Retrospective on vulture declines in South Asia and its wider implications for avian populations worldwide
Vultures are obligate scavengers who subsist entirely on carrion, the decaying flesh of dead animals [9]. Negative stigmas often surround these birds of prey due to their macabre appearance and association with death, but it is essential to recognize vultures’ ecological importance. These birds help maintain ecosystem health by efficiently disposing of dead animals and preventing the spread of toxins and pathogens. They are key to maintaining balance in ecosystems and protecting the health of not just wildlife, but human populations [6].
However, vultures around the world are facing the threat of extinction, especially in Africa and South Asia [10]. 77% of vulture populations worldwide are declining [7]. The IUCN has reported that 16 out of the 22 extant vulture species around the world are considered extinction-prone (near threatened, vulnerable, endangered, critically endangered, and extinct). When compared to other avian scavengers, of which only 13% are extinction-prone and 70% have stable or increasing populations, vulture populations are the most threatened avian functional guild in the world [7]. A functional guild refers to a group of species that share similar ecological roles or perform similar functions within an ecosystem.
Anthropogenic activity is the main driver behind vulture decline worldwide, ranging from harmful interactions with human infrastructure, such as electrocution by power lines, to direct actions such as illegal hunting [10]. Of these forms of anthropogenic activity, dietary toxins are the most pressing threat to vulture populations worldwide as they are the leading cause of decline for 88% of threatened vulture species [7]. Exposure to dietary toxins ranges from accidental exposure to intentional poisoning, and the three main types of poisons that vultures interact with are pesticides, lead poisoning, and veterinary drugs. [11].
The recent deaths of large groups of vultures in South Africa and Botswana in 2022 [8] along with the spread of unprecedented nephrotoxicity deaths in regions of Europe in 2020 [7] have sparked concern and highlighted the need for urgent action to protect these birds. Understanding the underlying reasons why vulture poisonings occur and how the decline of vultures impacts wildlife and human communities helps inform what steps we can take to protect and restore their populations. One of the most well-documented vulture declines is that of the South Asian vulture population in 2012, which primarily impacted three Old-World species of vulture endemic to the region: Gyps bengalensis, Gyps indicus, and Gyps tenuirostris [9]. Understanding the South Asian vulture population collapse and the subsequent conservation efforts can help prevent the same from happening to other vulture populations around the world.
Causes and Consequences of Vulture Decline in South Asia
Vulture populations fell by 99.7% across South Asia between 1993 and 2002 [12]. Today, there are an estimated 20,000 vultures in India [13], an extremely sharp decline from an estimated population of about 40 million in the 1980s [12]. Once abundant in South Asia, white-rumped vultures (Gyps bengalensis), Indian vultures (Gyps indicus), and slender-billed vultures (Gyps tenuirostris) are now critically endangered due to the accidental poisoning caused by the consumption of diclofenac-contaminated cattle and other livestock carcasses [9]. Diclofenac is used to treat pain and inflammation in livestock and was widely used in South Asia in the 1990s. In vultures, diclofenac inhibits the enzyme cyclooxygenase, leading to the accumulation of uric acid in their kidneys. The drug’s nephrotoxicity (extremely damaging effect on the kidneys) results in visceral gout and, ultimately, renal failure, or the ability to excrete harmful metabolites from their bodies [15]. Only 1% of the cattle carcasses on which vultures feed would need to be contaminated with diclofenac to cause catastrophic population declines. Due to the widespread usage of diclofenac in livestock carcasses in the early 1990s to 2000s, the actual percentage of contaminated carcasses was much higher [14]
The impacts of the South Asian vulture population decline, which reached extinction level in some regions, have been profound. Contrary to the belief that vultures spread diseases, these birds inhibit the spread of pathogens, including those responsible for diseases like rabies and botulism [11]. Vultures have highly acidic stomachs and more powerful digestive enzymes than most species [16]. When vultures consume carrion, the acidic environment in their stomachs effectively kills the many harmful bacteria and viruses associated with dead or decaying matter. They are also extremely efficient scavengers, able to consume soft tissue from carcasses at much higher rates than other scavengers. However, in their absence, carcasses accumulate and decompose for longer periods, leading to the proliferation of pathogens in waterways and agricultural soils [6]. After the South Asian vulture population decline, feral dog populations boomed, accompanied by an increase in zoonotic disease transmission as the scavengers that replaced the vultures became carriers for these pathogens instead of eliminating them. For example, there were an estimated 40,000 human deaths due to rabies between 2002 and 2006 in India [17]. While vultures are not the only factor in disease control and carcass elimination, their decline and the subsequent replacement by scavengers that are less effective at pathogen elimination demonstrate the importance of these birds.
Restoring and Protecting Vultures in South Asia
In response to the population decline of the 2000s, a range of different programs were put into place to protect vultures. These consisted of practices in two main areas: removing diclofenac and similar nephrotoxic drugs from the market and conservation programs. These have had differing levels of success in restoring vulture populations in South Asia. Understanding why some programs were more successful than others can help guide legislators, researchers, and others when implementing future programs to keep vultures and other threatened species safe.
Diclofenac was banned for veterinary use in 2006 in India, Nepal, and Pakistan and in 2010 in Bangladesh [2] Vulture-safe alternatives such as meloxicam were pushed as promising replacements, however, diclofenac residue continues to be found in cattle carcasses and dead vultures [2]. To understand how, researchers used covert surveys of pharmacies in India, Nepal, and Bangladesh to investigate the availability and prevalence of diclofenac, similarly nephrotoxic Non-Steroidal Anti-Inflammatory drugs (NSAIDs), and vulture-safe alternatives like meloxicam. They found that while the availability of diclofenac declined, its presence on the market varied. In Nepal, diclofenac virtually disappeared from sale and the availability of meloxicam was the most common veterinary NSAID, accounting for 89.9% of available NSAIDs sold [2]. It was found that while diclofenac sales decreased in all three countries, it still made up for a significant portion of NSAIDs offered for sale in India [2]. Although meloxicam availability increased, other nephrotoxic drugs ultimately made up a greater share of the market [2]. These results show that continued legislation and enforcement are needed to remove diclofenac and other nephrotoxic drugs from the market, especially in India and Bangladesh.
Another area of policy aimed at protecting and restoring vulture populations in South Asia was the establishment of protected areas. Researchers examined spatial patterns in the diets of Gyps vultures in India using fecal metabarcoding[1]. Fecal metabarcoding is commonly employed in ecological and wildlife studies to non-invasively assess the diet, microbiome, and overall biodiversity of animals based on the genetic material present in their feces. Fecal metabarcoding provides insights into an organism's diet, its role in the ecosystem, and can aid in conservation efforts. Scientists used samples from sites located inside and outside protected areas and found that while diets varied across landscapes, protection status, and vulture species, domestic livestock was present in >95% of the samples from central, west, and north India [1]. In comparison, 77% of the samples in South India had only wild species [1]. Because of this, establishing protected areas is not enough to protect vulture species; continued bans and removal of nephrotoxic drugs like diclofenac from veterinary use must be pursued. Most recent surveys of vulture populations in 2015, following similar surveys conducted between 1991 and 2011, across northern, central, western, and north-eastern India have found that since the ban of diclofenac for veterinary use in 2006, the decline of White-rumped Vultures has slowed and may have reversed, however, the population of all three Gyps species continues to decline [18].
Other populations at risk
Though South Asia’s vulture populations are still recovering from the devastating effects of diclofenac, they are not the only vulture population worldwide that is at risk of population collapse due to pharmacological poisonings. For example, diclofenac was still registered for livestock usage in 2013 in Spain. Researchers have found that 3.6% of the avian scavengers sampled contained residue of flunixin, a nephrotoxic NSAID similar to diclofenac also found in livestock carcasses [3]. At the time of this study, diclofenac poisoning had not been observed in the Iberian Peninsula. However, Herrero-Villar et al. (2020) state that flunixin poisoning poses a clear and immediate threat. Because of these threats, better-managed carrion disposal and appropriate risk labeling of disposal sites are needed [2]. One difficulty in developing safer alternatives to nephrotoxic drugs is the lack of understanding of the mechanisms behind diclofenac toxicity in vultures and avian susceptibility to nephrotoxic drugs. It is not well understood why meloxicam does not cause the same levels of nephrotoxicity and uric acid poisoning as diclofenac, though some have attributed it to meloxicam’s lower half-life [2]. However, Old World vultures are not the only birds that have been found to be susceptible to diclofenac & similar drug’s nephrotoxicity.
Assessing the difference in NSAID susceptibility between Old World and New World raptors may give researchers insight into the mechanisms of nephrotoxicity and where conservation efforts should be focused. Old World raptors inhabit Europe, Asia, and Africa while New World raptors, such as the Bald Eagle and Red-tailed Hawk, are found in the Americas. Using mitochondrial genome analysis, researchers found several species of the Accipitridae family, which are closely evolutionarily linked to Old World vultures, are also susceptible to NSAID poisoning [5]. This has implications for conservation efforts as more species than previously thought can be impacted by NSAIDs. Another group of researchers investigated the mechanisms behind nephrotoxicity in vultures using chickens as a model organism [19]. Scientists concluded that there were changes in both renal perfusion and renal plasma flow through the destruction of tubular secretion functionality. They found that diclofenac treatment led to decreased uric acid clearance in all the birds and signs of hyperuricemia and death in 1/3 of the birds[19]. This provides more insight into the mechanisms of damage by diclofenac on these birds and could lead to the development of more widespread avian-safe alternatives.
Conclusion
Understanding the causes of the population collapse of Gyps vultures in South Asia and the efficacy of programs implemented to restore and protect those populations in the aftermath can help us understand how to protect other avian populations around the world at risk of similar threats. Nephrotoxic drug poisoning threatens more populations than we once thought, such as Old-World vultures and other members of the Accipitridae family. We must reflect on the impact and fallout of the vulture population collapse in South Asia, and act proactively to protect these essential avian populations, rather than stand by and deal with the far-reaching consequences retrospectively. Raising awareness about the dangers of such drugs and the importance of these birds to the ecosystem is the first step in protecting vultures and preventing another catastrophic decline in their populations.
About the Author: Adyasha Padhi
Adyasha is a fourth-year Biochemistry & Molecular Biology and Sociocultural Anthropology double major with minors in Public Health & Computer Science. She is an undergraduate researcher in the Gomes Lab, studying the side effects of commonly used drugs such as ibuprofen on the heart and the signaling pathways involved in proteostasis (protein homeostasis) in cardiac and skeletal muscle diseases. She hopes to attend graduate school to pursue a career in translational research. In her free time, she enjoys doing puzzles, playing video games, reading, and baking.
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