In an echo of events that unfolded earlier in the West, declines of vulture populations in the Indian subcontinent are linked to an environmental poison. Three species of these birds approach extinction.
An unusually high death rate among three species of vulture in south Asia has been perplexing scientists for several years. The consequences have been severe, not just for the vultures themselves but also for their supporting natural and human ecosystems. Vultures are natural scavengers, cleaning up carrion of wildlife and domestic livestock, and also of cattle, sacred to Hindus, which cannot be consumed by people. Moreover, to avoid contamination of the earth, water and fire, people of the Parsi faith, descendants of the Zoroastrians of the Persian empires, have traditionally left their dead to vultures for disposal.
On page 630, Oaks et al.1 offer a convincing reason for the plight of the vultures. The birds have been poisoned by diclofenac, a widely used painkiller and anti-inflammatory drug that is also an all-purpose veterinary medicine for domestic livestock in the Indian subcontinent. Diclofenac is toxic to vultures that consume the carcasses of treated livestock.
The unusual pattern of mortality was first observed in early 1997 among the Oriental white-backed vultures, Gyps bengalensis (Fig. 1), nesting in Keoladeo National Park in northwestern India. Birds dropped from their perches to die shortly afterwards; many remained suspended in branches until their carcasses were finally dispersed by the wind. The number of breeding pairs in the park dropped from 150 in the 1996–97 nesting season to 25, 20 and 0 over the following years2,3. Anecdotal reports began to circulate of local declines of white-backed vulture populations throughout India and also of a related species, the long-billed vulture Gyps indicus, which occurs in peninsular India and in southeast Pakistan. In consequence, a conference was convened in Mumbai in August 1999 by Asad Rahmani, director of the Bombay Natural History Society, to consider the possible causes. In the following year, numbers of the slender-billed vulture Gyps tenuirostris were also found to be declining rapidly over its range in northern and northeast India. East of the subcontinent, relict populations of white-backed and slender-billed vultures survive in northern Cambodia, but very little is known of their status.
The meeting at Mumbai had a parallel with events 34 years earlier. Then, reports of the local disappearance of peregrine falcons, Falco peregrinus, prompted a conference that was held in Madison, Wisconsin, at the behest of J. J. Hickey4. Here, too, explanations for the population declines were proposed, but none could gain adequate support. At the Madison meeting, Derek Ratcliffe described his observations in Great Britain of peregrine falcons eating their own broken eggs4. In a now-classic paper5, published in 1967, he demonstrated that a physical change had begun in about 1947 in the form of reduced weights of the eggshells of peregrines and of several other species of raptorial bird. Only after an additional two years of intensive research could it be concluded that a new environmental contaminant in the form of the DDT-derived compound DDE (dichlorodiphenyldichloroethylene) was responsible for both the shell thinning of peregrine falcon eggs in Britain and the extinction of breeding peregrines in the eastern United States.
After a comparable time from the 1999 Mumbai conference, Oaks et al.1 demonstrate that the collapse of vulture populations in Pakistan has also been caused by a new environmental poison. Diclofenac is a very different kind of toxin from DDT, and travels along a very different pathway. But these findings are likely to have an equivalent impact to that produced by Ratcliffe's 1967 paper.
The Peregrine Fund, based in Boise, Idaho, began investigations of the vulture mortalities in Pakistan in 2000, in collaboration with the Ornithological Society of Pakistan. Parallel investigations were under way in India by the Bombay Natural History Society, in collaboration with the UK Royal Society for the Protection of Birds. Both groups initially focused on the search for a new disease factor, possibly one that had ‘jumped’ from another species; a disease hypothesis had remained the only plausible explanation for the observed mortalities6,7.
In both countries, necropsies of birds that had died suddenly in good physical condition showed that they had suffered from visceral gout — the accumulation of uric acid throughout the body cavity following kidney malfunction. Kidney failure has been an infrequent but serious side effect of the non-steroidal anti-inflammatory drugs that have come into widespread use over the past 30 years8,9,10. That the vulture mortalities might be caused by a veterinary medicine is not a hypothesis that comes easily from a wildlife biologist. But it emerged more naturally from two of the veterinarians working with the Peregrine Fund in Pakistan, Lindsay Oaks and Martin Gilbert, who put it to the test.
An initial survey indicated that diclofenac, introduced as a human medicine in the 1970s as a painkiller and anti-inflammatory agent, had recently come into widespread use in Pakistan as a veterinary medicine. Oaks et al. found that kidneys of vultures dying with the visceral gout syndrome contained residues of diclofenac, whereas vultures dying of other, known, causes did not. They also found that doses prescribed for domestic animals, and meat from domestic animals treated with such doses, were lethal to captive vultures, which died with the same symptoms as observed in wild birds. Oaks et al. are careful to limit their conclusions to Pakistan. But diclofenac is widely used as a veterinary medicine in India11, where populations of all three species continue to decline; the conclusions apply also to Nepal and Bangladesh.
Has this discovery come in time to save the three species from extinction in the subcontinent? Banning most uses of DDT permitted the recovery of peregrine falcons, but adequate, although more expensive, substitute pesticides were available. Most, if not all, of the potential substitutes for diclofenac are related drugs11 that act in a similar way12,13,14 and are also known to affect kidney function8,9,10,14. Settling on an acceptable substitute is very unlikely to happen before the birds are extinct in the wild; moreover, ways of implementing and enforcing a ban on the use of diclofenac as a veterinary medicine must be considered in any conservation strategy. India alone has an estimated 20,000 pharmaceutical companies and 500,000 pharmacists, who take “competition to a questionable extreme”15.
The California condor, Gymnogyps californianus, also being poisoned by an environmental contaminant in the form of fragments of lead ammunition, was rescued from extinction by bringing all surviving birds into captivity. Such a programme, which would permit vultures to survive until they or their progeny might be reintroduced into the wild, is being discussed in India, and could yet be implemented in Pakistan. But talk has not resulted in action. In India, as occurred earlier in California, the argument is being made that ‘nature’ should be allowed to take its course. The immediate need to quarantine a sufficient number of each species to ensure their survival is ignored in discussions that focus on longer-term captive breeding and who would undertake it.
The surviving vultures are increasingly difficult to find, and because of the abundance of carcasses in the countryside, are increasingly difficult to trap. An effective conservation programme that might yet permit the survival of these birds in south Asia must emerge from the talking stage within the next several months. In demonstrating the cause of the mortalities, Oaks et al. also provide the impetus for the development of such a conservation programme; the timing of their paper is indeed propitious.
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This article was published online on 28 January 2004 (doi:10.1038/nature02365).
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