The role of infectious diseases in biological conservation

Abstract

Recent increases in the magnitude and rate of environmental change, including habitat loss, climate change and overexploitation, have been directly linked to the global loss of biodiversity. Wildlife extinction rates are estimated to be 100–1000 times greater than the historical norm, and up to 50% of higher taxonomic groups are critically endangered. While many types of environmental changes threaten the survival of species all over the planet, infectious disease has rarely been cited as the primary cause of global species extinctions. There is substantial evidence, however, that diseases can greatly impact local species populations by causing temporary or permanent declines in abundance. More importantly, pathogens can interact with other driving factors, such as habitat loss, climate change, overexploitation, invasive species and environmental pollution to contribute to local and global extinctions. Regrettably, our current lack of knowledge about the diversity and abundance of pathogens in natural systems has made it difficult to establish the relative importance of disease as a significant driver of species extinction, and the context when this is most likely to occur. Here, we review the role of infectious diseases in biological conservation. We summarize existing knowledge of disease-induced extinction at global and local scales and review the ecological and evolutionary forces that may facilitate disease-mediated extinction risk. We suggest that while disease alone may currently threaten few species, pathogens may be a significant threat to already-endangered species, especially when disease interacts with other drivers. We identify control strategies that may help reduce the negative effects of disease on wildlife and discuss the most critical challenges and future directions for the study of infectious diseases in the conservation sciences.

Full text

REVIEW
The role of infectious diseases in biological conservation
K. F. Smith
1,2

, K. Acevedo-Whitehouse
3

& A. B. Pedersen
4

1 Brown University, Ecology and Evolutionary Biology, Providence, RI, USA
2 The Consortium for Conservation Medicine at Wildlife Trust, New York, NY, USA
3 Wildlife Epidemiology, Institute of Zoology, London, UK
4 Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK
Keywords
conservation; extinction; biodiversity;
environmental change; pathogens; disease;
wildlife.
Correspondence
Katherine F. Smith, Brown University,
Ecology and Evolutionary Biology,
Providence, RI 02912, USA.
Email: katherine_smith@brown.edu

All authors contributed equally.
Received 1 May 2008; accepted 21
November 2008
doi:10.1111/j.1469-1795.2008.00228.x
Abstract
Recent increases in the magnitude and rate of environmental change, including
habitat loss, climate change and overexploitation, have been directly linked to the
global loss of biodiversity. Wildlife extinction rates are estimated to be 100–1000
times greater than the historical norm, and up to 50% of higher taxonomic groups
are critically endangered. While many types of environmental changes threaten the
survival of species all over the planet, infectious disease has rarely been cited as the
primary cause of global species extinctions. There is substantial evidence, however,
that diseases can greatly impact local species populations by causing temporary or
permanent declines in abundance. More importantly, pathogens can interact with
other driving factors, such as habitat loss, climate change, overexploitation,
invasive species and environmental pollution to contribute to local and global
extinctions. Regrettably, our current lack of knowledge about the diversity and
abundance of pathogens in natural systems has made it difficult to establish the
relative importance of disease as a significant driver of species extinction, and the
context when this is most likely to occur. Here, we review the role of infectious
diseases in biological conservation. We summarize existing knowledge of disease-
induced extinction at global and local scales and review the ecological and
evolutionary forces that may facilitate disease-mediated extinction risk. We
suggest that while disease alone may currently threaten few species, pathogens
may be a significant threat to already-endangered species, especially when disease
interacts with other drivers. We identify control strategies that may help reduce the
negative effects of disease on wildlife and discuss the most critical challenges and
future directions for the study of infectious diseases in the conservation sciences.
Introduction
At the advent of a century characterized by dramatic
environmental changes, the global community is challenged
to reconcile the stresses such changes place on the planet’s
resources (Committee on Grand Challenges in Environmen-
tal Sciences, 2001). Of increasing importance is the need to
fully understand the drivers of species extinction, as loss of
biodiversity has the potential to alter the ecosystem services
on which humans and wildlife depend. The current extinc-
tion rate is already estimated to be 100–1000 times greater
than the historical norm (Pimm et al., 1995), and 10–50% of
well-studied higher taxonomic groups are at high risk of
extinction [Millenium Ecosystem Assessment (MEA), 2005].
The threats to biodiversity are numerous and largely result
from anthropogenic changes to the environment, including
habitat loss, climate change, non-native species invasion and
overexploitation (Pimm et al., 1995; Wilcove et al., 1998).
Here, we review an additional threat to biological conserva-
tion that is critical to consider – infectious disease.
A large number of infectious diseases have recently
emerged in wildlife or humans around the world (Daszak,
Cunningham & Hyatt, 2000; Jones et al., 2007a). In wildlife,
some of the more pressing examples include marine mam-
mal morbillivirus (Osterhaus et al., 1989), increased fre-
quency of disease outbreaks in coral reefs (Harvell et al.,
2002), a chytridiomycosis pandemic in amphibians (Daszak
et al., 1999; Schloegel et al., 2006) and the rapid spread of
infectious facial tumors in Tasmanian devils (Jones et al.,
2007b). The diversity and apparent increase in these and
other diseases in wildlife have raised concerns that patho-
gens may pose a substantial threat to biodiversity (Wilcove
et al., 1998; Daszak et al., 2000; Harvell et al., 2002).
However, infectious disease has not traditionally been
regarded as a significant driver of species extinction (Smith,
Sax & Lafferty, 2006). In part, this may be due to a lack of
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 1
Animal Conservation. Print ISSN 1367-9430

adequate historical information on pathogens and to levels
of uncertainty in existing data (see Smith et al., 2006) that
make it difficult to gain a reliable understanding of the role
infectious disease plays in species extinction.
In this review on the role of infectious diseases in
biological conservation, we seek to accomplish four objec-
tives. First, to summarize existing knowledge on the impor-
tance of disease in local and global species extinctions.
Second, to review the ecological and evolutionary forces
that facilitate disease-mediated extinction risk. Third, to
identify science-backed control strategies that may signifi-
cantly reduce the negative effects of disease on wildlife.
Fourth, to consider the most critical challenges and future
directions for the study of infectious diseases in the con-
servation sciences. We use the term ‘pathogen’ to include
both microparasitic and macroparasitic pathogens, and
‘infectious disease’ to represent disease syndromes which
are caused by a contagious pathogen.
Infectious disease and wildlife
extinction
The International Union for the Conservation of Nature
(IUCN, 2004) Red List reports that in the past 500 years,
833 animal species are known to have gone extinct. Of these
known extinctions, only 3.7% have been attributed, at least
partly, to infectious disease (Smith et al., 2006; Table 1).
These include numerous Hawaiian birds, the thylacine
Thylacinus cynocephalus, a Polynesian tree snail Partula
turgida and the sharp-snouted day frog Taudactylus acutir-
ostris (Schloegel et al., 2006; Smith et al., 2006). Whereas
forces such as habitat loss or overexploitation are often
listed as the single and most common causal driver of
species’ extinction (IUCN, 2004), infectious disease is sig-
nificantly less likely than other drivers to act in isolation
(Smith et al., 2006). These patterns also appear to hold for
species on the verge of extinction. Of the 2852 plants and
animals listed as critically endangered, only 8% are threa-
tened by infectious disease (Smith et al., 2006). Over 24% of
the world’s extant mammals are currently threatened with
extinction, yet infectious disease has only been listed as a
major threat for a small fraction (1.1%) (IUCN, 2007). It is
likely that disease is underrepresented as a contributing
threat to wildlife extinction, especially given that less than
half (39%) of critically endangered and endangered artio-
dactyls, carnivores and primates from the 2006 IUCN Red
List have any published records of pathogens from wild
populations (Pedersen et al., 2007). While the IUCN repre-
sents the best available evidence on the factors threatening
species with extinction, it is not without limitations. Parti-
cularly the level of uncertainty about the actual threat of
infectious disease and a temporal bias in the collection of
data may affect the results (but see Smith et al., 2006).
Mathematical models and epidemiological theory have
been increasingly used to understand the population impact
of infectious diseases (Anderson & May, 1992). Within this
basic epidemiological framework, pathogens are not pre-
dicted to drive their hosts to extinction when their transmis-
sion is density-dependent (i.e. likelihood of transmission
increases with increasing host density). These models sug-
gest that pathogens will be lost before the host population
goes extinct, because they will drive their hosts below a
density threshold that is critical for disease persistence.
Under these circumstances, pathogens suffer from local
extinction or ‘fade-outs’ (McCallum, Barlow & Hone,
2001). There are several cases, however, where pathogens
are more likely to cause extinction (see de Castro & Bolker,
2005).
First, pathogens that negatively affect host fitness can
decrease host population density by causing a population
crash after a recent epidemic or at the trough of a pathogen-
driven population cycle. Small, fragmented populations can
have increased extinction risk due to decreases in genetic
variability which may also increase susceptibility to infec-
tious diseases (Lyles & Dobson, 1993), and increased like-
lihood of stochastic events (McCallum & Dobson, 1995).
Second, many pathogens are transmitted as a function of
the frequency of infected individuals and therefore are not
subject to population density thresholds. Sexually trans-
mitted diseases and vector-borne pathogens are commonly
frequency-dependent, and their prevalence can increase even
when population densities are low, therefore being more
likely to cause host extinction (Thrall, Antonovics & Hall,
1993; Boots & Sasaki, 2003). In addition, when host popula-
tions are spatially structured by territoriality or social
interactions, or when pathogens cause sterility, as opposed
to reductions in survival, transmission may approximate a
frequency-dependent model (O’Keefe & Antonovics, 2002).
Third, disease-mediated extinction becomes more likely
when pathogens have reservoir hosts where they can remain
viable, and when the pathogen dynamics become disen-
tangled from the specific one host–one pathogen dynamics
(i.e. a reservoir host serves as the source for pathogen
epidemics that would fade out in another host).
Lastly, when dispersal rates among small populations (in
which a pathogen would normally fade out) are artificially
high, due to anthropogenic translocation events, pathogens
may also represent an important threat to species persis-
tence. Most pathogens can infect multiple hosts and these
generalist pathogens pose the greatest threat to disease-
mediated extinction (Pedersen et al., 2007), because high
prevalence in alternate hosts, coupled with cross species
transmission, can increase the likelihood of disease persis-
tence and host extinction (Fenton & Pedersen, 2005).
Drivers of disease-mediated
extinction
There is concern that the extent of environmental changes in
recent decades is increasing the odds of infectious disease
emergence in both humans and wildlife. Today, 436 species
are threatened by global environmental change (IUCN,
2007). Environmental change is likely to influence disease
emergence as a result of both effects on host and pathogen
physiology, and of indirect effects following changes in
interactions with other species (Lips et al., 2008). Many
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emerging infectious diseases are driven by human activities
that force novel pathogens into new ecological niches or
modify the environment to facilitate their establishment or
transmission – an outcome termed ‘pathogen pollution’
(Cunningham, Daszak & Rodr ´
ıguez, 2003; MEA, 2005).
Examples of anthropogenic drivers that promote disease
emergence are numerous and include habitat loss, climate
change, non-native species introductions, overexploitation
and pollution (Daszak et al., 2000; Lafferty, 2003; MEA,
2005). Here, we review how these human-induced drivers of
disturbance can lead to specific changes in the environment
that may also facilitate disease-mediated extinction via
mechanisms that are directly linked to the biology of
pathogens.
Habitat loss and alteration
Habitat loss and alteration is commonly cited as the primary
factor driving the loss of biodiversity worldwide (Wilson,
1992). The rate at which habitats are degraded or changed
into unsuitable environments accurately predicts the rate of
species loss and the proportion of threatened species in that
area (Pimm & Askins, 1995). At the turn of the century,
85% of endangered species in the United States were
threatened by habitat loss, mostly related to agricultural,
commercial, infrastructural development and outdoor activ-
ities (Wilcove et al., 1998).
Endangered species at greatest risk of habitat loss are
those that have small geographic ranges and patchy distri-
butions within their ranges (Gaston, 1991). The importance
of infectious disease to the conservation of species threa-
tened with habitat loss will likely increase with decreasing
habitat size and quality. Infectious diseases can be impor-
tant for fragmented populations because habitat loss will
often restrict species movement and dispersal, likely increas-
ing contact rates among individuals and ultimately the
spread of disease (Scott, 1988). While several studies have
demonstrated that density-dependent pathogens are likely
to be lost in small populations, this may be limited to host-
specific pathogens, while multi-host pathogens, which can
be maintained by other host species, may not be affected by
a reduction in the population size of one host. In addition to
increasing transmission and thus prevalence, limited host
movement and dispersal in fragmented habitats may be
important for the maintenance of genetic diversity and the
persistence of resistance alleles (Altizer & Pedersen, 2008).
For example, bighorn sheep populations have suffered from
highly fragmented landscapes that reduce local population
sizes, and in these herds, infectious disease epidemics are
most likely to cause extinction (Flather, Joyce & Bloom-
harde, 1994). The largest population of bighorn sheep in
New Mexico (4200 individuals in 1978) was reduced to 25
individuals by 1989, and then to a single ewe by 1997 due to
a severe epidemic of psoroptic scabies, drought and preda-
tion (Boyce & Weisenberger, 2005). However, species recov-
ery efforts have demonstrated that maintaining larger
population sizes and increased dispersal rates between big-
horn sheep populations are associated with faster recovery
rates from bronchopneumonial epidemics and lower local
extinction rates (Singer, Zeigenfuss & Spicer, 2001).
Climate change
During the twentieth century, average world surface tem-
perature increased by 0.6 1C and almost two-thirds of that
warming has occurred since 1975 [Intergovernmental Panel
on Climate Change (IPCC), 2007]. Climatologists forecast
further warming, along with changes in precipitation and
climatic variability, during the coming century and beyond
(IPCC, 2007). Such effects may be a major threat to living
organisms, affecting species directly or altering their habi-
tats.
Changes in regional or local climate may directly or
indirectly modify pathogen survival rates, transmission and
host susceptibility (Harvell et al., 2002). Shifts in contem-
porary climatic regimes also have the potential to influence
disease by shifting patterns of the abundance and distribu-
tion of pathogens and their vectors (Daszak et al., 2000).
Dengue fever and malaria are predicted to spread dramati-
cally in the face of global warming as high temperatures lead
to higher rates of pathogen reproduction and faster time to
maturity, increased geographic ranges and bite-frequency of
mosquito vectors (Epstein, 2000). A well-known case of
wildlife disease emergence that may be related, at least
partially, to environmental change is chytridiomycosis
(Box 1), a fungal infection caused by Batrachochytrium
dendrobatidis (Bd). The role of chytridiomycosis as a driver
of amphibian population declines has been linked to envir-
onmental change, a hypothesis known as the climate-linked
epidemic hypothesis (Pounds et al., 2006; Bosch et al., 2007),
which has found correlational evidence from empirical
studies that report a significant association between local
increases in temperature and rainfall, and the occurrence of
chytridiomycosis (e.g. Kriger, Pereoglou & Hero, 2007).
However, there is an ongoing debate about the strength of
the relationship between the emergence of chytridiomycosis
and climate change (Pounds et al., 2006, 2007; Alford,
Bradfield & Richards, 2007; Lips et al., 2008). Both amphi-
bians and Bd are strongly affected by temperature and
moisture, and there is widespread agreement that environ-
mental factors are indeed likely to influence their survival
and growth (Pounds et al., 2006, 2007; Alford et al., 2007;
Lips et al., 2008). To date, however, there is no direct
evidence that climate change causes outbreaks of chytridio-
mycosis (Lips et al., 2008).
Domestic–wildlife–human interface
Interactions between humans, domestic animals and wildlife
occur widely and can result in the spread of pathogens
between species. This interaction typically involves the
spread of microparasites with broad host ranges from
domestic to wild animals, and in many cases, these patho-
gens have substantial negative effects on host fitness that
lead to population declines and often dramatic conse-
quences for wildlife (Pedersen et al., 2007). Over 80% of
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domesticated animal pathogens can infect wildlife (Cleave-
land, Laurenson & Taylor, 2001). Given that pathogens are
more likely to be shared or jump between closely related
hosts (Davies & Pedersen, 2008), it is not surprising that
close relatives of domestic animals are at the greatest risk of
disease-mediated extinction. For instance, 88% of mammals
listed by IUCN as threatened by infectious disease belong to
two orders of mammals: carnivores and artiodactyls (Ped-
ersen et al., 2007), in particular, those species most closely
related to domestic animals. In contrast, no bats (0.0% of
1024) and only one rodent species (o0.01% of 2041) were
identified by the IUCN as threatened by pathogens. This
nonrandom distribution of extinction risk across mammals
suggests that relatedness to domestic animals may indeed
predispose disease-mediated extinction risk. However, the
pattern may also be affected by unequal sampling of patho-
gens across the mammalian families, with an inclination
toward artiodactyls because they are hunted and often easier
to sample for pathogens, or artiodactyls and carnivores
based on a preference by veterinarians due to their related-
ness to domestic animals.
Most of the pathogens identified as causing declines or
reduced fitness in IUCN-threatened mammals are well-
known diseases such as rinderpest, canine distemper, rabies,
anthrax and toxoplasmosis (Pedersen et al., 2007); all
microparasites with short generation times, high mutation
rates and broad host ranges (Cleaveland et al., 2001; Taylor,
Latham & Woolhouse, 2001). Furthermore, over 70% of the
viruses identified as agents of disease-mediated extinction
are ssRNA viruses (Pedersen et al., 2007), which have the
highest mutation rates (Domingo & Holland, 1997) and
possibly the greatest evolutionary potential for host switch-
ing. All threatening pathogens could infect multiple host
species, with the majority (66%) able to infect mammals
from several orders, and in some cases non-mammals. More
importantly nearly all (96%) of the threatening pathogens
were reported to infect domesticated carnivores or livestock.
Contrary to theoretical expectations, 75% of all pathogens
were transmitted by close contact between hosts, as opposed
to being stable in the environment or being transmitted by
vectors (Pedersen et al., 2007).
As domestic animals are globally distributed and main-
tained at high densities, they can easily act as reservoirs for
pathogens shared with wildlife (Lafferty & Gerber, 2002;
Pedersen et al., 2007). Spillover from domestic animals to
their wildlife relatives can have dramatic negative effects.
For example, spillovers of canine distemper virus have led to
massive declines in many wild carnivores (i.e. African
wild dog, bat-eared fox, spotted hyena and black-footed
ferrets; McCarthy, Shaw & Goodman, 2007) and continue
to be a conservation threat to these populations. Another
example is Sarcoptic mange (caused by Sarcoptes scabiei),
which is commonly transmitted by infected domesticated
animals, infects 104 species, and can cause high-mortality
epidemics in wildlife (Box 2). While more ecologically stable
species may recover from sarcoptic mange outbreaks and
return to pre-epidemic population sizes, hosts that are
threatened by other factors, or are already limited to small
population sizes can be pushed to extinction by mange
outbreaks (i.e. red foxes population on Borrnholm Island
in Denmark; Henriksen et al., 1993; Pence & Ueckermann,
2002).
Box 1. An infectious fungus and the global decline in amphibians
Over the last 30 years 43% of the world’s amphibian species (o1800) have undergone severe declines: 32.5% are globally threatened, 434
have gone extinct and many more are believed to be extinct (Blaustein & Wake, 1990; Stuart et al., 2004). 18.8% of Australia’s frog species are
currently threatened with extinction (Hero & Morrison, 2003), 67% of harlequin frogs (genus Atelopus) endemic to tropical America have
experienced extreme population declines in the past 20 years (IUCN, 2004), and rapidly declining species are commonly found throughout
Neotropical riparian habitats (Lips et al., 2006). It is widely believed that the recently discovered fungal pathogen, Batrachochytrium
dendrobatidis (Bd), is directly linked to declines and extinctions of amphibians worldwide (Berger et al., 1998; Daszak, Cunningham & Hyatt,
2003). Bd causes chytridiomycosis, an emerging infectious disease associated with declines in at least 43 amphibian species across Latin
America and 93 species worldwide (Berger et al., 1998; Daszak et al., 2003; Lips et al., 2006). Most recently, the fungus was directly linked to
the extinction of the Australian sharp-snouted day frog Taudactylus acutirostris – perhaps the first case of extinction of a free-ranging wildlife
species where disease acted as both the proximate and ultimate cause of extinction (Schloegel et al., 2006). Arguably, Bd is the most
significant infectious disease threat to species biodiversity at both local and global scales.
Researchers identified chytridiomycosis in 1998 (Berger et al., 1998) and many believe the international trade in amphibians has played a key
role in its now global distribution. The oldest-known hosts of Bd are African-clawed frogs (genus Xenopus) (Ouellet et al., 2005), first recorded
in South Africa in 1938. A worldwide trade of the species flourished in the 1950s following the development of pregnancy tests that used
Xenopus tissue, and museum records suggest the fungus had achieved a global distribution by the 1960s (Ouellet et al., 2005; Rachowicz
et al., 2005). Today, though different carrier species appear to be implicated, the spread of Bd through the global trade in wildlife continues.
Several studies document the presence of Bd in frogs farmed for the trade (Mazzoni et al., 2003; Hanselmann et al., 2004). The American
bullfrog Rana catesbiana, which is farmed and transported worldwide for consumption, poses a particular threat as it is resistant to
chytridiomycosis and acts as a carrier host (Mazzoni et al., 2003; Hanselmann et al., 2004). The diversity of human activities that facilitate the
spread of Bd, its extreme virulence, broad suite of potential hosts and ability to spread quickly (via direct contact between individuals as well as
through the environment where zoospores remain viable for up to 3 months) make chytridiomycosis an alarming reminder of how disease-
driven extinction can affect biodiversity at both local and global scales (Lips et al., 2006).
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Overexploitation
Overexploitation is a significant factor affecting the conser-
vation of species worldwide, specifically because areas with
high biodiversity often co-occur with populations of poor
and malnourished humans, who rely on wildlife (e.g. in the
form of bushmeat) for subsistence (Mainka, 2002). Exploi-
tation, or the use of species for food or body parts, is a
common cause of extinction risk in clades of bats, primates,
carnivores, ungulates and rabbits (Mace & Balmford, 2000).
Particularly, large-bodied and slow reproducing species are
at greatest risk of extinction from overexploitation (Purvis,
2001).
Bushmeat hunting has significantly depleted populations
of several species in Africa (Bassett, 2005). While bushmeat
hunting is most commonly associated with emerging infec-
tious diseases moving to humans (i.e. SIV, Ebola and STLV-
1; Nunn & Altizer, 2006), overexploitation of animals can
result in small, fragmented populations with high rates of
human contact and increased risk of disease-mediated
declines. Recently, 50% declines in chimpanzee and gorilla
populations have been documented in central Africa (Leroy
et al., 2004), and nearly half of a monitored population of
chimpanzees in Tai National Park Ivory Coast was deci-
mated during two Ebola epidemics in 1992 and 1994 (For-
menty et al., 1999). This latter population of chimpanzees
also suffered sudden deaths from Anthrax infection, raising
alarm over the vulnerability of even protected populations
to disease-mediated extinction.
While the overexploitation of species may increase their
likelihood of disease-mediated extinction in hunted species,
the global scale decline in ocean fisheries (Myers & Worm,
2003), and subsequent increase in aquaculture to compen-
sate for the demand for fish protein, may also pose a threat
to wild populations. This may be primarily due to the spread
of infectious diseases from farmed fish into natural popula-
tions. A recent study by Krkosek et al. (2007) found that
salmon lice Lepeophtheirus salmonis, commonly found on
farmed fish, are spreading to wild juvenile pink salmon as
they migrate past farms. Salmon lice, which feed on tissues
and impair osmotic ability, are usually found on adults
during the saltwater phase of their life cycle. However,
juvenile pink salmon passing fish farms were 73 times more
likely to be infected than those not passing fish farms, and
juvenile infections resulted in 9–95% mortality rates. At this
pace, it is believed that wild pink salmon populations will
plummet by 99% in British Columbia within four genera-
tions (Krkosek et al., 2007).
Invasive species
The success of introduced species has been attributed, in
part, to release from the pathogens that regulate their native
population, as these species may escape 475% of the
pathogens found in their native range (Torchin & Mitchell,
2004). The missing pathogens of introduced species can
result from a number of factors including a lack of adequate
host species for pathogens with complex life cycles, unin-
fected founder populations, or a threshold host density
below which a pathogen cannot persist (Torchin & Mitchell,
2004). However, the pathogens that do become established
with invasive species, while they may be few in number, have
the potential to seriously threaten native wildlife (Lyles &
Dobson, 1993; Smith & Carpenter, 2006). Consequently,
these novel pathogens can cause dramatic declines in local
populations of native species; altering community dynamics
and contracting geographic ranges (McCallum & Dobson,
1995; Daszak et al., 1999, 2000).
There are numerous pathways by which non-native
species can introduce pathogens to new regions, but one of
the largest appears to be the global trade in wildlife. The
scale of the global wildlife trade is extraordinary. Estimates
suggest many billions of live animals and products are
Box 2. Sarcoptic mange: a global epidemic with a wide host range
Sarcoptic mange, caused by the mite Sarcoptes scabei, has recently been indicated as the cause of countless mange epizootics that have
significantly affected wild mammals worldwide (Bornstein, Morner & Samuel, 2001; Pence & Ueckerman, 2002). Sarcoptes scabei is a highly
contagious mite that burrows into the epidermis of the skin, causing intense irritation in the host. The life cycle lasts about 2 weeks, and while
lightly infected individuals may only suffer short-term negative effects, mites on heavily infected individuals can reach densities of over
5000 mites cm
2
and can lead to death resulting from secondary infections, starvation and hypothermia (Bornstein et al., 2001).
It is likely that S. scabei originated in human populations and then spread to domesticated animals, which in turn, transmitted sarcoptic mange
to a diverse array of wild mammals (Fain, 1978). There is debate about the taxonomy of S. scabei, however, it has been suggested that
infections in both domestic and wild animals is caused by one highly variable species (Pence, Casto & Samuel, 1975), and infection can be
transmitted between species, even those that have limited or no direct contact (Stone et al., 1974). In fact, sarcoptic mange has been found in
over 104 species of domestic and wild mammals, including 10 orders and 27 families (Bornstein et al., 2001; Pence & Ueckerman, 2002). Even
more impressive than its wide host range, is the fact that severe sarcoptic mange epizootics have occurred in populations of wild carnivores
around the world (i.e. coyotes, foxes and grey wolves in North America; artic foxes, red foxes, lynx and grey wolves in Europe, foxes and
dingoes in Australia, lions and cheetahs in Africa), wild populations of artiodactyls (wild boars, chamois, ibex and Iberian ibex in Europe, impala,
hartebeest, wildebeest, buffalo, eland, kudu, Grant’s gazelle, Thompson’s gazelle and sable antelopes in Africa), wild primates in Africa (gorillas
and chimpanzees) and other mammals (wombats, koalas in Australia; reviewed in Pence & Ueckerman, 2002). Sarcoptic mange epidemics
cause significant population declines in wildlife (up to 50–90%, Pence & Ueckerman, 2002), and in species that are already threatened by other
factors, such as habitat loss or overexploitation, these crashes can cause local extirpation of populations. Because many of these epidemics
are seeded by cross-species transmission from domestic animals, limiting direct or close environmental contact between these groups, for
example by introducing barrier zones, may be a successful strategy for reducing future outbreaks and threat.
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traded globally each year, generating commodities totaling
in the hundred billions of dollars (Karesh et al., 2005).
International trade has facilitated the introduction of non-
native species to new regions where they compete with
native species for resources, alter ecosystem services, da-
mage infrastructure, destroy crops and introduce pathogens
that threaten public health, agricultural production and
biodiversity (Jenkins, Genovese & Ruffler, 2007). Box 1
illustrates how chytridiomycosis, one of the most deadly
contemporary infectious diseases of wildlife, may be spread-
ing globally through the wildlife trade, causing massive
amphibian population declines and extinctions. Shipments
of imported fish also pose a risk as they can carry novel
infectious agents that threaten native wildlife, particularly
when contaminated aquarium water, or infected animals are
dumped into natural systems (Smith et al. 2008). In Florida
alone, more than 95% of the emerging infectious agents in
native fishes were reported in recently imported fish ship-
ments (Sindermann, 1990). In the spring of 2003, monkey-
pox virus was introduced to the United States via a pet-trade
shipment of Africa rodents, including Gambian giant rats
Cricetomys gambianus. The rats were sold to a dealer who
housed the animals with a group of prairie dogs (native to
the United States) subsequently sold to private individuals.
Within months the virus infected both the prairie dogs and
their new owners (Centers for Disease Control, 2003).
The scope of wildlife trade is increasing and poor regula-
tion in many countries, including the United States, suggests
that future infectious diseases may be introduced through
imported animals. A recent report of US live animal imports
identified 302 non-native species regularly imported as
posing a potential ecological or economic risk to the nation.
Of these, 74 vertebrate species were determined to carry
harmful infectious agents that may spread to humans, native
wildlife or livestock if importation continues without in-
formed risk assessments (Jenkins et al., 2007). There is
growing concern that the continued shuffling of species
around the global will ultimately contribute to losses in
biological diversity by introducing novel infectious diseases
to susceptible, naı
¨ve, potentially high-risk populations.
Environmental pollution
Environmental accumulation of anthropogenic pollutants
has increased greatly in recent decades (Fairbrother, 1993;
Boon et al., 2002), and over 1500 animal species are
currently believed to be threatened by pollutants (IUCN,
2004). The majority of these are amphibians, with 696 Red
Listed species, nearly 20% of which are critically endan-
gered (IUCN, 2004). While the reliability of records on
historically cited causes of declines may be questioned (see
critique in Smith et al., 2006), there is growing evidence that
pollutants may pose a risk to wildlife because they can alter
the immune system. For instance, organochlorines are
known to decrease the efficiency of cellular and humoral
immunity in laboratory animals (Ahmed, 2000). Evidence of
similar effects in wildlife has been more difficult to establish,
partly because natural populations are exposed to complex
mixtures of persistent organic pollutants and our under-
standing of differences in species sensitivity to contaminants
is extremely limited (Raimondo, Mineau & Barron, 2007).
However, an increasing number of studies show that com-
mon environmental pollutants may impair the immune
system of a wide range of animal taxa (Selgrade, 2007).
Particular attention has been focused on marine mammals
that have experienced morbillivirus-related mortalities, and
several studies have shown a link between contaminant
concentrations and disease. Polychlorinated biphenyls and
other persistent organic pollutants have been associated
with immunotoxicity and disease outbreaks in marine mam-
mals by rendering them vulnerable to infection by patho-
gens, particularly viruses and bacteria (e.g. Hammond, Hall
& Dyrynda, 2005; Hall et al., 2006). Similar associations
have also been reported for amphibians and birds, where
exposure to metals, pesticides and herbicides was correlated
with decreased immunocompetence (Snoeijs et al., 2005;
Koprivnikar, Forbes & Baker, 2007), including resistance
to iridoviruses (Forson & Storfer, 2006), a group of the
pathogens implicated in amphibian mortality events (Das-
zak et al., 1999; Schloegel et al., 2006). Taken together, these
studies highlight the role that environmental contaminants
might play in rendering wildlife populations vulnerable to
disease. It is possible that sustained exposure to complex
contaminant mixtures may interact with other stressors (e.g.
climate change, habitat loss and invasive species, all dis-
cussed previously), resulting in wildlife with a reduced
ability to face infectious challenges and increasing their
chances of disease-mediated extinction.
The role of host genetics
In addition to anthropogenic drivers, disease emergence and
disease-induced extinction risk can be influenced by genetic
factors (see Spielman, Brook & Frankham, 2004), particu-
larly in terms of inbreeding (i.e. close-kin mating). At every
generation, genomes undergo new mutations, some of which
are harmful (Amos & Balmford, 2001), although generally
recessive, and thus expressed only when homozygous (re-
viewed in Charlesworth & Charlesworth, 1999). As inbred
offspring will have an increased proportion of homozygous
alleles, their recessive mutations are more likely to be
expressed. Furthermore, a higher proportion of homozy-
gous alleles in immune-related regions might hamper patho-
gen recognition (reviewed in Potts & Wakeland, 1993).
Several studies have associated inbreeding with lower
immunocompetence, higher pathogen loads, susceptibility
to infections and higher disease severity in wildlife (e.g.
Coltman et al., 1999; Reid, Arcese & Keller, 2003; Markert
et al., 2004), suggesting that inbred populations may be
more susceptible to disease. While of particular importance
for small or fragmented populations, where close-kin mat-
ings are more likely to occur, inbreeding could also be
relevant for large populations in which philopatry (tendency
of a migrating animal to return to a specific location) and
polygamous mating systems may increase the rate of in-
breeding by reducing the effective population size (Briton
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London6
Diseases in biological conservation K. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen

et al., 1994). For instance, sick California sea lions Zalophus
californianus were found to have relatively high inbreeding
levels, and were more prone to cancer and infections than
outbred individuals (Acevedo-Whitehouse et al., 2003,
2006), although their population is large and intercolony
migration ensures fairly high gene flow (Schramm Urrutia,
2002). This result is relevant for disease emergence, because
inbred individuals could act as sources of entry for ‘new’
pathogens into the population, or act as reservoirs for
immunologically naı
¨ve hosts. Some evidence for this has
been found by Valsecchi et al. (2004) in a study of Mediter-
ranean striped dolphins Stenella coeruleoalba stranded dur-
ing the 1990–1992 morbillivirus outbreak, where the first
dolphins affected by the disease were more inbred than those
that died during later stages of the epidemic, suggesting that
inbred dolphins facilitated transmission of the virus.
Genetic variation may also be relevant to disease-
mediated extinction. An example of this is the facial tumor
disease (DFTD) affecting Tasmanian devils Sarcophilus
harrisi since 1996 (McCallum & Jones, 2006). DFTD is a
contagious tumor spread between individuals, most likely
through biting and aggressive interactions. Low genetic
diversity due to an ancient genetic bottleneck of Tasmanian
devils followed by intense inbreeding, is the most likely
explanation of the high rate of DFTD spread (Siddle et al.,
2007). This, combined with frequency-dependent transmis-
sion, makes the disease an immediate threat to the survival
of the Tasmanian devil. DFTD has already caused popula-
tion declines up to 90% and is expected to drive the species
to extinction (Jones et al., 2007b).
As diversity at genetic regions involved with pathogen
recognition is generated and maintained over generations in
response to quickly evolving pathogens (Sommer, 2005;
Acevedo-Whitehouse & Cunningham, 2006), long-term
geographical restriction to specific pathogens may have
devastating effects for wildlife. Populations challenged by
novel pathogens will be immunologically naı
¨ve and thus,
less likely to recognize them. For example, the Spanish
invasion of the 1500s brought European diseases to the
Native American inhabitants (Settipane, 1995), who were
immunologically naı
¨ve and thus extremely susceptible to
their effects. Severe epidemics of smallpox, measles and
typhus caused drastic population declines, which together
with war and forced labor, caused the death of 60–80 million
people (up to 90% mortality rates for some ethnic groups;
Ayala, 1995). Similar events in immunologically naı
¨ve wild-
life populations could be devastating to their stability and
persistence. However, the relatively few published studies on
immunogenetic diversity of threatened populations, as well
as the limited evidence of their associations with pathogen
load and disease risk in wildlife, make it difficult to use such
information as a tool to identify vulnerable populations
likely to be at risk from new pathogens.
Control and when to intervene?
Efforts to provide a more comprehensive view of the role of
pathogens in wildlife extinction risk will require increased
collaboration among wildlife ecologists, veterinarians and
conservation organizations. Characteristics of threatening
pathogens highlight the possibility that future control stra-
tegies targeted at reducing cross-species transmission of
high-risk pathogens, either by vaccination or by limiting
contact with domesticated animals, may significantly reduce
the risk of pathogen-mediated wildlife declines (Pedersen
et al., 2007). In the case of the massive African rinderpest
epidemic, once targeted vaccination of domestic cattle
began, prevalence and disease-associated declines dropped
dramatically in wild artiodactyl populations (Plowright,
1982). Similar vaccination campaigns are currently under-
way in Tanzania, using a three part vaccine to eliminate
rabies, canine distemper virus and canine parvovirus from
domestic dogs, in the hopes that this will reduce transmis-
sion of these deadly diseases to threatened wildlife hosts,
such as African lions, African wild dogs and bat-eared foxes
(Cleaveland et al., 2000, 2003). In addition, because many of
the threatening pathogens are transmitted by close contact
between individuals (Pedersen et al., 2007), alternative
strategies could also involve minimizing contact between
wildlife and domesticated animals, by creating physical
barriers that reduce the potential for cross species transmis-
sion, or by setting temporal limitations on the use of shared
water resources or grazing land. These strategies, specifically
the construction of buffer zones between agricultural areas
with domestic sheep and wild populations of bighorn sheep
have been successful in reducing infectious disease out-
breaks in western North America (Jessup, Boyce & Torres,
1995).
A recent study by Altizer, Nunn & Lindenfors (2007)
found that threatened primates had fewer pathogens than
their non-threatened counterparts. This finding may seem
on the surface to be positive for threatened hosts suffering
from disease mediated extinction risk. However, it also
could suggest that endangered wildlife species lose patho-
gens due to their small, fragmented population size. This
ultimately could lead to the loss of genetic variation for
immunity, making threatened species more susceptible to
future disease outbreaks. In terms of management and
captive breeding programs, it is possible that hosts raised in
captivity, who are continually treated to eliminate infec-
tions, may suffer a disadvantage when released into the wild,
due to increased susceptibility to infection caused from
relaxed selection for resistance, especially in traits that are
costly to maintain. Given this possibility, species manage-
ment programs, especially those that include captive breed-
ing and re-introductions, may need to focus on maintaining
the levels of immunity or variation in resistance that are
present in natural populations (Altizer & Pedersen, 2008).
While we have focused this review on cases where pathogens
cause host population declines and extinction risk, in terms
of management, the best strategy for the conservation of
natural populations may be to conserve geographically
structured species interactions (i.e. predator–prey, host–par-
asite) that can maintain the evolutionary history that has
occurred between species. This type of strategy will need to
take a landscape-scale approach to species conservation,
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 7
Diseases in biological conservationK. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen

that accounts for the various habitats were interacting
species occur, and includes corridors between fragmented
populations to increase dispersal and genetic diversity be-
tween isolated populations.
Future directions and conclusions
Infectious diseases are of concern to conservation for several
reasons: (1) they can deplete population sizes; (2) they can
hinder the recovery of rare species; (3) they necessitate
management actions that often impact the environment; (4)
they can act on their own or in concert with other drivers
and be the ultimate cause of species extinction (Lafferty,
2003). Future studies of the complex interactions that occur
between human activities, environmental change and the
emergence of infectious disease will promote healthy ecosys-
tems and help protect biological diversity. Here, we outline
what we see as the most critical challenges and future
directions for the study of infectious diseases in the con-
servation sciences.
What do we need?
1. Quantitative understanding of habitat destruction, cli-
mate change, overexploitation, invasive species, pollution
and infectious disease as threats to biodiversity, as well as
how these factors are likely to interact to drive species
extinction.
2. Better understanding of the circumstances when infec-
tious diseases are most likely to cause extinction. This can
occur when a pathogen is novel to a susceptible host species
or utilizes a reservoir host, when the pathogen spreads via
frequency-dependent transmission, when the host has small
pre-epidemic population sizes or highly susceptible indivi-
duals that act as entry points for disease.
3. Enhanced methods for identifying infectious agents that
cause significant pathologies, population-level effects, and
increased likelihood of extinction in a threatened host.
What can we do?
1. Conduct rigorous studies to gather baseline information
on pathogen prevalence and diversity for declining species;
especially small, fragmented populations at risk from sev-
eral other stressors.
2. Combine evidence and theory to weigh the relative effects
and likelihood of threats to species. Incorporate findings
into IUCN criteria used to assess threats.
3. Promote conservation medicine – interdisciplinary colla-
borations that link wildlife disease, human health and
environmental change.
4. Advance existing surveillance programs associated with
economic initiatives and incorporate these into ecological
research. Current methods for tracking changes in disease
ecology depend on the detection of infections in target
populations. Monitoring can be improved by establishing
disease registries that permit molecular identification of new
diseases or new variants of existing diseases.
5. Increase efforts to determine the immunogenetic archi-
tecture of endangered and threatened populations as a
means to identify those likely to be at risk from the
introduction of novel pathogens.
While infectious diseases as a driver of species extinction
may have been historically overlooked, contemporary ex-
tinctions – due in part to pathogens – are becoming increas-
ingly documented and are likely to play a significant role in
future species endangerment. If we are to make progress in
conserving biodiversity, we need to understand the role of
pathogens in natural populations, and, more importantly,
how pathogens interact with other drivers of extinction to
cause species loss. Currently, the majority of studies suggest
that habitat fragmentation, climate change, over-exploita-
tion and invasive species are the dominant factors causing
species extinction. We suggest that while disease alone may
have caused extinction in few species, pathogens may
provide one of the biggest threats to already-endangered
species, especially when disease interacts with other drivers.
As ecologists and conservation biologists, we are just begin-
ning to understand the role of pathogens in natural popula-
tions; however, it is imperative that we focus efforts on
threatened species and their diseases, such that we can
inform control and management strategies. Understanding
the host species that are at highest risk of disease-mediated
extinction, the pathogens likely to cause disease and their
interaction with other drivers of extinction, will ultimately
inform future control and prevention strategies and help
preserve biological diversity.
Acknowledgments
A.B.P. was funded as a Royal Society Incoming Research
Fellow. K.F.S. received funding from a David H. Smith
Conservation Research Fellowship, a Switzer Leadership
Grant and Brown University. K.A. received funding from
Morris Animal Foundation and the British Ecological
Society.
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