UOA05-01: A novel vaccination strategy to safeguard the Ethiopian wolf from extinction
Submitting Institution
University of OxfordUnit of Assessment
Biological SciencesSummary Impact Type
EnvironmentalResearch Subject Area(s)
Agricultural and Veterinary Sciences: Veterinary Sciences
Medical and Health Sciences: Clinical Sciences
Summary of the impact
The Ethiopian wolf is the most endangered carnivore in Africa. It is
chiefly threatened by rabies outbreaks that occur every 5-10 years with a
mortality rate of up to 77% in affected populations. Dr Claudio
Sillero-Zubiri and colleagues have developed a novel low-coverage
vaccination strategy, now at the heart of a strategic plan to protect this
species from extinction. Containment of rabies through a cordon
sanitaire protects these rare wolves beyond the initial outbreak,
offering a potential model for wildlife disease management elsewhere, and
significant socio-economic and health benefits for the communities living
in and around wolf areas.
Underpinning research
Fewer than 500 Ethiopian wolves survive in six small, isolated, mountain
pockets across Ethiopia, over half in the Bale Mountains. Expanding
agriculture and grazing in the Afroalpine region in which the wolves live
brings them into closer contact with domestic dogs, the main reservoir of
rabies. The risk posed by rabies is amplified by the wolves' social habits
and high density; their small population size makes them vulnerable to
extinction. Researchers at the Wildlife Conservation Research Unit
(WildCRU) at Oxford University's Zoology Department, led by Dr Claudio
Sillero-Zubiri and Professor David Macdonald, have carried out long-term
studies to identify the major threats faced by the wolves, and to
establish the most effective ways to ensure their continued survival.
As part of these long-term studies, Sillero-Zubiri observed that over a
4-month period in the early 1990s, 77% of the largest wolf population in
the Bale Mountains died or disappeared. Rabies (a major threat to wild
canids, and widespread amongst domestic dogs in Ethiopia) was the
suspected cause, and a virus type consistent with dog-associated rabies
was isolated from wolf carcasses. The results of all this research,
published in 1996, provided clear evidence that rabies outbreaks linked to
local domestic dogs were the main threat to the survival of wolves1.
Further research suggested that canine distemper virus might also affect
wolves, and reinforced the need to protect the wolves against diseases
carried by local dogs, of which there are very large numbers2.
Owing to their fragmented distribution, Ethiopian wolves effectively live
on islands in a sea of dogs.
A breakthrough as to how this protection might be achieved was provided
in a paper published in 2002. Sillero-Zubiri and colleagues used
Population Viability Analysis (PVA) modelling to quantify the impact of
rabies outbreaks on wolf populations. Modelling showed that, in the
absence of disease, populations were remarkably stable, but that rabies
epizootics caused extinction probabilities to rise substantially,
particularly in smaller populations. Importantly, the model suggested that
direct vaccination of as few as 20-40% of wolves against rabies might be
sufficient protection from the largest epizootics3. By averting
low population densities, and pack extinctions, this approach would
ameliorate delayed population recovery exacerbated by social constraints
on independent breeding4. This was a new approach to
vaccination: rather than attempting to eliminate the disease altogether
(often impractical in wild populations), targeted vaccination could
curtail the largest and most damaging outbreaks, reducing extinction risk.
Another major rabies outbreak in 2003-04 gave the team an opportunity to
test their vaccination strategy in practice. More than three-quarters
(76%) of wolves in the Web Valley of the Bale Mountains died over a period
of less than 6 months. Just under 40% of surviving wolves in neighbouring
packs were strategically vaccinated in a cordon sanitaire, to
prevent the spread of rabies along the narrow valley `corridors' used by
the wolves; this intervention was successful in halting the spread of the
disease5, 6. Further modelling demonstrated that, even if
carcass detection rates fell as low as 20%, there would be sufficient time
to implement a reactive corridor vaccination campaign triggered by the
detection of two carcasses in a rabies outbreak6.
References to the research
1. Sillero-Zubiri C, King AA, Macdonald DW. (1996) Rabies and mortality
in Ethiopian wolves (Canis simensis). Journal of Wildlife Diseases
32: 80-86. doi: 10.7589/0090-3558-32.1.80 First published evidence
of confirmed deaths from rabies amongst Ethiopian wolves.
2. Laurenson K, Sillero-Zubiri C, Thompson H, Shiferaw F, Thirgood S,
Malcolm J. (1998) Disease as a threat to endangered species: Ethiopian
wolves, domestic dogs and canine pathogens. Animal Conservation 1:
273-280. doi: 10.1111/j.1469-1795.1998.tb00038.x Paper confirming
dog-borne diseases as a major threat to the Ethiopian wolf.
3. Haydon DT, Laurenson MK, Sillero-Zubiri C. (2002) Integrating
epidemiology into population viability analysis: Managing the risk posed
by rabies and canine distemper to the Ethiopian wolf. Conservation Biology
16: 1372-1385. doi: 10.1046/j.1523-1739.2002.00559.x Paper
reporting on the results of computer-based modelling, demonstrating
that rabies vaccination levels of below 40% were likely to be
effective in preventing extinction.
4. Marino J, Sillero-Zubiri C, Johnson PJ, Macdonald DW. (2013) The fall
and rise of Ethiopian wolves: a natural experiment on the regulation of
populations of social carnivores. Animal Conservation doi:
10.1111/acv.12036 Paper reporting wolf population recovery and
social effects on population growth.
5. Randall DA, Williams SD, Kuzmin IV, Rupprecht CE, Tallents LA, Tefera
Z, Argaw K, Shiferaw F, Knobel DL, Sillero-Zubiri C, Laurenson MK. (2004)
Rabies in endangered Ethiopian wolves. Emerging Infectious Diseases 10:
2214-2217. doi: 10.3201/eid1012.040080 Initial report on the
management of the 2003-04 rabies outbreak amongst Ethiopian wolves.
6. Haydon DT, Randall DA, Matthews L, Knobel DL, Tallents LA, Gravenor
MB, Williams SD, Pollinger JP, Cleaveland S, Woolhouse MEJ, Sillero-Zubiri
C, Marino J, Macdonald DW, Laurenson MK. (2006) Low-coverage vaccination
strategies for the conservation of endangered species. Nature 443:
692-695. doi: 10.1038/nature05177 Paper reporting on the successful
implementation of the cordon sanitaire vaccination approach with
<40% of wolves inoculated against rabies during an outbreak.
Funding for research: Research since 1993 has been supported by
~£200,000 a year in grants, primarily from the Born Free Foundation and
the Frankfurt Zoological Society.
Details of the impact
The key contribution of the research led by Sillero-Zubiri has been to
provide robust, detailed evidence of the specific threats facing the
Ethiopian wolf. This evidence has enabled proper strategic planning for
the wolf's conservation and secured funds to implement effective
protection programmes, within which vaccination against rabies has played
the key role.
The first phase of the research documenting the importance of rabies as a
source of mortality in Ethiopian wolves1 catalysed several new
and important conservation actions. It led immediately to the species
being reclassified as Critically Endangered by the IUCN Red List of
Threatened Species7, and resulted in the first Ethiopian wolf
action plan (drawn up by the IUCN/SSC Canid Specialist Group8).
It also led to the establishment of the Ethiopian Wolf Conservation
Programme (EWCP), a science-driven conservation initiative that has gone
on to play a crucial role in the protection of the wolf and its habitat9,10,11.
EWCP implemented a campaign of rabies vaccination in local dogs (later
including canine distemper virus), aiming to inoculate 70% of the dog
population around wolf habitats; since 1996 more than 62,000 dogs have
been vaccinated. Ethiopian wolves had been protected by law since 1974;
due to their rarity the authorities were reluctant to authorize any
management requiring handling or vaccination of the wolves themselves.
Thanks to the compelling evidence provided by the underpinning research
carried out by Sillero-Zubiri and colleagues, immediate funding and
federal permission was forthcoming for the vaccination campaign that
neutralized the 2003 rabies epizootic; vaccination began a mere two weeks
after rabies was identified in the wolf population12.
Confirming the success of this strategy the species was uplisted to
Endangered from Critically Endangered by the IUCN in 20047.
The vaccination approach developed by creating a protective barrier or cordon
sanitaire of vaccinated wolf packs was deployed again in August 2008
when a major rabies outbreak hit the wolves in the Bale Mountains. The
Ethiopian authorities immediately approved an emergency vaccination
campaign, and 98 wolves were vaccinated, using a more refined and
systematic approach than previously, targeting the dominant pair to
preserve breeding units. Vaccination was associated with successfully
containing disease to the original outbreak (Fig 1)10-13.
A consequential impact of the implementation of this research has been on
the local people who co-exist with the wolves. Some 8,500 households with
12,500 dogs live in and around wolf habitats in the Bale Mountains,
largely engaged in subsistence farming and grazing of livestock9,14.
Dogs are essential to local people for herding and also for consuming
human waste, but pose the greatest threat to wolves as vectors of canine
diseases. EWCP's ongoing domestic dog rabies vaccination campaign results
in significant economic and health benefits for local communities12,
which otherwise lose livestock to rabies and are also vulnerable to the
disease themselves. The incidence of rabies in humans in villages where
dogs were not vaccinated was up to five times higher than in villages
where dogs were vaccinated14.
The protection of the Afroalpine ecosystem, part of the Eastern
Afromontane biodiversity hotspot, has increased due to the attention
focussed on the Ethiopian wolf through this research. The efforts of EWCP
and partner Frankfurt Zoological Society have helped to extend the areas
designated as protected areas, with consequent impact for other rare
endemic species. As a result, the amount of suitable wolf habitat that is
protected has increased from 40% in 2000 to 87% in 201115. The
tourism value of the wolf is also important; wildlife tourism in Ethiopia
is increasing, with associated benefits to the Ethiopian economy (most of
the 2,000 people trekking in Bale each year come to see wolves). EWCP
provides other economic benefits through capacity-building and
conservation jobs within the Ethiopian conservation community (for
example, EWCP has funded 8 MSc and 2 PhDs by Ethiopian students). EWCP
employs 36 field staff, of whom 5 work for the Vet team vaccinating dogs
and wolves; 16 wolf monitors and Wolf Ambassadors monitor wolf
populations, in order to ensure a swift response to rabies outbreaks9,15.
As the apex predator in the Ethiopian highlands, the Ethiopian wolf has
an important role as a flagship species for Afroalpine biodiversity:
conservation of the species translates into the protection and maintenance
of habitats and ecological processes. The vaccination strategy developed
by Oxford University researchers has led both to the continued survival of
the wolf as well as associated benefits for local people. There is now a
robust National Action Plan in place for the wolf15, and the
current active level of research, together with the strong partnership of
Ethiopian and international organisations involved, will ensure that
conservation actions can be adapted to changing circumstances. The example
provided by this initiative, of a science-led conservation programme which
delivers timely targeted actions, offers a blue-print to similar
conservation challenges elsewhere16.
Sources to corroborate the impact
- IUCN Red List entry for the Ethiopian wolf, including a history of its
status. The species was reassessed in 2011, and on the basis of response
to vaccination and resulting population recovery, Endangered status was
upheld: http://www.iucnredlist.org/details/3748/0
- Status and species conservation action plan for the Ethiopian wolf,
prepared by the IUCN/SSC Canid Specialist Group in 1997: http://canids.org/PUBLICAT/EWACTPLN/ewaptoc.htm
- EWCP Annual Report (2013). http://www.ethiopianwolf.org/publications/EWCP-Annual-Report-April-2013.pdf
Evidence of community education programmes, wolf vaccination
programmes and new areas under protection.
- Letter from Ethiopia Country Director, Frankfurt Zoological Society
(held on file), confirming the importance of research and
intervention in controlling recent rabies epizootics.
- Letter from Director Born Free Foundation Ethiopia (held on file), confirming
importance of vaccination strategy in containing 2008 & 2009
rabies epizootics.
- Letter from Ethiopia's Chief Veterinary Officer (up to 2011);
currently FAO Director Animal Production & Health Division, Rome
(held on file).
- Letter from Head of Wildlife Zoonoses and Vector-borne Disease Group,
Animal Health and Veterinary Laboratories Agency (AHVLA), UK (held on
file), stating support for vaccination strategies developed in
underpinning research.
- Report on research carried out by Abera Yilma (MSc Diss.) into the
impact of EWCP rabies vaccination of dogs on local people:
http://www.ethiopianwolf.org/publications/JeedalaGazette_july09.pdf
demonstrating no human casualties in wards where vaccination took
place, and lower livestock losses to disease, when compared with
wards without vaccination.
- Strategic Plan for Ethiopian Wolf Conservation, prepared by the
IUCN/SSC Canid Specialist Group in December 2011. http://www.ethiopianwolf.org/SPEWC.pdf
Includes evidence of the scope of dog vaccination campaign, and of
range extension, resulting from research findings.
- Letter from Co-Chair IUCN/SSC Wildlife Health Specialist Group (held
on file), stating opinion that research has enabled a rare success
in veterinary intervention in wildlife conservation.