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Abstract

The widespread use in cattle of the painkiller and anti-inflammatory drug, diclofenac, led to the unprecedented and dramatic disappearance of vultures over the past 20 years. This inadvertently poisoned around 40 million vultures, causing populations to plummet across South Asia. It's tempting to think that with the government bans now in place for over ten years, the job is done. While there are indeed some early indications that the remnant vulture populations may be stabilising, albeit at very low levels (Prakash et al. 2012), there is no room for complacency. Unfortunately, four of the five vultures endemic to Asia remain 'Critically Endangered' according to IUCN criteria (Birdlife 2017), which is the highest threat category short of extinction. These are: white-rumped vulture (Gyps bengalensis), Indian or long-billed vulture (Gyps indicus), slender-billed vulture (Gyps tenuirostris) and the red-headed or king vulture (Sarcogyps calvus). Back in 2004, two key actions were identified as priority (MoEF 2005): one was banning or removal of diclofenac from veterinary practice (requiring identification of safe substitutes for vets), and the second was to establish viable ex-situ or captive populations for breeding and future release. These were aggressively taken up in the years that followed (Pain et al. 2008), with meloxicam successfully identified as a safe alternative, and bans on veterinary diclofenac largely in place by 2006. Conservation breeding programmes were established in India, Nepal and Pakistan and, since 2008, all three of the most affected vulture species (1-3 above) have been breeding successfully and in genetically diverse and viable numbers (Ishtiaq et al.
http://www.conservationindia.org/articles/asian-vulture-crisis-its-not-over-yet Posted October 2017
Asian Vulture Crisis It’s Not Over Yet
by Chris Bowden
The widespread use in cattle of the painkiller and anti-inflammatory drug, diclofenac, led to the
unprecedented and dramatic disappearance of vultures over the past 20 years. This inadvertently
poisoned around 40 million vultures, causing populations to plummet across South Asia. It’s tempting
to think that with the government bans now in place for over ten years, the job is done. While there
are indeed some early indications that the remnant vulture populations may be stabilising, albeit at
very low levels (Prakash et al. 2012), there is no room for complacency. Unfortunately, four of the
five vultures endemic to Asia remain ‘Critically Endangered’ according to IUCN criteria (Birdlife
2017), which is the highest threat category short of extinction. These are: white-rumped vulture (Gyps
bengalensis), Indian or long-billed vulture (Gyps indicus), slender-billed vulture (Gyps tenuirostris)
and the red-headed or king vulture (Sarcogyps calvus).
Back in 2004, two key actions were identified as priority (MoEF 2005): one was banning or removal
of diclofenac from veterinary practice (requiring identification of safe substitutes for vets), and the
second was to establish viable ex-situ or captive populations for breeding and future release. These
were aggressively taken up in the years that followed (Pain et al. 2008), with meloxicam successfully
identified as a safe alternative, and bans on veterinary diclofenac largely in place by 2006.
Conservation breeding programmes were established in India, Nepal and Pakistan and, since 2008, all
three of the most affected vulture species (1-3 above) have been breeding successfully and in
genetically diverse and viable numbers (Ishtiaq et al. 2011, Bowden 2009, Bowden 2017).
Vulture densities in 1984 near Timarpur, New Delhi
Photo: Goutam Narayan
It seems extraordinary that these species are now facing a real threat of extinction having been so abundant and so recently.
Conservation breeding of vultures
The reasons for the ongoing concerns however are many: one is that, despite the ban, many veterinary
practitioners illegally use human diclofenac formulations for veterinary purposes. So although the use
of this drug has come down dramatically, it is still very much an ongoing threat. We were delighted
that the Indian Government took another step in 2015 to ban large vials of the human formulation (not
legitimately needed for humans) that made the drug available in convenient veterinary-sized
packages. However, it’s sobering to note that one drug company, ‘Laborate’, has challenged the ban
in the high court. We can but hope that the ban will be upheld. I’d like to congratulate Coimbatore-
based NGO ‘Arulagam’ and the drug authorities for their efforts to ensure that it is.
At the most recent SAVE (Saving Asia’s Vultures from Extinction) consortium annual meeting of
experts, held in Mumbai, there was a one-day ‘NSAIDs Alert’ symposium, highlighting recent studies
and further alarming trends concerning other veterinary drugs that are now being used by vets in the
region. Some of these are also proving to be toxic to vultures (Galligan et al. 2015, Cuthbert et al
2014). So, there is a real risk that one toxic drug for vultures may be replaced by others. Meloxicam is
currently the only drug with similar properties that is considered safe, and although it’s becoming
more popular, so are some other dangerous compounds like ketoprofen, aceclofenac and nimesulide.
Ketoprofen is one unsafe drug that is already being widely used as a replacement for diclofenac, and,
despite work showing its toxicity to Gyps vultures, it has not been widely banned. See: Evidence for
the toxicity to vultures of NSAIDs other than diclofenac.
The very first breeding success at the BNHS-Haryana Govt centre in 2008. The programme now fledges over 60 birds each
year.
Photo: Vibhu Prakash/BNHS
Senior drug controllers from Bangladesh, India, Nepal and Pakistan attended the above SAVE
meeting, and the early signs are rather positive, with Bangladesh quickly declaring a regional ban of
ketoprofen and aceclofenac in February 2017, which we hope will pave the way for national and
wider measures in the region. The urgent priority and need is for safety-testing of such drugs on
vultures, and this is being taken up in India. What we hope will be ground breaking for vulture
conservation is a collaboration between SAVE partners, including the Government body, Indian
Veterinary Research Institute, which could ultimately lead to only vulture-safe drugs being licensed
for veterinary use, and also to identifying other safe alternatives.
India’s Deputy Drug Controller was among senior drug authority officials from all four South Asian countries who attended
the 6th annual SAVE meeting in Mumbai.
Photo: BNHS
There are other, more localised threats, which could prevent vulture recoveries even if the painkiller
problem is fully resolved, and these need careful monitoring and attention. The use of poison baits
targeting dogs, leopards and other mammals can inadvertently kill large numbers of vultures. This is a
growing problem, particularly in Africa and in parts of India. Powerlines and windfarms can also
sometimes kill large numbers of vultures. Other factors like kite string injuries can also impact
populations in some places. A full review of threats will soon appear in the Convention of Migratory
Species Multi-species Action plan for old world vultures (this will hopefully be ratified in Manila in
October), which draws heavily on the agreed action plan or Blueprint for south Asian Gyps vultures.
In India, the conservation-breeding programme was initiated in Haryana as a joint BNHS and State
government project with significant support from the Royal Society for Protection of Birds (RSPB)
and other SAVE partners, initially bringing Darwin Initiative (UK Government) support. This
extended to other centres in West Bengal, Assam and Madhya Pradesh and also involved the Central
Zoo Authority, which has established other similar centres. Nepal (Bird Conservation Nepal, National
Trust for Nature Conservation and the Government Wildlife Department) and Pakistan (WWF
Pakistan with Punjab Provincial Government with Hawk Conservancy support) also established
smaller facilities for one of the three species, Gyps bengalensis, and have more recently reached the
stage of fledging their first chicks. Meanwhile, the vulture conservation breeding programme in India
produces over 60 fledged birds per year (species 1-3 above), where the Government (in partnership
with BNHS) is now supporting an increasing proportion of the costs (particularly in Haryana).
A preliminary trial release of two Himalayan Griffons happened in Haryana in 2016. Apart from
being an instructive process, this event drew much attention to the breeding program due to visits
from high profile members of the government such as India’s Environment Minister and the Chief
Minister of Haryana.
Meanwhile, the first release of the Critically Endangered white-rumped vulture is moving ahead in
Nepal. The birds, which were moved to a pre-release aviary in April 2017, are all set for release in
November 2017. The RSPB-Bird Conservation Nepal team has satellite-tagged six wild birds in the
area to monitor their movements and survival and this has already yielded important information on
trans-boundary movements and newly recognised feeding sites in Uttar Pradesh. The released,
captive-reared birds will be similarly monitored. We anticipate release of this species in Haryana,
India in early 2018, once satellite tagging permissions are in place, and further work by the BNHS and
Haryana Government has been carried out to ensure that diclofenac and other toxic drug use within a
100 km radius have been sufficiently reduced. Monitoring the success of these releases will be crucial
to finding out how safe the environment really is, and the prospects for vulture populations in the
future.
References:
1. Birdlife International (2017) IUCN Red List for Birds. Accessed from http://www.birdlife.org September 2017
2. Bowden, C (2009). The Asian Gyps vulture crisis: the role of captive breeding in India to prevent total extinction.
BirdingASIA 12:121-123.
3. Bowden, C (2017). Asian vulture crisis: Some positive signs? BirdingASIA 27:94-95.
4. Cuthbert, R.J., Taggart, M.A., Mohini, S., Sharma, A., Das, A., Kulkarni, M.D., Deori, P., Ranade, S.,
Shringarpure, R.N., Galligan, T.H. and Green, R.E. (2016) Continuing mortality of vultures in India associated
with illegal veterinary use of diclofenac and a potential threat from nimesulide. Oryx 50: 104-112.
5. Galligan, T. H., Taggart, M. A., Cuthbert, R. J., Svobodova, D., Chipangura, J., Alderson, D., Prakash, V.M., and
Naidoo, V. (2016) Metabolism of aceclofenac in cattle to vulture-killing diclofenac. Conserv. Biol. 30: 11221127.
6. Ishtiaq, F, Prakash, V, Green RE & Johnson J (2014). Management implications of genetic studies for ex-situ
populations of three critically endangered Asian Gyps vultures. Animal Conservation:1-12 doi 10.1111.acv,12166
7. Pain, D. J., Bowden, C. G. R., Cunningham, A. A., Cuthbert, R., Das, D., Gilbert, M., Jakati, R., Jhala, Y., Khan,
A. A., Naidoo, V., Gilbert, M., Jakati, R. D., Jhala, Y., Khan, A. A., Naidoo, V., Oaks, J.L., Parry-Jones, J.,
Prakash, V., Rahmani, A.R., Ranade, S.P., Sagar Baral, H, Saravanan, S., Senacha, K.R., Shah, N., Swan, G.,
Swarup, D., Taggart, M.A., Watson, R.T., Virani, M., Wolter, K., and Green, R.E. (2008) The race to prevent the
extinction of South Asian vultures: Bird Conservation International 18: 30-48.
8. Prakash, V., Bishwakarma, M.C., Chaudhary, A., Cuthbert, R, Dave, R., Kulkarni, M., Kumar, S., Paudel, K.,
Ranade, S., Shringarpure, R. and Green, R.E. (2012) The Population Decline of Gyps Vultures in India and Nepal
Has Slowed Since Veterinary Use of Diclofenac Was Banned. PLoS ONE 7: e49118.
About the author
Chris Bowden
Chris has worked for the RSPB and BirdLife International for over 30 years, mainly coordinating
research and conservation efforts for Critically Endangered Northern Bald Ibis and Asian vultures. He
is International Species Recovery Officer & Saving Asia’s Vultures from Extinction (SAVE)
Programme Manager. He is currently based in Bangalore.
ResearchGate has not been able to resolve any citations for this publication.
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Article
The collapse of South Asia's Gyps vulture populations is attributable to the veterinary use of the non-steroidal anti-inflammatory drug (NSAID) diclofenac. Vultures died after feeding on carcasses of recently-medicated animals. The governments of India, Nepal and Pakistan banned the veterinary use of diclofenac in 2006. We analysed results of 62 necropsies and 48 NSAID assays of liver and/or kidney for vultures of five species found dead in India between 2000 and 2012. Visceral gout and diclofenac were detected in vultures from nine states and three species: Gyps bengalensis, Gyps indicus and Gyps himalayensis . Visceral gout was found in every vulture carcass in which a measurable level of diclofenac was detected. Meloxicam, an NSAID of low toxicity to vultures, was found in two vultures and nimesulide in five vultures. Nimesulide at elevated tissue concentrations was associated with visceral gout in four of these cases, always without diclofenac, suggesting that nimesulide may have similar toxic effects to those of diclofenac. Residues of meloxicam on its own were never associated with visceral gout. The proportion of Gyps vultures found dead in the wild in India with measurable levels of diclofenac in their tissues showed a modest and non-significant decline since the ban on the veterinary use of diclofenac. The prevalence of visceral gout declined less, probably because some cases of visceral gout from 2008 onwards were associated with nimesulide rather than diclofenac. Veterinary use of nimesulide is a potential threat to the recovery of vulture populations.
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Captive breeding and ex situ conservation have become important tools in species conservation programmes. The effectiveness of the management of captive populations can be hampered by the absence of pedigree data, but molecular markers can be used to inform conservation objectives and reduce inbreeding in the captive population. Using microsatellite markers, we examined the genetic diversity and relatedness among wild-caught individuals of three critically endangered Asian vulture species, Gyps bengalensis, Gyps indicus and Gyps tenuirostris, populations established for captive breeding. Estimates of the inbreeding coefficient (f) were low, indicating that populations of all three species do not appear to be inbred. Moreover, the data show that a large proportion of wild-taken birds were unrelated individuals (94.6, 87.1 and 85.3% in G. bengalensis, G. indicus and G. tenuirostris, respectively). No significant genetic differentiation (FST) was observed between historic and 2000/2001 populations of G. bengalensis in Pakistan and India. However, the more recent sampling (2002–2006) in Pakistan showed a significant difference from India. A genetic signal of a demographic bottleneck in all three species was found in some (M-ratio test), but not all, tests (heterozygote excess and mode shift in allele frequencies). Levels of genetic diversity in G. bengalensis and G. indicus populations were comparable to levels prior to or soon after the start of their decline, respectively, suggesting that adequate numbers of birds exist in captivity for these two species and reflect neutral diversity levels observed in the wild. The genetic data obtained from this study allow us to minimize the loss of neutral genetic diversity in small wild and captive populations and to identify related pairs to avoid inbreeding depression.
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Populations of oriental white-backed vulture (Gyps bengalensis), long-billed vulture (Gyps indicus) and slender-billed vulture (Gyps tenuirostris) crashed during the mid-1990s throughout the Indian subcontinent. Surveys in India, initially conducted in 1991-1993 and repeated in 2000, 2002, 2003 and 2007, revealed that the population of Gyps bengalensis had fallen by 2007 to 0.1% of its numbers in the early 1990s, with the population of Gyps indicus and G. tenuirostris combined having fallen to 3.2% of its earlier level. A survey of G. bengalensis in western Nepal indicated that the size of the population in 2009 was 25% of that in 2002. In this paper, repeat surveys conducted in 2011 were analysed to estimate recent population trends. Populations of all three species of vulture remained at a low level, but the decline had slowed and may even have reversed for G. bengalensis, both in India and Nepal. However, estimates of the most recent population trends are imprecise, so it is possible that declines may be continuing, though at a significantly slower rate. The degree to which the decline of G. bengalensis in India has slowed is consistent with the expected effects on population trend of a measured change in the level of contamination of ungulate carcasses with the drug diclofenac, which is toxic to vultures, following a ban on its veterinary use in 2006. The most recent available information indicates that the elimination of diclofenac from the vultures' food supply is incomplete, so further efforts are required to fully implement the ban.
Article
The non-steroidal anti-inflammatory drug (NSAID) diclofenac is highly toxic to Gyps vultures and its recent widespread use in South Asia caused catastrophic declines in at least three scavenging raptors. The manufacture of veterinary formulations of diclofenac has since been banned across the region with mixed success. However, at least 12 other NSAIDs are available for veterinary use in South Asia. Aceclofenac is one of these compounds and it is known to metabolise into diclofenac in some mammal species. The metabolic pathway of aceclofenac in cattle, the primary food of vultures in South Asia, is unknown. In this study, we give six cattle the recommended dose of aceclofenac (2 mg/kg), collect blood along a time series and undertake a pharmacokinetic analysis of aceclofenac and diclofenac-metabolites in their plasma using liquid chromatography with mass spectrometry. We found that nearly all of the aceclofenac administered to the cattle was very rapidly metabolised into diclofenac. Therefore, treating livestock with pure diclofenac or aceclofenac poses the same risk to vultures. This fact, coupled with the risk that aceclofenac may replace diclofenac in the veterinary market, fortifies the need for an immediate ban on all aceclofenac formulations that can be used to treat livestock. Without such a ban, the recovery of vultures across South Asia will not be successful. This article is protected by copyright. All rights reserved
IUCN Red List for Birds. Accessed from http://www.birdlife
Birdlife International (2017) IUCN Red List for Birds. Accessed from http://www.birdlife.org September 2017
The Asian Gyps vulture crisis: the role of captive breeding in India to prevent total extinction
  • C Bowden
Bowden, C (2009). The Asian Gyps vulture crisis: the role of captive breeding in India to prevent total extinction. BirdingASIA 12:121-123.