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The role of infectious diseases in biological conservation



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.
The role of infectious diseases in biological conservation
K. F. Smith
, K. Acevedo-Whitehouse
& A. B. Pedersen
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
conservation; extinction; biodiversity;
environmental change; pathogens; disease;
Katherine F. Smith, Brown University,
Ecology and Evolutionary Biology,
Providence, RI 02912, USA.
All authors contributed equally.
Received 1 May 2008; accepted 21
November 2008
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.
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 c2009 The Authors. Journal compilation c2009 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
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,
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
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
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London2
Diseases in biological conservation K. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
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
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-
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
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 3
Diseases in biological conservationK. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
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,
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).
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London4
Diseases in biological conservation K. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
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,
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
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.
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 5
Diseases in biological conservationK. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
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 c2009 The Authors. Journal compilation c2009 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,
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 c2009 The Authors. Journal compilation c2009 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
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.
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
Acevedo-Whitehouse, K. & Cunningham, A. (2006). Is MHC
enough for understanding wildlife immunogenetics? Trends
Ecol. Evol. 21, 433–438.
Acevedo-Whitehouse, K., Gulland, F.M.D., Greig, D. &
Amos, W. (2003). Inbreeding: disease susceptibility in
California sea lions. Nature 422, 35.
Acevedo-Whitehouse, K., Spraker, T.R., Lyons, E., Melin,
S.R., Gulland, F., Delong, R.L. & Amos, W. (2006).
Contrasting effects of heterozygosity on survival and
hookworm resistance in California sea lion pups. Mol.
Ecol. 15, 1973–1982.
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London8
Diseases in biological conservation K. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
Ahmed, S.A. (2000). The immune system as a potential target
for environmental estrogens (endocrine disrupters): a new
emerging field. Toxicology 150, 191–206.
Alford, R.A., Bradfield, K.S. & Richards, S.J. (2007). Ecol-
ogy: global warming and amphibian losses. Nature 447,
Altizer, S., Nunn, C.L. & Lindenfors, P. (2007). Do threa-
tened hosts have fewer parasites? A comparative study in
primates. J. Anim. Ecol. 76, 304–314.
Altizer, S. & Pedersen, A.B. (2008). Host–pathogen evolution,
biodiversity and disease risks for natural populations. In
Conservation biology: evolution in action: 259–278. Carroll,
S. & Fox, C. (Eds). Oxford, UK: Oxford University Press.
Amos, W. & Balmford, A. (2001). When does conservation
genetics matter? Heredity 87, 257–265.
Anderson, R.M. & May, R.M. (1992). Infectious diseases of
humans, dynamics and control. New York: Oxford Univer-
sity Press.
Ayala, F.J. (1995). The myth of Eve: molecular biology and
human origins. Science 270, 1930–1936.
Bassett, T.J. (2005). Card-carrying hunters, rural poverty, and
wildlife decline in northern Cote d’Ivoire. Geogr. J. 171,
Berger, L., Speare, R., Daszak, P., Green, D.E., Cunningham,
A.A., Goggin, C.L., Slocombe, R., Ragan, M.A., Hyatt,
A.D., McDonald, K.R., Hines, H.B., Lips, K.R., Maran-
telli, G. & Parkes, H. (1998). Chytridiomycosis causes
amphibian mortality associated with population declines in
the rain forests of Australia and Central America. Proc.
Natl. Acad. Sci. USA 95, 9031–9036.
Blaustein, A.R. & Wake, D.B. (1990). Declining amphibian
populations: a global phenomenon. Trends Ecol. Evol. 5,
Boon, J.P., Lewis, W.E., Tjoen-A-Choy, M.R., Allchin, C.R.,
Law, R.J., De Boer, J., Ten Hallers-Tjabbes, C.C. &
Zegers, B.N. (2002). Levels of polybrominated diphenyl
ether (PBDE) flame retardants in animals representing
different trophic levels of the North Sea food. Web.
Environ. Sci. Technol. 36, 4025–4032.
Boots, M. & Sasaki, A. (2003). Parasite evolution and extinc-
tions. Ecol. Lett. 6, 176–182.
Bornstein, S., Morner, T. & Samuel, W.M. (2001). Sarcoptes
scabei and sarcoptic mange. In Parasitic disease of wild
mammals. 2nd edn. 107–119. Samuel, W.M., Pybus, M.J. &
Kocan, A.A. (Eds). Ames: Iowa State University Press.
Bosch, J., Carrascal, L.M., Dur ´
an, L., Walker, S. & Fisher,
M.C. (2007). Climate change and outbreaks of amphibian
chytridiomycosis in a montane area of Central Spain; is
there a link? Proc. Biol. Sci. 274, 253–260.
Boyce, W.M. & Weisenberger, M.E. (2005). The rise and fall
of psoroptic scabies in bighorn sheep in the San Andres
Mountains, New Mexico. J. Wildl. Dis. 41, 525–531.
Briton, J., Nurthen, R.K., Briscoe, D.A. & Frankham, R.
(1994). Modelling problems in conservation genetics using
Drosophila: consequences of harems. Biol. Conserv. 69,
de Castro, F. & Bolker, B. (2005). Mechanisms of disease-
induced extinction. Ecol. Lett. 8, 117–126.
Centers for Disease Control. (2003). Morb. Mortal. Wkly.
Rep. 52, 642–646. Update: Multistate Outbreak of Mon-
keypox Illinois, Indiana, Kansas, Missouri, Ohio and
Wisconsin. Available at
Committee on Grand Challenges in Environmental Sciences.
(2001). National research council report: grand challenges in
environmental sciences. Washington, DC: National Acad-
emy Press. Available at
Charlesworth, B. & Charlesworth, D. (1999). The genetic basis
of inbreeding depression. Genet. Res. 74, 329–340.
Cleaveland, S., Appel, M.G.J., Chalmers, W.S.K., Chilling-
worth, C., Kaare, M. & Dye, C. (2000). Serological and
demographic evidence for domestic dogs as a source of
canine distemper virus infection for Serengetti wildlife. Vet.
Microbiol. 72, 3–4.
Cleaveland, S., Kaare, M., Tiringa, P., Mlegngeya, T. &
Barrat, J. (2003). A dog rabies vaccination campaign in
rural Africa: impact on the incidence of dog rabies and
human dog-bite injuries. Vaccine 21, 17–18.
Cleaveland, S., Laurenson, M.L. & Taylor, L.H. (2001).
Disease of humans and their domestic mammals: pathogen
characteristics, host range and the risk of emergence.
Philos. Trans. Roy. Soc. B 356, 991–999.
Coltman, D.W., Pilkington, J.G., Smith, J.A. & Pemberton,
J.M. (1999). Parasite-mediated selection against inbred
Soay sheep in a free-living, island population. Evolution 53,
Cunningham, A.A., Daszak, P. & Rodr´
ıguez, J.P. (2003).
Pathogen pollution: defining a parasitological threat to
biodiversity conservation. J. Parasitol. 89, S78–S83.
Daszak, P., Berger, L., Cunningham, A.A., Hyatt, A.D.,
Green, D.E. & Speare, R. (1999). Emerging infectious
diseases and amphibian population declines. Emerg. Infect.
Dis. 5, 735–748.
Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2000). Emer-
ging infectious diseases of wildlife threats to biodiversity
and human health. Science 287, 443–449.
Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2003). Infec-
tious disease and amphibian population declines. Divers.
Distrib. 9, 141–150.
Davies, T.J. & Pedersen, A.B. (2008). Phylogeny and geogra-
phy predict pathogen community similarity in wild pri-
mates and humans. Proc. Roy. Soc. Lond. Ser. B,275,
Domingo, E. & Holland, J.J. (1997). RNA viruses and fitness
for survival. Annu. Rev. Microbiol. 51, 151–178.
Epstein, P.R. (2000). Is global warming harmful to health?
Sci. Am. 8, 36–43.
Fain, A. (1978). Epidemiological problems of scabies. Int. J.
Dermatol. 17, 20–30.
Fairbrother, A. (1993). Immunotoxicology of captive and
wild birds in wildlife toxicology and population modeling.
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 9
Diseases in biological conservationK. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
In Integrated studies of agro-ecosystems: 251–262. Kendall, R.
& Lacher, T.E. (Eds). Boca Raton, FL: Lewis Publishers.
Fenton, A. & Pedersen, A.B. (2005). Community epidemiol-
ogy in theory and practice: a conceptual framework for
classifying disease threats in human and wild populations.
Emerg. Infect. Dis. 11, 1815–1821.
Flather, C.H., Joyce, L.A. & Bloomharde, C.A. (1994).
Species endangerment patterns. In United States Service
General Technical Report RM-241, 1–42.
Formenty, P., Boesch, C., Wyers, M., Steiner, C., Donati, F.,
Dind, F., Walker, F. & Le Guennom, B. (1999). Ebola
virus outbreak among wild chimpanzees living in a rain-
forest of Cote d’Ivoire. J. Infect. Dis. 179 (Suppl. 1):
Forson, D.D. & Storfer, A. (2006). Atrazine increases rana-
virus susceptibility in the tiger salamander, Ambystoma
tigrinum.Ecol. Appl. 16, 2325–2332.
Gaston, K.J. (1991). Rarity. Oxford, UK: Blackwell Scientific.
Hall, A.J., Hugunin, K., Deaville, R., Law, R.J., Allchin,
C.R. & Jepson, P.D. (2006). The risk of infection from
polychlorinated biphenyl exposure in the harbor
porpoise (Phocoena phocoena): a case–control approach.
Environ. Health. Perspect. 114, 704–711.
Hammond, J.A., Hall, A.J. & Dyrynda, E.A. (2005). Com-
parison of polychlorinated biphenyl (PCB) induced effects
on innate immune functions in harbour and grey seals.
Aquat. Toxicol. 74, 126–138.
Hanselmann, R., Rodriguez, A., Lampo, M., Fajardo-Ra-
mos, L., Aguirre, A.A., Kilpatrick, A.M., Rodriguez, J.P.
& Daszak, P. (2004). Presence of an emerging pathogen of
amphibians in introduced bullfrogs Rana catesbeiana in
Venezuela. Biol. Conserv. 120, 115–119.
Harvell, C.D., Mitchell, C.E, Ward, J.R., Altizer, S., Dobson,
A.P., Ostfield, R.S. & Samuel, M.D. (2002). Climate
warming and disease risk for terrestrial and marine biota.
Science 296, 2158–2162.
Henriksen, P., Dietz, H.H., Henriksen, S.A. & Gjelstrup, P.
(1993). Sarcoptic mange in red fox in Denmark. Dansk
Veterin. 76, 12–13.
Hero, J.-M. & Morrison, C. (2003). Frog declines in Austra-
lia: global implications. Herpetol. J. 14, 175–186.
Intergovernmental Panel on Climate Change (IPCC). (2007).
Climate change 2007: synthesis report. Contribution of
Working Groups I, II and III to the Fourth Assessment
Report of the Intergovernmental Panel on Climate Change.
Core Writing TeamPachauri, R.K. & Reisinger, A. (Eds)
Geneva, Switzerland: IPCC.
International Union for the Conservation of Nature (IUCN).
(2004). IUCN red list of threatened species. Available at
International Union for the Conservation of Nature (IUCN).
(2007). IUCN red list of threatened species. Available at
Jenkins, P.T., Genovese, K. & Ruffler, H. (2007). Defenders of
wildlife: broken screens: the regulation of live animal imports
in the United States. Washington, DC.
Jessup, D.A., Boyce, W.M. & Torres, S.G. (1995). Bighorn
sheep health management in California: a fifteen year
retrospective. In Proceedings of the joint conference of the
American Association of Zoo Veterinarians, the Wildlife
Disease Association and the American Association of Wild-
life Veterinarian: 55–67. Junge, R.E. (Ed.). Philadelphia,
PA: American Association of Zoo Veterinarians
Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Bulk,
D., Gittleman, J.L. & Daszak, P. (2007a). Global trends in
emerging infectious diseases. Nature 451, 990–993.
Jones, M.E., Jarman, P.J., Lees, C.M., Estermen, H., Ha-
mede, R.K., Mooney, N.J., Mann, D., Pukk, C.E., Berg-
feld, J. & McCallum, H. (2007b). Conservation
management of Tasmanian devils in the context of an
emerging, extinction-threatening disease: devil facial tumor
disease. EcoHealth 4, 326–337.
Karesh, W.B., Cook, W.B., Bennet, E.L. & Newcomb, J.
(2005). Wildlife trade and global disease emergence. Emerg.
Infect. Dis. 11, 1000–1002.
Koprivnikar, J., Forbes, M.R. & Baker, R.L. (2007). Con-
taminant effects on host–parasite interactions: atrazine,
frogs, and trematodes. Environ. Toxicol. Chem. 26,
Kriger, K.M., Pereoglou, F. & Hero, J.M. (2007). Latitudinal
variation in the prevalence and intensity of chytrid (Batra-
chochytrium dendrobatidis) infection in eastern Australia.
Conserv. Biol. 21, 1280–1290.
Krkosek, M., Ford, J.S., Morton, A., Lele, S., Myers, R.A. &
Lewis, M.A. (2007). Declining wild salmon populations in
relation to parasites from farm salmon. Science 318,
Lafferty, K.D. (2003). Is disease increasing or decreasing, and
does it impact or maintain biodiversity? J. Parasitol. 89,
Lafferty, K.D. & Gerber, L.R. (2002). Good medicine for
conservation biology: the intersection of epidemiology and
conservation theory. Conserv. Biol. 6, 593–604.
Leroy, E.M., Rouquet, P., Formenty, P., Souquiere, S.,
Kilbourne, A., Froment, J.M., Bermeljo, M., Smit, S.,
Karesh, W., Swanepoel, R., Zaki, S.R. & Rollin, P.E.
(2004). Multiple Ebola virus transmission events and
rapid decline of Central African wildlife. Science 303,
Lips, K.R., Bren, F., Brenes, R., Reeve, J.D., Alford, R.A.,
Voyles, J., Careys, C., Livo, A., Pessier, A.P. & Collins, J.P.
(2006). Emerging infectious disease and the loss of biodi-
versity in a Neotropical amphibian community. Proc. Natl.
Acad. Sci. USA 103, 3165–3170.
Lips, K.R., Diffendorfer, J., Mendelson, J.R. III & Sears,
M.W. (2008). Riding the wave: reconciling the roles of
disease and climate change in amphibian declines. PLoS
Biol. 6, 441–454.
Lyles, A.M. & Dobson, A.P. (1993). Infectious disease and
intensive management: population dynamics, threatened
hosts, and their parasites. J. Zoo. Wildl. Med. 24, 315–326.
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London10
Diseases in biological conservation K. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
Mace, G.M. & Balmford, A. (2000). Patterns and processes in
contemporary mammalian extinction. In Priorities for the
conservation of mammalian diversity: 27–52. Entwistel, A. &
Dunstone, N. (Eds). Cambridge, UK: Cambridge Univer-
sity Press.
Mainka, S.A. (2002). Biodiversity, poverty and hunger: where
do they meet? In Links between biodiversity conservation,
livelihoods and food security: the sustainable use of wild
species for meat: 11–18. Gland, Switzerland: World Con-
servation Union.
Markert, J.A., Grant, P.R., Grant, B.R., Keller, L.F.,
Coombs, J.L. & Petren, K. (2004). Neutral locus hetero-
zygosity, inbreeding and survival in Darwin’s ground
finches (Geospiza fortis and G. scandens). Heredity 92,
Mazzoni, R., Cunningham, A.A., Daszak, P., Apolo, A.,
Perdomo, E. & Speranza, G. (2003). Emerging pathogen of
wild amphibians in frogs (Rana catesbeiana) farmed for
international trade. Emerg. Infect. Dis. 9, 995–998.
McCallum, H., Barlow, N. & Hone, J. (2001). How should
pathogen transmission be modelled? Trends Ecol. Evol. 16,
McCallum, H. & Dobson, A. (1995). Detecting disease and
parasite threats to endangered species and ecosystems.
Trends Ecol. Evol. 10, 190–194.
McCallum, H. & Jones, M. (2006). To lose both would look
like carelessness: Tasmanian devil facial tumour disease.
PLoS Biol. 4, 1671–1674.
McCarthy, A.J., Shaw, M. & Goodman, S.J. (2007). Patho-
gen evolution and disease emergence in carnivores. Proc.
Roy. Soc. Lond. Ser. B 274, 3165–3174.
Millenium Ecosystem Assessment (MEA). (2005). Ecosystems
and human well-being: current state and trends: Findings of
the Condition and Trends Working Group. Washington
D.C.: Island Press.
Myers, R.A. & Worm, B. (2003). Rapid worldwide
depletion of predatory fish communities. Nature 423,
Nunn, C.L. & Altizer, S. (2006). Infectious diseases in
primates: behavior, ecology and evolution. Oxford, UK:
Oxford Series in Ecology and Evolution, Oxford University
O’keefe, K.J. & Antonovics, J. (2002). Playing by different
rules: the evolution of virulence in sterilizing pathogens.
Am. Nat. 159, 597–605.
Osterhaus, A.D.M.E., Groen, J., UytdeHaag, F.G.C.M.,
Visser, I.K.G., Bildt, M.W.G., van de Bergman, A. &
Klingeborn, B. (1989). Distemper virus in Baikal seals.
Nature 338, 209–210.
Ouellet, M., Mikaelian, I., Pauli, B.D., Rodrigue, J. & Green,
D.M. (2005). Historical evidence of widespread chytrid
infection in North American amphibian populations. Con-
serv. Biol. 19, 1431–1440.
Pedersen, A.B., Jones, K.E., Nunn, C.L. & Altizer, S.A.
(2007). Infectious disease and mammalian extinction risk.
Conserv. Biol. 21, 1269–1279.
Pence, D.B., Casto, S.D. & Samuel, W.M. (1975). Variation
in the chaetotaxy and denticulation of Sarcoptes scabei
(Acarina: Sarcoptidae) from wild canids. Acarology 17,
Pence, D.B. & Ueckermann, E. (2002). Sarcoptic mange in
wildlife. Rev. Sci. Tech. Off. Int. Epiz. 21, 385–398.
Pimm, S.L. & Askins, A. (1995). Forest losses predict bird
extinction in eastern North America. Proc. Natl. Acad. Sci.
USA 92, 9343–9347.
Pimm, S.L., Russell, G.J., Gittleman, J.L. & Brooks, T.M.
(1995). The future of biodiversity. Science 269, 347–350.
Plowright, W. (1982). The effects of rinderpest and rinderpest
control on wildlife in Africa. Symp. Zoo. Soc. Lond. 50,
Potts, W.K. & Wakeland, E.K. (1993). Evolution of MHC
genetic diversity: a tale of incest, pestilence and sexual
preference. Trends Genet. 9, 408–412.
Pounds, J.A., Bustamante, M.R., Coloma, L.A., Consuegra,
J.A., Fogden, M.P., Foster, P.N., La Marca, E., Masters,
K.L., Merino-Viteri, A., Puschendorf, R., Ron, S.R.,
anchez-Azofeifa, G.A., Still, C.J. & Young, B.E. (2006).
Widespread amphibian extinctions from epidemic disease
driven by global warming. Nature 439, 161–167.
Pounds, J.A., Bustamante, M.R., Coloma, L.A., Consuegra,
J.A., Fogden, M.P., Foster, P.N., La Marca, E., Masters,
K.L., Merino-Viteri, A., Puschendorf, R., Ron, S.R.,
anchez-Azofeifa, G.A., Still, C.J. & Young, B.E. (2007).
Global warming and amphibian losses; the proximate
cause of frog declines? (Reply). Nature 447, E5–E6.
Purvis, A. (2001). Mammalian life histories and responses of
populations to exploitation. In Conservation of exploited
species: 169–181. Reynolds, J., Mace, G.M., Redford, K.H.
& Robinson, J.G. (Eds). Cambridge, UK: Cambridge
University Press.
Rachowicz, L.J., Hero, J.M., Alford, R.A., Taylor, J.W.,
Morgan, J.A.T., Vredenburg, V.T., Collins, J.P. & Briggs,
C.J. (2005). The novel and endemic pathogen hypotheses:
competing explanations for the origin of emerging infec-
tious diseases of wildlife. Conserv. Biol. 19, 1441–1448.
Raimondo, S., Mineau, P. & Barron, M.G. (2007). Estimation
of chemical toxicity to wildlife species using interspecies
correlation models. Environ. Sci. Technol. 41, 5888–5894.
Reid, J.M., Arcese, P. & Keller, L.F. (2003). Inbreeding
depresses immune response in song sparrows (Melospiza
melodia): direct and inter-generational effects. Proc. Roy.
Soc. Lond. Ser. B 270, 2151–2157.
Schloegel, L.M., Hero, J.M, Berger, L., Speare, R., McDo-
nald, K. & Daszak, P. (2006). The decline of the sharp-
snouted day frog (Taudactylus acutirostris): the first docu-
mented case of extinction by infection in a free-ranging
wildlife species? EcoHealth 3, 35–40.
Schramm Urrutia, Y. (2002). Genetic structure and phylo-
geography of California sea lions (Zalophus californianus
californianus) along the Baja California Peninsula, Mexico.
PhD dissertation, Universidad de Baja Califrornia,
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London 11
Diseases in biological conservationK. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
Scott, M.E. (1988). The impact of infection and disease on
animal populations: implications for conservation biology.
Conserv. Biol. 2, 40–56.
Selgrade, M.K. (2007). Immunotoxicity: the risk is real.
Toxicol. Sci. 100, 328–332.
Settipane, G.A. (1995). Columbus and the new world: medical
implications. Providence, RI: Ocean Side Publications.
Siddle, H.V., Kreiss, A., Eldridge, M.D.B., Noonan, E.,
Clarke, C.J., Pyecroft, S., Woods, G.M. & Belov, K.
(2007). Transmission of a fatal clonal tumor by biting
occurs due to depleted MHC diversity in a threatened
carnivorous marsupial. Proc. Natl. Acad. Sci. USA 104,
Sindermann, C.J. (1990). Principal diseases of marine fish and
shellfish: diseases of marine fish. San Diego, CA: Academic
Singer, F.J., Zeigenfuss, L.C. & Spicer, L. (2001). Role of
patch size, disease, and movement in rapid extinction of
bighorn sheep. Conserv. Biol. 15, 1347–1354.
Smith, K.F. & Carpenter, S.M. (2006). Spread of exotic
black rat parasites to endemic deer mice on the
California Channel Islands. Divers. Distrib. 12, 742
Smith, K.F., Sax, D.F. & Lafferty, K.D. (2006). Evidence for
the role of infectious disease in species extinction. Conserv.
Biol. 20, 1349–1357.
Smith, K., Behrens, M.D., Max, L.M., Daszak, P. (2008).
U.S. drowing in unidentified fishes: Scope, implications
and regulation of live fish imports. Conserv. Letts. 1,
Snoeijs, T., Dauwe, T., Pinxten, R., Darras, V.M., Arckens,
L. & Eens, M. (2005). The combined effect of lead exposure
and high or low dietary calcium on health and immuno-
competence in the zebra finch (Taeniopygia guttata). En-
viron. Pollut. 134, 123–132.
Sommer, S. (2005). The importance of immune gene varia-
bility (MHC) in evolutionary ecology and conservation.
Front. Zool. 2, 16–33.
Spielman, D., Brook, B.W. & Frankham, R. (2004). Most
species are not driven to extinction before genetic factors
impact them. Proc. Natl. Acad. Sci. USA 101,
Stone, W.B., Parks, E., Weber, B.L. & Parks, F.J. (1974).
Experimental transfer of sarcoptic mange from red foxes
and wild canids to captive wildlife and domestic animals.
New York Fish Game J. 19, 1–11.
Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodri-
gues, A.S.L. & Fischman, D.L. (2004). Status and trends of
amphibian declines and extinctions worldwide. Science
306, 1783–1786.
Taylor, L.H., Latham, S.M. & Woolhouse, M.E.J. (2001).
Risk factors for human disease emergence. Philos. Trans.
Roy. Soc. B 356, 983–989.
Thrall, P.H., Antonovics, J. & Hall, D.W. (1993). Host and
pathogen coexistence in sexually-transmitted and vector-
borne diseases characterized by frequency-dependent dis-
ease transmission. Am. Nat. 142, 543–552.
Torchin, M.E. & Mitchell, C.E. (2004). Parasites, pathogens,
and invasions by plants and animals. Front. Ecol. Environ.
2, 183–190.
Valsecchi, E., Amos, W., Raga, J.A., Podesta, M. & Sherwin,
W. (2004). The effects of inbreeding on mortality during a
morbillivirus outbreak in the Mediterranean striped
dolphin (Stenella coeruleoalba). Anim. Conserv. 7,
Wilcove, D.S., Rothstein, D., Dubow, J., Phillips, A. &
Losos, E. (1998). Quantifying threats to imperiled species
in the United States. Bio-Science 48, 607–615.
Wilson, E.O. (1992). The diversity of life. New York, NY:
W. W. Norton & Company.
Animal Conservation 12 (2009) 1–12 c2009 The Authors. Journal compilation c2009 The Zoological Society of London12
Diseases in biological conservation K. F. Smith, K. Acevedo-Whitehouse and A. B. Pedersen
... The extinction risk of wildlife populations following the emergence of a novel pathogen has been strongly linked to host population sizes and pathogen transmission patterns [5,27]. Evaluating host numbers and pathogen prevalence in natural populations will therefore be an essential step in characterizing variation in population-level responses following disease emergence. ...
... Notably however, this single extinction event occurred in an initially small-sized population, which was likely introduced from a small founder base. Hence, in line with theoretical risk factors for disease-induced extinction [5], Bsal may especially imperil species and populations with low initial population sizes or those thinned by pre-outbreak perturbations, including endemic and already endangered species [27]. This will particularly hold true given at least partial density-independent transmission patterns (also see further below). ...
... Overall, our findings illustrate how the impacts of emerging hypervirulent pathogens can be unpredictable, even for some of the most susceptible host species. For one, we confirm the possibility of extinction, and point at the role of pre-epidemic population sizes in determining extinction risk [5,27]. Yet, we additionally show how host responses within surviving populations may vary in a demographic, ecological as well as a molecular context, despite showing similar (reduced) host encounter rates after outbreaks. ...
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Understanding wildlife responses to novel threats is vital in counteracting biodiversity loss. The emerging pathogen Batrachochytrium salamandrivorans (Bsal) causes dramatic declines in European salamander populations, and is considered an imminent threat to global amphibian biodiversity. However, real-life disease outcomes remain largely uncharacterized. We performed a multidisciplinary assessment of the longer-term impacts of Bsal on highly susceptible fire salamander (Salamandra salamandra) populations, by comparing four of the earliest known outbreak sites to uninfected sites. Based on large-scale monitoring efforts, we found population persistence in strongly reduced abundances to over a decade after Bsal invasion, but also the extinction of an initially small-sized population. In turn, we found that host responses varied, and Bsal detection remained low, within surviving populations. Demographic analyses indicated an ongoing scarcity of large reproductive adults with potential for recruitment failure, while spatial comparisons indicated a population remnant persisting within aberrant habitat. Additionally, we detected no early signs of severe genetic deterioration, yet nor of increased host resistance. Beyond offering additional context to Bsal-driven salamander declines, results highlight how the impacts of emerging hypervirulent pathogens can be unpredictable and vary across different levels of biological complexity, and how limited pathogen detectability after population declines may complicate surveillance efforts.
... Las enfermedades infecciosas han sido raramente citadas como una amenaza importante para la conservación de especies de fauna silvestre. Entre las principales amenazas se suelen describir la destrucción de los hábitats, la introducción de especies exóticas, la contaminación ambiental, el cambio climático y el tráfico de especies silvestres (Smith 2009). Sin embargo, los agentes infecciosos pueden interactuar con otros factores impulsores y causar declinaciones temporales o permanentes en las poblaciones de fauna silvestre, atentando de esa manera contra su conservación (Valenzuela-Sánchez y Medina-Vogel 2014). ...
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Las enfermedades infecciosas han sido raramente citadas como una amenaza importante para la conservación de especies de fauna silvestre. No obstante, la interacción con otros factores impulsores y la evidencia de declinaciones poblacionales de fauna y afecciones muy graves mediada por agentes patógenos ha aumentado en los últimos años, generando mayor atención hacia las enfermedades infecciosas como una amenaza para la conservación. Los camélidos silvestres comparten hábitat con diversas especies silvestres, domésticas y ferales, lo cual puede propiciar la persistencia y transmisión interespecie de diferentes agentes patógenos. Las investigaciones sobre enfermedades infecciosas de origen viral en camélidos silvestres se han centrado principalmente en determinar la circulación de estos patógenos, mediante la detección de anticuerpos en sangre. Mientras que, en el caso de enfermedades producidas por bacterias y protozoarios, las investigaciones han buscado en particular el aislamiento o la detección directa de estos microorganismos. Sin embargo, todavía urge realizar mayor investigación sobre las enfermedades infecciosas que afectan a vicuñas y guanacos, ya que la incidencia de estas enfermedades puede afectar procesos evolutivos y ecológicos que atenten contra su conservación ergo su aprovechamiento sostenible
... Outbreaks of infectious diseases pose significant threats to the population health and conservation of freeranging wildlife 1,2 , and seasonality can have profound impacts on the dynamics of these outbreaks 3 . Langwig et al. 4 outlined five mechanisms through which seasonality may alter transmission dynamics via: (1) variation in sociality, (2) birth pulses causing influxes of new susceptibles, (3) variation in habitat use, (4) variation in climatic factors, and (5) variation in host immune function. Yet these are not necessarily mutually exclusive mechanisms. ...
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Seasonal variation in habitat use and animal behavior can alter host contact patterns with potential consequences for pathogen transmission dynamics. The endangered Florida panther (Puma concolor coryi) has experienced significant pathogen-induced mortality and continues to be at risk of future epidemics. Prior research has found increased panther movement in Florida’s dry versus wet seasons, which may affect panther population connectivity and seasonally increase potential pathogen transmission. Our objective was to determine if Florida panthers are more spatially connected in dry seasons relative to wet seasons, and test if identified connectivity differences resulted in divergent predicted epidemic dynamics. We leveraged extensive panther telemetry data to construct seasonal panther home range overlap networks over an 11 year period. We tested for differences in network connectivity, and used observed network characteristics to simulate transmission of a broad range of pathogens through dry and wet season networks. We found that panthers were more spatially connected in dry seasons than wet seasons. Further, these differences resulted in a trend toward larger and longer pathogen outbreaks when epidemics were initiated in the dry season. Our results demonstrate that seasonal variation in behavioral patterns—even among largely solitary species—can have substantial impacts on epidemic dynamics.
... Temperature variations may occur during the glazing process, leading to unwanted glazing/devitrification between steps, somewhat hampering the whole process. In addition, the SSV device comprises an open system with direct contact with liquid nitrogen, making the process more critical for wild animals due to biosafety issues, mainly for wild animals, which generally harbor infectious diseases [37]. In this way, NL filtration has been performed to avoid these problems [38]. ...
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Vitrification is essential for successful tissue cryopreservation and biobanking in wild cats. This study aimed to compare different methods of vitrification (Ovarian Tissue Cryosystem—OTC, Straws—STW, and Solid Surface vitrification—SSV) for testicular fragment vitrification in tom cats. Testicular fragments were recovered from five adult tom cats and subjected to equilibrium vitrification using different cryovials and methods under the same conditions of vitrification solutions and cryoprotectants. The efficiencies of the methods were evaluated using histological analysis of spermatogonia and Sertoli cell nuclei, seminiferous tubular basement membrane detachment, and the gonadal epithelium shrinkage score scale. Cell viability was assessed using Hoechst PI and Terminal deoxynucleotidyl transferase nick end labeling (TUNEL) assay. The results showed that OTC is an effective vitrification method for maintaining the distinction between spermatogonia and Sertoli cells. OTC was similar to the control for basal membrane detachment parameters (p = 0.05). Epithelial shrinkage was low in the SSV group, which showed the highest percentage of viable cells among the vitrified groups (p = 0.0023). The OTC and SSV vitrification methods were statistically similar in terms of the percentage of TUNEL-positive cells (p = 0.05). Therefore, OTC and SSV provide favorable conditions for maintaining viable cat testicular tissue cells after vitrification.
... species: 34 31 or 1 32 . Among them is Sarcoptes scabiei, one of the most virulent multi-host mites, responsible for epidemics in wild and domesticated mammals and skin disease outbreaks in humans 33 . ...
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Parasitic organisms have large impacts on wildlife, livestock, and human health, however, little is known about ecological and biological factors influencing their host range. When single-host mites are shifted to new hosts, they are likely to become more virulent and cause epidemics as new hosts may lack natural defenses against new parasites (high epidemic risk). Here, we assembled the largest and complete dataset on mites permanently parasitic on mammals and conducted an analysis of factors affecting the probability of single-host parasites becoming multi-hosts, while accounting for potentially unobserved host-parasite links and class imbalance. We identified statistically significant predictors related to parasites (5 variables), hosts (2), climate (2), and habitat disturbance (1). Among mite-related variables, the most important was the proximity to the host immune system which was correlated with the mouthpart morphology. The accuracy of predicting the multi-host risk group was estimated at 0.721. When our model was used for forecasting, it identified Chiroptera (bats) and Carnivora as hosts having the largest number of parasites belonging to the multi-host risk group category. Of them, several single-host bat parasitic species of Notoedres were identified as having the potential to become multi-hosts that are probably capable of causing an epidemic. Our study provides a robust quantitative framework showing how ecological and biological factors can affect the ability of a single-host parasite to become multi-host.
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Mycoplasma spp. are wall-less bacteria able to infect mammals and are classified as hemotropic (hemoplasma) and nonhemotropic. In aquatic mammals, hemoplasma have been reported in California sea lions (Zalophus californianus) and river dolphins (Inia spp.). We investigated Mycoplasma spp. in blood samples of West Indian manatees (Trichechus manatus), pinnipeds (5 species), and marine cetaceans (18 species) that stranded or were undergoing rehabilitation in Brazil during 2002–2022. We detected Mycoplasma in blood of 18/130 (14.8%) cetaceans and 3/18 (16.6%) pinnipeds. All tested manatees were PCR-negative for Mycoplasma. Our findings indicate that >2 different hemoplasma species are circulating in cetaceans. The sequences from pinnipeds were similar to previously described sequences. We also detected a nonhemotropic Mycoplasma in 2 Franciscana dolphins (Pontoporia blainvillei) that might be associated with microscopic lesions. Because certain hemoplasmas can cause disease and death in immunosuppressed mammals, the bacteria could have conservation implications for already endangered aquatic mammals.
Wildlife diseases are a major global threat to biodiversity. Boreal toads ( Anaxyrus [Bufo] boreas ) are a state‐endangered species in the southern Rocky Mountains of Colorado and New Mexico, and a species of concern in Wyoming, largely due to lethal skin infections caused by the amphibian chytrid fungus Batrachochytrium dendrobatidis ( Bd ). We performed conservation and landscape genomic analyses using single nucleotide polymorphisms from double‐digest, restriction site‐associated DNA sequencing in combination with the development of the first boreal toad (and first North American toad) reference genome to investigate population structure, genomic diversity, landscape connectivity and adaptive divergence. Genomic diversity ( π = 0.00034–0.00040) and effective population sizes ( N e = 8.9–38.4) were low, likely due to post‐Pleistocene founder effects and Bd ‐related population crashes over the last three decades. Population structure was also low, likely due to formerly high connectivity among a higher density of geographically proximate populations. Boreal toad gene flow was facilitated by low precipitation, cold minimum temperatures, less tree canopy, low heat load and less urbanization. We found >8X more putatively adaptive loci related to Bd intensity than to all other environmental factors combined, and evidence for genes under selection related to immune response, heart development and regulation and skin function. These data suggest boreal toads in habitats with Bd have experienced stronger selection pressure from disease than from other, broad‐scale environmental variations. These findings can be used by managers to conserve and recover the species through actions including reintroduction and supplementation of populations that have declined due to Bd .
Marine pollution and bacterial disease outbreaks are two closely related dilemmas that impact marine fish production from fisheries and mariculture. Oil, heavy metals, agrochemicals, sewage, medical wastes, plastics, algal blooms, atmospheric pollutants, mariculture-related pollutants, as well as thermal and noise pollution are the most threatening marine pollutants. The release of these pollutants into the marine aquatic environment leads to significant ecological degradation and a range of non-infectious disorders in fish. Marine pollutants trigger numerous fish bacterial diseases by increasing microbial multiplication in the aquatic environment and suppressing fish immune defense mechanisms. The greater part of these microorganisms is naturally occurring in the aquatic environment. Most disease outbreaks are caused by opportunistic bacterial agents that attack stressed fish. Some infections are more serious and occur in the absence of environmental stressors. Gram-negative bacteria are the most frequent causes of these epizootics, while gram-positive bacterial agents rank second on the critical pathogens list. Vibrio spp., Photobacterium damselae subsp. Piscicida, Tenacibaculum maritimum, Edwardsiella spp., Streptococcus spp., Renibacterium salmoninarum, Pseudomonas spp., Aeromonas spp., and Mycobacterium spp. Are the most dangerous pathogens that attack fish in polluted marine aquatic environments. Effective management strategies and stringent regulations are required to prevent or mitigate the impacts of marine pollutants on aquatic animal health. This review will increase stakeholder awareness about marine pollutants and their impacts on aquatic animal health. It will support competent authorities in developing effective management strategies to mitigate marine pollution, promote the sustainability of commercial marine fisheries, and protect aquatic animal health.
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There are 22 species of mesocarnivores (carnivores weighing < 15 kg) belonging to five families that live in rangelands of the western United States. Mesocarnivores are understudied relative to large carnivores but can have significant impacts on ecosystems and human dimensions. In this chapter, we review the current state of knowledge about the biology, ecology, and human interactions of the mesocarnivores that occupy the rangelands of the central and western United States. In these two regions, mesocarnivores may serve as the apex predator in areas where large carnivores no longer occur, and can have profound impacts on endemic prey, disease ecology, and livestock production. Some mesocarnivore species are valued because they are harvested for food and fur, while others are considered nuisance species because they can have negative impacts on ranching. Many mesocarnivores have flexible life history strategies that make them well-suited for future population growth or range expansion as western landscapes change due to rapid human population growth, landscape development, and alterations to ecosystems from climate change; however other mesocarnivores continue to decline. More research on this important guild is needed to understand their role in western working landscapes.
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The current study investigated the scabicidal potential of Egyptian mandarin peel oil (Citrus reticulata Blanco, F. Rutaceae) against sarcoptic mange-in-rabbits. Analysis of the oil's GC–MS identified a total of 20 compounds, accounting for 98.91% of all compounds found. Mandarin peel oil topical application improved all signs of infection, causing a scabicidal effect three days later, whereas in vitro application caused complete mite mortality one day later. In comparison to ivermectin, histopathological analysis showed that the epidermis' inflammatory-infiltration/hyperkeratosis-had disappeared. In addition to TIMP-1, the results of the mRNA gene expression analysis showed upregulation of I-CAM-1-and-KGF and downregulation of ILs-1, 6, 10, VEGF, MMP-9, and MCP-1. The scabies network was constructed and subjected to a comprehensive bioinformatic evaluation. TNF-, IL-1B, and IL-6, the top three hub protein-coding genes, have been identified as key therapeutic targets for scabies. From molecular docking data, compounds 15 and 16 acquired sufficient affinity towards the three screened proteins, particularly both possessing higher affinity towards the IL-6 receptor. Interestingly, it achieved a higher binding energy score than the ligand of the docked protein rather than displaying proper binding interactions like those of the ligand. Meanwhile, geraniol (15) showed the highest affinity towards the GST protein, suggesting its contribution to the acaricidal effect of the extract. The subsequent, MD simulations revealed that geraniol can achieve stable binding inside the binding site of both GST and IL-6. Our findings collectively revealed the scabicidal ability of mandarin peel extract for the first time, paving the way for an efficient, economical, and environmentally friendly herbal alternative for treating rabbits with Sarcoptes mange.
Parasites are thought to provide a selective force capable of promoting genetic variation in natural populations. One rarely considered pathway for this action is via parasite-mediated selection against inbreeding. If parasites impose a fitness cost on their host and the offspring of close relatives have greater susceptibility to parasites due to the increased homozygosity that results from inbreeding, then parasite-mediated mortality may select against inbred individuals. This hypothesis has not yet been tested within a natural vertebrate population. Here we show that relatively inbred Soay sheep (Ovis aries), as assessed by microsatellite heterozygosity, are more susceptible to parasitism by gastrointestinal nematodes, with interactions indicating greatest susceptibility among adult sheep at high population density. During periods of high overwinter mortality on the island of Hirta, St. Kilda, Scotland, highly parasitised individuals were less likely to survive. More inbred individuals were also less likely to survive, which is due to their increased susceptibility to parasitism, because survival was random with respect to inbreeding among sheep that were experimentally cleared of their gastrointestinal parasite burden by anthelminthic treatment. As a consequence of this selection, average microsatellite heterozygosity increases with age in St. Kildan Soay sheep. We suggest that parasite-mediated selection acts to maintain genetic variation in this small island population by removing less heterozygous individuals.