What happened to the vultures of India?

An unanticipated consequence of being kind to cattle

India has a vulture problem. 

More precisely, big parts of India have a missing vulture problem.

Flock of white-rumped vultures near carcasses in Mangaon. P/C Shantanu Kuveskar. Wikimedia. Where are they now?

India was once home to about 40 million vultures belonging to nine different species. But in the last four decades, the numbers have nose-dived to just a few thousand for the entire nation. Four species — white-rumped vultures (Gyps bengalensis), Indian vultures (Gyps indicus), slender-billed vultures (Gyps tenuirostris), and the red-headed vultures (Sarcogyps calvus) are all in danger of extinction after a rapid population collapse in recent decades. [IUCN species]

The vulturine population crashed in the late 90s due to an inflammatory drug called diclofenac, which was given to livestock to reduce their aches and pains. Dead animals containing the drug proved lethal for vultures feeding on them, leading to extreme liver and kidney failure and death within a few days, sometimes spelling death for many birds attending one feeding.

The sudden die-off that caused the missing vulture problem became known as the Indian vulture crisis. [IVC] While you might think of vultures as big, carrion-eating, ugly-headed birds, a world without vultures runs the risk of damaging ecological threats.  Because vultures are such an effective scavenger of other dead animals, losing vultures means that other species can step into that ecological niche, and they’re not really up to the task of replacing the vultures.

The vultures have evolved a number of adaptations that allow them to locate and dispose of carcasses quickly and efficiently. The decline of vultures leads to increased carcass decomposition times and more rapid development of pathogenic bacteria—the kind of microbes that can make you seriously sick.

As a result of vultures disappearing, feral dog populations and other, less-effective scavengers have skyrocketed all over India. While feral dogs are a problem on their own, since the vultures have disappeared, their free food source has suddenly increased.  More feral dogs roaming around also bring about an increase in the cases of rabies to humans and wildlife.

Other animals such as crows and rats also try to fill in where the vultures once were.   Where carcasses were once completely scavenged by vultures, they’re now picked on by small animals, leaving them to mostly rot in village fields causing contaminated drinking water supplies. These newly abundant scavengers are just not as efficient as vultures, who can clean up a cow body in less than one hour. [SciNews]

Unlike many other animals, a vulture's metabolism remarkably effective at digesting pathogens and not getting sick.  They’ve evolved over eons to tolerate decomposed flesh and microbial loads that would slay nearly any other animal. In their absence, dogs and rats (who can’t digest such nasties) become carriers of the pathogens. [LiveSci, Raptor Research] India has around 18 million feral dogs, the largest population of carnivores in the world, which has led to increase in leopards (who quite enjoy feral dog snacks) invading inhabited areas and leading to conflicts with humans.  To make things worse, mammals also carry diseases from rotting carcasses--rabies, anthrax, plague, and all the rest are directly or indirectly responsible for thousands of deaths each year.

It's a huge problem.  In India, each year more than 30,000 people die from rabies, more than half the world's total. [Sudarshan] Around half a million Indians are treated for rabies each year, at a cost of ₹1,500 (US$19) per person.  That sounds like a small amount but remember that the average wage in India is ₹120 (US$1.50) per day.

According to a study in 2007, the expenses for medical care to treat animal bites cost India ₹750 million (US$9.4 million) per year. In addition to the cost of care, the government faces the problem of managing the population of disease carriers. Vaccination, elimination, or sterilization of the offending animals costs real money. As a consequence of the vulture loss, is estimated that the loss of scavengers costs India at least ₹1.7 trillion (US$21 billion) per year. [Abbas]

At the same time, increased crow populations at carcass sites near settlement areas pose a risk of infections to poultry, domesticated birds, and humans.  These are not the only catastrophic consequences for human health. Previously, if a cow died of anthrax, its flesh would be quickly consumed by vultures, so the deadly spores would not have time to spread. Since vultures’ digestive systems are so robust, they act as a dead end for microbial pathogens.  In essence, vultures stop disease spread before it can get started. By contrast, the rate of carcass consumption by dogs or rats is not nearly so fast, and their digestive systems are not nearly so robust, giving the spores and diseases ample time to spread around.    

The loss of vultures has been felt especially keenly by India's Zoroastrian community (also known as Parsis). For centuries they have relied on vultures to dispose of their dead, leaving bodies exposed to the sky on their ritual “Towers of Silence” (also called Dakhma) to be consumed by the birds in a process called excarnation.  For centuries, the Towers of Silence concentrated all of the Zoroastrian dead into a single location where vultures would traditionally consume their bodies. 

A Tower of Silence. Early 20th century drawing of a dakhma on Malabar Hill, Bombay, with vultures perched on the periphery.

It is against the Parsis' faith to bury, burn, or commit their dead to the water, which left vultures to provide a quick, easy, and clean solution. An entire human body can be consumed to the bone within a matter of hours by a large group of vultures in what the Parsi see as the most sacred act of charity. But with nearly no vultures at the Towers of Silence, half-eaten bodies can be left for days, leaving the community susceptible to disease.  Today, the loss of vultures has left excarnation a fragile practice with the very real possibility of vanishing as a practical matter.  [Umar]

What happened to the vultures?  It turns out that this was tricky to discover.   

The Indian vulture population crashed in the late 1990s.  Sick and dying birds were suddenly everywhere, and the unscavenged carcasses started piling up. 

As vultures disappeared from the landscape, the international scientific community found it difficult to find the cause of such a decline. Part of the problem was that the decline was rapid and widespread. The vulture population in India declined by an estimated 97% between 1992 and 2007. This made it difficult to identify the specific factors that were causing the decline. Furthermore, vultures could not legally be killed for scientific study in India, and obtaining fresh naturally dead animals for study became extremely rare, a situation made far more complicated by extremely hot weather in India where temperatures before the monsoon season routinely exceed 40 °C (104 °F). A freshly dead vulture is, naturally enough, a vulture magnet, which only magnified the problem. 

Then, in 2006, scientists investigating the massive decline in vulture numbers throughout South Asia made a surprising discovery. They found that diclofenac, a commonly-used non-steroidal anti-inflammatory drug (NSAID), was causing vultures to die off. The drug is often used to ease the pain of dying cattle and to alleviate their chronic illnesses. And while it is safe and effective for humans and livestock, it turns out to be fatal to vultures that eat cattle carcasses with just traces of diclofenac.

“Consumption of even small quantities of diclofenac causes elevated uric acid levels within the blood of vultures. It then leads to the deposition of uric acid crystals on and within the internal organs, resulting in kidney failure and death,” according to John Mallord, a leading vulture researcher. [Galligan]

Just a small proportion (< 0.1 mg/kg) of cattle carcasses containing lethal levels of diclofenac is enough to cause the observed rapid decline of vulture population. And it’s not just the concentration of diclofenac in the carcass. The overall number diclofenac-treated animals in the livestock population makes a big difference. If the fraction of animals with the drug in their system is just under 1%, then vulture populations crash.  [Iyer]

India banned the widespread use of diclofenac in 2006, with nearby nations following suit. But by then, vulture populations in various locations had dropped by up to 99%.

However, the ban against diclofenac didn’t remove the threat of anti-inflammatory drugs.  India the vulture population has still not recovered. It is still legal for pharmacies to sell diclofenac for human use, and covert studies of retail pharmacies have shown the drug is still being used to treat cattle. A big part of the problem is that it is amazingly effective in helping cattle with pain issues. Diclofenac is sometimes called a “cup of tea” drug because ill cows improve by the time the veterinarian finishes a drink with the owner. [Stokstad]  

After the diclofenac disaster, you’d think that it would be straightforward to simply ban diclofenac and resolve the issue.  But other drugs still legally sold can cause problems, too. Aceclofenac, for example, breaks down in the bodies of cattle into diclofenac, which causes the problem all over again. [Chandramohan] Another pain medication, ketoprofen, is also toxic to vultures.  This toxicity led Bangladesh to completely ban its use in 2021 to create “vulture safe zones.”  Meanwhile, another drug, the easily available and fast-acting nimesulide, has been growing in popularity, but seems to cause the same problems as diclofenac.

The problem keeps popping up.  Will the agricultural drug abuse pattern repeat?  Can a nation of livestock-loving, sympathetic people who only want to comfort ailing cattle make the connection between cattle-care and the deaths of those distinctly unlovable birds, the vultures, each of which provides an essential ecological service? 

Translating wide-scale issues like this into corrective actions typically takes both a contribution from science (needed to find equally effective drugs that also do not cause the side-effect of killing vultures), and government (needed to enact regulations nation-wide to limit the sale of vulture-killing medicines) to make the transition before the problem becomes permanent. 

Fortunately, a newer pain-relieving drug is being offered on the market (meloxicam) and nations are enacting regulations to minimize the sale of vulture-toxic drugs. [UICN drugs]

But in the face of a 99% die-off of native vultures, will the regulations be in time?  How quickly can the vulture population rebound from such a loss?

Only time will tell.  In the meanwhile, workarounds are the only solution, and none of them are attractive. 

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References

[Abbas] Abbas, S. S., Kakkar, M., Rogawski, E. T., & Roadmap to Combat Zoonoses in India (RCZI) initiative. (2014). Costs analysis of a population level rabies control programme in Tamil Nadu, India. PLoS Neglected Tropical Diseases, 8(2), e2721. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937306/

[Chandramohan] Chandramohan, S., Mathesh, K., Mallord, J. W., Naidoo, V., Mahendran, K., Kesavan, M., ... & Prakash, V. M. (2022). Metabolism of aceclofenac to diclofenac in the domestic water buffalo Bubalus bubalis confirms it as a threat to Critically Endangered Gyps vultures in South Asia. Environmental toxicology and pharmacology, 96, 103984. https://pubmed.ncbi.nlm.nih.gov/36182041/

[Galligan, et al.] Galligan, T. H., Mallord, J. W., Prakash, V. M., Bhusal, K. P., Alam, A. S., Anthony, F. M., ... & Green, R. E. (2021). Trends in the availability of the vulture-toxic drug, diclofenac, and other NSAIDs in South Asia, as revealed by covert pharmacy surveys. Bird Conservation International, 31(3), 337-353. https://www.cambridge.org/core/journals/bird-conservation-international/article/trends-in-the-availability-of-the-vulturetoxic-drug-diclofenac-and-other-nsaids-in-south-asia-as-revealed-by-covert-pharmacy-surveys/B8AD82F61B5361043EDE0EBB61952931

[IUCN species] IUCN critically endangered species list: https://www.iucnredlist.org/search?query=india%20vulture&searchType=species

[UICN drugs] https://www.iucn.org/news/bangladesh/201706/blog-mainstreaming-meloxicam-vulture-friendly-drug

[IVC] https://en.m.wikipedia.org/wiki/Indian_vulture_crisis

[Iyer] Kamakshi Iyer (19 August 2021). "Born to be wild: India's first captive-bred endangered vultures set free" The Guardian. https://www.theguardian.com/environment/2021/aug/19/india-critically-endangered-vultures-wild-release-aoe

[LiveSci] https://www.livescience.com/48899-vultures-bacteria-microbiome.html (Nov, 2014)

[Raptor research] Van Den Heever, L., Thompson, L. J., Bowerman, W. W., Smit-Robinson, H., Shaffer, L. J., Harrell, R. M., & Ottinger, M. A. (2021). Reviewing the role of vultures at the human-wildlife-livestock disease interface: An African perspective. Journal of Raptor Research, 55(3), 311-327.  https://bioone.org/journals/journal-of-raptor-research/volume-55/issue-3/JRR-20-22/Reviewing-the-Role-of-Vultures-at-the-Human-Wildlife-Livestock/10.3356/JRR-20-22.pdf

[Raman] Vulture-toxic drugs linger. Deccan Herald, Sep 29, 2020.   https://www.deccanherald.com/science/vulture-toxic-drugs-linger-894655.html

[Rana] Rana, G.; Prakash, V. (2003). "Cannibalism in Indian White-backed Vulture Gyps bengalensis in Keoladeo National Park, Bharatpur, Rajasthan" Journal of the Bombay Natural History Society. 100 (1).

[SciNews] https://www.snexplores.org/article/watching-out-vultures  (January, 2010)

[Stokstad] Stokstad, Erik. "Vultures face new toxic threat." Science 373.6560 (2021): 1187-1187. https://www.science.org/content/article/cattle-drug-poses-new-threat-asia-s-vultures

[Sudarshan] Sudarshan, M. K., Madhusudana, S. N., Mahendra, B. J., Rao, N. S. N., Narayana, D. A., Rahman, S. A., ... & Ravikumar, K. (2007). Assessing the burden of human rabies in India: results of a national multi-center epidemiological survey. International Journal of Infectious Diseases, 11(1), 29-35.   https://www.who.int/docs/default-source/searo/india/health-topic-pdf/piis1201971206000117.pdf

[Swan] Swan, Gerry E., Richard Cuthbert, Miguel Quevedo, Rhys E. Green, Deborah J. Pain, Paul Bartels, Andrew A. Cunningham et al. "Toxicity of diclofenac to Gyps vultures." Biology letters 2, no. 2 (2006): 279-282. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1618889/

[Umar] Umar, Baba. “Without vultures, fate of Parsi ‘sky burials’ uncertain” Aljazeera, Apr 7, 2015.  https://www.aljazeera.com/features/2015/4/7/without-vultures-fate-of-parsi-sky-burials-uncertain