Veterinary agents and poisons threaten avian scavengers in Africa and Europe
Ngaio Richards, Working Dogs for Conservation, Three Forks, Montana, USA; ngaio@workingdogsforconservation.org
Darcy Ogada, The Peregine Fund, Nairobi, Kenya; darcyogada@yahoo.com
ECG Bulletin January 2015
Darcy Ogada, The Peregine Fund, Nairobi, Kenya; darcyogada@yahoo.com
ECG Bulletin January 2015
Perceived to be in competition with hunters and to prey on livestock, predators in Europe and Africa are deliberately poisoned via carcass baits laced with agricultural pesticides. As communal scavengers, vulture populations in these areas have been especially hard hit by the presence of poison-laced carcasses. Species that migrate between Europe and Africa face poisoning risks in either region. Residues of veterinary agents in the carcasses available to vultures, especially in Europe, are also of concern.
Europe has a long history of poisoning wildlife. In particular, predators that are in direct competition with hunters and may prey on livestock, are generally maligned. As communal scavengers, vultures have been hit particularly hard and have even been directly targeted because of the belief that they prey on young animals. Following severe declines of population in birds of prey (for example the Imperial Eagle, the Red Kite, and Cinereous and Egyptian Vultures), anti-poaching and anti-poisoning initiatives have been implemented in the EU over the past decade, but these problems nevertheless persist (1). In Africa, deliberate poisoning of wildlife has been documented for hundreds of years (2). When Africa’s human population began to explode in the 1980s, the increasing need for agricultural and grazing lands exacerbated conflict between people and wildlife, especially carnivores (3). The commodification of Africa’s natural resources also began in earnest around this time. All these factors led to an increase in wildlife poisoning, particularly with agricultural pesticides, a practice that continues today (3). Added to these deliberate poisonings, there is a new threat from veterinary agents that are highly toxic to vultures. Thus, avian scavengers migrating between Europe and Africa face the prospect of poisoning in either region.
Threats to vultures in Europe
In 2013, the nonsteroidal anti-inflammatory drug (NSAID) diclofenac, which nearly drove three Gyps vulture species to extinction in Asia (4), was registered for veterinary use in Spain, Italy, and several other EU countries (5, 6). Given that Spain is the main European vulture stronghold and that populations of some species (such as the Egyptian and Bearded vultures) in Europe are faltering, the drug’s presence on the veterinary market is perplexing and troubling. Sharma et al. (7) recently showed that diclofenac is also toxic to Steppe Eagles, raising additional concerns for Aquila eagles (such as the Imperial Eagle) and other avian scavengers.
Other NSAIDs (e.g. flunixin and ketoprofen) shown to be toxic to vultures and other birds (8) are also registered for veterinary use in Europe (9). Residues of these and various other veterinary agents (e.g. antibiotics and euthanasia drugs) are therefore also potentially available to avian scavengers in livestock carcasses, whether at specially managed feeding stations, in captive/rehabilitation facilities, or in remote rural grazing areas where an affected animal cannot readily be retrieved after death. The potential repercussions of these other NSAIDs warrant further investigation (8, 9), but the relative threats (or lack thereof) in the European Union have not yet been established (10). And while the campaign against deliberate wildlife poisoning in Southern Spain is providing affected populations with temporary respite, this is still very far from resolved. A two-pronged response is still needed to address deliberate exposure to poisons and also non-deliberate exposure to veterinary agents.
Europe has a long history of poisoning wildlife. In particular, predators that are in direct competition with hunters and may prey on livestock, are generally maligned. As communal scavengers, vultures have been hit particularly hard and have even been directly targeted because of the belief that they prey on young animals. Following severe declines of population in birds of prey (for example the Imperial Eagle, the Red Kite, and Cinereous and Egyptian Vultures), anti-poaching and anti-poisoning initiatives have been implemented in the EU over the past decade, but these problems nevertheless persist (1). In Africa, deliberate poisoning of wildlife has been documented for hundreds of years (2). When Africa’s human population began to explode in the 1980s, the increasing need for agricultural and grazing lands exacerbated conflict between people and wildlife, especially carnivores (3). The commodification of Africa’s natural resources also began in earnest around this time. All these factors led to an increase in wildlife poisoning, particularly with agricultural pesticides, a practice that continues today (3). Added to these deliberate poisonings, there is a new threat from veterinary agents that are highly toxic to vultures. Thus, avian scavengers migrating between Europe and Africa face the prospect of poisoning in either region.
Threats to vultures in Europe
In 2013, the nonsteroidal anti-inflammatory drug (NSAID) diclofenac, which nearly drove three Gyps vulture species to extinction in Asia (4), was registered for veterinary use in Spain, Italy, and several other EU countries (5, 6). Given that Spain is the main European vulture stronghold and that populations of some species (such as the Egyptian and Bearded vultures) in Europe are faltering, the drug’s presence on the veterinary market is perplexing and troubling. Sharma et al. (7) recently showed that diclofenac is also toxic to Steppe Eagles, raising additional concerns for Aquila eagles (such as the Imperial Eagle) and other avian scavengers.
Other NSAIDs (e.g. flunixin and ketoprofen) shown to be toxic to vultures and other birds (8) are also registered for veterinary use in Europe (9). Residues of these and various other veterinary agents (e.g. antibiotics and euthanasia drugs) are therefore also potentially available to avian scavengers in livestock carcasses, whether at specially managed feeding stations, in captive/rehabilitation facilities, or in remote rural grazing areas where an affected animal cannot readily be retrieved after death. The potential repercussions of these other NSAIDs warrant further investigation (8, 9), but the relative threats (or lack thereof) in the European Union have not yet been established (10). And while the campaign against deliberate wildlife poisoning in Southern Spain is providing affected populations with temporary respite, this is still very far from resolved. A two-pronged response is still needed to address deliberate exposure to poisons and also non-deliberate exposure to veterinary agents.
The situation in Africa
In Africa, deliberate wildlife poisoning has been implicated in population-level declines in large carnivores, raptors, and vultures, particularly in southern and East Africa (3). Scavenging species (e.g. lions, hyenas, jackals, vultures, and eagles) have been the most impacted (3), with poisoning being the main driver in >60% of vulture declines over the past 30 years (11). During 2013, known vulture poisonings exceeded 2000 individuals—the highest figure to date and likely a gross underestimate, because most poisoning incidents are never reported (3, 11). The recent surge in elephant and rhino poaching using poisons and the associated poisoning of vultures likely represents one of the most important new threats to African vultures, one that is little reported even among conservationists.
There is also increasing concern about the use of veterinary diclofenac and other NSAIDs in livestock in Africa and their potential to harm African vultures (12), particularly in South Africa, where vulture ‘restaurants’ (feeding stations) are comparatively abundant and stocked primarily with the carcasses of dead livestock (13). Elsewhere on the continent, the NSAID threat to vultures is probably low because of (believed) minimal use of NSAIDs in livestock. Even where NSAIDS are used, the likelihood of vultures feeding on a treated carcass is small because dead livestock tends to be consumed by people (D. Ogada personal observation). However, residues in domestic animals kept for transportation (e.g. horses, camels and donkeys) that may not be eaten upon death must still be verified.
Exposure to veterinary agents versus deliberate poisoning
The term “poisoning” is now frequently (and, at least for the present time, misleadingly) used in conjunction with the exposure of vultures and other species to diclofenac. The drug is highly toxic to Old World vultures, which succumb to visceral gout after ingesting residues accumulated in the tissues of animals administered the drug during veterinary treatments. Other (often mammalian) scavengers appear to be far less susceptible to the drug. The key point is that any ensuing harm to vultures and other susceptible scavengers exposed to diclofenac-containing carcasses is unintentional. By contrast, in a “true” poisoning case, carcasses and other desirable food items (depending on the intended wildlife target) are intentionally laced with potent compounds such as strychnine, aldicarb, carbofuran, or chlorfenvinphos – anything that is readily available, highly effective, and inexpensive. All of these compounds are acutely toxic and indiscriminately kill any animal that feeds on the bait.
The availability of potentially toxic veterinary drug residues in livestock carcasses and that of toxic compounds deliberately added to carcasses and other edible lures are, for now, two distinct threats, requiring different investigatory and remedial approaches. However, if would-be poisoners in European countries where diclofenac has been registered realize its potency to vultures, they may adopt it, or other available NSAIDs, as a poison. If this happens, the line between unintentional intoxication and deliberate poisoning will be blurred, and wildlife forensic investigations will have to be adapted accordingly. This concern should also be proactively extended to other veterinary agents that have been shown to harm scavengers feeding on previously treated livestock carcasses (15).
In both Europe and Africa, the deliberate poisoning menace to predatory and scavenging wildlife is particularly pressing, as several populations are being driven towards extinction. Local wildlife poisonings undermine national and international conservation efforts. The current surge in the use of poisons to poach elephants and rhinos is extremely worrying. The slightest additional threat, in this case in the form of available toxic residues of veterinary agents, can place an unsustainable strain on an already plummeting population. Concerted and sustained vigilance and monitoring of all veterinary agents known to be in use and potentially harmful is of utmost importance. Understanding the relative magnitude of, and inherent complexities presented by, each likely threat is essential to enacting stringent legal procedures and determining penalties in the ongoing battle to safeguard scavenging wildlife and the critical ecosystem balance they help maintain.
Acknowledgements
We thank Jose Rafael Garrido, Alvaro Camiña, and Rafael Mateo for their feedback regarding the situation in Europe. We thank Iñigo Fajardo for providing the photographs of Griffon vultures at El Picacho Vulture feeding station, Cadiz Province, Andalucia, Spain. The feeding station is run for conservation purposes.
References
1.Fajardo Ruiz et al., in Carbofuran and Wildlife Poisoning: Global Perspectives and Forensic Approaches, N. L. Richards, Ed. (Wiley, Chichester, UK, 2011), Chapter 5, pp 147-155.
2.H. Stadler, in Prevention is the Cure. Proceedings of a workshop on holistic management of human-wildlife conflict in the agricultural sector of South Africa, B. Daly et al., Eds. (Endangered Wildlife Trust, Johannesburg, South Africa, 2006), pp 11-16.
3.D. L. Ogada, Power of poison: pesticide poisoning of Africa’s wildlife, Annals of the New York Academy of Sciences 10.1111/nyas.12405 (2014).
4.J. L. Oaks et al., Diclofenac residues as the cause of vulture population decline in Pakistan, Nature, 427, 630 (2004).
5.A. Camiña, J. R. Garrido, J. Martin, C. H. Lopez-Hernández, R. Alfaro, A new threat to European vultures, Science, 344, 150 (2014).
6.A. Margalida, J. A. Sanchez-Zapata, G. Blanco, F. Hiraldo, J. A. Donazar, Diclofenac approval as a threat to Spanish vultures, Cons. Biol., 28, 631 (2014).
7.A. K. Sharma et al.. Diclofenac is toxic to the Steppe Eagle Aquila nipalensis: widening the diversity of raptors threatened by NSAID misuse in South Asia. Bird Conservation International , 24, 282 (2014).
8.R. Cuthbert, J. Parry-Jones, R. E. Green, D. J. Pain, NSAIDs and scavenging birds: potential impacts beyond Asia’s critically endangered vultures. Biological Letters, 3, 91 (2007).
9.Commission Regulation (EU) No 37/2010 of 22 December 2009 on pharmacologically active substances and their classification regarding maximum residue limits in foodstuffs of animal origin, Official Journal of the European Union L15, pp1-72 (2010).
10.R. J. Cuthbert et al., Assessing the ongoing threat from veterinary non-steroidal anti-inflammatory drugs to critically endangered Gyps vultures in India, Oryx, 45, 420 (2011).
11.N. L. Richards et al., Merging wildlife and environmental monitoring approaches with forensic principles: application of unconventional and non-invasive sampling in eco-pharmacovigilance, Journal of Forensic Research, 10.4172/2157-7145.1000228 (2014).
12.D. L. Ogada et al., Another continental vulture crisis: Africa’s vultures collapsing toward extinction, in preparation.
13.V. Naidoo, K. Wolter, R. Cuthbert, N. Duncan, N. 2009. Veterinary diclofenac threatens Africa’s endangered vulture species, Regulatory Toxicology and Pharmacology, 53, 205 (2009).
14.M. D. Anderson, S. E. Piper, G. E. Swan, Non-steroidal anti-inflammatory drug use in South Africa and possible effects on vultures, South African Journal of Science, 101, 112 (2005).
15.K. O’Rourke, Euthanatized animals can poison wildlife: Veterinarians receive fines, Journal of the American Veterinary Medical Association, 220, 146 (2002).
In Africa, deliberate wildlife poisoning has been implicated in population-level declines in large carnivores, raptors, and vultures, particularly in southern and East Africa (3). Scavenging species (e.g. lions, hyenas, jackals, vultures, and eagles) have been the most impacted (3), with poisoning being the main driver in >60% of vulture declines over the past 30 years (11). During 2013, known vulture poisonings exceeded 2000 individuals—the highest figure to date and likely a gross underestimate, because most poisoning incidents are never reported (3, 11). The recent surge in elephant and rhino poaching using poisons and the associated poisoning of vultures likely represents one of the most important new threats to African vultures, one that is little reported even among conservationists.
There is also increasing concern about the use of veterinary diclofenac and other NSAIDs in livestock in Africa and their potential to harm African vultures (12), particularly in South Africa, where vulture ‘restaurants’ (feeding stations) are comparatively abundant and stocked primarily with the carcasses of dead livestock (13). Elsewhere on the continent, the NSAID threat to vultures is probably low because of (believed) minimal use of NSAIDs in livestock. Even where NSAIDS are used, the likelihood of vultures feeding on a treated carcass is small because dead livestock tends to be consumed by people (D. Ogada personal observation). However, residues in domestic animals kept for transportation (e.g. horses, camels and donkeys) that may not be eaten upon death must still be verified.
Exposure to veterinary agents versus deliberate poisoning
The term “poisoning” is now frequently (and, at least for the present time, misleadingly) used in conjunction with the exposure of vultures and other species to diclofenac. The drug is highly toxic to Old World vultures, which succumb to visceral gout after ingesting residues accumulated in the tissues of animals administered the drug during veterinary treatments. Other (often mammalian) scavengers appear to be far less susceptible to the drug. The key point is that any ensuing harm to vultures and other susceptible scavengers exposed to diclofenac-containing carcasses is unintentional. By contrast, in a “true” poisoning case, carcasses and other desirable food items (depending on the intended wildlife target) are intentionally laced with potent compounds such as strychnine, aldicarb, carbofuran, or chlorfenvinphos – anything that is readily available, highly effective, and inexpensive. All of these compounds are acutely toxic and indiscriminately kill any animal that feeds on the bait.
The availability of potentially toxic veterinary drug residues in livestock carcasses and that of toxic compounds deliberately added to carcasses and other edible lures are, for now, two distinct threats, requiring different investigatory and remedial approaches. However, if would-be poisoners in European countries where diclofenac has been registered realize its potency to vultures, they may adopt it, or other available NSAIDs, as a poison. If this happens, the line between unintentional intoxication and deliberate poisoning will be blurred, and wildlife forensic investigations will have to be adapted accordingly. This concern should also be proactively extended to other veterinary agents that have been shown to harm scavengers feeding on previously treated livestock carcasses (15).
In both Europe and Africa, the deliberate poisoning menace to predatory and scavenging wildlife is particularly pressing, as several populations are being driven towards extinction. Local wildlife poisonings undermine national and international conservation efforts. The current surge in the use of poisons to poach elephants and rhinos is extremely worrying. The slightest additional threat, in this case in the form of available toxic residues of veterinary agents, can place an unsustainable strain on an already plummeting population. Concerted and sustained vigilance and monitoring of all veterinary agents known to be in use and potentially harmful is of utmost importance. Understanding the relative magnitude of, and inherent complexities presented by, each likely threat is essential to enacting stringent legal procedures and determining penalties in the ongoing battle to safeguard scavenging wildlife and the critical ecosystem balance they help maintain.
Acknowledgements
We thank Jose Rafael Garrido, Alvaro Camiña, and Rafael Mateo for their feedback regarding the situation in Europe. We thank Iñigo Fajardo for providing the photographs of Griffon vultures at El Picacho Vulture feeding station, Cadiz Province, Andalucia, Spain. The feeding station is run for conservation purposes.
References
1.Fajardo Ruiz et al., in Carbofuran and Wildlife Poisoning: Global Perspectives and Forensic Approaches, N. L. Richards, Ed. (Wiley, Chichester, UK, 2011), Chapter 5, pp 147-155.
2.H. Stadler, in Prevention is the Cure. Proceedings of a workshop on holistic management of human-wildlife conflict in the agricultural sector of South Africa, B. Daly et al., Eds. (Endangered Wildlife Trust, Johannesburg, South Africa, 2006), pp 11-16.
3.D. L. Ogada, Power of poison: pesticide poisoning of Africa’s wildlife, Annals of the New York Academy of Sciences 10.1111/nyas.12405 (2014).
4.J. L. Oaks et al., Diclofenac residues as the cause of vulture population decline in Pakistan, Nature, 427, 630 (2004).
5.A. Camiña, J. R. Garrido, J. Martin, C. H. Lopez-Hernández, R. Alfaro, A new threat to European vultures, Science, 344, 150 (2014).
6.A. Margalida, J. A. Sanchez-Zapata, G. Blanco, F. Hiraldo, J. A. Donazar, Diclofenac approval as a threat to Spanish vultures, Cons. Biol., 28, 631 (2014).
7.A. K. Sharma et al.. Diclofenac is toxic to the Steppe Eagle Aquila nipalensis: widening the diversity of raptors threatened by NSAID misuse in South Asia. Bird Conservation International , 24, 282 (2014).
8.R. Cuthbert, J. Parry-Jones, R. E. Green, D. J. Pain, NSAIDs and scavenging birds: potential impacts beyond Asia’s critically endangered vultures. Biological Letters, 3, 91 (2007).
9.Commission Regulation (EU) No 37/2010 of 22 December 2009 on pharmacologically active substances and their classification regarding maximum residue limits in foodstuffs of animal origin, Official Journal of the European Union L15, pp1-72 (2010).
10.R. J. Cuthbert et al., Assessing the ongoing threat from veterinary non-steroidal anti-inflammatory drugs to critically endangered Gyps vultures in India, Oryx, 45, 420 (2011).
11.N. L. Richards et al., Merging wildlife and environmental monitoring approaches with forensic principles: application of unconventional and non-invasive sampling in eco-pharmacovigilance, Journal of Forensic Research, 10.4172/2157-7145.1000228 (2014).
12.D. L. Ogada et al., Another continental vulture crisis: Africa’s vultures collapsing toward extinction, in preparation.
13.V. Naidoo, K. Wolter, R. Cuthbert, N. Duncan, N. 2009. Veterinary diclofenac threatens Africa’s endangered vulture species, Regulatory Toxicology and Pharmacology, 53, 205 (2009).
14.M. D. Anderson, S. E. Piper, G. E. Swan, Non-steroidal anti-inflammatory drug use in South Africa and possible effects on vultures, South African Journal of Science, 101, 112 (2005).
15.K. O’Rourke, Euthanatized animals can poison wildlife: Veterinarians receive fines, Journal of the American Veterinary Medical Association, 220, 146 (2002).