Parasites & Vectors

Open Access

Review

Wild canids as sentinels of ecological health: a conservation

medicine perspective
A Alonso Aguirre*
Address: Wildlife Trust, 460 West 34th St., 17th Fl, New York, NY 10001, USA
Email: A Alonso Aguirre* - aguirre@wildlifetrust.org
*Corresponding author

from 4th International Canine Vector-Borne Disease Symposium

Seville, Spain. 2628 March 2009
Published: 26 March 2009
Parasites & Vectors 2009, 2(Suppl 1):S7 doi:10.1186/1756-3305-2-S1-S7

This article is available from: http://www.parasitesandvectors.com/content/2/S1/S7

2009 Aguirre; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract
The extinction of species across the globe is accelerating, directly or indirectly due to human
activities. Biological impoverishment, habitat fragmentation, climate change, increasing toxification,
and the rapid global movement of people and other living organisms have worked synergistically to
diminish ecosystem function. This has resulted in unprecedented levels of disease emergence,
driven by human-induced environmental degradation, which poses a threat to the survival and
health of biodiversity.The emerging discipline of conservation medicine addresses these concerns
through the following entities: humans; global climate; habitat destruction and alteration;
biodiversity, including wildlife populations; domestic animals; and pathogens, parasites and
pollutants. Furthermore, conservation medicine focuses on explicit linkages between these entities.
As a crisis discipline, the usefulness of conservation medicine ultimately will depend on its applicability to solving problems.The perspectives and scientific findings of conservation medicine provide
input into biomedical education; and policy and management of ecosystems, habitats and imperiled
species. A sentinel species is one that has presented itself, or has been selected, to provide insight
into the state (health) of an ecosystem, based on user-defined (e.g., researchers, conservationists
or policymakers) objectives (e.g., disease, parasites, toxics, climate change, habitat destruction),
coupled with the utility and vulnerability of this species to the perceived stress. The scientific
information generated by the sentinel species should empower stakeholders and decision-makers
to take mitigative action or support predictive capabilities; the utility of the species selected
should consider its value and relevance to conservationists and to society at large (e.g., education
and outreach; social sciences). Wild canids may serve as excellent sentinel species of emerging
canine vector-borne diseases. Several canine vector-borne diseases or antibodies to these
pathogens have been identified in wild canids including visceral leishmaniosis, Lyme disease,
heartworm, hepatozoonosis and anaplasmosis to name a few.These reports are relatively recent as
they relate to wildlife-domestic animal interactions, globalisation, translocations, habitat fragmentation and climate change. These pathogens and their relationship to wild canids are described
herein. Further research needs to be performed to elucidate the role of the 36 extant species of
wild canids in the epidemiology of canine vector-borne diseases.

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Background
The global loss of biological diversity affects the well
being of both animals and people. Human impact on
ecosystems and ecological processes is well documented.
Habitat destruction and species loss have led to ecosystem
disruptions that include, among other impacts, the
alteration of disease transmission patterns (i.e., emerging
diseases), the accumulation of toxic pollutants and the
invasion of alien species and pathogens [1]. Ecological
perturbations are creating a medium for new disease
patterns and health manifestations. For example, in the
marine environment, new variants of Vibrio cholerae have
been identified within red tide algal blooms. These toxic
blooms are occurring in greater frequency and size
throughout the temperate coastal zones of the world. In
arid zones of the southwestern United States, Brazil and
Argentina, hantavirus epidemics have emerged in
ecosystems that exhibit habitat degradation and climatic
disturbances [2]. These brief examples illustrate our
growing awareness of the interrelationship between
health and the environment. When the natural resilience
of ecosystems is stressed and barriers to disease transmission are reduced the emergence, resurgence and redistribution of infectious diseases are obvious symptoms
of a deteriorating planet. According to the World Health
Organization [3], 30 new diseases have been described in
people including AIDS, Legionnaires disease, and toxic
E. coli infections since the mid 1970s. Diseases like
tuberculosis, temperate-zone malaria, hemorrhagic dengue
fever and diphtheria are also re-emerging as threats.
Anthropogenic change can be considered the primary
factor causing the emergence of infectious diseases
including vector-borne diseases. Global warming, human
population growth, deforestation, globalisation, wildlife
trade and pollution of oceans and freshwater bodies may
have an impact on the prevalence and distribution of
infectious pathogens. The dynamics of disease emergence
from wildlife are complex and bring human and domestic
animal populations into increasing contact with wild
animals potentially infecting wildlife with new pathogens
causing high mortality, decline and even local extinctions.
In some cases, wildlife will survive infection and will
become reservoirs. As human populations continue to
augment exponentially and globalisation is imminent
with increased travel and trade, these anthropogenic
pressures on wildlife habitat and populations also will
increase. The result can be predicted as a continuing
spillover of new pathogens shared among wildlife,
domestic animals and humans [4,5].

Conservation medicine: ecological health in

practice
Conservation medicine studies the two-way interactions
between pathogens and disease on the one hand, and

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species and ecosystems on the other. It focuses on the

study of the ecological context of health and the
remediation of ecological health problems. In response to
the growing health implications of environmental
degradation, conservation medicine purview includes
examining the linkages among a) changes in habitat
structure and land use; b) emergence and re-emergence of
infectious agents, parasites and environmental contaminants; c) maintenance of biodiversity and ecosystem
functions as they sustain the health of plant and animal
communities including humans. Conservation medicine
is concerned with the effects of disease on rare or
endangered species and on the functioning of ecosystems.
It is also concerned with the impacts of changes in species
diversity or rarity on disease maintenance and
transmission. The dynamic balance that we term health
is viewed on a series of widely varying spatial scales by
many disciplines including human and public health,
epidemiology, veterinary medicine, toxicology, ecology
and conservation biology. Conservation medicine
represents an approach that bridges these disciplines to
examine health of individuals, groups of individuals,
populations, communities, ecosystems and the landscapes in which they live as an indivisible continuum, it
is truly a transdiscipline. By reaching out to multiple
disciplines, conservation medicine provides new skills,
tools and vision to the field of both conservation biology
and medicine. This includes bringing biomedical research
and diagnostic resources to address conservation problems, e.g., development of new non-invasive health
monitoring techniques; training veterinarians, physicians
and conservation biologists in the promotion and
practice of ecological health; and by establishing transdisciplinary teams of health and ecological professionals
to assess and address ecological health problems [4-7].
The ecological impacts of humans can ripple throughout
ecological communities. The demise of one species, or the
rise of one species at the expense of another may establish
a trophic cascade of ecological responses. When predatorprey or species competition relationships are disrupted,
ecological impacts may extend beyond the predator and
prey or the competitors [8-10]. The spread of Lyme
disease as a result of the changing ecology of white-tailed
deer (Odocoileus virginianus) and white-footed mice
(Peromyscus leucopus) in a landscape devoid of large
predators and diminished biodiversity is a good example
of ecological magnification of disease. Until recently we
are beginning to understand the dilution effect as
empirical evidence that host diversity decreases infection
and transmission of infectious diseases [11].
Conservation medicine receives input from both the
social sciences and bioinformatics. Fields such as
sociology, economics and anthropology inform the

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science and the practice of conservation medicine by

revealing potential causes of human behaviour relevant to
human-induced environmental change. Top-down
approaches to wildlife management are being replaced by
adaptive management strategies that reflect uncertainty
and complexity. These new management techniques are
necessary to further develop the field. Bioinformatics and
the creation, management and dissemination of databases relevant to wildlife, their habitats and their diseases
may be crucial to this new discipline.
Global climate change and disease emergence
Climate change is one of the most pressing ecological
health concerns today. By all scientific evidence climate
change is a reality. The health consequences are pervasive.
The effects of climate change in promoting the spread of
infectious disease from more tropical ranges to temperate
areas are being observed in such diseases as malaria and
dengue fever [2,9,12]. The impact of climate change on all
ecological processes is profound: increased precipitation
in some regions and drought in others; increased erosion
of the coastal zone with rising sea levels; and the inability
of many species to adapt to the relatively rapid changes in
climatic regimes potentially resulting in mass extinctions
[13,14]. Changes in atmospheric volatilisation and
deposition of pollutants are of equal concern. The
impacts of climate change on biodiversity are still
underestimated. Up to 37% of over 1,000 animal and
plant species in six regions of the planet are at risk of
extinction from climate change. Several scenarios produce
projections of species committed to extinction of 18%
(minimal climate-warming), 24% (mid-range warming)
and 35% (maximum-warming) [15,16]. A more recent
example described by Rausch et al. [17] hypothesized that
retreating sea ice is changing the feeding behavior of
pagophilic pinnipeds such as the walrus (Odobenus
rosmarus) with a usual diet of benthic invertebrates
inhabiting coastal waters to a depth of approximately
100 m now shifting to a more pelagic diet including ring
seals (Pusa hispida) due to the retreating ice substrate, thus
inducing to modification of the helminth fauna. A higher
prevalence of trichinellosis caused by Trichinella spiralis
has been observed with a huge zoonotic potential to
indigenous peoples feeding on these pinnipeds.
Trichinellosis is widespread worldwide with a generally
low prevalence and restricted to specific areas in Europe.
Low intensity infections occur in wildlife (wild boar, red
fox, raccoon dog, polar bear, rodents), keeping alive the
risk of infection to humans [18].

Current evidence suggests that inter-annual and interdecadal climate variability have a direct influence on the
epidemiology of vector-borne diseases. Opportunists that
multiply rapidly such as insects, rodents and microorganisms colonize stressed environments at higher rates.

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Because they are sensitive to climate, the distribution and

number of vectors are also affected by climate change.
According to the IPCC 2007 Climate Change Report
(http://www.ipcc.ch/), climate change has already altered
the distribution of some disease vectors. There is evidence
that the geographic range of ticks and mosquitoes that
carry disease has changed in response to climate change.
Tick and mosquito vectors have extended their range
North in Sweden and Canada and into higher altitudes in
other countries worldwide. While future climate change is
expected to continue to alter the distribution of disease
vectors, it is important to recognize that there are several
other factors (such as changes in land use, population
density and human behavior) that can also change the
distribution of disease vectors as well as the extent of
infection.
Climate is closely associated with the natural history of
vectors so warmer temperatures will increase their range
and distribution including altitudinal gradients. Ixodes
pacificus is the main tick vector for transmission of
Anaplasma phagocytophilum and Borrelia burgdorferi to large
vertebrates in California. A recent study examined spatial
and temporal relationships among A. phagocytophilumand B. burgdorferi-exposed coyotes (Canis latrans) with
vegetation type and climate. The overall seroprevalences
were 39.5% and 18.9%, respectively. Increased seroprevalence was a positive function of rainfall [19].
Vector-borne diseases: a threat to human health and
conservation
The role of emerging vector-borne diseases on global
health cannot be underestimated within the context of
conservation medicine. Parasitic vector-borne diseases are
classical emerging infectious diseases in human populations such as leishmaniosis, Lyme disease and
ehrlichiosis among others. Eukaryotic parasites are
among the most significant agents of emerging diseases of
wildlife and domestic animals [20]. Parasites are part of
biological diversity; however, pathogenic species may
pose a threat to conservation of their natural hosts or of
new species of hosts. A striking example cited is translocation of animals from their natural habitat to another
habitat or to a different region of the world when their
parasite fauna are also exposed to new species of hosts. In
fact, when the new hosts become infected with these
novel parasites, the pathogenicity and epidemiology of
the infection become unpredictable. The introduction of
a parasite to a new environment may or may not affect
population density of the host, but runs the risk of
introducing non-indigenous parasitic infections [18].

Vector-borne diseases of wildlife have implications for

wildlife conservation, for evaluating wildlife-domestic
interactions, and for determining their public health

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significance. Both parasite and host adapt to one another

in a mutual co-existence [21]. When a population of freeranging wildlife is exposed to an emerging infectious or
parasitic disease the response of the host might be to
(a) resist the parasite, (b) develop severe clinical
parasitism or (c) adapt to the new parasite and become a
carrier. The source of exposure may be from: (1) domestic
animals, (2) re-introduction of wild animals (raised in
captive propagation programmes) and/or (3) the spread
of a related species in new habitats [18].
Cross-species transmission
The importance of parasites in wild mammals and their
association with domestic animals and humans cannot
be overemphasised. Forrester [22] reported that 119
parasites and infectious diseases were interchangeable
between wild and domestic mammals in Florida. From
these, more than 46% were helminths (45 nematodes,
five cestodes, four trematodes and one acanthocephalan)
when wild and domestic swine were included. In
addition, 10% (seven nematodes, four cestodes and one
trematode) were considered zoonotic.

The movement of wild animals can also introduce exotic

diseases into the native population and conversely, can
expose translocated animals to diseases for which they
have not developed resistance. Several species are
susceptible to diseases of domestic animals and humans.
The possibilities of transmission are potentially high
during capture, transport and release. Emerging parasites
in new hosts are becoming more evident as diagnostic
techniques are refined, wildlife-human-domestic animal
interactions increase and new diseases are identified [18].
The threat of disease transmission from domestic animals
to wildlife has become recognised as an increasing
concern within the conservation community in recent
years. Domestic dogs pose a significant risk as reservoirs
for infectious diseases, especially for wild canids. As
human populations expand into wild habitats with their
pets and livestock the greater the risk of emerging
infections reaching rare species or vice versa. Population
density represents a disease risk in these situations where
feral dogs have established large packs. Dogs may exist in
very high densities, so where infection was once sporadic
it may turn potentially into an epidemic that in the right
circumstances may spillover to wild populations [23]. A
classical example is the devastating outbreak of canine
distemper in Serengeti lions (Panthera leo). It was
estimated that the disease killed over 1000 lions, a third
of the Serengeti population, before spreading North
across the border in the Masai Mara National Reserve in
Kenya by August 1994, with a neurologic syndrome. Over
85% of the surviving Serengeti lions were found with
anti-CDV antibodies. Also, uncounted hyaenas, bat-eared

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foxes and leopards were also affected [24]. Speculation

exists on how this outbreak was initiated, as village dogs
rarely get sufficiently close to a lion to pass on the virus,
and there are likely other reservoir hosts. Spotted hyaenas
(Crocuta crocuta) are probably the final link in the chain,
because they mix with lions at the kill [23-25]. Canine
distemper may have played a part in the extinction of the
marsupial wolf Thylacinus spp. in the early 20th century,
and it pushed the black-footed ferret (Mustela nigripes) of
North America to the brink of extinction in the 1970s
[23,26]. During the early 1990s rabies claimed more than
half of the Ethiopian wolves (Canis simensis) in the Bale
Mountain National Park. Rabies was also responsible for
the death of African wild dogs (Lycaon pictus) in the Masai
Mara reserve in Kenya in 1989 and in the Serengeti in
1990 [27].
An assessment of which pathogens might pose a problem
and their patterns of infection in natural hosts is
necessary with increasing awareness of disease as an endangering process. The exposure of sympatric Ethiopian
wolves and domestic dogs to canine distemper virus
(CDV), canine adenovirus (CAV) and canine parvovirus
(CPV) in the Bale region, Ethiopia, has been documented
[28]. The wolf population in the region declined in the
late 1980s and early 1990s, with rabies responsible for a
dramatic population reduction between 1990 and 1992.
Although the population declined further up until 1995,
it is not possible to assess whether the concurrent canine
distemper epidemic in park dogs also affected wolves.
Nevertheless, with evidence of rabies, CDV, CAV and CPV
infections in sympatric domestic dogs and Ethiopian
wolves, canid diseases clearly pose a significant threat to the
future persistence of this Ethiopian wolf population [28].

Vector-borne diseases and wild canids

Canine vector-borne diseases are emerging and reemerging following global patterns. For example,
leishmaniosis in the Americas caused by Leishmania
braziliensis has been highly correlated to deforestation and
human penetration. Previously considered an exotic
disease, canine leishmaniosis caused by Leishmania
infantum has recently been detected within the foxhound
population in the United States and parts of Canada. The
following sections describe selected canine vector-borne
diseases and their relationship to wild canid species as
reported in the literature and their imminent emergence
across continents. Diseases are described in alphabetical
order for practical purposes.
Anaplasmosis
Anaplasma phagocytophilum (formerly Ehrlichia phagocytophila, Ehrlichia equi and Anaplasma phagocytophila) is the
causative agent of granulocytic ehrlichiosis (anaplasmosis) in humans, horses, sheep, cattle, dogs and cats.

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Over 450 European sheep ticks (Ixodes ricinus) collected

from 100 red foxes (Vulpes vulpes) in Hungary were tested
for the pathogen as 112 pools each containing five or
fewer ticks from one fox. Six foxes were found infected in
the PCR-based test [29]. The epidemiological consequences of these findings are unknown.
Babesiosis
Young coyotes (Canis latrans) were experimentally infected
with Babesia gibsoni developing pale mucous membranes,
splenomegaly and a positive haeme reaction in urine. One
of the coyotes exhibited mild depression and anorexia.
The mild clinical signs coupled with the high level and
long duration of parasitemia indicated that coyotes could
serve as reservoirs of this emerging disease [30].
Bartonellosis
Bartonella vinsonii subsp. berkhoffii was originally isolated
from a dog with infectious endocarditis and was recently
identified as a zoonotic agent causing human endocarditis. An epidemiological study was conducted following a child bitten by a coyote who developed clinical signs
compatible with Bartonella infection in California. Among
109 coyotes from central coastal California, 31 animals
(28%) were found to be bacteremic with B. vinsonii subsp.
berkhoffii and 83 animals (76%) presented antibodies.
These findings suggest these animals could be the
wildlife reservoir. Further studies are necessary to
elucidate the mode of transmission especially to identify
potential vectors and to determine how humans become
infected [31].
Borreliosis
Different Borrelia species and serotypes were tested for
their sensitivity to serum complement from various
animals and humans; and wolves were identified as a
probable reservoir in nature [32]. Seven of 100 skin
samples of red foxes (Vulpes vulpes) were tested positive
for B. burgdorferi in Brandenburg, Germany [33]. A new
species denominated Candidatus B. texasensis was isolated
in 1998 from an adult male Dermacentor variabilis tick
feeding on a coyote from Texas, characterised with several
molecular techniques, but isolation attempts were not
fruitful [34]. Coyotes have been previously used as
sentinels of Lyme disease to correlate with infection in
humans in the USA. One thousand canine sera (917 dogs,
83 coyotes) obtained from field personnel were screened
with an ELISA test and results were validated by Western
blot and indirect fluorescent antibody (IFA) tests at
reference laboratories. A total of 22/1000 canines were
confirmed serologically positive (21 dogs and 1 coyote;
seroprevalence 2.3% and 1.2%, respectively). The low
prevalence of seropositivity in sentinel canines suggests
the Lyme disease hazard is minimal in San Diego,
California [35].

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Canine heartworm
Canine heartworm caused by Dirofilaria immitis affects
wild canids and may be a factor impacting the health and
population dynamics of coyotes. Coyotes may serve also
as a potential reservoir for transmission of these parasites
to domestic dogs. Almost a 1000 coyotes were surveyed in
Illinois for the presence of heartworm identifying a statewide prevalence of 16%. The authors concluded that
heartworm disease is only a minor factor influencing
coyote population dynamics in Illinois and possesses
perhaps low risk to the domestic canine population [36].
Dirofilaria immitis
As part of a multifaceted ecologic study of maned wolves
(Chrysocyon brachyurus) and other canids in the large,
remote Noel Kempff Mercado National Park in northeastern Bolivia, 40 domestic dogs in two villages and at two
smaller settlements bordering the national park were
sampled for exposure to canine diseases. High levels of
exposure were found to CDV and CPV, both of which are
known to cause mortality in maned wolves and other
carnivores. Moderate to high levels of exposure were found
to rabies virus, E. canis, and Toxoplasma gondii, as well as
significant levels of infection with D. immitis. This study
reports evidence of exposure to several diseases in the
domestic dogs bordering the park. Contact between wild
carnivores and dogs has been documented in the sampled
villages, therefore dogs likely pose a substantial risk to the
carnivores within and near the park. Further measures
should be undertaken to decrease the risk of spillover
infection from domestic animals into the wild species of
this region [37]. Maned wolves are neotropic canids, listed
as a CITES Appendix II species, with a distribution in
Argentina, Brazil, Bolivia and Paraguay. Primary threats to
the survival of free-ranging wolves include habitat loss,
road kills and shooting by farmers. An additional threat is
the risk of morbidity and mortality due to infectious and
parasitic diseases [37]. It has been documented that captive
maned wolves are susceptible to, and die from, common
infectious diseases of domestic dogs including CDV, CPV,
rabies virus and CAV. A survey documenting these agents
indicated that free-ranging wolves in the same park in
Bolivia have been exposed to multiple infectious and
parasitic agents of domestic carnivores, including the
viruses previously mentioned, canine coronavirus, rabies
virus, Leptospira interrogans spp., T. gondii and D. immitis,
and may be at increased disease risk due to these pathogens
originating in the domestic dog population [38].
Canine Ehrlichiosis
A seroepidemiological survey was conducted to investigate the prevalence of antibodies reactive with the
Ehrlichia canis and E. phagocytophila (newly named
Anaplasma phagocytophilum) genogroup antigens, and the
spotted-fever group rickettsiae antigens in jackals (Canis

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aureus syriacus) in Israel, to assess the possible role of this

species in the epidemiology of these diseases. A total of
53 serum samples were tested and antibodies were detected
in 36% to E. canis, 26% were positive to E. chaffeensis. In
addition, 26% were seropositive to E. phagocytophila [39].
In another study performed in coyotes from California, a
total of 68/149 (46%) samples were seropositive to
E. equi, two (1%) to E. risticii (newly named Neorickettsia
risticii) and none of the samples had antibodies reactive to
E. canis demonstrating that coyotes have been exposed to
granulocytic ehrlichiae and E. risticii and may play a role in
the epidemiology of these ehrlichial agents in California
[40]. Red foxes and grey foxes (Urocyon cinereoargenteus)
were evaluated for their susceptibility to experimental
infection with E. chaffeensis, the causative agent of human
monocytotropic ehrlichiosis [41]. The results imply that
red foxes, but not grey foxes, are potential vertebrate
reservoirs illustrating the need to verify serologic evidence
of E. chaffeensis infection among wild animals.
Canine visceral leishmaniosis (CVL)
CVL has been recently documented in wild canids in
endemic regions of Europe. Pathologic and parasitologic
analysis of a grey wolf (Canis lupus) found dead and
confirmed by PCR, indicated that lesions associated with
infection by L. infantum were typical for CVL commonly
described in dogs [42]. A serologic survey of captive
wolves in southwestern Europe determined that three of
33 wolves (9%) presented low levels of antibodies to L.
infantum infection using an ELISA test [43]. An
epizootiological survey of leishmaniosis in 67 foxes
(Vulpes vulpes) was conducted in Guadalajara, Spain,
identifying a prevalence of 74% positives determined by
molecular methods [44].

Visceral leishmaniosis occurs in many parts of the world

and dogs are considered a major reservoir host for human
infections. Human visceral leishmaniosis has recently
emerged as an opportunistic infection among individuals
co-infected with HIV/AIDS and in persons taking
immunosuppressive drugs. Royspal et al. [45] reported 3
naturally infected foxhounds from Virginia by culture.
The disease has been documented extensively in Brazil.
Among 15 captive canids from a zoo in Belo Horizonte,
Minas Gerais, Brazil, two animals, a bush dog (Spheotos
venaticos) and a hoary fox (Lycalopex vetulus), were
serologically positive and developed clinical signs of CVL,
whereas three other canids, including a crab-eating fox
(Cerdocyon thous), a maned wolf and a hoary fox had
positive serological results without clinical signs [46].
During 1999-2003 parasitology and serology tests were
performed in domestic dogs (n = 1568), wild jackals
(Canis aureus, n = 10), red foxes (n = 10) and wolves (n =
10) in Iran demonstrating that 10% of wild canids were
infected by L. infantum. Ten out of 11 Leishmania spp.

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isolated from dogs and wild canines were identified as L.

infantum and one other as L. tropica by molecular and
biochemical techniques [47].
Hepatozoonosis
The first PCR detection of Hepatozoon canis in a naturally
infected red fox from Slovakia, a Rhipicephalus sanguineusfree region, was recently performed [48]. It is believed
that the infection was spread by infected R. sanguineus
that might have been brought to Slovakia by travellers,
golden jackals, or foxes migrating because of expansion of
golden jackals and environmental and climate changes. A
seroepidemiological survey was conducted to investigate
the prevalence of antibodies reactive with E. canis and
H. canis antigens in free-ranging red foxes in Israel. Of 84
fox sera assayed, 36% were seropositive for E. canis by IFA
test and 24% were positive using the ELISA test. Canine
ehrlichiosis and hepatozoonosis appear to be endemic in
the wild red fox populations in Israel, and foxes may serve
as a reservoir for infection of domestic dogs and other
wild canine species [49].

Wild canids as sentinels of ecological health

The canidae family includes 16 recent genera distributed
in most land masses of the world. Nine of the 36 canid
taxa are threatened: Darwins fox, island fox and red wolf
are listed as Critically Endangered, while Ethiopian wolf,
African wild dog and dhole (Cuon aplinus) are endangered. Others are rare and even declining, while many
wild canids like coyotes are common, therefore they are
involved in major wildlife management issues (such as
disease transmission, predation on livestock, sport
hunting, fur trade). Many wild canid species may serve as
sentinels of ecological health as they may be critical to
proactively identify potentially pathogenic emerging
canine vector-borne diseases parasites.
Sentinel species are the proverbial canaries in the mine
shaft. They serve as indicators of their environment and
may reflect the quality of health in their ecosystems. The
scientific information generated by the sentinel species
should empower stakeholders to take mitigative action or
support predictive capabilities. The utility of the species
selected should consider its value and relevance to
decision makers, conservationists and to society at large.
Assessing the health an ecosystem will require of a suite
of sentinel species including different trophic levels,
ecological roles, taxa and different spatial/temporal
scales. It will require conservation medicine teams to
apply transdisciplinary efforts. It will require the
involvement of decision makers and the general public to
change our behaviour towards the planet [50,51].
Sentinel species may assist in increasing monitoring
efficiency at the ecosystem level. They can be utilised

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during rapid risk assessments to provide information on

the environmental conditions of an area during an
emerging parasitic disease outbreak. Sentinel species or
health indicator species can be selected for their ability to
reflect environmental perturbations. Based on their life
history and physiological attributes, selected species can
provide insightful information about environmental
changes at various spatial, temporal and trophic scales.
Given the complexity of ecosystems, sentinel species
should be thought of as being specific to particular
environmental conditions during a pandemic. In some
cases, an assemblage of species may be suitable for providing a umbrella effect in monitoring the cumulative
impacts of multiple environmental variables that create
the complexity of an emerging canine vector-borne
disease [50,51].
On the one hand, wild canid populations may suffer
severe epizootics and declines related to domestic dog
diseases; on the other hand, there are species like jackals,
coyotes and foxes that are highly adaptable to ecosystems
and human-impacted environments and are reservoirs of
several diseases of zoonotic or domestic animal importance including rabies, parvovirus infection, canine
distemper and mange. These species are ideal to monitor
vector-borne diseases. In addition, wild caninds adapted
to the human condition host innumerable parasites,
bacteria and viruses, which in turn may contribute to
density-dependent mortality. By increasing wildlifedomestic animal interactions the potential of spread of
disease to domestic dog populations is real [25,52].
Further research is necessary to identify wild reservoirs,
susceptible hosts and zoonotic interactions for all canine
vector-borne diseases at a global level and to establish
protective measures to dwindling wild canid populations
such as wolves to ensure their long-term survival.

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Competing interests
The author declares that they have no competing interests.

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Acknowledgements

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I am grateful to N. Rossi for acquisition of data and literature review. This

article was possible with the funding of V. Kann Rasmuen Foundation,
Overbrook Foundation, MarIsla Foundation and Tamarind Foundation.
This article is published as part of Parasites & Vectors Volume 2 Supplement
1, 2009: Proceedings of the 4th International Canine Vector-Borne Disease
Symposium. The full contents of the supplement are available online at
http://www.parasitesandvectors.com/supplements/2/S1.

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Publication of the supplement has been sponsored by Bayer Animal Health

GmbH.
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