Diclofenac is a non-steroidal anti-inflammatory drug that has been widely used worldwide to treat both humans and animals since first developed by Ciba-Geigy, now Novartis, in 1973. Trade names include Voltaren, Cataflam, Acoflam and many others. Concerns regarding the safety of such products for European vultures and other carrion-eaters like the golden eagle and the rare Spanish imperial eagle were raised earlier this year by a coalition of nature protection organizations led by the Vulture Conservation Foundation. The EU Commission subsequently initiated a referral procedure pursuant to article 35 of Directive 2001/82/EC on veterinary medicinal products to screen the drug for its possible impact on the scavengers.
The assessment, performed by the European Medicines Agency (EMA), concluded that the veterinary use of diclofenac in livestock animals poses a risk to European vultures and other necrophageous bird species. By acknowledging such a risk despite the lack of evidence “that a vulture in the European Union has been exposed or died as a result of feeding on carcasses from food-producing animals treated with diclofenac”, the EMA adopts a preventive approach and reasons by analogy with cases of intoxication seen in non-European countries to fill this “major data gap.”
The direct connection between diclofenac ingestion and vulture mortality is indeed well established. Poisoning occurs when the birds feed on livestock animals treated with the drug generally less than 9-10 days before dying. Concentrations of the substance in body tissues are then lethal, i.e. above 3 µg/kg, causing renal failure followed by fatal visceral gout within 36-58 hours of ingestion.
This problem was first observed and documented in India, Nepal, Pakistan, and Bangladesh. Back in the 1980’s, these four countries were home to thriving vulture populations, but from the early 1990’s, the numbers of long-billed vulture (Gyps indicus), oriental white-rumped vulture (Gyps bengalensis) and slender-billed vulture (Gyps tenuirostris) suddenly began dwindling at an abnormally rapid rate of over 50% a year, in coincidence with the recent mass introduction of diclofenac on the Asian market. However, it is not until 2004 that scientific research identified the direct correlation and another two to six years passed before the deadly substance was phased out from the affected zones. By then, vulture populations had crashed by more than 97%, nearly reaching a point of no return. Owing to the high toxicity of diclofenac and strongly gregarious foraging behavior of these birds, it was estimated that as little as 1 in 760 carcasses needed to contain the active molecule to trigger the collapse.
At present, all three vulture species are listed as “critically endangered” (last stage before “extinct in the wild”) by the International Union for Conservation of Nature Red List. Decline appears to have stopped since the ban and captive breeding programs are underway, but recovery takes time due to the slow reproductive cycle of vultures (typically one chick per clutch, one clutch per year and sexual maturity at 4-5 year old) and to mortality by causes other than diclofenac.
In Europe, the veterinary drug has been used in Italy since 1993 without objection because the Asian crisis had not yet been discovered at the time and the country only counts few vultures. However, when in early 2013 the substance was authorized in Spain (under the trade names Dolofenac and Diclovet) which is home to the largest European vulture population, nature protection organizations alerted without delay the EU Commission and member states that action should be taken to avoid another disaster.
The destruction of vultures can indeed have dramatic consequences for the ecosystem they pertain to and the humans who depend on it.
The birds fulfill a key ecological cleansing role for which they have evolved a unique, highly pathogenic gut microbial flora with an acidic pH of 1-1,5 capable of destroying the deadliest germs that flourish on decaying flesh. This symbiosis protects vultures against most infections that other, less specialized scavengers may contract when feeding on carrion. Moreover, unlike other necrophageous animals, the raptors are not picky eaters and devour carcasses down to the bones at an impressive speed. Vultures therefore facilitate nutrient cycling, contain the spread of diseases and regulate populations of other scavenger species.
These qualities were well-known to ancient civilizations like the Egyptians or some native North American tribes who associated vultures with purification and renewal. This symbolism persists today through the practice of sky burials by Tibetan Buddhists and the Parsees, a religious Zoroastrian minority, who offer their dead to the birds on so-called tower of silence (Dakhma in Persian language) to prevent putrefaction of corpses which they believe would otherwise pollute the four sacred elements―water, earth fire and air. These rituals were disrupted by the diminution of vultures and alternatives had to be found. On the Indian subcontinent, this mutualistic relationship is not restricted to the religious sphere. People have also long relied on vultures for the disposal of domestic animal carcasses which are thrown in dedicated communal dumps in both rural and urban areas, including Mumbai, Jaipur or New Delhi where, at times, up to 15,000 individuals could be observed.
Public salubrity in the region substantially depended on this free, natural service, so the accidental destruction of most Indian vultures resulted in a major sanitary crisis. Other scavengers like rats, crows and especially feral dogs took advantage of the birds’ absence to proliferate and propagate diseases like rabies, brucellosis, tuberculosis, anthrax or the bubonic plague. Biting and infecting locals with rabies, feral dogs have long been a hazard in the region which only got worse without the vultures—and since an astonishing 2001 law prohibits the killing of the dogs. The human health cost of such crisis has been estimated to be roughly $1.5 billion a year due to a significant increase in dog bites and human deaths from rabies.
Accidental intoxication by diclofenac was also documented in Africa where it was introduced in 2007. There, the veterinary drug is far from the only cause of vulture poisoning which in many cases is deliberate. Ivory poachers poison elephant and rhinoceros carcasses to get rid of the birds on which rangers rely to locate and pursue the criminals; vultures are directly poisoned for use of their heads and other body parts in traditional medicine; and farmers incidentally kill the scavengers when they fill livestock carcasses with noxious pesticides (Furadan) intended for large predators such as lions, hyenas or leopards to avenge the killings. Causes of mortality other than poisoning add up to this list. As a result, vultures populations across the continent have declined by 42% to 95% over the past 30 years depending on the species and the region, and sanitary problems may arise as carcasses rot for much longer, turning into hubs of infection. BirdLife International is currently fundraising to help conservationists better identify vulnerabilities and threats in order to find effective remedies.
In this context, the recent opinion of the EMA merely translates the lessons of the disastrous Indian experience and its African sequel to Europe where people are least aware of the importance of the raptors. Yet, on the Old Continent too, vultures have been a precious ally of pastoral communities—a relationship defined as commensalism—since ancient times as illustrated by the Roman saying “Ubi pecora, ibi vultures”, i.e. where livestock is, vultures are.
Europeans vultures were nearly extirpated by men during the first half of the 20th century. Nowadays, their cleansing role is restricted to the wild areas where they were successfully reintroduced over the past 40 years and to subsequently conquered rural areas. Until the early 2000’s, their role was generally appreciated by farmers who could dispose of their carcasses quickly, safely and at no cost. However, in 2002, Regulation CE 1774/2002, adopted in response to the bovine spongiform encephalopathy (BSE) crisis, changed the landscape by organizing the systematic removal and destruction of most animal carcasses and byproducts at authorized plants. Abruptly deprived of their primary food source, the raptors had to adapt which may have changed their behavior to some extent. In the following decade, some farmers reported incidents involving vultures “attacking” living animals and occasionally poisoned carcasses as a deterrent. Such occurences, which received strong media coverage, were in fact extremely rare, representing less than 0,2% of total livestock mortality, because vultures are not morphologically capable of killing. In all cases, the “victims” were dying or extremely feeble animals.
Since 2011, Regulation CE 142/2011 softened the 2002 sanitary framework. The natural cleansing role of vultures is being promoted again and more carrion is being offered. Many farmers acknowledge the utility of the ecological service provided and have chosen the mutualistic track for practical and financial reasons. A recent study found that Spanish vultures remove hundreds of tons of meat and bones each year which equals to $1.19-1.94 million when quantified; similarly, French vultures saved the state some €430,000 in disposal costs in 2010.
By supporting vulture conservation efforts in Europe, the EMA opinion is in phase with a renewed, green model in which ecological services, such as the cleansing role of vultures, are rehabilitated. It seems unlikely that the EU Commission would rule against the recommendations of the agency, especially since a safe alternative drug (Meloxican, developed by Boehringer Ingelheim) is available on the market and out of patent, thus making the transition an easy, non-costly one to implement by all member states.