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Since the 1990s vulture populations across the Indian subcontinent have collapsed (Gilbert et al. 2002; Prakash et al. 2003; The Peregrine Fund 2004). At least three species have been affected: the oriental white-backed vulture [OWBV; Gyps bengalensis (Gmelin)], long-billed vulture [LBV; Gyps indicus (Scopoli)] and slender-billed vulture (Gyps tenuirostris Rasmussen & Parry). Populations have declined by more than 95% within about 10 years (Prakash et al. 2003; The Peregrine Fund 2004), leading the IUCN–World Conservation Union to list all three species as critically endangered (Hilton-Taylor 2000). Much evidence indicates that the decline of OWBV in Pakistan has been caused by toxic effects of diclofenac, a non-steroidal anti-inflammatory drug used widely on cattle Bos indicus L. and water buffalo Bubalus bubalis (L.) in the Indian subcontinent to reduce inflammation caused by trauma and infectious disease (Oaks et al. 2004). Diclofenac poisoning of wild vultures is thought to occur when they feed on carcasses of treated livestock. Diclofenac causes renal disease in OWBV. In experiments, captive vultures died after feeding on tissues of domestic animals that had received a normal veterinary dose of the drug a few hours before death. At post-mortem examination, these birds showed extensive visceral gout: deposits of uric acid on and within internal organs due to kidney failure (Oaks et al. 2004).
A high proportion (85%) of OWBV found dead and dying in Pakistan had extensive gout. All kidney samples analysed from birds with gout contained residues of diclofenac, whereas none of the samples from birds without gout did so (Oaks et al. 2004). These findings led Oaks et al. (2004) to propose that that diclofenac was the cause of the OWBV population decline in Pakistan and possibly elsewhere in the subcontinent, wherever diclofenac is widely used in the treatment of livestock. Recent post-mortem and diclofenac data collected from dead or dying OWBV and LBV in India and Nepal also show a high proportion with gout, and the same perfect association of gout with diclofenac in both species (Shultz et al. 2004) as found for OWBV in Pakistan. However, neither of these studies established whether diclofenac poisoning is sufficient, on its own, to cause the very rapid rates of population decline observed across the subcontinent. In this study, we used a simulation model of vulture demography and foraging ecology to estimate the proportion of vulture deaths caused by diclofenac that would be expected, at observed rates of vulture population decline, if diclofenac was the only cause of the declines. We then compared the modelling results with post-mortem data from Pakistan, India and Nepal. We also used the model, with post-mortem and population survey data, to estimate the proportion of excess mortality, beyond that expected in a stable population, that is caused by diclofenac.
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Our analyses of population trends show that vulture declines occurred at a rapid rate up to 2003 and indications are that the decline is continuing. The results of Prakash et al. (2003) for northern India in the period 1992–2000 indicate maximum values for the annual rate of population change λ of 0·67 for OWBV and 0·73 for LBV (declines of 33% and 27% year−1, respectively). The results for this region since 2000 show that the declines have continued at a broadly similar rate (λ = 0·52 for OWBV and 0·78 for LBV). A lower value of λ for the more recent period cannot be taken to indicate an acceleration of the rate of decline because the decline may have begun later than 1992. Data collected by The Peregrine Fund (The Peregrine Fund 2004) give a rate of decline for OWBV in Pakistan similar to that for OWBV in India (λ = 0·50).
The demographic model indicates that a low incidence of contamination of ungulate carcasses available to vultures with lethal levels of diclofenac (0·13–0·75%, depending on model assumptions and vulture population) is sufficient for diclofenac poisoning to be the sole cause of the observed vulture declines. An implication of this result is that it may be difficult to establish, from field surveys of diclofenac levels in ungulate carcasses, that the proportion, C, contaminated with a lethal concentration is sufficient to account for the decline. To demonstrate that C was significantly lower than the levels required to cause the observed vulture population declines would require that no carcass with a lethal diclofenac concentration is found in a random sample of 400–2300 carcasses (one-sided P-value = 0·05; range of carcass numbers includes the extreme values of C in Table 1). This does not mean that such surveys are not worth doing, but they may require a large number of samples that must be representative of carcasses used by vultures with respect to geographical location, circumstances of ungulate death and disposal, ungulate species and time since death.
Density-dependence of demographic rates would cause the rate of population decline at a given level of contamination to be lower than that predicted by the model, although density-dependence would have to be str ong to make much difference to the conclusions. Even in the absence of competition and with all other environmental factors optimal, Gyps vultures cannot rear more than one juvenile to independence per year, and the age of first breeding is unlikely to be reduced by more than about 2 years, so there is limited scope for density-dependent effects on these life-history parameters to reduce rates of decline. There is no indication that the rate of population decline has slowed recently, even with populations at less than 1% of their pre-decline level (for OWBV in India), so it is unlikely that there are strong density-dependent effects in these populations.
Comparison between observed proportions of dead vultures that had symptoms of diclofenac poisoning and modelling results provides a useful test of the hypothesis that diclofenac poisoning is the sole or main cause of the population decline. The validity of the comparison depends upon the assumption that the causes of death in birds found dead or dying were representative of those of all birds. Dead birds were collected during searches by research staff or after reports from the public. Bias with respect to cause of death cannot be ruled out, but we have no reason to believe that it occurred.
The observed proportions of dead adult and subadult vultures with visceral gout and/or diclofenac contamination were broadly similar in India and Nepal and closely similar in Pakistan, to the proportions of deaths expected to be caused by diclofenac if the observed rate of population decline was entirely due to diclofenac. Variation among countries, species and age classes was correlated with modelled values. The slower population decline of LBV than OWBV was associated with a lower proportion of dead LBV with gout and/or diclofenac. This might occur because of a lower susceptibility of LBV to diclofenac or preferences for types of livestock or tissue with lower levels of contamination. In addition, LBV nest on cliffs (OWBV nest in trees) and may find more of their food in remote, mountainous areas, where there is a greater proportion of carcasses of domestic livestock untreated with diclofenac and where wild ungulates are also available. The match in the average level of observed and modelled proportions and the strength of the correlation between them was stronger if adult survival rate before the decline was towards the lower end of the most plausible range. Explicit estimates of the proportion of the excess mortality required to cause the population declines that are attributable to diclofenac range between 71% and 100%, depending on vulture population and model assumptions, and confidence limits included 100% over all or most of the plausible range of the assumed value for adult survival. Hence, we conclude that diclofenac poisoning is at least the major cause, and possibly the only cause, of rapid population declines of OWBV and LBV across the Indian subcontinent.
We therefore recommend that urgent action is taken in the main range states of the three currently threatened species, namely Bangladesh, Bhutan, Cambodia, India, Myanmar, Nepal and Pakistan, to prevent the exposure of vultures to livestock carcasses contaminated with diclofenac. This can probably only be achieved by a ban on veterinary use in livestock species likely to be eaten by vultures. We also recommend that, in countries where vultures feed on carcasses of domestic livestock and where diclofenac is not in widespread veterinary use, action is taken to prevent future exposure of vultures to diclofenac. Prevention or restriction of the veterinary use of diclofenac is likely to increase the veterinary use of other non-steroidal anti-inflammatory drugs, so research is needed to identify alternative drugs that are effective in livestock and safe for vultures. Efforts should also be made to raise awareness of the problem of diclofenac contamination and the availability of safe alternatives among veterinarians, pharmacists, livestock owners and the general public. Diclofenac may not only be a problem for the currently threatened vulture species, but perhaps also for other Gyps species and other scavenging birds. Research is needed to monitor better populations of scavenging birds and their causes of death and to assess their level of exposure to diclofenac and other non-steroidal anti-inflammatory drugs.
Given that diclofenac is widely used in Pakistan and India (Risebrough 2005) and is produced and distributed by many companies, it may take a considerable time to remove it from the food supply of vultures. In view of this, and the continuing rapid vulture population declines, it is probable that some or all of the three threatened Gyps species will soon become extinct in the wild, either completely or over large parts of their range. Therefore, captive holding and breeding of vultures until diclofenac is controlled is recommended as a precaution to ensure the long-term survival of the threatened species and to provide a stock of birds for future reintroduction programmes.