-tors need to be aware that their presence, along withthat of their domestic pets and food animals, increasethe risk of introducing diseases to wildlife populations(Karesh et al. 1997

b

; Wallis & Lee 1999).

TRAINING

Worldwide, wildlife-agency workers, veterinarians, andconservation biologists must be trained to design andconduct wildlife studies that incorporate crucial healthconsiderations. Training should cover how to conduct

1230



research on wildlife safely, humanely, and in a mannerconsistent with conservation goals, and should providepractical information on the ecology of diseases. Wemust raise awareness among professionals in other disci-plines and within local communities. Everyone, from bi-ologists to policymakers to cattle ranchers, should bewelcome to participate in organized workshops andother outreach programs that inform them about theirrelationships to and effects on the health of wildlife. AsOsofsky (1997) says, “think link.”

INTERDISCIPLINARY

COLLABORATION

Interdisciplinary collaboration should be directed at stud-ies that shed light on the effects of pathogens and toxicchemicals on the persistence of wildlife populations.These studies often involve the investigation of relation-ships among disturbed habitats and the health of wild-life, domesticated animals, and human beings. This re-quires collaboration between livestock and wildlifeveterinarians, physicians, and other workers in basic andapplied biomedical research, as well as epidemiologists,conservation biologists, and ecologists. Some conserva-tion biologists object to such collaboration, fearing thatinformation on the diseases of wildlife will be miscon-strued by the human medical community and politi-cians, resulting in the persecution of wildlife as diseasecarriers. This objection is based on suspicion and willnot help protect wildlife. Whether or not veterinariansand conservation biologists choose to contribute theiropinions and professional expertise to the human medi-cal community, research directed at public health willcontinue. It is therefore imperative that veterinariansand conservation biologists take every opportunity toprovide input to ensure that research is conducted in amanner consistent with a conservation ethic and thatfindings are interpreted with conservation goals in mind.

DATA

COLLECTION

AND

MANAGEMENT

The community of people working on aspects of wild-life health as related to conservation is growing and willcontinue to grow as awareness of the effects of diseaseincreases. It is important that we create software and da-tabases that can make wildlife health information easy torecord, disseminate, share, and interpret. Although a va-riety of programs exist for experimenting with theoreti-cal epidemiological models, only recently have a few ef-forts been directed at standardizing and tracking currentinformation collected on wildlife die-offs or at mappingthese data.

Along similar lines, biologists, ecologists, veterinari-ans, and medical researchers need to coordinate their ef-forts better to capitalize on all opportunities for gather-ing information. Procedures for animal handling and/orsample collection should not be designed exclusively to

serve one’s special research interest. Simple guidelinescan be followed that will allow samples to be collectedfor gathering a variety of health-related information si-multaneously. For example, death should not representwaste in the context of conservation-oriented studies.Necropsies could be conducted on every animal founddead, which could provide critically needed informationand would require only training in proper sample han-dling and human safety precautions.

DIAGNOSTIC

CAPABILITIES

Better diagnostic capabilities are needed to identify thewide range of pathogens that are presently and will in-creasingly be found in wildlife. Identification of expo-sure to infectious diseases is often limited by the avail-ability of tests developed for domestic animals and humans.For example, sensitive and specific antemortem diagnos-tic tests for tuberculosis are not currently available forwildlife species. Finding antibodies to morbillivirus insouthern elephant seals (

Mirounga leonine

) using avail-able tests developed for canine and phocid morbillivi-ruses does not identify the virus that caused the immuneresponse in the seals (Karesh et al. 1997

d

). Diagnosticcapabilities need to be developed to identify diseaseagents in wildlife. Although genetic and toxicology testshave advanced, there is still a need to refine and im-prove these techniques.

POLICY

The importance of integrating health issues, as one com-ponent of conservation, into policy development cannotbe overemphasized. For instance, we must recognizethreats to the health of wildlife posed by conservationand development strategies involving ecotourism, im-provements in livestock production, and wildlife har-vesting programs. Tourists and the food needed to sup-port them may transport infectious organisms (Kareshet al. 1997

c

). Unvaccinated domestic animals may becarriers of infectious diseases. In the case of wildlife har-vesting, a frequently overlooked health threat is thetracker or lure animals (e.g., dogs and parrots) used byhunters, which may transmit diseases to free-rangingwildlife. These situations underscore the importance ofconsidering health implications when establishing poli-cies and initiating new programs. Finally, theoreticallysustainable harvesting models based on recruitment andharvest rates must take into account the effects of healthand disease on sexual maturation, reproductive success,and longevity. These effects may vary from year to year,depending on factors such as host and sympatric speciesdensities, vector abundance, environmental conditions,and agent pathogenicity.

We have used four policy-related strategies to preventwildlife disease problems: (1) to inform and educateworkers in funding agencies of the important relation-



1231

ships among the health of ecosystems, wildlife, domes-tic animals, and humans; (2) to offer input into planningconservation or development projects that involve themanagement or manipulation of wildlife or domestic an-imals; (3) to analyze data on wildlife health and diseaserisks and integrate it into the creation of buffer zones,multiple land-use zones, and corridors; and (4) to sup-port stringent regulations and guidelines on wildlife re-habilitation, reintroduction, and translocation to preventthe introduction of novel pathogens to wild popula-tions.

Conclusion

The effects of disease on wildlife populations have beenrecognized for years. It is also clear that Earth’s wild placeshave become smaller and more artificial in the past cen-tury, leading to a greater potential for infectious andnoninfectious diseases to adversely affect conservationefforts. As a result, viable conservation initiatives can nolonger be designed without addressing the health issuesof wildlife. Considering that human intervention in wild-life populations occurs daily all over the world, in mostlynegative ways (i.e., human expansion into previouslyuninhabited regions, poaching, and the collection andmovement of animals internationally), it is no longerpossible or ethical to justify a “hands-off” approach whenconfronted with wildlife disease issues in a conservationcontext. Instead, the expertise of all relevant disciplines,including that of health specialists, should be employedin developing better management for wildlife and eco-systems. We have presented specific suggestions for in-tegrating wildlife health into conservation efforts, andwe have emphasized that although veterinarians andother health professionals have an obvious role to playin protecting the health of wildlife, conservation work-ers in every discipline have the ability and responsibilityto help address this issue. With minimal additional effortand cost, conservation researchers can maximize thedata collected for monitoring wildlife health, can keepin mind potential disease issues in their studies, and cantake a precautionary approach to preventing transmis-sion of diseases in research, conservation, and develop-ment activities. We hope our suggestions will stimulateinnovative collaborations in the field and in the policyarena and raise awareness of the need for a new para-digm that integrates considerations of wildlife healthand disease into mainstream conservation.

Acknowledgments

We thank K. Redford, J. Robinson, R. Cook, and the re-viewers and editors of

Conservation Biology

for theirvaluable input.

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Putting Theory into Practice: Wildlife Health in Conservation