Asian Vulture Research Articles

Comprehensive genome assembly reveals genetic diversity and carcass consumption insights in critically endangered Asian king vultures

The Asian king vulture (AKV), a vital forest scavenger, is facing globally critical endangerment. This study aimed to construct a reference genome to unveil the mechanisms underlying its scavenger abilities and to assess the genetic relatedness of the captive population in Thailand. A reference genome of a female AKV was assembled from sequencing reads obtained from both PacBio long-read and MGI short-read sequencing platforms. Comparative genomics with New World vultures (NWVs) and other birds in the Family Accipitridae revealed unique gene families in AKV associated with retroviral genome integration and feather keratin, contrasting with NWVs’ genes related to olfactory reception. Expanded gene families in AKV were linked to inflammatory response, iron regulation and spermatogenesis. Positively selected genes included those associated with anti-apoptosis, immune response and muscle cell development, shedding light on adaptations for carcass consumption and high-altitude soaring. Using restriction site-associated DNA sequencing (RADseq)-based genome-wide single nucleotide polymorphisms (SNPs), genetic relatedness and inbreeding status of five captive AKVs were determined, revealing high genomic inbreeding in two females. In conclusion, the AKV reference genome was established, providing insights into its unique characteristics. Additionally, the potential of RADseq-based genome-wide SNPs for selecting AKV breeders was demonstrated.

Do Pharmaceuticals in the Environment Pose a Risk to Wildlife?

The vast majority of knowledge related to the question "To what extent do pharmaceuticals in the environment pose a risk to wildlife?" stems from the Asian vulture crisis (>99% decline of some species of Old World vultures on the Indian subcontinent related to the veterinary use of the nonsteroidal anti-inflammatory drug [NSAID] diclofenac). The hazard of diclofenac and other NSAIDs (carprofen, flunixin, ketoprofen, nimesulide, phenylbutazone) to vultures and other avian species has since been demonstrated; indeed, only meloxicam and tolfenamic acid have been found to be vulture-safe. Since diclofenac was approved for veterinary use in Spain and Italy in 2013 (home to ~95% of vultures in Europe), the risk of NSAIDs to vultures in these countries has become one of the principal concerns related to pharmaceuticals and wildlife. Many of the other bodies of work on pharmaceutical exposure, hazard and risk to wildlife also relate to adverse effects in birds (e.g., poisoning of scavenging birds in North America and Europe from animal carcasses containing pentobarbital, secondary and even tertiary poisoning of birds exposed to pesticides used in veterinary medicine as cattle dips, migratory birds as a vector for the transfer of antimicrobial and antifungal resistance). Although there is some research related to endocrine disruption in reptiles and potential exposure of aerial insectivores, there remain numerous knowledge gaps for risk posed by pharmaceuticals to amphibians, reptiles, and mammals. Developing noninvasive sampling techniques and new approach methodologies (e.g., genomic, in vitro, in silico, in ovo) is important if we are to bridge the current knowledge gaps without extensive vertebrate testing. Environ Toxicol Chem 2024;43:595-610. © 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Genetic polymorphism in the mitochondrial D-loop of Oriental White-backed Vultures (Gyps bengalensis)

Abstract Vultures are among nature’s most successful scavengers, providing tractable models for ecological, economic, and cultural studies. Asian vultures have undergone dramatic declines of 90–99% in the subcontinent due to consequences of poisoning drugs, thereby being at a high risk of extinction. In Pakistan, surveys conducted previously focused mostly the cause of decline and breeding strategies only. Genetic profiling of vultures was still unmapped that could play a particular role in conservation endeavors and let researchers to genetically label individuals of threatened or endangered species. In this study, we examined genetic diversity and molecular phylogeny of Oriental White-backed Vultures by analyzing mitochondrial DNA (mtDNA) sequences. Genetic polymorphism was detected among individuals, and, on that basis, phylogenetic analysis was conducted through Bayesian analysis of DNA sequences using MCMC. Using multiple sequence alignment, two mutations, transversion T>G and transition G>A, were observed at nucleotide positions 1 and 2, respectively. Similarly, T/C heterozygosity at two positions, 53 and 110, and one heterozygous T/G locus at 130 position were also observed. The reference sequence, along with other samples of V1, V6, V7 and V9, was placed into a clade, while V2, V5, V11, V3, V4 and V10 samples were grouped into a two clade.

Livestock prevalence in the Egyptian vulture diet during European sanitary restrictions on carcass disposal

Food is a primary factor driving animal population dynamics. Low quality food (e.g. poisoned carrion) has caused large declines of Asian and African vulture populations pushing some species to the brink of extinction. Although Europe emerges as a stronghold for the guild, European vultures face potential food shortages due to sanitary restrictions banning the disposal of livestock carcasses in the field after the Bovine Spongiform Encephalopathy (BSE). Determining the diet of European vultures and in particular the role livestock plays in it is needed for preserving these species and their scavenging role in food webs. We analysed the diet composition of 13 nests of the endangered Egyptian vulture (Neophron percnopterus) in a species stronghold in Europe (NW Spain), during the period of BSE restrictions (2007, 2009 and 2010). We identified 312 remains from 25 species, mainly mammals (70.8%), birds (17.0%) and fishes (7.7%). Livestock dominated the Egyptian vulture diet, comprising 23.9% of total items (11.8% of sheep-goat, 7.0% of bovine). Differences in diet composition among nests responded to habitat characteristics determining the availability of some food items (e.g. water for fishes). Our findings support a major role of livestock in the Egyptian vulture diet, suggesting a lack of compliance with sanitary restrictions banning the disposal of livestock carcasses in the field, with potential to affect vulture conservation and their scavenging function in ecosystems.

The past and future role of conservation science in saving biodiversity

AbstractGlobal biodiversity losses continue despite tremendous growth in the volume of conservation science and many local successes. Research that can achieve conservation science's aims—arresting declines in biodiversity and preventing extinctions—is therefore of ever greater importance. Here, we ask whether conservation science, as currently performed, is progressing in such a way as to maximize its impact. We present a simple framework for how effective conservation research could progress, from identifying problems to diagnosing their proximate and ultimate causes, and from proposing, to designing, implementing, and testing responses. We then demonstrate that for three well‐known examples—South Asian vultures, whooping cranes, and bycatch of procellariform seabirds—published studies appear to follow this sequence, with considerable benefits. However, for a representative sample of the wider conservation literature, we find no evidence of such a progression. Instead, the vast majority of papers remain focused on describing the state of nature or on mechanisms directly causing changes, with very little research on designing or implementing conservation responses. This lack of research on the sorts of questions that might most help conservation science deliver its stated mission strongly suggests we will struggle to translate the huge increase in research activity into real‐world benefits.

Sighting of Red-headed Vultures (Sarcogyps calvus) in a group

Asian vultures are endangered birds included in Schedule 1 of the Wildlife Protection Act, 1972. From the nine species of vultures found in India, five are reported from the Bundelkhand region in central India. An exhaustive survey was done in the Panna Tiger Reserve, Madhya Pradesh, from January to June 2016. Red-headed Vultures (Sarcogyps calvus) are solitary in nature but during the survey we collectively sighted a total of 12 Red-headed Vultures in Panna Tiger Reserve, whilst eight were recorded in the region between Hinauta and Dhudhua Seha in one group. Red-headed Vultures are facing serious threats of habitat loss and lack of food availability along with diclofenac poisoning, and they require various conservation measures to maintain their population.

Vultures and people: Local perceptions of a low-density vulture population in the eastern mid-hills of Nepal

The cause for rapid decline of the South Asian vulture population in 1990s was unknown for many years until diclofenac was proved to be the main reason for such decline in 2004. The vulture populations from Nepal has also undergone rapid decline that causes low awareness among people about its ecological importance. For declining species that have large range and are mostly associated with humans, people’s attitudes can have direct effects on their survival because of the multiple linkages and potential for both positive and negative impacts of human behaviour for these large scavengers. However, little is known about vultures in the eastern mid-hills of Nepal. Therefore, we conducted a study in Ramechhap, a district in the eastern mid-hills of Nepal, to assess the vultures’ status and human relations using transect and questionnaire surveys respectively. Himalayan Griffons Gyps himalayensis and Egyptian Vultures Neophron percnopterus were found in the area, and the majority of respondents interviewed had a positive attitude towards vultures (58.8%) and their conservation (47.3%). Although neglected in previous studies, a neutral attitude (20% towards vultures and 15.8% towards vulture conservation) can be significant (largely related to ignorance) and can be readily turned to negative due to the vulture’s carcass consuming behaviour and lack of conventional appeal to many people, with implications for the success of a conservation programme. In our study, carcass scarcity appeared to be an increasing concern with about 90% of the respondents reporting burying cattle carcasses, and that this practice has recently increased. In the course of the study period, however, two (unburied) carcasses were observed. Our study found that nimesulide, a potentially toxic NSAID for vultures, was used for veterinary purpose in the study area, which could be a serious threat to vultures. Other human activities such as carcass poisoning pose threats to vultures in the study area. Therefore, for long term vulture conservation, local attitudes and behaviour should be considered along with ecological aspects of vultures.

Lead ingestion as a potential contributing factor to the decline in vulture populations in southern Africa

Vulture populations in southern Africa have been on the decline for years, which unlike the Asian vulture crisis, has no one specific cause. Reasons attributable are deliberate and secondary poisonings, drowning, power line injuries, electrocutions, traditional medicine (“muti” trade) and calcium deficiencies. However, lead toxicity as a potential causal factor is hardly mentioned. The potential for lead toxicity needs to be considered as substantial game hunting occurs in the region with little regulatory control on bullet types. In this study, we determined the whole blood lead concentrations of captive and wild vulture populations in South Africa and Namibia (n=185). Results were compared to previous published ranges indicative of background exposure (<10μg/dL), non-toxic point exposure based upon the range established from captive birds and subclinical exposure. In general, whole blood lead concentrations were higher for wild African White-backed vultures (Gyps africanus)(AWBV) than Cape vultures (G. coprotheres)(CGV) at 15.54±12.63μg/dL vs 12.53±8.88μg/dL (non-significantly different), while in the Bearded vultures (Gypaetus barbatus) no indication of exposure was evident. Very similar exposures resulted irrespective of the birds being in captivity or under wild, free-roaming conditions. A proportion of wild birds did, however, appear to be exposed to another source of lead than purely environmental (±12% and 30.6% for AWBV and CGV respectively). One bird, which had a whole blood concentration of 100μg/dL, died soon after capture. To find the relationship between whole blood lead concentration and likely exposure factors, birds were compared by their rural/urban location, vicinity to mines and surrounding soil lead concentrations. With no relationship being present for the latter factors, we believe that this is evidence that the portion of southern African vultures being exposed to unknown source of lead, which we suggest arises from leaded ammunition remaining from hunting

Foraging behaviour at carcasses in an Asian vulture assemblage: towards a good restaurant guide

SummaryVulture populations are declining steeply worldwide. Vulture ‘restaurants’ or feeding stations are a tool for maintaining and monitoring numbers, but individual species may be disadvantaged by the effects of carcass distribution, carcass size and interspecific aggression. To test the degree to which restaurants give opportunities for each species to access the food provided, we studied behaviour and morphology in three Critically Endangered species of vulture in Cambodia: the gregariously breeding and feeding White-rumped Vulture Gyps bengalensis and Slender-billed Vulture G. tenuirostris, and the solitary Red-headed Vulture Sarcogyps calvus. We video-recorded attendance time, attendance order and dominance behaviour at different-sized carcasses. Interspecific aggression at carcasses was least frequently shown by the ‘small’ White-rumped Vulture. The relatively ‘large’ Slender-billed and ‘medium’ Red-headed Vultures showed aggression more regularly and at similar levels. However, the latter avoids conflict by waiting until Gyps vultures are no longer crowding at the carcass, although its arrival at carcasses was correlated with total number of vultures present. While more numerous than Red-headed, the two Gyps vultures are more dependent on large carcasses, which increases their vulnerability to further declines in wild large ungulate species. Body size, number of individuals, hunger levels and carcass size and availability all influence carcass attendance behaviour. An increase in the number and spatial distribution of restaurants as well as of carcass size range could boost numbers of all vulture species.

Detection and drivers of exposure and effects of pharmaceuticals in higher vertebrates.

Pharmaceuticals are highly bioactive compounds now known to be widespread environmental contaminants. However, research regarding exposure and possible effects in non-target higher vertebrate wildlife remains scarce. The fate and behaviour of most pharmaceuticals entering our environment via numerous pathways remain poorly characterized, and hence our conception and understanding of the risks posed to wild animals is equally constrained. The recent decimation of Asian vulture populations owing to a pharmaceutical (diclofenac) offers a notable example, because the exposure route (livestock carcasses) and the acute toxicity observed were completely unexpected. This case not only highlights the need for further research, but also the wider requirement for more considered and comprehensive ‘ecopharmacovigilance’. We discuss known and potential high risk sources and pathways in terrestrial and freshwater ecosystems where pharmaceutical exposure in higher vertebrate wildlife, principally birds and mammals, may occur. We examine whether approaches taken within existing surveillance schemes (that commonly target established classes of persistent or bioaccumulative contaminants) and the risk assessment approaches currently used for pesticides are relevant to pharmaceuticals, and we highlight where new approaches may be required to assess pharmaceutical-related risk.

The case for banning diclofenac and the vanishing vultures

Critically endangered vulture species like Gyps (Gyps bengalensis, G. indicus and G. tenuirostris, constituting 99 per cent of the total vulture population) are under persistent threat from non-steroidal diclofenac and its isomers, despite it being banned since 2006. Livestock drugs such as these continue to threaten the existence of vultures. Diclofenac is a generic drug available over-the-counter and is approved for human use in treating conditions like minor aches, pains and fevers. India is the third largest drug manufacturer in the world and produces diclofenac in bulk for human consumption. Regrettably, it is often diverted illegally for veterinary purposes, often having dire consequences. Vultures are vital avian raptor species, providing an important ecosystem cleaning service, renowned for their crucial scavenging abilities. However, when they feed on dead animal carcasses treated with diclofenac, the birds succumb to kidney failure and visceral gout as a result. That said, after the much needed diclofenac ban in 2006, rapid vulture decline has slowed down, providing some hope for these birds. There is still some way to go, however, as research shows the drug has still not been completely eradicated from the vultures’ food supply. Further efforts are thus still very much required to fully implement the ban. In addition to illegal diclofenac usage, drugs with similar properties (e.g. aceclofenac and ketoprofen) are gaining momentum in the marketplace. It is predominantly within developing nations that inadequate systems exist for regulating drug usage, making the very purpose of banning diclofenac often redundant. This paper argues that more scrupulous monitoring and cross-checking of veterinary drugs such as ketoprofen, aceclofenac and meloxicam is necessary, whilst also arguing that research should be encouraged to focus on toxicities of such drugs to non-target animals like scavengers. Stringent banning of toxic killer drugs as well as interim measures like captive breeding, provision of supplemental food at ‘vulture restaurants’ (areas where fresh and poison-free meat and/or carcasses are provided) and ‘vulture safe zones’ integrated with intensive conservation campaign efforts are imperative if Asian vultures are to be safe.

Management implications of genetic studies for ex situ populations of three critically endangered Asian Gyps vultures

AbstractCaptive breeding and ex situ conservation have become important tools in species conservation programmes. The effectiveness of the management of captive populations can be hampered by the absence of pedigree data, but molecular markers can be used to inform conservation objectives and reduce inbreeding in the captive population. Using microsatellite markers, we examined the genetic diversity and relatedness among wild‐caught individuals of three critically endangered Asian vulture species, Gyps bengalensis, Gyps indicus and Gyps tenuirostris, populations established for captive breeding. Estimates of the inbreeding coefficient (f) were low, indicating that populations of all three species do not appear to be inbred. Moreover, the data show that a large proportion of wild‐taken birds were unrelated individuals (94.6, 87.1 and 85.3% in G. bengalensis, G. indicus and G. tenuirostris, respectively). No significant genetic differentiation (FST) was observed between historic and 2000/2001 populations of G. bengalensis in Pakistan and India. However, the more recent sampling (2002–2006) in Pakistan showed a significant difference from India. A genetic signal of a demographic bottleneck in all three species was found in some (M‐ratio test), but not all, tests (heterozygote excess and mode shift in allele frequencies). Levels of genetic diversity in G. bengalensis and G. indicus populations were comparable to levels prior to or soon after the start of their decline, respectively, suggesting that adequate numbers of birds exist in captivity for these two species and reflect neutral diversity levels observed in the wild. The genetic data obtained from this study allow us to minimize the loss of neutral genetic diversity in small wild and captive populations and to identify related pairs to avoid inbreeding depression.

Development of microsatellite markers and a restriction endonuclease digest assay for non-invasive sampling of endangered White-rumped, Slender-billed and Red-headed vultures

Southeast Asian vultures have been greatly reduced in range and population numbers, but it is challenging to use traditional tagging and monitoring techniques to track changes in their populations. Genotypes derived from non-invasively collected feather samples provide an alternative and effective means to ‘capture’ individual vultures for mark-recapture analyses. We describe a restriction endonuclease digest assay that distinguishes the visually similar feathers of three species of critically endangered Asian vultures (Gyps bengalensis, G. tenuirostris, and Sarcogyps calvus). In addition, we describe a panel of eight polymorphic microsatellite loci. In combination, the restriction endonuclease assay and microsatellite marker set developed here are powerful molecular tools for investigating the genetic and demographic status of these Asian vultures species.

Diclofenac – Affirmation of Carson’s Concerns

12 of the 23 species of Vulture, sole scavenger amongst vertebrate birds, are classified as “near threatened” or “endangered”. Across the Indian subcontinent and South Asia there is particular concern with an observed 92 percent reduction of Gyps vultures. The vulture species found in South Asian region has a scientific name given as Gyps bengalensis , common name is Asian Whitebacked vulture and the local name in the subcontinent region is Gidh .

Assessing the exposure risk and impacts of pharmaceuticals in the environment on individuals and ecosystems

The use of human and veterinary pharmaceuticals is increasing. Over the past decade, there has been a proliferation of research into potential environmental impacts of pharmaceuticals in the environment. A Royal Society-supported seminar brought together experts from diverse scientific fields to discuss the risks posed by pharmaceuticals to wildlife. Recent analytical advances have revealed that pharmaceuticals are entering habitats via water, sewage, manure and animal carcases, and dispersing through food chains. Pharmaceuticals are designed to alter physiology at low doses and so can be particularly potent contaminants. The near extinction of Asian vultures following exposure to diclofenac is the key example where exposure to a pharmaceutical caused a population-level impact on non-target wildlife. However, more subtle changes to behaviour and physiology are rarely studied and poorly understood. Grand challenges for the future include developing more realistic exposure assessments for wildlife, assessing the impacts of mixtures of pharmaceuticals in combination with other environmental stressors and estimating the risks from pharmaceutical manufacturing and usage in developing countries. We concluded that an integration of diverse approaches is required to predict ‘unexpected’ risks; specifically, ecologically relevant, often long-term and non-lethal, consequences of pharmaceuticals in the environment for wildlife and ecosystems.

Pharmaceuticals and personal care products in the environment: Cultural and spiritual perspectives

Pharmaceuticals and personal care products in the environment: Cultural and spiritual perspectives

Around the World

In science news around the world this week, environmental restoration projects and scientific research will get a major windfall from the BP oil spill fine; scientists lobbied the E.U. presidents to prevent budget cuts; South Asian vulture populations are recovering; a generous gift has breathed new life into the search for extraterrestrial intelligence; California has launched a cap-and-trade system; and the Global Fund to Fight AIDS, Tuberculosis and Malaria hired a new executive director, fired its inspector general, and made a controversial decision about financing malaria drugs.

First evidence that populations of the critically endangered Long-billed Vulture Gyps indicus in Pakistan have increased following the ban of the toxic veterinary drug diclofenac in south Asia

SummaryThe cliff-nesting Long-billed Vulture Gyps indicus is one of four critically endangered Asian Vultures. In India, this species has declined catastrophically, but in Pakistan only small population declines have been recorded. Mortality of this species has been linked to poisoning by veterinary diclofenac, which was banned throughout south Asia in 2006. Between 2003 and 2012 we measured abundance of adult, sub-adult, juvenile, and dead vultures, and nest occupancy and productivity at the largest known Long-billed Vulture colony in Pakistan. We compared population parameters from before (2003−2006) and after (2007−2012) the ban on veterinary diclofenac. Our data and models indicate that vulture abundance, nest occupancy, and nest productivity declined 61%, 73%, and 95%, respectively, in the three years before the diclofenac ban, and then increased 1–2 years after the ban by 55%, 52%, and 95%. Furthermore, we observed 87% of total vulture mortalities prior to the diclofenac ban. Our results demonstrate for the first time since the onset of the Asian vulture crisis that the ban on veterinary diclofenac is an effective management tool for reversing Long-billed Vulture population declines.

Dropping dead: causes and consequences of vulture population declines worldwide

Vultures are nature's 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

AbstractGyps 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.