CR
Indian Vulture Gyps indicus



Justification

Justification of Red List Category
This species is classified as Critically Endangered because it has suffered an extremely rapid population decline as a result of mortality from feeding on carcasses of animals treated with the veterinary drug diclofenac.

Population justification
A population estimate of c.45,000 individuals has been extrapolated from 2007 survey results published by Prakash et al. (2007), who recorded 337 individuals along 18,000 km of road transects. This very roughly equates to 30,000 mature individuals.

Trend justification
Survey results indicate that declines throughout the Indian Subcontinent probably began in the 1990s and were extremely rapid, resulting in an overall population decline of greater than 97% over a 10-15 year period.

Distribution and population

Gyps indicus breeds in south-east Pakistan and peninsular India south of the Gangetic plain, north to Delhi, east through Madhya Pradesh, south to the Nilgiris, and occasionally further south (Collar et al. 2001). The species was first recorded in Nepal in 2011 (Subedi and DeCandido 2013). It was common until very recently, but since the mid-1990s has suffered a catastrophic decline (over 97%) throughout its range. This was first noticed in Keoladeo National Park, India (Prakash et al. 2003), where counts of feeding birds fell from 816 birds in 1985-1986 to just 25 in 1998-1999. Only tiny populations in the Ramanagaram Hills of Karnataka and Nilgiri Forest Division in Tamil Nadu are known to remain in inland southern India, and it is rare elsewhere within its former range (Prakash et al. 2007, Venkitachalam and Senthilnathan 2015, 2016). Extensive research has identified the non-steroidal anti-inflammatory drug (NSAID) diclofenac to be the cause behind this rapid population collapse (Green et al. 2004, Oaks et al. 2004a, Shultz et al. 2004, Swan et al. 2006b), and other drugs have subsequently been identified to have similar effects on Gyps vultures (Naidoo et al. 2010, Zorrilla et al. 2015, Cuthbert et al. 2015). Diclofenac, used to treat domestic livestock, is ingested by vultures feeding on their carcasses leading to renal failure causing visceral gout (Oaks et al. 2004a,b; Swan et al. 2006b, Gilbert et al. 2006). It is now rare in Pakistan, although a colony of 200-250 pairs was discovered in 2003 in Sindh Province (A. A. Khan in litt. 2003). In 2007, the total Indian population, based on extrapolations from road transects, was estimated at 45,000 individuals, with a combined average annual decline for this species and G. tenuirostris of over 16% during 2000-2007 (Prakash et al. 2007), though data indicate that the rate of population decline of G. tenuirostris and G. indicus combined has now slowed in India (Prakash et al. 2012). It is estimated that its relative abundance in Pakistan declined by 61% between 2003-2004 and 2006-2007, this was followed by a 55% increase by 2007-2008 (Chaudhry et al. 2012), and a new breeding colony appears to have developed near the India-Pakistan border in the Bikaner District, India.

Ecology

It is found in cities, towns and villages near cultivated areas, and in open and wooded areas. This species feeds almost entirely on carrion, and often associates with White-rumped Vulture G. bengalensis when scavenging at carcass dumps and slaughterhouses. It nests almost exclusively in colonies on cliffs and ruins, although in one area, where cliffs are absent, it has been reported nesting in trees. Vultures also play a key role in the wider landscape as providers of ecosystem services, and were previously heavily relied upon to help dispose of animal and human remains in India; which in turn reduces the amount of food available for potentially problematic species, such as feral dogs (Prakash et al. 2012b).

Threats

By mid-2000, Gyps vultures were being found dead and dying in Pakistan and throughout India, and major declines and local extirpations were being reported. The anti-inflammatory drug diclofenac, used to treat domestic livestock, has been identified as the cause of mortality, with renal failure resulting in visceral gout in the vast majority of examined vultures (Oaks et al. 2004a, Shultz et al. 2004, Swan et al. 2006b, Gilbert et al. 2006). Vultures are exposed to diclofenac and other NSAIDs through scavenging on the carcasses of largely cattle and buffalo that have been treated with the drugs prior to death and left for scavengers to consume (as is tradition in Hindu cultures). Vultures are unable to process diclofenac and other vulture-toxic NSAIDs that then cause renal failure and death. Modelling has shown that to cause the observed rate of decline in the species just one in 760 livestock carcasses need contain diclofenac residues (Green et al. 2004), and sampling livestock carcasses in India between 2004 and 2005 showed that 10% were contaminated with diclofenac (Taggart et al. 2009). Despite awareness programmes to educate locals about the association between diclofenac and vulture mortality, a survey in Nepal indicated that the vast majority of people still do not link diclofenac use to a decline in vulture populations (Paudel 2008), potentially leading to a slower uptake of meloxicam (a safe alternative). Recent bans of diclofenac in the region still have not eradicated its use in veterinary treatments, as it is still found in the carcasses of livestock and vultures (Cuthbert et al. 2014, 2015). This may be because the drug continues to be produced for human consumption, which is then sold on for veterinary purposes (Cuthbert et al. 2011, T. Galligan in litt. 2016); though this is not somuch of a problem in Nepal and Pakistan (SAVE 2015). A second veterinary drug in use in India and particularly Bangladesh, ketoprofen, has also been identified to be lethal to the species, and measurements of residue levels in ungulate carcasses in India indicates that concentrations are sufficient to cause vulture mortalities (Naidoo et al. 2010). The availability of other NSAIDs, such as ketoprofen, is increasing (Cuthbert et al. 2011; Khan 2013) and concern has been raised about the toxicity of nimesulide and flunixin (Zorrilla et al. 2015, Cuthbert et al. 2015) as well as aceclofenac which is metabolised into diclofencac, and so is in effect as toxic to vultures as diclofenac (Galligan et al. 2016). Other likely contributory factors are changes in human consumption and processing of dead livestock (which have occurred in response to the collapse in vulture numbers), and poison and pesticide use, but these are probably of minor significance.

Conservation actions

Conservation Actions Underway
CITES Appendix II. It has been reported from many protected areas across its range. The Indian government has now passed a bill banning the manufacture of the veterinary drug diclofenac that has caused the rapid population decline across the Indian subcontinent; their aim was to phase out its use by late 2005 (Gilbert et al. 2006, Swan et al. 2006a), although its sale has not been banned and it is likely to remain in widespread use for several years. Similar laws banning import and manufacture of diclofenac are now in place in Nepal and Pakistan. A letter from the Drug Controller General of India in 2008 warned more than 70 drugs firms not to sell the veterinary form of diclofenac, and to mark human diclofenac containers 'not for veterinary use' (BirdLife International 2008). In October 2010, the government of Bangladesh banned the production of diclofenac for use in cattle, and the distribution and sale of the drug were due to be outlawed there during the first half of 2011 (M. M. H. Khan in litt. 2010). However, human diclofenac continues to be sold for veterinary use (Cuthbert et al. 2011), and as such the Government of India banned the manufacture of all diclofenac products in vial sizes larger than 3 ml (the single dose for humans) in 2015, which is predicted to make the drug too expensive and too complicated to use on large-bodied animals and thereby stop its misuse in livestock (T. Galligan in litt. 2016). Efforts to replace diclofenac with a suitable alternative are ongoing; drug companies have now developed meloxicam, an alternative to diclofenac, which has been tested on Gyps vultures with no ill-effects (Swan et al. 2006a). Outreach activities have promoted this as the only vulture-safe alternative to diclofenac (T. Galligan in litt. 2016).

The Report of the International South Asian Vulture Recovery Plan Workshop in 2004 gave a comprehensive list of recommendations including establishing a minimum of three captive breeding centres each capable of holding 25 pairs (Bombay Natural History Society 2004) - ultimately at least 150 pairs of the three species should be held in captivity to ensure sufficient birds are available to re-establish wild colonies in the future (Lindsay 2008). Captive breeding efforts are ongoing and during 2008-2009 there were 71 individuals in captivity at two captive breeding centres in India (Pain et al. 2008, Bowden 2009). In 2009, captive birds laid eggs, raising hopes that they will successfully breed in captivity in the near future (Bowden 2009). By November 2011 there were 83 individuals in captivity at two centres, 11 of these were juveniles that had successfully fledged (Bowden et al. 2012); and by 2015 the Indian breeding centres were fledgy 60 juveniles per year of all three resident Gyps vultures combined(V. Prakash pers. comm. per C. Bowden in litt. 2016). SAVE (Saving Asia's Vultures from Extinction) has developed the concept of Vulture Safe Zones; areas (with a minimum of 100 km radius, equating to 30,000 km2) around important vulture breeding colonies, where education and advocacy efforts are focused on eliminating the use of diclofenac and other vulture-toxic drugs (Galligan 2013, Mukherjee et al. 2014). Conservation activities include: meeting key groups (e.g. pharmacists, veterinarians and livestock owners); engaging government officials (e.g. drug control, livestock services and forest departments) at tehsil, district and state levels; engaging with the public (e.g. festival programmes, media coverage and signage); diclofenac-free district declaration; community-run formal or informal Vulture Safe Feeding Sites (i.e., vulture [Jatayu] restaurants); vulture-related income generation for villages at nesting or feeding sites; diclofenac-meloxicam exchanges; husbandry and veterinary training camps; and national and international ecotourism to feeding sites and conservation breeding sites (T. Galligan in litt. 2016). There are currently 12 provisional Vulture Safe Zones being established in India, Nepal, Pakistan and Bangladesh (Mukherjee et al. 2014). These areas will provide a safe environment into which birds bred in captivity can be released (Bowden et al. 2012). Diversionary feeding has been shown to reduce (but not eliminate) vulture mortality from diclofenac poisoning, and uncertainty over the movements of Asian Gyps vultures makes the effectiveness of measures such as these uncertain (Pain et al. 2008). Satellite tagging has been employed on Asian Gyps vultures to improve understanding of their movements and range use so as to aid the development of conservation strategies for the genus (Ellis 2004).

An action plan for vulture conservation in India was written in 2006 (Ministry of Environment & Forests 2006), but has not been updated. In 2012 the governments of India, Pakistan, Nepal and Bangladesh adopted a number of priority actions for the conservation of vultures, proposed by SAVE. These include banning large multi-dose vials of human diclofenac, testing other NSAIDs for toxicity to vultures and expanding the Vulture Safe Zones initiative (Galligan 2013). A multi-species action plan for African-Eurasian Vultures is under development and is due to be considered by CMS at COP12 in October 2017.

Conservation Actions Proposed
Identify the location and number of remaining individuals. Measure the frequency of diclofenac treated carcasses available to vultures. Support the ban on the veterinary use of diclofenac, and attempt to implement a ban on other vulture-toxic NSAIDs. Support species management or restoration, as needed. Monitor remaining populations. Support captive breeding efforts at a number of separate centres. Manage genetic stock in the captive-bred population (Bowden et al. 2012). Promote the immediate adoption of meloxicam as an alternative to diclofenac. Test other non-steroidal anti-inflammatory drugs (NSAIDs) to identify additional safe alternative drugs to diclofenac and also other toxic ones. Three drugs, aceclofenac, ketoprofen and nimesulide, are thought to be toxic to vultures (Cuthbert et al. 2015), and approximately another 10 drugs need to be tested (Galligan 2013). Fully implement restrictions in the size of diclofenac vials sold for human use to make them less practical to use for veterinary purposes and take action against companies that fail to comply with the diclofenac ban (Cuthbert et al. 2011). Attempt to estimate the potential value, in terms of ecosystem services, provided by wild vultures. Protect nesting areas. These and multiple other Conservation Actions were proposed as part of SAVE (2014) and SAVE (2015) for all Asian vultures. Maintain and promote Vulture Safe Zones, including trans-boundary efforts. Within VSZs, promote livestock management training and provide free veterinary camps.

Identification

92 cm. Typical Gyps vulture. Robust, strong features giving eagle-like bearing. Perched adults have pale-yellowish bill and cere; pale eyerings; large white neck-ruff; and buff back and upperwing coverts. The stout blackish neck has pale down. Juveniles have dark bill with pale culmen; pinkish head and neck covered in pale down and dingy heavily streaked underparts. In flight thighs are heavily feathered and concolourous with the rest of the underparts. Similar spp. Told from the allopatric and distinctive Slender-billed Vulture G. tenuirostris by robust build, clean plumage, pale bill (in adults) and downy head and neck (juveniles).

Acknowledgements

Text account compilers
Benstead, P., Taylor, J., Bird, J., Symes, A., Crosby, M., Calvert, R., Wheatley, H., Butchart, S., Westrip, J.

Contributors
Riseborough, R., Gilbert, M., Prakash, V., Galligan, T., Venkatachalam, R., Cuthbert, R., Rahmani, A., Khan, A., Bowden, C., Khan, M., Bohra, D.


Recommended citation
BirdLife International (2018) Species factsheet: Gyps indicus. Downloaded from http://www.birdlife.org on 23/04/2018. Recommended citation for factsheets for more than one species: BirdLife International (2018) IUCN Red List for birds. Downloaded from http://www.birdlife.org on 23/04/2018.