Munir Z. Virani

Diclofenac residues as the cause of vulture population decline in Pakistan.

The Oriental white-backed vulture (OWBV; Gyps bengalensis) was once one of the most common raptors in the Indian subcontinent. A population decline of >95%, starting in the 1990s, was first noted at Keoladeo National Park, India. Since then, catastrophic declines, also involving Gyps indicus and Gyps tenuirostris, have continued to be reported across the subcontinent. Consequently these vultures are now listed as critically endangered by BirdLife International. In 2000, the Peregrine Fund initiated its Asian Vulture Crisis Project with the Ornithological Society of Pakistan, establishing study sites at 16 OWBV colonies in the Kasur, Khanewal and Muzaffargarh–Layyah Districts of Pakistan to measure mortality at over 2,400 active nest sites. Between 2000 and 2003, high annual adult and subadult mortality (5–86%) and resulting population declines (34–95%) (ref. 5 and M.G., manuscript in preparation) were associated with renal failure and visceral gout. Here, we provide results that directly correlate residues of the anti-inflammatory drug diclofenac with renal failure. Diclofenac residues and renal disease were reproduced experimentally in OWBVs by direct oral exposure and through feeding vultures diclofenac-treated livestock. We propose that residues of veterinary diclofenac are responsible for the OWBV decline.

Dropping dead: causes and consequences of vulture population declines worldwide

Vultures are natures most successful scavengers, and they provide an array of ecological, economic, and cultural services. As the only known obligate scavengers, vultures are uniquely adapted to a scavenging lifestyle. Vultures’ unique adaptations include soaring flight, keen eyesight, and extremely low pH levels in their stomachs. Presently, 14 of 23 (61%) vulture species worldwide are threatened with extinction, and the most rapid declines have occurred in the vulture‐rich regions of Asia and Africa. The reasons for the population declines are varied, but poisoning or human persecution, or both, feature in the list of nearly every declining species. Deliberate poisoning of carnivores is likely the most widespread cause of vulture poisoning. In Asia, Gyps vultures have declined by >95% due to poisoning by the veterinary drug diclofenac, which was banned by regional governments in 2006. Human persecution of vultures has occurred for centuries, and shooting and deliberate poisoning are the most widely practiced activities. Ecological consequences of vulture declines include changes in community composition of scavengers at carcasses and an increased potential for disease transmission between mammalian scavengers at carcasses. There have been cultural and economic costs of vulture declines as well, particularly in Asia. In the wake of catastrophic vulture declines in Asia, regional governments, the international scientific and donor communities, and the media have given the crisis substantial attention. Even though the Asian vulture crisis focused attention on the plight of vultures worldwide, the situation for African vultures has received relatively little attention especially given the similar levels of population decline. While the Asian crisis has been largely linked to poisoning by diclofenac, vulture population declines in Africa have numerous causes, which have made conserving existing populations more difficult. And in Africa there has been little government support to conserve vultures despite mounting evidence of the major threats. In other regions with successful vulture conservation programs, a common theme is a huge investment of financial resources and highly skilled personnel, as well as political will and community support.

The race to prevent the extinction of South Asian vultures

Summary Gyps vulture populations across the Indian subcontinent collapsed in the 1990s and continue to decline. Repeated population surveys showed that the rate of decline was so rapid that elevated mortality of adult birds must be a key demographic mechanism. Post mortem examination showed that the majority of dead vultures had visceral gout, due to kidney damage. The realisation that diclofenac, a non-steroidal anti-inflammatory drug potentially nephrotoxic to birds, had become a widely used veterinary medicine led to the identification of diclofenac poisoning as the cause of the decline. Surveys of diclofenac contamination of domestic ungulate carcasses, combined with vulture population modelling, show that the level of contamination is sufficient for it to be the sole cause of the decline. Testing on vultures of meloxicam, an alternative NSAID for livestock treatment, showed that it did not harm them at concentrations likely to be encountered by wild birds and would be a safe replacement for diclofenac. The manufacture 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 the meantime, captive populations of three vulture species have been established to provide sources of birds for future reintroduction programmes.

Breeding and mortality of Oriental White-backed Vulture Gyps bengalensis in Punjab Province, Pakistan

Populations of Oriental White-backed Vulture Gyps bengalensis and Long-billed Vulture G. indicus declined in India between the mid 1980s and late 1990s. Regional reports from India described declines of 95–100% across a wide area. This study was conducted to investigate the breeding success and pattern of mortality in two vulture colonies (Dholewala and Changa Manga) within Punjab Province, Pakistan between December 2000 and June 2001. Breeding success was found to be 62% in Dholewala and 59% in Changa Manga. A total of 668 sick and dead vultures were collected of which 591 were less than one month post mortem . No significant variation was found in the weekly mortality rate of adult and subadult vultures during the study period spanning winter through summer. A peak in mortality rate was observed during late April and early May that corresponded to mortality of newly fledged juveniles. Minimum annual mortality rate in the adult breeding population was calculated to be 11.4% and 18.6% in Dholewala and Changa Manga respectively. In a subsample of dead vultures ( n = 185) visceral gout was found in 80% of adults, 63% of subadults, 19% of juveniles and 13% of nestlings. These mortality rates were consistent with a rapid population decline. Results imply that the mortality factor responsible for the decline in Gyps vultures described in India is also present in Pakistan and will potentially lead to a population decline of a comparable magnitude.

Carbofuran and its Toxic Metabolites Provide Forensic Evidence for Furadan Exposure in Vultures ( Gyps africanus ) in Kenya

Forensic analysis of carbofuran residues in weathered tissue samples for evidence of Furadan exposure in vultures (Gps africanus) by HPLC gave concentration (mg/Kg dry tissue weight) ranges of bdl – 0.07 (carbofuran), bdl – 0.499 (3-ketocarbofuran) and 0.013–0.147 (3-hydroxycarbofuran) in beaks, bdl–0.65 (carbofuran), 0.024–0.190 (3-ketocarbofuran) and 0.017–0.098 (3-hydroxycarbofuran) in feet, 0.179–0.219 (3-ketocarbofuran) and 0.081–0.093 (3-hydroxycarbofuran) in crop content, 0.078–0.082 (3-ketocarbofuran) and 0.091–0.101 (3-hydroxycarbofuran) in muscle of a laced carcass and 0.006–0.014 (carbofuran), 0.590–1.010 (3-ketocarbofuran) and 0.095–0.135 (3-hydroxycarbofuran) in soil sampled from a poisoning site. These compounds were confirmed by GC-MS. The results showed that HPLC combined with GC-MS is suitable for forensic analysis of carbofuran residues in bird tissue samples and that forensic investigation should include its two toxic metabolites, 3-hydroxycarbofuran and 3-ketocarbofuran.

Rapid population declines and mortality clusters in three Oriental white-backed vulture Gyps bengalensis colonies in Pakistan due to diclofenac poisoning

The population declines affecting Asian Gyps vultures are among the most rapid and geographically widespread recorded for any species. This paper describes the rates and patterns of mortality and population change over 4 years at three Oriental white-backed vulture Gyps bengalensis colonies in Pakistan: Dholewala (initially 421 pairs), Toawala (initially 445 pairs) and Changa Manga (initially 758 pairs). Vulture mortality led to the extirpation of two of these colonies (Changa Manga and Dholewala) in 3 years, and a decline of 54.3% in the third. Visceral gout, indicative of diclofenac poisoning, was the largest single cause of death in vultures examined. Annual adult mortality from diclofenac poisoning was significantly positively correlated with annual population declines at each colony indicating a direct causal relationship. Visceral gout occurred in temporal and spatial clusters suggesting multiple point sources of diclofenac expo- sure. The spatial and temporal distribution of dead vultures and approximate time since death were used to estimate minimum rates at which colonies encountered carcasses with sufficient diclofenac to cause mortality of 1.26-1.88 carcasses per colony per month. By estimating total carcass consumption at each colony, the percentage of carcasses contaminated with diclofenac was calcu- lated as 1.41-3.02%, exceeding the minimum required to have caused the observed population decline. With populations declining by approximately 50% annually, the long term survival of Gyps vultures in South Asia will require the removal of diclofenac from vulture food and establishment of captive populations for future restoration once the environment is free from contam- ination.

Soil and water contamination with carbofuran residues in agricultural farmlands in Kenya following the application of the technical formulation Furadan.

This study was undertaken to determine the concentrations of carbofuran residues in water, soil and plant samples from selected sites in the farmlands in Kenya and to demonstrate the impact of Furadan use on the local environment. Soil, water and plant samples obtained from agricultural farmlands where the technical formulation Furadan has been used extensively showed high environmental contamination with concentrations of carbofuran and its two toxic metabolites 3-hydroxycarbofuran and 3-ketocarbofuran, separately, ranging from 0.010–1.009 mg/kg of dry surface soil, 0.005–0.495 mg/L in water samples from two rivers flowing through the farms and bdl-2.301 mg/L in water samples from ponds and dams located close to the farms. Maize plant samples contained these residues in concentrations ranging from 0.04–1.328 mg/kg of dry plant tissue. The significantly high concentration levels of carbofuran and its metabolites, 3-ketocarbofuran and 3-hydroxycarbofuran, found in various matrices demonstrate that Furadan was used extensively in the two areas and that there was environmental distribution and exposure of residues in water which posed risks when used for domestic purposes or as drinking water for animals in two wildlife conservancies where the dams and ponds are located. Surface soil contamination was also high and posed risks through run-off into the dams and rivers as well as through secondary exposure to small birds and mammals.

Copper, lead and cadmium concentrations in surface water, sediment and fish, C. Carpio, samples from Lake Naivasha: effect of recent anthropogenic activities

Following recent concerns of chemical pollution around Lake Naivasha, especially originating from recent agricultural activities in the catchment, samples of water, sediments, and fish Common carp (Cyprinus carpio) were collected from the Hippo Point, Kasarani, Mouth of Malewa River, Mouth of Karati River, Crescent Island, Sher Karuturi Discharge outlet and Oserian Bay for analysis of Cu, Cd and Pb by FAAS. The mean heavy metal levels ranged from 5.12–58.11 (Pb), 1.06–1.73 (Cd), and <0.03–2.29 (Cu) mg/kg wet weight in C. carpio muscle, <100–179.83 (Pb), <10.00–10.06 (Cd) and <30.00–32.33 (Cu) μg/L in surface water, and 17.11–53.07 (Pb), 1.18–5.58 (Cd) and 3.00–8.48 (Cu) mg/kg dry weight in sediment and showed a wide variation within and between samples with relatively high concentrations in sediments and fish muscle tissues. The results indicate that Lake Naivasha, in some parts, is polluted with these heavy metals of which relatively higher concentrations are found at the discharge outlets near Sher Karuturi and Oserian Bay. This indicates possible contribution from surrounding horticultural/floricultural activities and the Mouths of the Rivers Malewa and Karati which flow from it’s upper catchment.

Identification of a Novel Mycoplasma Species from an Oriental White-Backed Vulture (Gyps bengalensis)

ABSTRACT An intracellular organism was isolated from the tissues of an Oriental white-backed vulture (Gyps bengalensis) in chicken embryo fibroblast cell cultures. Biochemical and physical properties, ultrastructural features, and 16S ribosomal DNA sequencing classified this organism as a new taxon of mycoplasma, for which the name “Mycoplasma vulturii” is proposed.

Mechanisms of Coexistence in Vultures: Understanding the Patterns of Vulture Abundance at Carcasses in Masai Mara National Reserve, Kenya

Abstract. Because of the high, albeit seasonal, availability of carcasses, the Mara-Serengeti ecosystem, Kenya, has a high diversity of scavengers, leading to considerable competition between species. From patterns of occurrence of vultures at 163 carcasses over an 8-year period in the Masai Mara National Reserve, we were able to identify some mechanisms that may reduce competition. Species are associated on the basis of similar dietary needs and beak morphology, and they are highly interdependent, showing little evidence of disassociation. Social vultures (genus Gyps) dominated the vulture scene at the reserve; they were more abundant at carcasses when migratory ungulates were present in the dry season, when more carcasses are likely to be available, than when migratory ungulates were absent. In addition, regardless of the predators identity, presence of a predator reduced the number of vultures, suggesting that vultures prefer carrion not killed by predators where available. Comparisons between past and current counts of carcasses suggest a substantial shift in Gyps vultures with an increase in the relative abundance of Rüppells Vulture (G. rueppellii) with respect to that of the White-backed Vulture (G. africanus). In addition, our findings suggest that as changing land use in the Mara-Serengeti ecosystem leads to reductions of large ungulates, social vultures will be the most adversely affected.