Aleem Ahmed Khan

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.

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.

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.

Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex morphological evolution, non-monophyletic genera and hidden species diversity

The Alaudidae (larks) is a large family of songbirds in the superfamily Sylvioidea. Larks are cosmopolitan, although species-level diversity is by far largest in Africa, followed by Eurasia, whereas Australasia and the New World have only one species each. The present study is the first comprehensive phylogeny of the Alaudidae. It includes 83.5% of all species and representatives from all recognised genera, and was based on two mitochondrial and three nuclear loci (in total 6.4 kbp, although not all loci were available for all species). In addition, a larger sample, comprising several subspecies of some polytypic species was analysed for one of the mitochondrial loci. There was generally good agreement in trees inferred from different loci, although some strongly supported incongruences were noted. The tree based on the concatenated multilocus data was overall well resolved and well supported by the data. We stress the importance of performing single gene as well as combined data analyses, as the latter may obscure significant incongruence behind strong nodal support values. The multilocus tree revealed many unpredicted relationships, including some non-monophyletic genera (Calandrella, Mirafra, Melanocorypha, Spizocorys). The tree based on the extended mitochondrial data set revealed several unexpected deep divergences between taxa presently treated as conspecific (e.g. within Ammomanes cinctura, Ammomanes deserti, Calandrella brachydactyla, Eremophila alpestris), as well as some shallow splits between currently recognised species (e.g. Certhilauda brevirostris-C. semitorquata-C. curvirostris; Calendulauda barlowi-C. erythrochlamys; Mirafra cantillans-M. javanica). Based on our results, we propose a revised generic classification, and comment on some species limits. We also comment on the extraordinary morphological adaptability in larks, which has resulted in numerous examples of parallel evolution (e.g. in Melanocorypha mongolica and Alauda leucoptera [both usually placed in Melanocorypha]; Ammomanopsis grayi and Ammomanes cinctura/deserti [former traditionally placed in Ammomanes]; Chersophilus duponti and Certhilauda spp.; Eremopterix hova [usually placed in Mirafra] and several Mirafra spp.), as well as both highly conserved plumages (e.g. within Mirafra) and strongly divergent lineages (e.g. Eremopterix hova vs. other Eremopterix spp.; Calandrella cinerea complex vs. Eremophila spp.; Eremalauda dunni vs. Chersophilus duponti; Melanocorypha mongolica and male M. yeltoniensis vs. other Melanocorypha spp. and female M. yeltoniensis). Sexual plumage dimorphism has evolved multiple times. Few groups of birds show the same level of disagreement between taxonomy based on morphology and phylogenetic relationships as inferred from DNA sequences.

Genetic Variation of Four Gyps Species (Gyps bengalensis, G. AFRICANUS, G. indicus and G. fulvus) Based on Microsatellite Analysis

Abstract Although several phylogenetic studies of Gyps species have been conducted, few studies have addressed the genetic diversity of these species on a finer scale such as microsatellite analyses. We collected samples of migratory adults and nestlings from four species of vultures in six different localities. We analyzed the samples using microsatellites in order to determine the genetic distance as well as the amount of variation within and among Gyps species populations. Low genetic diversity in Long-billed Vultures (G. indicus) was probably indicative of a single population with no immigration and low gene flow. As this species is critically endangered, future conservation programs should consider genetically suitable stock for a breeding and reintroduction program. High genetic diversity in African White-backed Vultures (G. africanus) was likely indicative of a number of populations, with immigration and gene flow. We confirmed previous findings of low genetic differentiation among Griffon Vulture (G. fulvus) populations, which indicated high mobility and gene flow among these populations.

Impacts of biological globalization in the Mediterranean: Unveiling the deep history of human-mediated gamebird dispersal

Significance Human-mediated species dispersal stretching back at least 10,000 y has left an indelible stamp on present day biodiversity. A major contributing factor to this process was the trade in a wide range of exotic species that was fueled by elite demand. The black francolin—now extinct in the western Mediterranean but once a courtly gamebird prized for its flavor, curative, and aphrodisiac qualities by European aristocracy—was one of these species. Using historical sources and DNA analysis of modern and archival specimens, we show that this bird was not native to the western Mediterranean, and document its introduction to Cyprus and westward through the Mediterranean Basin via several trade routes that reached as far east as South Asia. Humans have a long history of moving wildlife that over time has resulted in unprecedented biotic homogenization. It is, as a result, often unclear whether certain taxa are native to a region or naturalized, and how the history of human involvement in species dispersal has shaped present-day biodiversity. Although currently an eastern Palaearctic galliform, the black francolin (Francolinus francolinus) was known to occur in the western Mediterranean from at least the time of Pliny the Elder, if not earlier. During Medieval times and the Renaissance, the black francolin was a courtly gamebird prized not only for its flavor, but also its curative, and even aphrodisiac qualities. There is uncertainty, however, whether this important gamebird was native or introduced to the region and, if the latter, what the source of introduction into the western Mediterranean was. Here we combine historical documentation with a DNA investigation of modern birds and archival (13th–20th century) specimens from across the species’ current and historically documented range. Our study proves the black francolin was nonnative to the western Mediterranean, and we document its introduction from the east via several trade routes, some reaching as far as South Asia. This finding provides insight into the reach and scope of long-distance trade routes that serviced the demand of European aristocracy for exotic species as symbols of wealth and prestige, and helps to demonstrate the lasting impact of human-mediated long-distance species dispersal on current day biodiversity.

New insights into the intricate taxonomy and phylogeny of the Sylvia curruca complex

We use the mitochondrial cytochrome b from 213 individuals and the three nuclear introns BRM 15, myoglobin 2 and ODC 6-7 from a smaller subsample to evaluate the taxonomy of the Lesser Whitethroat Sylvia curruca (Aves, Passeriformes, Sylviidae) complex, which has long been controversial. We sequenced type material of the taxa althaea, blythi, margelanica and minula, and used topotypical material of caucasica, chuancheica, curruca and telengitica. The nuclear introns fail to resolve the complex, but cytochrome b recovers six major clades, revealing genetically identifiable populations corresponding to previously named taxa, and we propose that the names althaea, blythi, curruca, halimodendri, margelanica and minula, respectively, should be used for these. The margelanica clade is suggested to have a more extensive distribution than previously known, including both the taxon telengitica and a population in eastern Mongolia. The taxon minula is found to have a more restricted range than generally believed, only breeding in China. According to the mitochondrial gene tree, there is a basal dichotomy, with the taxa althaea, blythi, halimodendri and margelanica being part of one clade, well separated from a clade containing curruca and minula. Dating analysis suggests that a basal divergence separating curruca and minula from the other four taxa occurred between 4.2 and 7.2 mya; these two then diverged between 2.3 and 4.4 mya. The splits between the althaea, blythi, halimodendri and margelanica lineages is inferred to have occurred later, approximately between 1.0 and 2.5 mya (all 95% HPD). The nucleotide data suggest significant departure from demographic equilibrium in blythi (clade 1a), halimodendri (clade 2a) and minula, whereas tendencies are weaker for other clades. We propose that the names althaea, blythi, curruca, halimodendri, margelanica and minula should be used for the major clades. However, whether these are treated as subspecies or species is largely a matter of species definition and is not resolved by our data.

Neck-drooping Posture in Oriental White-Backed Vultures (Gyps bengalensis): An Unsuccessful Predictor of Mortality and Its Probable Role in Thermoregulation

ABSTRACT Populations of three Gyps vulture species in the Indian subcontinent have undergone recent rapid declines due to elevated mortality rates caused by diclofenac poisoning. Researchers have proposed that vultures adopt a previously-undescribed neck-drooping posture prior to death. Our study investigated two hypotheses: (1) neck drooping is temperature-dependent, (2) neck-drooping is indicative of poor health in Oriental White-backed Vultures (Gyps bengalensis) and is a prelude to death. Observations of neck-drooping were highly seasonal, with the majority of vultures observed neck-drooping in the hot season from April to October and no vultures observed neck-drooping during the cold months of December and January. Above a calculated threshold ambient temperature of 15.4°C (95% CI 9.9–22.5°C), there was a significant positive correlation between temperature and the proportion (expressed as an angular transformation) of vultures observed neck-drooping. Neck-drooping vultures were observed significantly more frequently with their back toward the sun with their head in their own shade than birds that were not neck-drooping, and vultures that were not neck-drooping were observed more frequently facing the sun than those neck-drooping. Together, these observations strongly suggest that neck-drooping posture has a role in thermoregulation. In contrast to the highly seasonal pattern of neck-drooping, mortality of vultures occurred in all months of the year. This finding indicates that neck-drooping has low specificity and sensitivity as an indicator of poor health and impending death in vultures.

Desert Ecosystem Management: A Sustainable and Wise Use

Rapid growth of the world population, started in 1950, resulted in an estimated recent population of more than seven billion. Indian sub-continent is the most densely populated and fastest growing region. The desert ecosystem encompasses some 313,851 km2 area including Thar, Kharan, Cholistan, Thal and Indus valley plains in this region. The biodiversity includes some estimated 764 species of desert flora and 769 species of fauna, which includes 123 mammals, 540 birds, 96 reptiles and 10 amphibians. The desert dwellers lead a nomadic to semi-nomadic life, moving from one place to another in search of water and fodder for their animals and trade. Deserts are already the most fragile ecosystems and facing an unprecedented vulnerability mainly due global warming phenomena by pushing its biological resources to their limits. There is a dire need to wisely use desert resources on sustainable basis, so that a symbiotic relationship between man and ecosystem may be guaranteed.