The SAVE Project: Saving Asia's Vultures from Extinction
Submitting InstitutionUniversity of Cambridge
Unit of AssessmentBiological Sciences
Summary Impact TypeEnvironmental
Research Subject Area(s)
Environmental Sciences: Environmental Science and Management
Biological Sciences: Ecology
Summary of the impact
Research from the Department of Zoology has been instrumental in
identifying residues of the veterinary painkiller diclofenac in cattle
carcasses as responsible for catastrophic declines in vulture populations
across the Indian subcontinent. As a result, the drug has been banned for
veterinary use in the relevant countries, and an international
conservation effort (SAVE) to Save Asia's Vultures from Extinction has
been set up. Declines have since slowed, captive breeding programmes have
been introduced, and local people have been trained in monitoring work and
advocacy. There has also been inter-government collaboration to support
conservation efforts, the first example of such collaboration on the
Professor Rhys Green is an RSPB Principal Research Biologist, fully
embedded in the Conservation Science Group in the Department of Zoology
where he is an Honorary Professor (since 1999). He spends 100% of his
non-fieldwork time in the Department and was returned as Category C in the
2008 RAE. Since 2004, a substantial part of his research has focused on
vulture conservation in the Indian subcontinent, in conjunction with other
scientists and government and non-government conservation agencies in the
region and in several other countries.
Since the early 1990s, populations of three vulture species in the Indian
subcontinent have decreased by more than 97%, one of the most rapid and
sustained declines of a bird species ever documented. In 2000, the World
Conservation Union (IUCN) listed all three species as `Critically
Endangered', the highest category of endangerment, indicating a high risk
of global extinction in the wild in the short term. These vultures, of the
genus Gyps, are obligate scavengers on dead vertebrate carcasses,
and in India their food is mostly domesticated ungulates. In 2004 a team
of American and Pakistani researchers discovered that the widely-used
veterinary anti-inflammatory drug diclofenac was the major cause of
observed mortality in one of the three species in Pakistan. Diclofenac
causes kidney failure, accumulation of uric acid (gout) and death when
vultures eat the carcass of a recently-treated animal.
In the early 2000's, Green and co-workers found that a high proportion of
dead vultures of two of the species across a large area of India, Pakistan
and Nepal tested positive for diclofenac residues and had evidence of
visceral gout1. This finding indicated that diclofenac was the
likely cause of the rapid population declines in all three species of
vultures across the entire subcontinent (the 2004 study mentioned above
took place in a single province of Pakistan, and on one species only).
Green then led work to develop a demographic model based on this data,
which demonstrated that even very low rates of diclofenac contamination
(0.13-0.76% of ungulate carcasses available to foraging vultures) would be
sufficient to have caused observed population declines, given its high
toxicity to vultures2. Data collected by the group validated
the model and showed that diclofenac-caused mortality was theoretically
sufficient to account for the observed vulture declines2 across
the affected areas.
Measurement of diclofenac concentration in tissues of treated cattle and
an experiment on captive vultures enabled Green and colleagues to
construct a model to define the period after treatment that cattle tissues
remained toxic to vultures, which was found to be a few days3;
this work had implications for conservation projects (both captive
breeding and supplementary feeding programmes), as it demonstrated
vultures should only be fed on carcasses of animals that had not been
dosed with diclofenac in the week prior to death.
Green and colleagues also surveyed the concentrations of diclofenac in
carcasses of domesticated ungulates in India, and determined that these
were sufficient to have caused vulture declines at the observed rates
without the involvement of any other factor4, thus confirming
the earlier model in practice. In addition, the results provided a basis
for estimating vulture population responses to changes in the prevalence
of diclofenac in ungulate carcasses; the effectiveness of the Indian ban
could therefore be monitored. Follow-up surveys showed a decline in
diclofenac contamination of cattle carcasses after the ban5.
Vulture population surveys in India and Nepal were carried out in 2011,
finding that whilst numbers of vultures remained low, the decline had
slowed, and may have reversed for one of the three species.
The very widespread veterinary use of diclofenac in the region meant that
compliance with the ban, and subsequent impact on vulture numbers, would
only occur if a comparative alternative (in terms of cost, effectiveness
and availability) existed and this was non-toxic to vultures. In 2006,
Green and colleagues in collaboration with the University of Pretoria and
others in South Africa and Namibia determined that the alternative drug
meloxicam, also out of patent, was non-toxic for related African vultures6;
follow-up tests demonstrated it was also safe for the endangered Indian
References to the research
1. Susanne Shultz, Hem Sagar Baral, Sheonaidh Charman, Andrew A.
Cunningham, Devojit Das, G. R. Ghalsasi, Mallikarjun S. Goudar, Rhys E.
Green*, Ainsley Jones, Prashant Nighot, Deborah J. Pain and Vibhu Prakash
(2004) Diclofenac poisoning is widespread in declining vulture populations
across the Indian subcontinent. Proc. R. Soc. Lond. B vol. 271 no. Suppl 6
S458-S460. doi: 10.1098/rsbl.2004.0223
2. Green RE, Newton I, Schultz S, Cunningham AA, Gilbert M, Pain DJ and
Prakash V (2004). Diclofenac poisoning as a cause of vulture population
declines across the Indian subcontinent. J Appl Ecol 41, 793-800. doi:
3. Green RE, Taggart MA, Das D, Pain DJ, Kumar S, Cunningham AC and
Cuthbert R (2006). Collapse of Asian vulture populations: risk of
mortality from residues of the veterinary drug diclofenac in carcasses of
treated cattle. J Appl Ecol 43, 949-956. Doi: 10.1111/j.1365-
4. Green RE, Taggart MA, Senacha KR, Raghavan B, Pain DJ, et al (2007)
Rate of Decline of the Oriental White-Backed Vulture Population in India
Estimated from a Survey of Diclofenac Residues in Carcasses of Ungulates.
PLoS ONE 2(8): e686. doi:10.1371/journal.pone.0000686
5. Cuthbert, R., Taggart, M.A., Prakash, V., Saini, M., Swarup, D.,
Upreti, S., Mateo, R., Chakraborty, S.S., Deori, P. & Green, R.E.
(2011) Effectiveness of Action in India to Reduce Exposure of Gyps
Vultures to the Toxic Veterinary Drug Diclofenac. PLoS ONE 6(5): e19069.
6. Swan G.E., Cuthbert R, Quevedo, M., Green R.E., Pain, D.J., Bartels
P., Cunningham, A.A., Duncan N., Meharg A.A., Oaks J.L., Parry-Jones J.,
Shultz S., Taggart M.A., Verdoorn G., Wolter, K.. (2006). Toxicity of
diclofenac to Gyps vultures. Biology Letters 2, 279-28
Details of the impact
Impacts on public policy and services, impacts on international
As a result of the research and allied studies, in 2006 the governments
of India, Nepal and Pakistan banned the manufacture and importation of
diclofenac for veterinary use, citing the toxicity of diclofenac to
vultures and the evidence of its effect on their populations7.
However, diclofenac came off patent in the 1990s, and by 2006 many
companies in India were manufacturing the drug for human and veterinary
use. The drug continues to be legal for human use and human diclofenac is
also used illegally on animals. As a result, the immediate impact on the
ban on levels of contamination of vulture food and vulture population
trends was limited. With the evidence from Green and colleagues that
diclofenac was still being used for veterinary purposes up to 2008 (Ref 4,
section 3), the Indian Government strengthened the ban by making it an
imprisonable offence to import, manufacture, retail or use diclofenac for
veterinary purposes. Human diclofenac also had to be labelled `not for
veterinary use'8. In 2010, the Government of Bangladesh banned
veterinary formulations of diclofenac, bringing it into line with
In May 2012, the governments of Bangladesh, India, Nepal and Pakistan
made a regional declaration on vulture conservation, with recommendations
based upon the work of Saving Asian Vultures from Extinction (SAVE), which
Green was instrumental in setting up (see below)9:
"Further commending the activities of SAVE and its members for their
notable contribution to vulture conservation in the region...
...Removing diclofenic and other toxic NSAIDs completely from the
vulture food chain, through measures including enhanced enforcement on
the ban on veterinary use of diclofenic."
The International Union for the Conservation of Nature (IUCN) is
co-ordinating collaboration among the governments through a Regional
Steering Committee. Such inter-governmental collaborations on bird
conservation are rare globally, and this is the first of its kind for the
Impacts on the environment, impacts on animal health and welfare
Continued monitoring of vulture numbers across the region (which Green is
involved in) has demonstrated that declines have slowed, and may even have
reversed for one species13. As this result is based on changes
to underlying survival rates and breeding success, it indicates that both
of these have increased rapidly (Green's modelling work supports the
partial removal of diclofenac from the birds' food supply as being the
sole cause of any slowing in decline5 above).
In 2011 an international consortium of conservation agencies, `Saving
Asia's Vultures from Extinction' (SAVE) was set up10. Green was
one of the founders of SAVE and is chair of its Technical Advisory
Committee. SAVE partners jointly manage a captive breeding programme in
India, Nepal and Pakistan, with associated research into improving captive
bird husbandry, and this programme is approved by the Government of
India's Central Zoo Authority. All three vulture species have now been
bred in captivity, with reintroductions of captive-bred birds scheduled to
begin within five years. Husbandry guidelines11 have also been
produced to improve the welfare of captive birds and the success rates of
breeding programmes; prior to the documented decline, no captive breeding
programmes existed and most captive vultures were held only in zoos.
Impacts on society, culture and creativity
SAVE is developing `vulture safe zones' in which local advocacy is
combined with training of local people in monitoring vulture populations
and the availability of veterinary drugs, and in undertaking studies of
vulture ranging behaviour using GPS PTT tagging. In some cases, ecotourist
projects have been linked with vulture safe zones12, raising
awareness, and providing additional income for local people.
Impacts on human health
Vultures provide a valuable ecosystem service: the breakdown of ungulate
carcasses. Their loss provides more food for other scavengers, notably
wild dogs, whose population in the region increased markedly with the
decline in vulture population. This in turn increases the number of dog
bites with the consequent possible transfer of rabies. An analysis by
Markanda et al16 estimates the monetised heath cost in
India of the decline of vultures over the period 1992 to 2006 as
approximately 1 trillion Rs (approx. £9 billion) with the cost more
heavily felt at the end of the period. While the as yet small recovery in
the vulture population has not yet eliminated this cost, it has slowed its
increase (and may now be reversing it).
Impacts on commerce - companies are producing a new product
Carcass monitoring has shown that meloxicam is starting to replace
diclofenac for veterinary use5 above, and work is underway to
improve the formulation of veterinary meloxicam used by Indian companies
to make it more acceptable to veterinarians and to assess the feasibility
of a government subsidy to encourage its use. In 2004, only one Indian
drug company was producing meloxicam. By 2011, this had increased to
Boehringer-Ingelheim (B-I), the company that developed meloxicam, have
donated the expertise of a technical expert on drug formulation and
manufacture to assist Indian companies to produce better formulations of
the drug and have made details of an improved formulation freely available
(meloxicam is out of patent, so B-I does not gain commercially from this).
The company has also funded some of the advocacy work that underpins the
vulture safe zones (see above)15.
Sources to corroborate the impact
- Indian Government Directive: http://save-vultures.org/Documents/06_05__DCGI_Diclofenac_Order.pdf"
- Additions to the 2006 ban in India: http://save-vultures.org/save_solution_advocasyprgramme.html
- Regional Declaration on the Conservation of South Asia's Critically
Endangered Vulture species: www.save-vultures.org/Documents/12%2005%20Regional%20Declaration%20on%20Vulture%20Conservation%20(Delhi).pdf"
- Saving Asia's Vultures from Extinction (SAVE): www.save-vultures.org
- Prakash, V., Bowden, C., Cuthbert, R., Lindsay, N., Prakash, N., Routh,
A. & Parry-Jones, J. (2012). Husbandry Guidelines for `in range'
conservation breeding programmes of Gyps bengalensis, Gyps indicus
and Gyps tenuirostris. Version 1.0 pp54. Royal Society for
Protection of Birds, Sandy, UK: ISBN - 978-1-905601-34-9
- Prakash V, Bishwakarma MC, Chaudhary A, Cuthbert R, Dave R, Kulkarni M,
Kumar S, Paudel K, Ranade S, Shringarpure R, Green RE (2012). The
population decline of Gyps vultures in India and Nepal has slowed
since veterinary use of diclofenac was banned. PLoS ONE 7(11): e49118.
- Data on meloxicam producing companies in India — p10: http://save-vultures.org/Documents/SAVE_Report_Nov_11_Final.pdf
- Markanda A., Taylor T., Longo A., Murty M.N., Murty S., Dhavala K.
(2008) Counting the cost of vulture decline — an appraisal of the human
health and other benefits of vultures in India. Ecological Economics 67