Diclofenac: A new environmental poison in South Asia

Robert W. Risebrough1

Key words: India, Gyps vultures, diclofenac, NSAIDs

There are relatively few precedents for the rapid collapse of populations of three species of Gyps vultures in South Asia; all of them followed the appearance of either a novel disease factor or a new environmental chemical. Studies in Pakistan have shown that diclofenac, a non-steroidal anti-inflammatory drug (NSAID) that has recently come into use as a veterinary medicine, is particularly toxic to white-backed vultures (Gyps bengalensis), providing an unexpected explanation for the high incidence of vulture mortalities that has caused the population declines. White-backed vultures died with the visceral gout that has been characteristic of the vulture mortalities in India, Pakistan and Nepal after feeding on the meat of livestock treated with prescribed doses; diclofenac residues were present in the kidneys of vultures found dead with visceral gout, but were not present in the kidneys of birds that had died of other causes. Diclofenac is widely used as a veterinary medicine in India in a minimum of 48 formulations produced by a minimum of 27 companies.

It was introduced as a veterinary medicine in or around 1994; a reduction in the number of nesting pairs of white-backed vultures and a pattern of unusual mortalities were first documented in the 1996-97 nesting season.

With a probable contribution of other NSAIDs that also affect kidney function, diclofenac rather than an infectious disease therefore appears to be responsible for the population declines of Gyps vultures in South Asia.

Since most if not all of the potential substitutes for the use of diclofenac in veterinary medicines are also NSAIDs that affect kidney function, and considering the continuing rapid rate of population decline, it is very unlikely that a substitute that is safe for vultures will be available before the birds are extinct in the wild.

Only the immediate shelter of an adequate number of each of the three species with monitoring of the food supply will permit their continuing survival; if an effective substitute is not introduced within 2-3 years a captive breeding program will be necessary to ensure that these vultures can eventually be reintroduced to the skies of the Subcontinent.

1The Bodega Bay Institute, 2711 Piedmont Ave.,
Berkeley CA 94705, USA
Email: pelecanus@igc.org

The population collapses in South Asia of three species of Gyps vultures, the white-backed vulture (Gyps bengalensis), the long-billed vulture (Gyps indicus) and the slender-billed vulture (Gyps tenuirostris) are events almost without precedent in their magnitude and their impact; fewer than 10 years ago these were among the most abundant bird species in the Indian Subcontinent. Prevention of their extinction has become a conservation priority, not only in India but throughout South Asia.

THE PRECEDENTS

The relatively few precedents for these rapid population declines have been associated with the appearance of either a new disease factor or of one or more new environmental chemicals. Of comparable ecological impact was the devastation of the American chestnut (Castanea dentata), a dominant hardwood species in eastern North America, by the chestnut blight fungus (Cryphonectria parasitica) in the early 1900s.

The consequences included a major change in the forest tree composition and a reduction in the food available for wildlife (Anagnostakis 1995). Introductions of avian malaria (Plasmodium relictum) and its mosquito vector Culex quinquefasciatus to the Hawaiian Islands resulted in the decline and extinction of native Hawaiian honeycreepers of the subfamily Drepanidinae; survivors are generally restricted to highland areas not inhabited by the mosquitoes (Warner 1968, Fonseca et al. 2000, Atkinson et al. 2000). The decimation of populations of other species following the appearance of a new disease factor has recently been reviewed by Daszak et al. (2000, 2001).

More similar to the pattern of population decline of the vultures appears to be the extinction of the peregrine falcon (Falco peregrinus) as a breeding species in eastern North America south of the Arctic between the end of World War II and sometime in the early 1960s.

This remarkable event occurred before any ornithologist was aware that a population decline was underway (Hickey 1969). It is attributed primarily to the appearance in the environment of a new poison in the form of DDE, a derivative of the insecticide DDT that impairs the reproduction of peregrine falcons and other sensitive species by affecting the structure of the eggshell (Hickey & Anderson 1968, Heath et al. 1969, Cade et al. 1971, Risebrough & Peakall 1988).

Contributing to this extinction process was an increase in the rate of adult mortality caused by the trophic accumulation of more toxic environmental chemicals, particularly the biocide dieldrin (Newton 1979, Nisbet 1988). If the range of the peregrine falcon had been restricted to eastern North America, the extinction of the species would have been assured.
There are also similarities with the population decline of the New World vulture the California condor (Gymnogyps californianus) over the twentieth century that almost resulted in the extinction of this species. Condors were being poisoned by fragments of lead ammunition in the carcasses of animals killed but not retrieved by hunters (Janssen et al. 1986); the increase in adult mortality in a species with a low rate of reproduction was sufficient to cause the population decline and near-extinction.

No new pesticides or a new combination or formulation of pesticides that could account for the vulture mortalities came into use in India over the past decade. Nor was there any indication of an increase in applications of poisons to carcasses that would explain the disappearance of vultures and the survival of other scavengers over the Indian Subcontinent within an interval of only a few years. A chemical poison had therefore been discounted as the cause of the population collapses (Risebrough in press).

DEVELOPMENT OF THE DISEASE HYPOTHESIS

Studies of Vibhu Prakash in Keoladeo National Park (KNP) had documented a decrease in the number of nesting pairs of the white-backed vultures from 353 nests in 1987-88 to 150 in 1996-1997 (Prakash 1999). In 1998 anecdotal reports of local disappearances of vultures were circulating throughout India, prompting the issuing of a 'Vulture Alert' by Dr. Asad Rahmani, Director of the Bombay Natural History Society (BNHS); among more than 50 responses from all over India to a questionnaire, many documented the increasing scarcity of Gyps vultures in areas where they had been common only a few years earlier.

On 6 August 1999 Dr. Rahmani (in litt. 1999) convened a Vultures Conservation Strategy Planning Meeting in Mumbai which discussed possible causes of the disappearance of vultures and steps that might be taken. A review later in 1999 of the causes that had been proposed lead to the conclusion that only an infectious disease, either one that had 'jumped' from another species or that had originated by mutation from a previously benign form, could explain the pattern and the magnitude of the mortalities (Risebrough 2000). Dr. A. A. Cunningham of the Zoological Society of London began an active program to look for a disease factor, in collaboration with the Poultry Diagnostic and Research Centre in Pune (Cunningham et al. 2001).

A workshop devoted to the vulture crisis convened by BNHS in Delhi in September 2000 (Rahmani and Prakash 2000), a workshop at the 4th Eurasian Conference on Raptors in Sevilla in September 2001 (Katzner & Parry-Jones, 2001), a Roundtable Discussion at the International Ornithological Congress in China in August 2002 (Risebrough et al. in press), and the introduction to a session on the Asian vulture crisis at the 6th World Conference on Birds of Prey and Owls in Budapest in May, 2003 (Risebrough in press) each adopted the disease hypothesis as the only plausible explanation of the vulture mortalities in the absence of a credible alternative.

All tests for pesticides, for other poisons present in food webs and for poisons applied to carcasses to kill tigers, wolves or other predators preying on livestock - had turned up negative. Yet intensive efforts to find a disease factor by several laboratories (Cunningham et al. 2001, Cunningham et al. 2003, Oaks et al. 2001, Oaks et al. in press 2004a, 2004b) were all unsuccessful.
The first necropsies of birds that had died of the new 'disease', a bird that had died shortly after falling into water in KNP in October 1999, and another that was found dead in a garden in Delhi in December 1999 reported visceral gout, the deposition of uric acid crystals throughout the visceral cavity (Mishra et al. (2002). The uric acid contains the waste nitrogen that must be excreted; its accumulation in the visceral cavity is an indication of kidney failure. Visceral gout has been a characteristic of birds dying of the 'disease factor' (Cunningham et al. 2003: 5 of 7 adults and subadults found dead; Oaks et al. 2001: 49 of 69 adult vultures found dead; Oaks et al. in press 2004b: 219 of 259 adults and subadults found dead).
Factors inducing kidney failure that result in the production of visceral gout were therefore given particular consideration in the search for the cause of the mortalities (M. Gilbert in litt. 2002). In January 2003, an African white-backed vulture (Gyps africanus) died with visceral gout at the San Diego Zoo two days after being
treated
with ketoprofen, a non-steroidal anti-inflammatory drug (NSAID (M. Busch and B.A. Rideout, quoted by Oaks et al. 2004b).

STUDIES IN PAKISTAN IMPLICATING DICLOFENAC

A survey undertaken by Peregrine Fund researchers in Pakistan of 74 veterinarians and veterinary pharmaceutical retailers to identify veterinary drugs known to cause kidney failure indicated that diclofenac, an NSAID, was widely used (Oaks et al. in press, 2004a, 2004b). NSAIDs came into use in human medicines in the 1970s as pain-killers that also reduced fevers and inflammations. Kidney damage or failure has long been recognized as a side-effect in sensitive individuals of diclofenac and other NSAIDs (O'Brien 1986, Schwarz et al. 1988, Murray and Brater 1993, 1997, Brater 1999).
Kidneys of 38 vultures were selected for analysis for diclofenac. Of these 25 had died with visceral gout; the cause of death had been determined for 8 of the remaining 13. Kidneys of all 25 vultures that had died with visceral gout contained detectable residues of diclofenac at concentrations from 0.051 to 0.64 Fg/g wet weight; none of the others contained detectable diclofenac (< 0.01 Fg/g); the possibility that this distribution would occur by chance is vanishingly small, establishing an association between the presence of diclofenac and the occurrence of visceral gout.
Two birds were given the doseage recommended for both large and small species of domestic livestock, 2.5 mg/kg of body weight; in two days the birds were dead with visceral gout. Another 2 birds were given a doseage of 0.25 mg/kg. One died in two days with visceral gout; the other survived although at 24 hrs there were elevated levels of uric acid in the blood, indicating kidney misfunction that was reversible.
Eleven weeks after the beginning of an experiment to test the transmission of a suspected disease factor, the food supply was changed. Seven of the ten birds in the experiment died over a three-day period, the others over 13 days, all with visceral gout. The new meat was later shown to contain 6.4 Fg/g of diclofenac. In a later experiment, a dose-dependent association between diclofenac ingestion and mortality with visceral gout was demonstrated (Oaks et al. in press 2004b).
These studies therefore demonstrated that doses of diclofenac prescribed for both small and large domestic animals are fatal to white-backed vultures, and that the diclofenac is sufficiently persistent in the carcasses of treated livestock to be ingested in lethal quantities by vultures.

DICLOFENAC USE IN INDIA

In August-September 2003 I visited the College of Veterinary Science in Guwahati, Assam (Dr. Nasser Ahmed, Prof. K.K. Sarma), the Veterinary Clinician Centre in Nagercoil, Tamil Nadu (Dr. C. Jeyapaul, Dr. A.T. Sekhar and Dr. A. Abokan), the Veterinary Poly Clinic and the Department of Animal Husbandry in Jaipur, Rajasthan (Dr. T.M. Ramchandani, Dr. C.M. Sharma and Dr. Y.P. Singh), the Central Veterinary Hospital in Dakha, Bangladesh (Dr. A.B.M. Shahid Ullah) and the Fauna Veterinary Clinic in Colombo, Sri Lanka. All confirmed that diclofenac is a very widely used veterinary medicine throughout the region for the treatment of lameness, for relieving symptoms of ephemeral fever, a viral disease affecting cattle, for all inflammatory conditions and fevers, as well as for general purposes when an illness is not diagnosed.
The Current Indian Veterinary Index (Anonymous 2002) is a yearly publication that lists the drugs and other medications currently available to veterinarians in India. Included is information about the symptoms, mechanisms of action of the drug, recommended doses, precautions about when not to use each drug, and the name of the manufacturer. The section on NSAIDs lists 19 products containing diclofenac alone, 19 additional products which contain a combination of diclofenac and paracetamol, and one consisting of a combination of diclofenac, paracetamol and dicyclomine hydrochloride, in a total of 46 formulations produced by 25 companies. Two additional formulations produced by an additional two companies were in the inventory of Professor Sarma; a minimum of 48 formulations of veterinary medicines containing diclofenac are therefore produced by a minimum of 27 companies in India.
Among other NSAIDs, the Veterinary Index lists 8 formulations of analgin (metamizole) and six additional formulations in combination with other drugs; analgin had been in use before the introduction of diclofenac to the veterinary market (K.K. Sarma, pers. comm). Also listed are two formulations of aspirin, three of ibuprofen, one of meloxicam, two of naproxen, and one of phenyl butazone (Anonymous 2002). Among the NSAIDs diclofenac is therefore present on the market in a greater number of formulations and is distributed by a larger number of companies than are the other NSAIDs.
A search of the internet yields the names of other companies that have diclofenac formulations in veterinary medicines on the market in India, e.g. Elder Veterinary Division (http://www.elder-group.com/div_vet.html) opens its website with the words "India, being the largest producer of milk in the world, has the largest population of cattle in the world. Prevention and health care of such population of cattle is of paramount importance for the country." Websites of Indian pharmaceutical companies indicates that the industry is very vigorously promoting veterinary medicines containing diclofenac, not only for use in India but also for the export market.
Diclofenac was first used in veterinary medicines in India in or around 1994 (Dr. Nasser Ahmed, College of Veterinary Science, Guwahati, Dr. C.M. Sharma, Deputy Director of the Animal Husbandry Department, Jaipur, and Dr. T.M. Ramchandani, Assistant Director of the Veterinary Polyclinic, Jaipur) . In a survey undertaken by The Peregrine Fund among 84 veterinarians and drug retailers in Pakistan , 71 respondents reported that use of diclofenac in veterinary medicines in Pakistan had begun within the past five years (Oaks et al. in press 2004b).
The major decline in the number of vultures in the skies over Mumbai occurred in the late 1980s ®. Naoroji personal communication). Diclofenac was already in widespread use in human medicines at that time; the consumption of human bodies by vultures may well have been the cause of their local disappearance. The population declines appear therefore to have begun after local exposures of vultures to diclofenac.

THE 'DICLOFENAC HYPOTHESIS': QUESTIONS AND RESPONSES

Can the diclofenac hypothesis account for the collapse of vulture populations in India? Questions and concerns have been raised that require responses and explanations before this hypothesis can be accepted as valid and fully credible.
1) "For any veterinary drug to have played a significant part in the declines in India, it must have been used across the Indian subcontinent on the majority of livestock, probably at frequent intervals over the last decade." (Website, Vulture Rescue, 5 December 2003; http://www.vulturerescue.org)
In India most of the cattle are feral and are not consumed by humans. Nor do most of them receive veterinary care. Previously almost all of them would eventually be consumed by vultures. Yet the data from Pakistan indicate that the carcass of one treated animal may cause the death of a number of vultures. If a vulture eats at a carcass once a week, over a ten-year period it would eat at 520 carcasses. If only one carcass in 500 were from a treated animal, each vulture would likely to be exposed to a treated carcass in the course of its lifetime. It would not therefore be necessary to treat the majority of livestock, or to repeat treatments, to account for the number of mortalities sufficient to have caused the population declines.
In Pakistan the animal husbandry is more intensive. Cattle are raised for beef, but animals destined for food must be slaughtered by Islamic ritual. Animals that have died of disease are left for the vultures. The percentage of carcasses in Pakistan that are of livestock treated with diclofenac is therefore expected to be higher than in India.
2) In Pakistan the doses recommended for diclofenac are 2.5 mg/kg of body weight, but in India the recommended doses are lower, 1 mg/kg body weight (Anonymous 2002).
If recommendations are usually followed, exposure of vultures to diclofenac in India would be correspondingly lower than in Pakistan. As noted below, there are as yet no data on the fate of vultures in the field that consume amounts of diclofenac lower than those shown in Pakistan to result in death within a 2-3 day period.
3) Kites (Milvus migrans) and other scavengers consume the same carcasses as the vultures but have shown no reductions in population numbers.
The empirical realities are that doses given to domestic animals are sufficient to kill vultures and that no data on the toxicity of diclofenac to other scavengers are yet available. Because the smaller Gyps vultures may consume proportionately more of the viscera than other scavengers, on the average they would ingest more of the diclofenac that is bound in kidneys and other visceral tissues. Differences in the rates of metabolism may exist among species, just as differences in the rate of metabolism of ketoprofen among human individuals are related to the magnitude of damage to the kidney; duration of half-life is positively correlated with severity of renal failure (Stafanger et al. 1983). If vultures were less efficient in metabolizing diclofenac, the magnitude of kidney damage would be greater.
4) Diclofenac "has been shown to be toxic to birds and dogs ..." (Website, Vulture Rescue, 5 December 2003; http://www.vulturerescue.org).
Since
populations of feral dogs are believed to have increased as a result of greater food availability, although data supporting this assumption are apparently not available, a sensitivity of dogs to diclofenac would weaken the diclofenac hypothesis. I have so far not been able to locate any information that would support this statement beyond the studies with vultures in Pakistan. The Current India Veterinary Index (Anonymous 2000) recommends the same dose for dogs, 1 mg/kg, as for cattle and other larger species of livestock. Dogs have been used in studies of physiological effects (i.e. Stierlin et al. 1979, Stierlin & Faigle 1979, Tsuchiya et al. 1980, Brideau et al. 2001) which did not record a particular sensitivity. Moskovitz et al. (1987) reported studies in which mature dogs were given diclofenac at 2.0 mg/kg subcutaneously once a day for 42 days; spermatogenesis was quantified and showed a marked and statistically significant increase.
5) The half-life of diclofenac is considered to be short, such that concentrations in livestock that die after treatment would not be toxic to vultures.
The empirical reality is that diclofenac was found in kidneys of vultures that had died with visceral gout and that comparable concentrations were present in the kidneys of vultures that died after consuming diclofenac-contaminated meat. Most of the half-life studies refer to concentrations in blood rather than in tissues where diclofenac is bound, either to the cyclo-oxygenase enzymes that promote biosythesis of prostaglandins that induce the expression of pain and inflammation or to a specific receptor molecule affecting the messenger RNA expression for the enzyme (Sommeraurer et al, 2001). It is the extent of binding to the receptors, i.e. concentrations in the kidney tissue, and its half-life in this phase that are the relevant parameters to measure and to consider, rather than the half-life of diclofenac in the blood.
6) In India "Affected birds exhibit signs of illness .... for approximately 30 days prior to death" (Cunningham et al. 2003) but in Pakistan birds died in 2-3 days after exposure to diclofenac.
Dr. Prakash had observed neck drooping at five nests of white-backed vultures in Keoladeo National Park for periods of approximately 30 days before the birds died. From these observations one can not conclude, however, that all of the mortalities were preceded by 30 days of neck-drooping behavior. Observations of a sufficient number of marked birds identifiable in the field would be necessary to determine the percentage of mortalities that are preceded by an extensive period of sickness. Most of the doses given to birds in Pakistan under experimental conditions in the laboratory were in the lethal range. Birds in the field are expected to be exposed to a wide range of concentrations, from those that have no adverse effect to those that are lethal within a short time. Missing are data on the effects in the field of the intermediate range of exposures. Surely some of these birds are sick or otherwise incapacitated until they either recover or succumb. The experiments in Pakistan did show an increase in uric acid in the blood of a bird that was exposed to diclofenac and eventually recovered. Dehydration or other stresses after exposure while uric acid concentrations remain high might provoke the conditions that lead to visceral gout and rapid death.
7) With the exception of lesions that appear to be caused by a viral disease, discussed below, all of the questions that have been raised about the diclofenac hypothesis appear to have answers.

THE 'INFECTIOUS DISEASE HYPOTHESIS':
QUESTIONS AND RESPONSES

1) "the observations and laboratory findings in India remain more suggestive of an infectious disease" (Website, Vulture Rescue, 5 December 2003; http://www.vulturerescue.org).
Considering the very wide range of side-effects produced by diclofenac and other NSAIDs, could the lesions observed by Cunningham et al. (2003) that died in captivity without visceral gout be attributed to diclofenac?
2) "once a vulture was seen to be sick, it invariably died " (Cunningham et al., 2003).
Yet all 23 'very sick' vultures recently brought into the Vulture Care Centre have survived after being given adequate food, water, and shade (V. Prakash & A.R. Rahmani pers. comm., Prakash et al. 2004). This is not the expected result of a fatal infectious disease, but is consistent with a sublethal poisoning.
3) Only one of twenty vultures that were picked up sick and that later died in captivity had visceral gout, in contrast to birds found dead in the wild; this difference between birds dying in the wild and in captivity was highly significant (Cunningham et al. 2003).
Might the provision of water have been the critical difference between the two groups? The provision of water to a sick bird would cure any dehydration,
keeping uric acid concentrations below the critical level that would induce visceral gout and a rapid death.
Can we not assume that most of these birds dying in captivity would have acquired visceral gout if they had been allowed to die in the wild? The symptoms detected at their necropsies must therefore be assumed to be caused or associated with the factor responsible for the visceral gout.
4) Of the twenty birds that were picked up sick and that later died in captivity, four had "haemorrhages within the intestinal mucosa", 13 of 20 had enteritis and 15 of 19 had vasculitis (Cunningham et al. 2003).
NSAIDs work by inhibiting the cyclo-oxygenase enzyme complex (COX) that is responsible for the biosynthesis of prostaglandins which induce the expression of pain and inflammation. This enzyme exists in two isoforms, COX-1 and COX-2. Inhibition of COX-1 is thought to be the main cause of the adverse gastrointestinal effects of NSAIDs, which include perforations, ulcerations and bleedings, (Zimmerman et al. 1995, Kawai 1998, Bjarnason 1999, Larousse &Veyrac 2000). Diclofenac, however, induces in people a lower level of gastrointestinal bleeding than the majority of NSAIDs (Garcia Rodriguez 1998). Yet diclofenac is a plausible cause of the four "haemorrhages within the intestinal mucosa". Moreover, NSAIDs have been shown to induce both enteritis (Sigthorssonet al. 2002, Tanaka et al. 2002) and vasculitis (Epelde & Boada 1995, Morros et al. 1995, Skowron et al. 2002, Schneider et al. 2002). The lesions attributed by Cunningham et al. (2003) to an infectious disease may therefore be plausibly attributed to diclofenac.
5) The rate of population decline has not slowed with the reduction of bird-to-bird contact as the birds have become rare (below).
Since the probability of a vulture consuming a treated carcass is related to the frequency of diclofenac use and not to the density of vultures, the probability of mortality would change only with an increase or decrease in diclofenac use. If, however, mortalities are caused by an infectious disease, transmission of the disease from bird to bird would be related to the densities of the vulture populations; the rate of mortalities would be expected to decrease as populations decline. To date, a slowing of the rate of mortalities has not been observed, favoring the 'diclofenac hypothesis' over the 'infectious disease' hypothesis.
6) The working conclusion that emerges from this analysis is that diclofenac induces in vultures the same range of effects that are induced in both humans and laboratory animals but that threshold concentrations are much lower. Of high priority among future investigations would be determination of rates of metabolism and excretion, since a lower rate of breakdown of diclofenac by vultures could account for their exceptional toxicity.

AN EFFECTIVE SUBSTITUTE FOR DICLOFENAC?

By the end if the 1960s sufficient evidence had accumulated to show that the DDT compound DDE was depressing the reproduction of a number of species of raptorial and fish-eating birds in North America, that the peregrine falcon had already become extinct as a breeding species in eastern North America, and that the bald eagle (Haliaeetus leucocephalus) was rapidly declining over its range in the lower 48 states. DDT was not needed for disease vector control. A critical component in the campaign to save these species of wildlife was the availability of adequate substitutes for the principal uses of DDT. This need was readily filled by a variety of other biocides that were less persistent, but more expensive. Cost will be a factor in a search for a substitute for diclofenac in South Asia, but the availability of a suitable substitute will be the critical factor.
It is unlikely that any of the other NSAIDs currently in use will meet this need. Development of the newer drugs has focused on the selective inhibition of the COX-2 component of the enzyme complex while reducing inhibition of the COX-1 component that is necessary for the maintenance of the integrity of the gastrointestinal system. The intent has been to produce NSAIDs that would be effective pain killers and suppressors of inflammation without producing the level of adverse gastrointestinal effects caused by diclofenac and other non-specific inhibitors of the COX enzyme system. These newer drugs include meloxicam (Barner 1996, Furst 1997), celecoxib and rofecoxib (Ahmad et al. 2002) .
As noted above, it is the depression of renal function resulting from prostaglandin inhibition that creates the toxicity of diclofenac to vultures. The depression of renal function appears to be a common adverse effect of other and perhaps all NSAIDs (O'Brien 1986, Brater 1999, Zhao et al. 2001, Niccoli et al 2002). Rofecoxib induces a particularly high level of renal dysfunction
(Papaioannides et al. 2001). Another NSAID can not therefore be recommended as a replacement for diclofenac without extensive testing of its toxicity to vultures.
The assistance and participation of the veterinary community is a necessary next step in finding a substitute for diclofenac that is safe for vultures.
Diclofenac is relatively cheap; the cost to a veterinarian for a single treatment of a 200 kg animal is about 4-6 rupees or $ 0.10. Meloxicam is about six times more expensive (Anonymous 2002).

CAN THE THREE SPECIES BE SAVED FROM EXTINCTION?

The continuing sightings by bird-watchers throughout India of small groups of vultures are usually interpreted as evidence of a 'recovery' - but as long as the mortality rates remain much too high to sustain the species, these are populations on their way out. At this conference, Shultz et al. (2004) report on the results of surveys undertaken at several sites in India over the past three years; the yearly rate of decline has been and remains in excess of 30%. Censuses in Rajasthan undertaken by the Tourism and Wildlife Society of India and the Rajasthan Patrika, the widely-distributed Hindi-language newspaper, have recorded a similar rate of population decline (Vardhan et al. in press). In Pakistan, studies of Dr. Martin Gilbert (personal communication) have documented an even higher rate of recent decline in some areas. All of these surveys have demonstrated a higher rate of decline of the white-backed vultures than that of the long-billed vultures. But data presented at this conference by BNHS researchers indicate a continuing steady decline in the numbers of long-billed vultures at Bayana in eastern Rajasthan (Gomathi et al. 2004).
Considering the continuing rapid rate of population decline, it is very unlikely that a substitute for diclofenac that is safe for vultures will be available before the birds are extinct in the wild. Only the immediate shelter of an adequate number of each of the three species in contained facilities, with monitoring of the food supply to ensure that it is free of NSAIDs, will permit their continuing survival. The immediate need is not for captive breeding facilities, but for holding facilities that would house birds captured over the next several months. The captive breeding facilities could be built over time as a recovery plan is developed.

There is no time to be lost.

ACKNOWLEDGEMENTS

Research in India was supported by the Division of International Conservation of the U.S. Fish and Wildlife Service; I thank David Ferguson for his continuing support. I am indebted to the following for their assistance in accomplishing this project: Dr. A. Abokan, Dr. Nasser Ahmed, Dr. Anwaruddin Choudhury, Dr. Robert Grubh, Dr. C. Jeyapaul, Mr. Kulojyoti Lahkar, Mr. Rishad Naoroji, Dr. T.M. Ramchandani, Prof. K.K. Sarma, Dr. A.T. Sekhar, Dr. C.M. Sharma, Dr. A.B.M. Shahid Ullah, Dr. Y.P. Singh, Mr. Harsh Vardhan and Mr. N.K. Vasu. I particularly thank Drs. Asad Rahmani and Vibhu Prakash for the invitation to participate in this conference.


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