The race to prevent the extinction of south asian vultures

Bird Conservation International (2008) 18:S30–S48. ß BirdLife International 2008doi: 10.1017/S0959270908000324 Printed in the United Kingdom The race to prevent the extinction of SouthAsian vultures DEBORAH J. PAIN, CHRISTOPHER G.R. BOWDEN, ANDREW A.
CUNNINGHAM, RICHARD CUTHBERT, DEVOJIT DAS, MARTIN GILBERT,RAM D. JAKATI, YADVENDRADEV JHALA, ALEEM A. KHAN, VINNYNAIDOO, J. LINDSAY OAKS, JEMIMA PARRY-JONES, VIBHU PRAKASH,ASAD RAHMANI, SACHIN P. RANADE, HEM SAGAR BARAL, KALU RAMSENACHA, S. SARAVANAN, NITA SHAH, GERRY SWAN, DEVENDRASWARUP, MARK A. TAGGART, RICHARD T. WATSON, MUNIR Z. VIRANI,KERRI WOLTER and RHYS E. GREEN Gyps vulture populations across the Indian subcontinent collapsed in the 1990s and continue todecline. Repeated population surveys showed that the rate of decline was so rapid that elevatedmortality of adult birds must be a key demographic mechanism. Post mortem examinationshowed that the majority of dead vultures had visceral gout, due to kidney damage. Therealisation that diclofenac, a non-steroidal anti-inflammatory drug potentially nephrotoxic tobirds, had become a widely used veterinary medicine led to the identification of diclofenacpoisoning as the cause of the decline. Surveys of diclofenac contamination of domestic ungulatecarcasses, combined with vulture population modelling, show that the level of contamination issufficient for it to be the sole cause of the decline. Testing on vultures of meloxicam, analternative NSAID for livestock treatment, showed that it did not harm them at concentrationslikely to be encountered by wild birds and would be a safe replacement for diclofenac. Themanufacture of diclofenac for veterinary use has been banned, but its sale has not. Consequently,it may be some years before diclofenac is removed from the vultures’ food supply. In themeantime, captive populations of three vulture species have been established to provide sourcesof birds for future reintroduction programmes.
Eight vulture species in the genus Gyps are widely distributed across Europe, Asia and Africa.
They are all obligate scavengers, feeding primarily on the carcasses of large ungulates andnesting and roosting, often colonially, on cliffs or in trees. They use energetically economicalsoaring flight to travel long distances from nests and roosts in search of ungulate carcasses(Houston 1974, Ruxton and Houston 2004). Gyps vultures are believed to have evolved inparallel with large herds of migratory ungulates, feeding on the remains of sick, injured anddepredated individuals (Mundy et al. 1992). These herds have disappeared from most of theworld range of Gyps vultures, remaining only in some of the larger protected areas. However,the food supply formerly provided by wild ungulates was replaced by traditional farmingpractices in some areas. For example, in the Spanish Pyrenees, transhumance pastoralism, inwhich herds of domestic ungulates graze the high mountain pastures in the summer and areshepherded to the lowlands in the winter, provided a food supply for Eurasian Griffon Vultures Gyps fulvus from the 18th to mid 20th centuries, although these practices have recently declineddramatically across Europe (Pain and Pienkowski 1997).
In spite of these changes in food supply, the Cape Griffon Gyps coprotheres of southern Africa was the only member of the genus considered to be in danger of global extinction until the late1990s. This species is believed to have been affected by multiple threats (BirdLife International2007). It was then recognised that populations of vultures endemic to South Asia were decliningrapidly across the Indian subcontinent for unknown reasons. This led to three species, theOriental White-backed Vulture Gyps bengalensis (OWBV), the Long-billed Vulture G. indicus(LBV) and the Slender-billed Vulture G. tenuirostris (SBV) being listed by IUCN as ‘CriticallyEndangered’. In this paper, we describe recent research to determine the causes of the populationdeclines and to identify ways to prevent the extinction of these species.
Population trends of Gyps vultures outside the Indian subcontinent In southern Africa, populations of the endemic Cape Griffon have declined slowly, principallybecause of accidental poisoning, collision and electrocution, food stress and disturbance (BirdLifeInternational 2007). In West Africa, vultures have undergone a large decline over the last 35years, with national parks being the only areas not showing significant declines (Thiollay 2006).
Many factors are thought to have contributed to these relatively recent declines, includinghabitat destruction or degradation, inadvertent poisoning from baits placed to kill other species,the capture of birds for local medicinal purposes or the wild bird trade. However, thedisappearance of wild large ungulates because of exploitation for bush meat and reducedavailability of the carcasses of domestic livestock may have been important factors in thedeclines.
Two South Asian Gyps species, OWBV and SBV, were widespread and generally common in Southeast Asia (Cambodia, Vietnam, Laos, Thailand, Malaysia) at the beginning of the 20thcentury, but by the end of that century only a few small relict populations remained, primarilyin Cambodia (Pain et al. 2003). Populations remain in Myanmar, but their numbers and statusremain uncertain. Whilst factors like persecution may have played a role in the Southeast Asiandeclines, their main cause is believed to be food shortage. Overhunting resulted in a collapse inthe populations of wild ungulates throughout the region (Srikosamatara and Suteethorn 1995,Duckworth et al. 1999, Hilton-Taylor 2000), and current livestock husbandry practices appearnot to provide a sufficiently large food supply to support large populations (Pain et al. 2003).
Collapse of Gyps vulture populations across the Indian subcontinent Although Gyps vulture populations were probably declining slowly in many parts of the worldduring the 20th century, a very different situation existed in India, Nepal and Pakistan. Here,large populations of OWBV and LBV remained until the 1990s. Large numbers of SBV, whichwas not distinguished as a separate species from LBV until recently (Rasmussen and Parry 2001),were also found in the northeastern parts of the subcontinent. Indeed, during the 1980s OWBVwas thought likely to be the commonest large bird of prey in the world (Houston 1985). In India,Gyps vulture densities were so high in some areas that they were considered a hazard to aircraft(Grubh et al. 1990). This abundance was undoubtedly due to a plentiful food supply, in the formof the carcasses of domesticated ungulates. The keeping of livestock for milk production and asbeasts of burden is common in rural areas across the Indian subcontinent and cattle are abundantin many towns and cities. Livestock numbers in India have exceeded 400 million since the 1980s,and reached 500 million in 2005 (ILC 2003, projection based on Animal Husbandry Statistics,Government of India). In large parts of the subcontinent, Hindu beliefs prohibit the slaughter ofcows. When feral and domestic cows die a natural death they are left in the open in rural areas ordisposed of in regulated carcass dumps around towns and cities. Skinners remove the hides fromdead cattle for the leather industry, leaving vultures to scavenge the remaining soft tissue. As vulture populations benefited from the large amounts of food available, Indian society gainedenvironmental health and other benefits from a free carcass disposal service. A flock of vulturescan pick a cow carcass clean in a few hours, leaving little more than bones, that then dry rapidlyin the sun, and are gathered by bone collectors for the fertilizer, gelatin and glue industries.
Whilst vultures feed primarily on large ungulates, they were also historically the key scavenger of the dead from the ancient Parsi religion, who lay their dead out in the open inenclosures or specially constructed ‘Towers of Silence’ (Pain et al. 1993). Vultures also havespiritual significance in Hindu mythology, as the vulture-king Jatayu died attempting to protectSita, one of the principal characters of the Hindu epic ‘Ramayana’, from the demon king Ravana,while her husband Prince Rama was away hunting (Griffith 1870–1874).
The era of abundant Gyps vultures in the Indian subcontinent came to a sudden end in the 1990s. By the mid 1990s, newspapers in north India started publishing reports of vulturesrapidly disappearing from carcass dumps. This was also documented by the Bombay NaturalHistory Society (BNHS) whilst monitoring raptor numbers in Keoladeo National Park, a WorldHeritage Site at Bharatpur in eastern Rajasthan. In the mid 1980s, foraging vultures werenumerous in the park. Several hundred pairs of OWBV nested within it and hundreds of pairs ofLBV nested on cliffs at Bayana, not far outside. Between the late 1980s and mid to late 1990s,numbers of these two species found in the park had declined dramatically (Prakash 1999).
Numbers of OWBV nests declined from 244–353 in the 1980s to none by the 1999/2000breeding season (Prakash 1999, Prakash et al. 2003). There was also anecdotal evidence of ageneral decline in vulture numbers throughout much of northern India during the late 1990s.
However, as there was little systematic bird monitoring, it was difficult to know whether reportsreflected a truly nationwide decline, or isolated local changes. With support from the US Fishand Wildlife Service, BNHS had conducted nationwide raptor surveys in many parts of Indiabetween 1991 and 1993 using a repeatable road transect method (Samant et al. 1995). Surveyswere carried out in, near, and along the routes travelled between protected areas. They coveredlarge parts of north, west and eastern India. Unfortunately, not all Gyps vultures were countedbecause they were considered too numerous for this to be practicable. However, the surveyorscounted vultures in any groups of five or more birds. BNHS, with support from the RSPB,repeated the road transect surveys in 2000. The results were dramatic. Both OWBV and LBV hadalmost disappeared from the areas surveyed. The population of OWBV across the surveyedrange had declined by 96% between 1991–93 and 2000 and that of LBV by 92% (Prakash et al.
2003, 2005a, 2005b). It should be noted that these were minimum declines because individualvultures and those seen in small groups were counted in 2000, but not in 1991–1993. Subsequentcounts on these and additional transects in 2002, 2003 and 2007 showed that OWBV and LBVcontinued to decline at an average rate of 44% (OWBV) and 16% (LBV) per year between 2000and 2007 (Prakash et al. 2007). SBV was not distinguished from LBV until the 2002 count, whenit was found to comprise less than 2% of the combined total of the LBV and SBV count (Greenet al. 2004). Comparison of the 2002, 2003 and 2007 counts indicated that the population of SBVwas declining in India about as rapidly as LBV (Prakash et al. 2007).
Following the results of the 2000 surveys, BNHS organised an international meeting in September 2000. The meeting, held in New Delhi, was supported by the Ministry ofEnvironment and Forests (MoEF) of the Government of India and the RSPB, and was attendedby national and international scientists, conservationists, and Indian government representa-tives. Among those represented was The Peregrine Fund, who joined forces with WashingtonState University and the Ornithological Society of Pakistan (OSP) to conduct vulture studies inPakistan. Subsequent counts of breeding pairs of OWBV in nesting colonies in Punjab province,Pakistan, revealed a population decline at a rate of 50% per year between 2000 and 2003 (Gilbertet al. 2004, 2006, Green et al. 2004). This decline continued to extinction at several formerlylarge OWBV colonies in the province (Gilbert et al. 2006). This group also counted nesting LBVin Sind province, Pakistan (Gilbert et al. 2004), where numbers have declined by about two-thirds between 2002 and 2006; an average annual decline rate of 25% per year (AVPP 2007).
Hence, both in India and Pakistan, the rates of population decline of LBV, though rapid, aresubstantially slower (16% and 25% per year respectively) than the catastrophic decline rates forOWBV (44% and 50%). The similarity of the recent average decline rates in the two countries isstriking for both species. Backwards extrapolation of log-linear Poisson regression models ofcounts of vultures across India (for methods see Cuthbert et al. 2006a), and of vulture nests atKeoladeo National Park, suggest that the vulture declines probably started in the early to mid1990s (Figure 1). Nest counts of OWBV by Bird Conservation Nepal (BCN) in eastern Nepalsuggested similar rates of decline there, with 65 active nests found at Koshi in 2000–01 falling tojust 14 in 2002–03 (Baral et al. 2004).
The work of two main research groups was to prove crucial in the search for the cause of declines and solutions. BNHS led one group, initially comprising the Forest Department of thestate government of Haryana, the RSPB, the Zoological Society of London (ZSL) and theNational Birds of Prey Trust (NBPT), and later expanding to include a wide range of nationaland international organisations. The second group comprised The Peregrine Fund (TPF),Washington State University and the Ornithological Society of Pakistan (OSP). Whilst theBNHS consortium focussed largely on India, the TPF/OSP group conducted a complementaryresearch programme in Pakistan, and BCN worked in Nepal in collaboration with both groups.
Figure 1. Population declines of Gyps vultures in India. Points show indices of population sizefrom counts on a logarithmic scale, plotted against calendar year. This index represents thevulture population size as a proportion of the initial level (5 1). Triangles represent the numberof active nests of Gyps bengalensis in Keoladeo National Park from Prakash et al. (2003)expressed as a proportion of the average in the 1980s. Indices of population size, relative to thatin 1992, of G. bengalensis (diamonds) and G. indicus and G. tenuirostris combined (squares) innorthern India were calculated from road transect count data as described by Prakash et al.
(2007). Lines represent fitted log-linear regression models (dashed line 5 G. bengalensis atKeoladeo, dotted line 5 G. bengalensis on road transects, solid line 5 G. indicus/tenuirostris onroad transects).
Bird population declines involve changes in breeding success, the proportion of adults breeding, orsurvival rate, which are in turn brought about by external causes such as changes in nest siteavailability, food supply, disease or predation. Comparison of demographic rates and externalinfluences on declining populations with those of stable populations of the same species is afrequently used and powerful method for diagnosing the cause of a population decline (Green 1995,2002). However, this approach was not possible for vultures because, except for a relict population inCambodia, all populations appeared to be declining rapidly throughout a huge area. Nonetheless, thevery rapidity of the declines gave at least some clues about the demographic mechanism.
Like other large scavenging birds, Gyps vultures are usually long-lived. One bird was reported to live for 37 years in captivity and annual survival rates of wild large raptors are typicallyaround 95% or higher (Newton 1979). An annual survival rate of 99% was reported for adultEurasian Griffons, though this was for a reintroduced population receiving supplementary foodand protection (Sarrazin et al. 1994). Adult survival rates have not been measured for Gypsvultures in the Indian subcontinent, but they too are likely to be high. If this is the case, then itis evident from their rapid rates that the demographic mechanism of the vulture declines in theIndian subcontinent must involve a substantial reduction in adult survival. Imagine that theadult survival rate of OWBV before the decline began was 95%. Even if breeding success andimmature survival were reduced so that no recruitment of young adults occurred, the adultpopulation could not decline by more than 5% per year if adult survival remained at its pre-decline level. However, the observed rate of population decline is about 50% per year for thisspecies. Such declines could only occur if there was abnormally high adult mortality. In 1985–86,when . 1,700 OWBV were counted in Keoladeo National Park, only 14 birds (7 adults and 7juveniles) were found dead. By contrast, by 1997–98, when only a few hundred OWBVremained, 73 adults and 10 juveniles were found dead (Prakash 1999). Prakash (1999) also foundthat the proportion of nests producing fledged young declined from 82% in 1985–1986 (n 5244) to none in 1997–98 (n 5 25). The causes of nest failure were unknown, but could haveresulted from factors affecting eggs or chicks directly, high adult mortality affecting nest success,or a combination of the two. At the nearby breeding colony of LBV at Bayana, numerous vulturecarcasses were found at the base of the cliffs.
In Pakistan the TPF/OSP research group made regular systematic searches for dead OWBV in and near the breeding colonies and roosts in their Punjab province study area (Gilbert et al.
2002). By comparing the number of birds found dead with the number counted at the beginningof a given time period, they were able to calculate minimum annual mortality rates. Theminimum proportion of adults dying per year in 2001 was 15% and the proportion for adultsand sub-adults combined was 26%. Mortality may have been considerably higher than thisbecause some dead vultures probably died away from the areas that were searched or wereremoved by scavengers. Breeding success did not appear to be unusually low, compared with thatof other Gyps species.
Both the high rate of the vulture population declines and the high directly observed death rate of adults and sub-adults indicated that an elevated mortality rate of full-grown vultures must bethe main demographic mechanism of the decline. Whether or not reduced breeding success,other than that associated with adult mortality, was also involved was not clear. However, thesefindings were sufficient to suggest that finding the most frequent cause of death of vultureswould be the key to diagnosing the cause of the population declines.
Vultures at Keoladeo National Park were observed looking ill with drooping necks foruncharacteristically protracted periods (Prakash 1999). In 1999 two OWBV were collected by BNHS and sent for post-mortem examination at the Indian Wildlife Cooperative (NorthDivision) at Hisar Veterinary College. One bird was seen to fall from a tree close to KeoladeoNational Park, from where it was recovered alive but died soon thereafter, and the second wasfound dead in the city of Delhi. The only unusual post-mortem finding was visceral gout, anaccumulation of uric acid crystals in the tissues. Extensive renal gout was evident in both birdsand was considered to have been the proximate cause of death. In both cases, the renal gout wasacute with extensive tissue destruction. There are several possible aetiologies of visceral gout,including abnormally high protein diet, primary renal failure and dehydration, but no causalfactor was identified at this stage (Cunningham 2000).
Further investigations of causes of vulture deaths in India were hampered because few fresh vulture carcasses were available for examination. This was largely due to the lengthy procedurerequired before permits to collect dead birds were issued. In 2000, the three Gyps speciesendemic to the Indian subcontinent were listed as ‘Critically Endangered’ by IUCN. Later, theywere also placed on Schedule 1 of India’s Wildlife Protection Act (1972), further increasing thedifficulty of obtaining permits to collect dead birds. This often resulted in vulture carcassesrotting or being removed by scavengers before they could be collected, and between February2000 and June 2001, only eight dead vultures were collected from the large numbers of carcassesencountered. Hence, legislation intended to protect vultures and other wildlife inadvertentlyhindered the process of identifying the cause of declines. Post-mortem examinations wereinitially conducted at the Poultry Diagnostic and Research Centre (PDRC) in Pune, India, and sixof eight birds collected were found to have visceral gout (Cunningham et al. 2003). The BNHSconsortium also engaged the Australian Animal Health Laboratory (AAHL), expert in theidentification of novel diseases, to help identify the causes of decline, although permits were onlygiven for the export of a very small number of samples, again after a very lengthy applicationprocess.
Investigations in India were made possible by funding to the BNHS consortium from the UK government’s Darwin Initiative grant scheme. As part of this programme, a captive care centrefor vultures was set up to aid in diagnostic work and develop the capacity for vulture husbandryshould conservation breeding become necessary. The centre was established in 2001 incollaboration with the Forest Department of Haryana at Pinjore and was opened in 2003 byElliot Morley, then under secretary of State for the Environment in the UK government.
Although the centre provided excellent facilities for post mortem examinations, the number ofvulture carcasses collected remained low. Despite these small numbers, it remained clear that ahigh proportion of carcasses showed evidence of visceral gout. Of 13 OWBV from India andNepal examined by February 2004, 10 (77%) had gout. Of 12 LBV, 8 (67%) had gout (Shultzet al. 2004).
The TPF/OSP group collected larger numbers of dead OWBV in Pakistan. Post mortem analyses of an initial sample of 36 birds found that 58% had renal failure as indicated by thepresence of visceral gout, but exhaustive analyses failed to find its cause (Oaks et al. 2001). Laterstudies of much larger samples confirmed this high proportion of visceral gout in OWBV inPakistan, with the highest prevalence (. 80%) being found in adult and subadult birds (Oaks etal. 2004a, Gilbert et al. 2006). Both the BNHS consortium and the TPF/OSP group looked hardfor the causes of renal damage and for other causes of death. The teams identified novel vulturepathogens. A mycoplasma was isolated from an OWBV in Pakistan (Oaks et al. 2004b) and theAAHL isolated a herpes virus from an LBV from India (Cardoso et al. 2005). However, there wasnothing to suggest that either of these played any part in the declines. Extensive analyses oftissues of dead vultures collected in Pakistan for a wide range of toxic environmental pollutants,including heavy metals, organophosphorus and organochlorine compounds and carbamates,failed to find significant numbers of birds contaminated at concentrations likely to have causeddeath (Oaks et al. 2001, 2004a).
In late 2002, the cause of the vulture declines was still eluding all of the researchers. A likely cause seemed to be an infectious disease (Pain et al. 2003, Cunningham et al. 2003). There was some evidence that declines had spread geographically. They were first noted in Rajasthan, UttarPradesh and Delhi, subsequently reported from other parts of India, and later reported fromPakistan and Nepal. This difference in timing may have been because of a spread in awarenessand thus reporting of the problem. However, good populations of vultures remained in Pakistanin 1999–2000, where they were reported to have started to decline only within the previous twoor three years (Khan et al. 2001), whereas vulture populations in most of India were alreadyseverely depleted by then (Prakash et al. 2003, 2005a). Numbers of OWBV in Pakistan thendeclined very rapidly (Gilbert et al. 2002). Work conducted in Pakistan in 2000 also found thatthe proportion of birds exhibiting neck or head-drooping behaviour, similar to that reported byPrakash (1999) for sick birds at Keoladeo National Park, was highest near the Indian border, aswere numbers of dead birds, and this was interpreted as a westward spread in the factorsresponsible for the decline (Khan et al. 2001). Head or neck-drooping was considered to be arelatively uncommon behaviour in vultures in South Asia (Prakash et al. 2003, Riseborough andVirani in Khan et al. 2001), and appears to be exhibited when vultures are sick or weak (Prakashet al. 2003; Bahat, in Katzner and Parry-Jones 2001) and during periods of extremely hotweather (Camin˜a 2001, Gilbert et al. 2007a). Whilst some considered this a noteworthybehaviour, potentially indicative of sick birds (Prakash et al. 2003), others suggested that thismay actually have low specificity and sensitivity as an indicator of poor health (Gilbert et al.
2007a).
Although these observations were consistent with the spread of an infectious disease from India to Pakistan, there were also other possible explanations (e.g. Cunningham et al. 2003). Themain reason that it was felt that infectious disease could have been the cause of the vulturedeclines was that other plausible explanations had been checked and found to be improbable.
Although no pathogen had been identified as the cause, it was well known that finding suchagents and demonstrating their effects is difficult. Hence, it seemed probable that continuedwork would uncover the pathogen. In fact, as subsequent events were to show, the same line ofreasoning can be applied to novel environmental pollutants.
In 2003 the TPF/OSP team, working in Pakistan, conducted a survey of 74 veterinarians andveterinary pharmaceutical retailers to identify livestock drugs that were known to be toxic tobird and mammal kidneys and capable of being absorbed after ingestion. Non-steroidal anti-inflammatory drugs (NSAIDs) are known to be potentially nephrotoxic in mammals, withtoxicity varying among drugs and species, and even between individuals (Hersh et al. 2005;Fletcher et al. 2006; Gooch et al. 2007). Several NSAIDs have been reported to cause renaldisease in birds (Nys and Rsaza 1983, Klein et al. 1994). The only NSAID identified as being inwidespread use was diclofenac, which was used to reduce pain, inflammation and fever inlivestock. It had been available for veterinary use in Pakistan only since 1998. In India however,diclofenac appears to have been available since circa 1990, and 19 of 23 veterinarians interviewedindicated that they had been using the drug since 1993–1994 or earlier (BNHS/RSPBunpublished data).
The team analysed kidney samples from 38 OWBV found dead in Pakistan between 2000 and 2002, and found that all of 25 birds that died with visceral gout had detectable diclofenac residuesin the kidney. By contrast, none of 13 birds that died without visceral gout had detectablediclofenac (Oaks et al. 2004a). Oaks’s team then established the toxicity of diclofenac to OWBVsexperimentally by administering high and low diclofenac oral doses to two groups of two captiveOWBVs, and then by feeding 20 OWBVs with meat from ungulates treated shortly before deathwith a standard veterinary dose of diclofenac. The vultures were affected by the diclofenac in adose-dependent way. Death occurred rapidly in all of the birds exposed to high doses and manyof those given low doses. In all cases, the dead birds had visceral gout. Histological examination revealed kidney damage similar to that found in the carcasses of wild vultures with gout (Oakset al. 2004a). It is not known how diclofenac causes renal failure, although a mechanism has beenproposed (Meteyer et al. 2005).
Oaks and colleagues announced their preliminary findings as soon as they became available, at a conference in Hungary in May 2003, well in advance of publication. This was crucial, as ithelped to speed up the process of checking whether the situation revealed so convincingly forOWBV in Punjab province, Pakistan, also held for other vulture species and across the wider areaof the Indian subcontinent from which catastrophic vulture declines had been reported.
The BNHS team moved rapidly to analyse frozen tissues collected from dead vultures found in India and Nepal. As had been found in Pakistan, all of the vultures with visceral gout haddetectable diclofenac in the kidneys or liver whilst none of the birds with no sign of gout werecontaminated (Shultz et al. 2004). This was the case for both OWBV and LBV and a highproportion of both species exhibited visceral gout. These results, taken together with those ofOaks et al. (2004a) indicated that diclofenac was associated with the rapid vulture declines beingobserved in all parts of the subcontinent. However, it was not yet clear that there was sufficientdiclofenac in the vultures’ food supply to fully account for the catastrophic declines. Manyscientists were sceptical and felt it unlikely that diclofenac alone could explain such large effects(Proffitt and Bagla 2004).
The case that diclofenac is the major or sole cause of the vulture declines There seemed to be good reasons to question whether diclofenac could be the sole cause of thevulture declines and the RSPB, BNHS and colleagues went on to investigate whether there wasany foundation to this scepticism. NSAIDs tend to have short residence times in mammaliantissue, including ungulates. In European cattle Bos taurus that receive standard veterinary dosesof diclofenac, tissue levels decline to undetectable levels after about a week (EMEA 2004, Greenet al. 2006). Hence, it seemed that an improbably large number of animals would have to betreated with diclofenac just before they died to pose a serious threat to vultures. A possibleexplanation might be that diclofenac is metabolised more slowly in Indian cattle Bos indicus thanin European cattle. However, experiments showed that this was not the case. Tissueconcentrations of diclofenac, taken from experiments in which Indian and European cattle werekilled at different intervals after dosing (Taggart et al. 2006, EMEA 2004), were used to calculatediclofenac concentrations averaged across all the edible tissues of a carcass at different times aftertreatment. A dose-response model of the toxicity of diclofenac to OWBV was derived from theexperiments of Oaks et al. (2004a) and used to estimate the proportion of vultures that would bekilled by a large meal of mixed tissues from a carcass in relation to the time of treatment and thecow’s death. The average diclofenac concentration in edible livestock tissues was sufficient to killmore than 10% of vultures feeding from the carcass of an animal treated with diclofenac onlywithin a day or two of treatment (Green et al. 2006). The rate of decline of tissue concentrationsand differences among tissues were similar for European and Indian cattle and there wereindications that a similar pattern is found in Water Buffalo Bubalus bubalis.
In order to establish the proportion of livestock carcasses that would need to contain concentrations of diclofenac lethal to vultures to have caused the observed population crash,Green et al. (2004) developed a simulation model of a vulture population using demographicrates based upon the scientific literature and expert opinion. The model assumed that thepopulation of full-grown vultures was exposed to a risk of death from diclofenac poisoning everytime they fed, because a proportion of ungulate carcasses contained a lethal concentration of thedrug. These deaths were assumed to elevate mortality rates and to reduce breeding success whenparent birds are killed. Using a range of plausible assumptions about normal mortality rates andintervals between meals, it was shown that less than 1% of livestock carcasses (0.13–0.75%,depending upon the vulture species, population and model parameter values) would have tocarry lethal concentrations of diclofenac to have caused the observed rates of OWBV and LBV population decline in India and Pakistan between 2000 and 2003. The model was also used tocalculate the proportion of dead adult and subadult vultures that would have visceral gout, thecharacteristic sign of diclofenac poisoning, if the observed declines were caused only bydiclofenac. It was found that the proportion of dead vultures observed to have gout in Pakistanand India was consistent with diclofenac being the most important cause of the decline, andperhaps its only cause, in both Pakistan and India and for both OWBV and LBV.
These analyses demonstrated that a sufficiently high proportion of dead vultures showed signs of diclofenac poisoning to account for the declines and that the proportion of contaminatedungulate carcasses need only be low. However, they do not show that sufficient ungulatecarcasses really are contaminated with high enough diclofenac concentrations to cause thedeclines. The only way to do that convincingly was to collect tissue samples from arepresentative sample of dead domesticated ungulates from many sites across India. The BNHSteam, in collaboration with the Wildlife Institute of India (WII), collected 1,848 liver samplesfrom domesticated ungulates from carcass dumps from 67 sites across 12 states in India, betweenMay 2004 and June 2005. Results of diclofenac analyses revealed that 10.1% of carcasses haddetectable concentrations. Diclofenac was found in cattle, water buffaloes, goats and horses, butnot sheep. All states showed evidence of contamination except one in which only one site wassampled (Taggart et al. 2007). These observed concentrations were then used, in combinationwith the dose-response toxicity model and the vulture population model described above, toestimate the rate of population decline expected for a population of OWBV with this levelexposure. The expected rate of decline was 80–99% per year, depending on modelassumptions, which is more than, and not significantly different from, the rate of populationdecline (48% per year) estimated from road transect surveys carried out a few years before(Green et al. 2007). Hence, there was sufficient diclofenac in ungulate carcasses available tovultures in India to cause their populations to decline at the observed rate without the need toinvoke any other causes. Studies in Pakistan estimated the proportion of diclofenaccontaminated ungulate carcasses encountered by OWBV by identifying clusters in space andtime of vultures killed by diclofenac (Gilbert et al. 2006). This research indicated thatcontamination was sufficient to account for the population decline and that variation amongcolonies and years in the rapidity of decline was strongly correlated with the mortality ratecaused by diclofenac.
Diclofenac is no longer covered by patent and more than 50 companies in India manufacturedveterinary formulations. Across the subcontinent, it appears to have been the welfare drug ofchoice for veterinarians treating livestock for a range of conditions. It is generally administeredas an intramuscular injection, although an ingestible bolus form also exists. It is likely to beuseful in a range of situations, including in rural communities, where families frequently keepwater buffalo and cattle for working the land and for milking. As a potent anti-inflammatorydrug, diclofenac can help to temporarily alleviate the effects of a range of veterinary problems(e.g. muscle inflammation in the limbs, and mastitis) and so potentially render domesticlivestock more able to continue to work productively or yield milk.
Prakash et al. (2005b) estimated that if 10–20% of the estimated 503 million livestock in India die annually and become available to vultures (only a small proportion are eaten by people), thena pharmaceutical industry estimate of 5 million annual diclofenac treatments would result in 5–10% of carcasses being contaminated with detectable concentrations of diclofenac. However,given the short residence time of diclofenac, this would only be the case if all treated animalsdied within a week of being given diclofenac. The observed 10% diclofenac prevalence in samplesfrom carcasses of domesticated ungulates (Taggart et al. 2007) suggests that considerably morethan the estimated 5 million courses of treatment are given annually, and/or that the majority ofanimals treated are fatally ill.
Finding practical ways to prevent the extinction of South Asian vultures In January 2004, as soon as the initial case for the importance of diclofenac in causing vulturedeclines had been assembled and tested, a group of conservation bodies, including both theBNHS and TPF/OSP groups, issued a Manifesto. This called for immediate action from thegovernments of all Gyps vulture range states to prevent the veterinary use of diclofenac. InFebruary 2004, two important international meetings were held to review the scientific evidence,present the emerging consensus to government representatives and to initiate the planning ofconservation action. The first was a Vulture Summit in Kathmandu, which was convened by TPFand BCN and the second was an International South Asian Recovery Plan Workshop convenedby the BNHS group (ISARPW 2004). Participants included NGOs, governmental organisationsand others from across South Asia and internationally. Two key recommendations emergedfrom these meetings and were presented in the report of the International South Asian RecoveryPlan Workshop. These were (1) that government authorities in all range states introducelegislation or regulations to prevent all veterinary uses of diclofenac that pose a risk to vultures,and (2) that captive populations of all three affected Gyps species be established immediately inSouth Asia, for the purposes of conservation breeding and subsequent reintroduction to adiclofenac-free environment.
The captive care facilities developed in India in 2001 were converted into a conservation breeding facility in 2004. These have now been expanded, and additional facilities have beenconstructed by BNHS in West Bengal and Assam. These three centres currently (as of 15th April2008) hold 83 OWBV, 71 LBV and 28 SBV. The aim of the conservation-breeding programme inIndia is to hold a minimum of 25 pairs of each species at each of a minimum of three sites. InPakistan, a facility, holding 11 OWBV, is run by the World Wide Fund for Nature (WWF)Pakistan and the Punjab Wildlife and Parks Department of the Provincial Government, withsupport from The Hawk Conservancy Trust and the Environment Agency of the United ArabEmirates. In Nepal, a facility is being developed by the National Trust for Nature Conservation,the Department of National Parks and Wildlife Conservation and Bird Conservation Nepal,supported by RSPB and ZSL. It holds 14 OWBV.
Given the widespread use of diclofenac, and the evident importance of veterinary use of this drug across South Asia, it soon became apparent that an alternative NSAID, of low toxicity tovultures and effective for the treatment of livestock, would need to be found to facilitate andexpedite a diclofenac ban. As an initial step, a questionnaire was sent to veterinarians at zoos andwildlife rehabilitation centres globally to ask which NSAIDs they had used to treat scavengingbirds, and the clinical outcome. Survey results identified the NSAID meloxicam as a potentialalternative. Meloxicam had been given to 39 Gyps vultures from six species and at least 700individuals from 54 other raptor and scavenging bird species with no ill effects. However,mortality with associated kidney damage (gout and/or renal failure) was reported with the use ofseveral other NSAIDs, including flunixin and carprofen (Cuthbert et al. 2006b).
Subsequently, a comprehensive safety-testing programme for meloxicam was initiated in South Africa, as a collaboration between South African (Pretoria University and DeWildtCheetah and Wildlife Trust), Namibian (Rare and Endangered Species Trust), Indian (BNHS,Indian Veterinary Research Institute) and UK (RSPB, Aberdeen University, CambridgeUniversity) research and conservation groups. The threatened South Asian Gyps species couldnot be used for initial testing because they were essential to the captive breeding programme andit was therefore necessary to find a surrogate species. An obvious candidate was the AfricanWhite-backed Vulture (AWBV), Gyps africanus, which is not considered to be threatened, beingclassified in the ‘Least Concern’ category by IUCN (IUCN 2007). Captive, injured or non-releasable AWBV were used to assess whether the toxicity of diclofenac to this species wassimilar to that of OWBV. Four AWBV were used for an experiment in which two wererandomly selected and given 0.8 mg kg21 of diclofenac by gavage and two were sham dosed withsterilised water. The dose was selected using the dose-response model previously established for OWBV. If diclofenac were as toxic to AWBV as it is to OWBV then there was a less than 1%chance that both of the treated birds would survive. The two diclofenac-treated birds died withintwo days with visceral gout, whilst the untreated controls remained healthy (Swan et al. 2006a).
The meloxicam safety testing trial on AWBV was implemented in stages to avoid unnecessary deaths if the drug proved to be toxic. The maximum likely level of exposure (MLE, 1.5 mg kg21body weight) to meloxicam in the wild was first estimated, based upon known concentrations inthe tissues of experimentally treated livestock and vulture food intake. At each stage of theexperiment, the dose of meloxicam administered by gavage was increased until the MLE wasexceeded. Eventually, a dose of 2.0 mg kg21 body weight was administered to a sample of 40AWBV. All birds survived these treatments with no obvious ill effects, and serum uric acidconcentration, which is greatly elevated in OWBV, AWBV and Eurasian Griffons treated withdiclofenac (Oaks et al. 2004a, Swan et al. 2006a), remained within normal limits. Next, anexperiment was performed in which captive AWBV were fed tissues from cattle treated justbefore slaughter with a higher than standard veterinary course of meloxicam. All of the sixtreated AWBV remained healthy with normal serum uric acid concentrations. Finally, tenindividuals from two of the threatened Asian vulture species (OWBV and LBV) were givenmeloxicam by gavage, five of them at a dosage above the MLE. All survived with no obvious illeffects, as did 21 birds (OWBV and LBV) fed muscle or liver tissue from water buffalo treatedwith double the standard veterinary dose of meloxicam until eight hours before slaughter (Swanet al. 2006b, Swarup et al. 2007). The results of these studies suggested that meloxicam is of lowtoxicity to Gyps vultures, and that in this respect it would be a suitable substitute for diclofenac.
Meloxicam also appears to have very low toxicity to a wide range of other raptors andscavenging birds that may encounter carcasses, with over 700 individuals from 54 speciesclinically treated with meloxicam and a further five species dosed with meloxicam at dosagesabove MLE (Cuthbert et al. 2006b, Swarup et al. 2007). Like diclofenac, meloxicam is out ofpatent, licensed for veterinary use in India, already produced for veterinary use in injectable andbolus (ingestible) form, and considered a very effective NSAID (Noble and Balfour 1996, DelTacca et al. 2002, Deneuche et al. 2004) used to treat a variety of livestock ailments (Friton et al.
2004, Hamman and Friton 2003, Milne et al. 2003).
In November 2004, BNHS, with support from RSPB, initiated an advocacy programme in India to promote a ban on the use of diclofenac. Throughout the various phases of meloxicamsafety testing, the researchers fed results through the advocacy programme to keep the Indianauthorities fully informed of preliminary research findings. A preliminary report was madeavailable to relevant government officials, and on 17 March 2005, Board Members of theNational Board for Wildlife recommended a ban on the veterinary use of diclofenac. The IndianMinistry of Environment and Forests adopted a constructive approach and held a two-dayinternational conference early in 2006. This meeting coincided with publication of the firstmeloxicam safety testing results (Swan et al. 2006b). A series of recommendations wereproduced during the meeting, of which the first was ‘to strongly recommend to theGovernments of the respective countries to take immediate steps to completely phase outveterinary diclofenac’ (MoEF 2006). In May 2006, a directive from the Drug Controller Generalof India was circulated to relevant officials for withdrawal of manufacturing licences forveterinary diclofenac. The Government of Nepal took similar action in August 2006, shortlyfollowed by the Government of Pakistan.
The governments of these countries are to be commended on the rapidity with which this action was taken. A two and a half year interval between identifying veterinary diclofenac as thecause of declines and banning its production may appear far too long given the annual vulturedecline rates, but it is rapid in comparison with many other efforts to resolve environmentalproblems. The widespread use of DDT from the mid-1940s onwards was identified as the causeof significant mortality, reduction of breeding success and population declines of birds and othernon-target species by the early 1960s (Barnett 1950, Mohr et al. 1951, Hickey and Hunt 1960,Wurster et al. 1965, Ratcliffe 1967). However, it was not until 1972 that the majority of uses of DDT were banned in the USA (Blus 2003) and 1986 before DDT was effectively banned in theUK (Pesticides Safety Directorate; http://www.pesticides.gov.uk/approvals.asp?id555).
Whilst the current bans on the manufacture of veterinary diclofenac are essential, much remains to be done to ensure that the affected species do not disappear from South Asia. Retailsale of veterinary diclofenac is still legal in India, and diclofenac is still being sold and used 9months after the ban (authors’ unpublished information). Awareness campaigns, incentives formeloxicam use and a ban on retail sale and use of veterinary diclofenac are likely to be necessaryto bring diclofenac contamination of domestic ungulate carcasses down to the very low levelsrequired for the safety of wild vultures. The use on livestock of diclofenac formulated for humanuse is also a possible barrier to the full removal of diclofenac from vulture food supplies.
Adequate monitoring is essential, both of the availability of veterinary diclofenac and its use.
The latter is best performed through carcass sampling as described by Taggart et al. (2007), withthe impact upon vultures of the observed level of contamination being assessed by modelling(Green et al. 2007). The rapidity of vulture declines and the uncertainty about when diclofenaccontamination will be removed make the establishment of conservation breeding centres acontinuing necessity. In situ conservation measures in combination with conservation advocacyand awareness programmes may also be necessary to help ensure that at least some of the smallremaining vulture populations remain extant. Two in situ measures have been proposed toreduce mortality in the wild; the exchange of diclofenac for meloxicam in areas surroundingbreeding colonies, and, in Nepal, diversionary feeding with diclofenac-free carcasses. Theefficacy of these measures will depend upon the availability of alternative food sources,the extent of use of diversionary feeding stations, and bird movements within and outside thebreeding season. Little is known of movements in Asian Gyps species. Throughout Africa andEurope, Gyps species can be sedentary, nomadic, partially migratory or migratory, withmovement patterns varying between regions and apparently in relation to seasonal resourceavailability (Bernis 1983, Mundy et al. 1992). In general, adult birds appear to be moresedentary, and juvenile and immature birds more migratory or dispersive in nature. However,preliminary results from satellite-tagged OWBV in Nepal indicate that even adult birds can passa high proportion of the non-breeding season distant from breeding sites (R. Cuthbert and H. S.
Baral unpublished data). Satellite tagging studies of 5 non-breeding adult OWBV in Pakistanfound that the maximum distance travelled from the colony varied considerably betweenindividuals, ranging from 35 to 316 km, and home range areas varied from 1,824 to 68,930 km2(Gilbert et al. 2007b).
Food provisioning near a colony of OWBV in Pakistan during the 2003–04 breeding season illustrated that the provision of clean food appeared to be able to reduce, but not eliminate,mortality from diclofenac (Gilbert et al. 2007b). There was also considerable seasonal variationin the extent to which vultures used the diversionary food, with the vulture restaurant visitedon, only 16% of days and by a relatively small number of birds at the end of the breeding seasoncompared with 74% of days by a far larger number of birds earlier in the season. There weresignificant declines in mortality when vultures were fed clean food, but no reduction in the rateat which numbers of breeding pairs (active nests) declined at the colony in the year following thediversionary feeding (298 nests in 2002–03, 203 nests in 2003–04 and 118 nests in 2004–05,AVPP 2007). These results show that, whilst food provisioning may be of some benefit, it did notprevent the population from declining. Whilst the impact of year-long food provisioningremains untested, it is likely to have a greater impact on vulture survival in areas wherealternative food is scarce, in colonies where a high proportion of birds tend to be sedentary, andwhere local diclofenac use is minimal or non-existent.
The impact on vulture populations of exchanging supplies of meloxicam for those of veterinary diclofenac is also untested, although exchange programmes are underway in Nepal, incombination with year round provisioning of safe food. Careful monitoring of the effectivenessof these programmes in reducing the rates of declines at colonies will inform future in-situactivities.
The known toxicity of diclofenac to four Gyps species (G. bengalensis, G. indicus, G. fulvus andG. africanus; Oaks et al. 2004a, Shultz et al. 2004, Swan et al 2006a), and the phylogeneticposition of these species each forming a sister relationship with one or more of the remainingGyps species (Johnson et al. 2006) suggest that all members of the Gyps genus are likely to besensitive to diclofenac. However, the NSAID survey that initially identified meloxicam as apotential alternative for diclofenac (Cuthbert et al. 2006b) also highlighted two additional issuesof concern. First, diclofenac was not the only NSAID to have been associated with gout and/orrenal failure in treated birds, and second, Gyps vultures were not the only bird species to beaffected. Five of 40 birds given carprofen died (with doses from 1.0–5.0 mg kg21), and seven of24 birds administered flunixin died (with doses from 0.5–12.0 mg kg21) with renal failure and/orgout, along with one bird given ibuprofen and one phenylbutazone at unknown dose levels. Bothcarprofen and flunixin are used to treat livestock in Europe, although not yet in South Asia, andinformation on residues of these NSAIDs in livestock tissues suggests that livestock dyingshortly after treatment could contain sufficient residues to pose a threat to scavenging birds(Cuthbert et al. 2006b).
Species that died following treatment with these NSAIDs included Gyps vultures, a Harris’s Hawk Parabuteo unicinctus, Northern Saw-whet Owl Aegolius acadicus, Red-legged SeriemaCariama cristata, Marabou Stork Leptoptilos crumeniferus, Cinereous Vulture Aegypiusmonachus and a Lappet-faced Vulture Torgus tracheliotus. The diversity of species affectedsuggests that the veterinary use of some NSAIDs may pose a problem for scavenging birds ofother species and in other areas. However, preliminary results suggest that some species,including at least one New World vulture, appear particularly insensitive to the effects ofdiclofenac (B. Rattner et al. in press). Whilst the situation in India is unique, in that vastnumbers of domestic livestock remain in the open after death, any situation in which recentlytreated livestock can be scavenged by birds presents a potential problem.
More work is urgently needed on the risks that NSAIDs pose to scavenging birds globally.
Governments should only licence NSAIDs for veterinary use if they have first been tested andfound to be sufficiently safe to scavenging birds likely to feed on the carcasses of treated animals.
It is possible that diclofenac use in India has resulted in mortality in a wider range of species than Gyps vultures. A lack of monitoring has made this difficult to investigate, but repeatedsurveys of Red-headed Sarcogyps calvus and Egyptian Neophron percnopterus Vultures haveshown that these species have declined rapidly across India, though apparently with a later onsetthan Gyps vultures (Cuthbert et al. 2006a). As no carcasses of these species have been collectedand analysed, it is not possible to determine the role that diclofenac may have played in theirdeclines.
The investigations described here have some interesting features. Quantification of the scale ofthe declines and estimation of minimum mortality rates by carcass searching were important inestablishing elevated adult mortality as the main demographic mechanism of the declines.
However, because of the absence of widespread bird population monitoring, it proved difficult tomeasure the declines and identify when and where they began. The mobilisation of scientificeffort was rapid, once the declines had been recognised, but wildlife protection legislation,though essential in other contexts, was an obstacle to identifying the cause of elevated mortality.
The engagement of a diversity of researchers from several countries and scientific disciplines andfrom academic institutions, NGOs and government agencies was vital. Their organisation intoseparate research groups, which were conducting complementary research, in competition, butalso in communication with one another, was a stimulus to progress and rigorous evaluation ofhypotheses.
Once the cause was identified, the international research and conservation community, and the Indian Ministry of the Environment and Forests, closely followed by the authorities in Nepaland Pakistan, pulled together with remarkable rapidity and determination to find a solution tothe problem. This international collaborative effort was exceptional, with academics setting asidetheir research agendas to give priority to this work alongside conservation scientists, advocates,civil servants and politicians. Conservation NGOs played a central role in arguing for action andin funding and designing relevant research. Considerable progress has already been made, butsaving Asian vultures remains a daunting challenge, requiring effort and vigilance for decades tocome. Establishing viable captive populations, removing diclofenac from the vulture food supplyin the Indian subcontinent and preventing its replacement by other toxic NSAIDs are the mainshort-term priorities. Maintaining and breeding vultures in captivity for reintroduction,restoring wild populations and preventing future adverse impacts of NSAIDs and otherveterinary drugs are tasks for the longer term.
We wish to express our appreciation of the contribution of the late Bill Burnham, formerpresident of The Peregrine Fund, to efforts to save the vultures of South Asia. We thank MarkAvery, Alistair Gammell, David Houston, Georgina Mace, Ian Newton and Stephen Piper foradvice and help, and David Gibbons for comments on the manuscript. We would like to thankthe Indian Veterinary Research Institute and the Indian Council of Agricultural Research, theIndian Ministries of Environment and Forest, Agriculture, Health, and the Drug ControllerGeneral of India, the governments of Haryana, West Bengal and Assam states, and thegovernments of Nepal and Pakistan for all of their help and support. Many thanks to the PoultryDiagnostic and Research Centre, Pune, India, and especially Dr Ghalsasi, for collaborative workand analyses. The RSPB, BNHS and ZSL would like to thank the UK government for fundingprovided under the Darwin Initiative for the Survival of Species, the British High Commission,New Delhi, the British High Commission Global Opportunities Fund, The Earth MattersFoundation, the Rufford Foundation and many individual donors. Funding for work conductedby The Peregrine Fund was provided by the Gordon and Betty Moore Foundation, The PeregrineFund, Disney Wildlife Conservation Fund, the UN, Summit, and Ivorybill Foundations,Zoological Society of San Diego, and other important donors. Finally, we thank all of theinstitutions to which the authors are affiliated for their financial and other support.
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DEBORAH J. PAIN*, CHRISTOPHER G. R. BOWDEN, RICHARD CUTHBERT, RHYS E.
GREEN1Royal Society for the Protection of Birds, The Lodge, Sandy, Bedfordshire, SG19 2DL, U.K.
1and Conservation Science Group, Department of Zoology, University of Cambridge, Downing ANDREW A. CUNNINGHAMInstitute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, U.K.
DEVOJIT DAS, VIBHU PRAKASH, ASAD RAHMANI, SACHIN P. RANADE, KALU RAMSENACHA, S. SARAVANAN, NITA SHAHBombay Natural History Society, Hornbill House, Mumbai, 400023, India.
MARTIN GILBERT, RICHARD T. WATSON, MUNIR Z. VIRANIThe Peregrine Fund, 5668 West Flying Hawk Lane, Boise, Idaho 83709, U.S.A.
RAM D. JAKATIHaryana Forest Department, Van Bhawan, sector 6, Panchkula, 134109, Haryana, India.
YADVENDRADEV JHALAWildlife Institute of India, Post Bag #18, Chandrabani, Dehradun, 248001, Uttaranchal, India.
ALEEM A. KHANOrnithological Society of Pakistan, 109/D P.O. Box 73, Dera Ghazi Khan, Pakistan.
VINNY NAIDOO, GERRY SWANDepartment of Paraclinical Sciences, Faculty of Veterinary Science, University of Pretoria, Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington 99164-7040, U.S.A.
JEMIMA PARRY-JONESInternational Centre for Birds of Prey, Little Orchard Farm, Eardisland, Herefordshire HR6 HEM SAGAR BARALBird Conservation Nepal, P.O. Box 12465, Lazimpat, Kathmandu, Nepal.
DEVENDRA SWARUPIndian Veterinary Research Institute, Izatnagar 243122, Uttar Pradesh, India.
MARK A. TAGGARTSchool of Biological Sciences, Dept of Plant & Soil Science, University of Aberdeen, AB24 3UU, KERRI WOLTERRhino & Lion Wildlife Conservation NPO, ‘‘Vulture Programme’’, Kromdraai, South Africa.
* Author for correspondence; Director of Conservation, Wildfowl & Wetlands Trust (WWT), Slimbridge, Glos GL2 7BT, U.K.; e-mail: Debbie.Pain@wwt.org.uk

Source: http://www.globalraptors.org/grin/researchers/uploads/163/08_bci_race_to_save_s_asian_vultures.pdf