Abstract
Carrion is rarely managed as a food resource, and there is an acute lack of awareness about its importance to a host of scavenging species. While availability of carrion is a serious problem for some populations of scavengers, its decreasing quality is a global issue that has decimated others, and contaminated food webs. We now know that carrion is widely tainted with veterinary agents, among them antibiotics and the non-steroidal anti-inflammatory drugs, or NSAIDs, which are used to treat livestock. Numerous antimicrobial agents have been found to negatively affect micro-scavengers such as coprophagous beetles. Carrion is also frequently used as a poisoning conduit—in particular, being laced with highly toxic organophosphorus and carbamate pesticides to kill predators such as lions, wolves, eagles and hyenas. Secondary poisoning following the consumption of rodenticide or organophosphate pesticide residues in pest species has also severely harmed scavenger populations. Presence of heavy metals—primarily lead, in the carcasses of animals killed by hunters using lead ammunition—has devastated populations of the Critically Endangered California Condor, via both lethal and sub-lethal effects. Carrion must be managed in concert with the ecosystem services that scavengers provide, and to benefit biodiversity. Regulatory policies aimed at controlling the quantity or quality of carrion have had both negative and positive effects on scavengers. Supplementary feeding stations may bolster vulture populations, but they must ensure both the intrinsic safety and quality of carrion available to scavengers. We outline the factors that make carrion unsafe to scavengers, especially obligate feeders such as vultures, and offer recommendations and guidelines for further research, appropriate regulatory policies, and vigilant management practices to properly safeguard scavengers from carrion—a resource still largely perceived to be benign.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Aguilar RF, Yoshicedo JN, Parish CN (2012) Ingluviotomy tube placement for lead-induced crop stasis in the California condor (Gymnogyps californianus). J Avian Med Surg 26:176–181
Alterio N (2000) Controlling small mammal predators using sodium monofluoroacetate (1080) in bait stations along forestry roads in a New Zealand beech forest. N Z J Ecol 24(1):3–9
Anderson MD, Anthony A (2005) The advantages and disadvantages of vulture restaurants versus simply leaving livestock (and game) carcasses in the veldt. Vult News 53(1):42–45
Balcomb R (1983) Secondary poisoning of red-shouldered hawks with carbofuran. J Wildl Manag 47(4):1129–1132
Batuman V, Landy E, Maesaka J, Wedeen R (1983) Contribution of lead to hypertension with renal impairment. N Engl J Med 309:17–21
Behmke S, Fallon J, Duerr AE et al (2015) Chronic lead exposure is epidemic in obligate scavenger populations in eastern North America. Environ Int 79:51–55
Berny P, Gaillet JR (2008) Acute poisoning of Red Kites (Milvus milvus) in France: data from the SAGIR network. J Wildl Dis 44(2):417–426
Berny PJ, Buronfosse T, Buronfosse F et al (1997) Field evidence of secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo) by bromadiolone, a 4-year survey. Chemosphere 35(8):1817–1829
Berny P, Vilagines L, Cugnasse JM et al (2015) VIGILANCE POISON: illegal poisoning and lead intoxication are the main factors affecting avian scavenger survival in the Pyrenees (France). Ecotoxicol Environ Saf 118:71–82
Boshoff AF, Vernon CJ (1980) The past and present distribution and status of the Cape Vulture in the Cape Province. Ostrich 51(4):230–250
Brakes CR, Smith RH (2005) Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning. J Appl Ecol 42(1):118–128
Bridgeford P (2001) More vulture deaths in Namibia. Vult News 44:22–26
Bruggers RL, Jaeger MM, Keith JO et al (1989) Impact of fenthion on nontarget birds during quelea control in Kenya. Wildl Soc Bull 17(2):149–160
Canfield RL, Henderson CR, Cory-Sletchta DA et al (2003) Intellectual impariment in children with blood lead concentrations below 10 μg per deciliter. N Engl J Med 348:1517–1526
Carpenter JW, Pattee OH, Fritts SH et al (2003) Experimental lead poisoning in turkey vultures (Cathartes aura). J Wildl Dis 39:96–104
Casas-Díaz E, Cristòfol C, Cuenca R et al (2016) Determination of fluoroquinolone antibiotic residues in the plasma of Eurasian griffon vultures (Gyps fulvus) in Spain. Sci Total Environ 557–558:620–626
Chardonnet P, Belemsobgo U, Crosmary W et al (2005) Influences directes et indirectes sur la conservation du lion en Afrique de l’Ouest et en Afrique Centrale. Atelier sur la Conservation du Lion d’Afrique de l’Ouest et d’Afrique Centrale, Douala, Cameroon, 5–7 October
Chaudhry MJI, Ogada DL, Malik RN et al (2012) First evidence that populations of the critically endangered Long-billed Vulture Gyps indicus in Pakistan have increased following the ban on diclofenac in South Asia. Bird Conserv Int 22(4):389–397
Cherkaoui I (2005) The Bearded Vulture Gypaetus barbatus in Morocco. Vult News 52:37
Church ME, Gwiazda R, Risebrough R et al (2008) Ammunition is the principal source of lead accumulated by California condors re-introduced to the wild. Environ Sci Technol 42:1809–1811
Cook RC, Trainer DO (1966) Experimental lead poisoning of Canada geese. J Wildl Manag 30:1–8
Cortés-Avizanda A, Blanco G, DeVault TL et al (2016) Supplementary feeding and endangered avian scavengers: benefits, caveats, and controversies. Front Ecol Environ 14(4):191–199
Craighead D, Bedrosian B (2008) Blood lead levels of common ravens with access to big-game offal. J Wildl Manag 72(1):240–245
Cuthbert R, Parry-Jones J, Green RE, Pain DJ (2007) NSAIDs and scavenging birds: potential impacts beyond Asia’s critically endangered vultures. Biol Lett 3(1):90–93
Cuthbert R, Taggart MA, Prakash V et al (2011) Effectiveness of action in India to reduce exposure of Gyps Vultures to the toxic veterinary drug diclofenac. PLoS One 6:e19069
Cuthbert RJ, Taggart MA, Prakash V et al (2014) Avian scavengers and the threat from veterinary pharmaceuticals. Philos Trans R Soc Lond Ser B Biol Sci 369(1656). pii: 20130574
Cuthbert RJ, Taggart MA, Saini M et al (2015) Continuing mortality of vultures in India associated with illegal veterinary use of diclofenac and a potential threat from nimesulide. Oryx 50:104–112
Deygout C, Gault A, Sarrazin F, Bessa-Gomes C (2009) Modeling the impact of feeding stations on vulture scavenging service efficiency. Ecol Model 220(15):1826–1835
Dietrich K, Ris M, Succop P et al (2001) Early exposure to lead and juvenile delinquency. Neurotoxicol Teratol 23:511–518
Donázar JA, Margalida A, Campión D (2009) Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology. Munibe 29:1–551
Dupont H, Mihoub JB, Bobbe S, Sarrazin F (2012) Modelling carcass disposal practices: implications for the management of an ecological service provided by vultures. J Appl Ecol 49(2):404–411
Eason CT, Milne L, Potts M et al (1999) Secondary and tertiary poisoning risks associated with brodifacoum. N Z J Ecol 23(2):219–224
Eason CT, Murphy EC, Wright GR, Spurr EB (2002) Assessment of risks of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicology 11(1):35–48
Elliott JE, Langelier KM, Mineau P, Wilson LK (1996) Poisoning of bald eagles and red-tailed hawks by carbofuran and fensulfothion in the Fraser Delta of British Columbia, Canada. J Wildl Dis 32(3):486–491
Elliott JE, Wilson LK, Langelier KM et al (1997) Secondary poisoning of birds of prey by the organophosphorus insecticide, phorate. Ecotoxicology 6(4):219–231
Elliott JE, Birmingham AL, Wilson LK et al (2008) Fonofos poisons raptors and waterfowl several months after granular application. Environ Toxicol Chem 27(2):452–460
Endangered Wildlife Trust (2011) The Sasol guide to the establishment and operation of supplementary feeding sites for vultures. http://www.ewt.org.za/eBooks/booklets/Vulture%20Restuarant%20booklet.pdf. Accessed 10 Apr 2016
Epps CW (2014) Considering the switch: challenges of transitioning to non-lead hunting ammunition. Condor 116(3):429–434
Espín S, Martínez-López E, Jiménez P et al (2014) Effects of heavy metals on biomarkers for oxidative stress in Griffon vulture (Gyps fulvus). Environ Res 129:59–68
Fielding D, Newey S, van der Wal R, Irvine RJ (2014) Carcass provisioning to support scavengers: evaluating a controversial nature conservation practice. Ambio 43(6):810–819
Finkelstein ME, Doak DF, George D et al (2012) Lead poisoning and the deceptive recovery of the critically endangered California condor. Proc Natl Acad Sci U S A 109(28):11449–11454
Floate K (2006) Endectocide use in cattle and fecal residues: environmental effects in Canada. Can J Vet Res 70(1):1–10
Floate KD, Düring RA, Hanafi J et al (2015) Validation of a standard field test method in four countries to assess the toxicity of residues in dung of cattle treated with veterinary medical products. Environ Toxicol Chem 35:1934–1946
Frank L (2011) Living with lions: lessons from Laikipia. In: Georgiadis NJ (ed) Conserving wildlife in African landscapes: Kenya’s Ewaso ecosystem. Smithsonian Contributions to Zoology No. 632, pp 73–84
Galligan TH, Taggart MA, Cuthbert RJ et al (2016) Metabolism of aceclofenac in cattle to vulture-killing diclofenac. Conserv Biol 30(5):1122–1127
Gangoso L, Álvarez-Lloret P, Rodríguez-Navarro A et al (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157(2):569–574
García-Ripollés C, López-López P, García-López F (2004) Management and monitoring of a vulture restaurant in Castellón Province, Spain. Vult News 50:5–14
Gilbert M, Watson RT, Ahmed S et al (2002) Breeding and mortality of Oriental White-backed Vulture Gyps bengalensis in Punjab Province, Pakistan. Bird Conserv Int 12(4):311–326
Gilbert M, Watson RT, Ahmed S et al (2007) Vulture restaurants and their role in reducing diclofenac exposure in Asian vultures. Bird Conserv Int. 17(01):63–77
Gillies CA, Pierce RJ (1999) Secondary poisoning of mammalian predators during possum and rodent control operations at Trounson Kauri Park, Northland, New Zealand. N Z J Ecol 23(2):183–192
Giorgi M, Mengozzi G (2011) Malicious animal intoxications: poisoned baits. Vet Med 56(4):173–179
Glen AS, Gentle MN, Dickman CR (2007) Non-target impacts of poison baiting for predator control in Australia. Mammal Rev 37(3):191–205
González LM, Margalida A, Mañosa S et al (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperial eagle Aquila adalberti during a recovery period. Oryx 41(04):495–502
Guitart R, Sachana M, Caloni F et al (2010) Animal poisoning in Europe. Part 3: wildlife. Vet J 183(3):260–265
Haig SM et al (2014) The persistent problem of lead poisoning in birds from ammunition and fishing tackle. Condor 116(3):408–428
Hayes B (1988) British Columbia: deaths caused by barbiturate poisoning in bald eagles and other wildlife. Can Vet J 29(2):173–174
Helander B, Axelsson J, Borg H et al (2009) Ingestion of lead from ammunition and lead concentrations in white-tailed sea eagles (Haliaeetus albicilla) in Sweden. Sci Total Environ 407(21):5555–5563
Henny CJ, Mineau P, Elliott JE, Woodbridge B (1999) Raptor poisonings and current insecticide use: what do isolated kill reports mean to populations. In: Proceedings of the 22nd international ornithological congress, University of Natal, Durban
Hernández M, Margalida A (2008) Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 17(4):264–272
Hernández M, Margalida A (2009) Poison-related mortality effects in the endangered Egyptian vulture (Neophron percnopterus) population in Spain. Eur J Wildl Res 55(4):415–423
Houston DC, Copsey JA (1994) Bone digestion and intestinal morphology of the Bearded Vulture. J Raptor Res 28(2):73–78
Hunt WG, Burnham W, Parish CN et al (2006) Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc Bull 34(1):167–170
Jackson FJ (1938) The birds of Kenya colony and the Uganda protectorate. Gurney and Jackson, London
Jarvis MJ, La Grange M (1982) Problem vertebrate management in Zimbabwe. In: Proceedings of the tenth vertebrate pest conference, paper 25. http://digitalcommons.unl.edu/vpc10/25. Downloaded 18 Dec 2013
Kahumbu P (2012) Banned in America killing in Kenya: the story of a poison. Swara 3:30
Kaukeinen D (1982) A review of the secondary poisoning hazard potential to wildlife from the use of anticoagulant rodenticides. In: Proceedings of the tenth vertebrate pest conference, p 27. http://digitalcommons.unl.edu/vpc10/25. Accessed 10 Apr 2016
Kelly TR, Johnson CK (2011) Lead exposure in free-flying turkey vultures is associated with big game hunting in California. PLoS One 6:e15350
Kenny D, Reading R, Maude G et al (2015) Blood lead levels in White-Backed Vultures (Gyps africanus) from Botswana, Africa. Vult News 68:25–31
Knott J, Gilbert J, Hoccom DG, Green RE (2010) Implications for wildlife and humans of dietary exposure to lead from fragments of lead rifle bullets in deer shot in the UK. Sci Total Environ 409(1):95–99
Krueger B, Krueger KA (2002) U.S. fish and wildlife service fact sheet: secondary pentobarbital poisoning of wildlife. Habitat and Animal Health Concern, Inc., Stafford, VA. http://www.fws.gov/southeast/news/2002/12-03SecPoisoningFactSheet.pdf Accessed 6 Mar 2016
Langelier KM (1993) Barbiturate poisoning in twenty-nine bald eagles. In: Redig PT, Hunter B (eds) Raptor biomedicine. University of Minnesota Press, Minneapolis, MN, pp 231–232
Leopold AS, Cain SA, Cottam CM et al (1964) Predator and rodent control in the United States. US Fish and Wildlife Publications. Paper 25. http://digitalcommons.unl.edu/usfwspubs/254. Downloaded 15 Oct 2015
Lewis JC (1968) Use of poison bait to control rabies in Tennessee wildlife. Public Health Rep 83(1):69–74
Lewis CA, Cristol DA, Swaddle JP, Varian-Ramos CW, Zwollo P (2013) Decreased immune response in zebra finches exposed to sublethal doses of mercury. Arch Environ Contam Toxicol 64:327–336
Linhart SB, Kappeler A, Windberg LA (1993) A review of baits and bait delivery systems for free-ranging carnivores and ungulates. Contraception in wildlife: Animal and Plant Health Inspection Service. United States Department of Agriculture, Oakland, CA, pp 69–132
Locke LN, Thomas NJ (1996) Lead poisoning of waterfowl and raptors. In: Fairbrother A, Locke LN, Hoff GL (eds) Noninfectious diseases of wildlife. Manson, London, pp 108–117
Lumaret JP, Errouissi F (2002) Use of anthelmintics in herbivores and evaluation of risks for the nontarget fauna of pastures. Vet Res 33(5):547–562
Margalida A (2010) Supplementary feeding during the chick-rearing period is ineffective in increasing the breeding success in the bearded vulture (Gypaetus barbatus). Eur J Wild Res 56(4):673–678
Margalida A (2012) Baits, budget cuts: a deadly mix. Science 338(6104):192–192
Margalida A, Heredia R, Razin M, Hernández M (2008) Sources of variation in mortality of the Bearded vulture Gypaetus barbatus in Europe. Bird Conserv Int 18(01):1–10
Margalida A, Donázar JA, Carrete M, Sánchez-Zapata JA (2010) Sanitary versus environmental policies: fitting together two pieces of the puzzle of European vulture conservation. J Appl Ecol 47(4):931–935
Margalida A, Carrete M, Sánchez-Zapata JA, Donázar JA (2012) Good news for European vultures. Science 335(6066):284–284
Margalida A, Campión D, Donázar JA (2014a) Vultures vs. livestock: conservation relationships in an emerging conflict between humans and wildlife. Oryx 48(02):172–176
Margalida A, Sánchez-Zapata JA, Blanco G et al (2014b) Diclofenac approval as a threat to Spanish vultures. Conserv Biol 28(3):631–632
Margalida A, Colomer MA, Oro D (2014c) Man-induced activities modify demographic parameters in a long-lived species: effects of poisoning and health policies. Ecol Appl 24(3):436–444
Markandya A, Taylor T, Longo A et al (2008) Counting the cost of vulture decline—an appraisal of the human health and other benefits of vultures in India. Ecol Econ 67(2):194–204
Martínez-Haro M, Mateo R, Guitart R et al (2008) Relationship of the toxicity of pesticide formulations and their commercial restrictions with the frequency of animal poisonings. Ecotoxicol Environ Saf 69(3):396–402
Mateo R, Sánchez-Barbudo IS, Camarero PR, Martínez JM (2015) Risk assessment of bearded vulture (Gypaetus barbatus) exposure to topical antiparasitics used in livestock within an ecotoxicovigilance framework. Sci Total Environ 536:704–712
Mateo-Tomás P, Olea PP (2010) When hunting benefits raptors: a case study of game species and vultures. Eur J Wildl Res 56:519–528
Mateo-Tomás P, Olea PP, Sánchez-Barbudo IS, Mateo R (2012) Alleviating human-wildlife conflicts: identifying the causes and mapping the risk of illegal poisoning of wild fauna: mapping illegal poisoning of wildlife. J Appl Ecol 49(2):376–385
Mateo-Tomás P, Olea PP, Moleón M et al (2015) From regional to global patterns in vertebrate scavenger communities subsidized by big game hunting. Divers Distrib 21(8):913–924
Meenken D, Booth LH (1997) The risk to dogs of poisoning from sodium monofluoroacetate (1080) residues in possum (Trichosurus vulpecula). N Z J Agric Res 40(4):573–576
Mendelssohn H, Paz U (1977) Mass mortality of birds of prey caused by Azodrin, an organophosphorus insecticide. Biol Conserv 11(3):163–170
Mielke HW, Zahran S (2012) The urban rise and fall of air lead (Pb) and the latent surge and retreat of societal violence. Environ Int 43:48–55
Mills MGL, Hofer H (1998) Hyaenas: status survey and conservation action plan. IUCN/SSC Hyaena Specialist Group. IUCN, Gland, Switzerland and Cambridge
Mineau P (2013) Bird: pesticide use impacts. Encycl Environ Manag. https://doi.org/10.1081/E-EEM-120046191
Mineau P, Fletcher MR, Glaser LC et al (1999) Poisoning of raptors with organophosphorus and carbamate pesticides with emphasis on Canada, US and UK. J Raptor Res 33(1):1–37
Morales-Reyes Z, Pérez-García JM, Moleón M et al (2015) Supplanting ecosystem services provided by scavengers raises greenhouse gas emissions. Sci Rep 5:7811
Moreno-Opo R, Margalida A, García F et al (2012) Linking sanitary and ecological requirements in the management of avian scavengers: effectiveness of fencing against mammals in supplementary feeding sites. Biodivers Conserv 21(7):1673–1685
Moreno-Opo R, Trujillano A, Arredondo A et al (2015) Manipulating size, amount and appearance of food inputs to optimize supplementary feeding programs for European vultures. Biol Conserv 181:27–35
Mundy P, Butchart D, Ledger J, Piper S (1992) The vultures of Africa. Academic, London
Nadjafzadeh M, Hofer H, Krone O (2015) Lead exposure and food processing in white-tailed eagles and other scavengers: an experimental approach to simulate lead uptake at shot mammalian carcasses. Eur J Wildl Res 61(5):763–774
Needleman H (2004) Lead poisoning. Ann Rev Med 55:209–222
Nevin R (2007) Understanding international crime trends: the legacy of preschool lead exposure. Environ Res 104:315–336
Newton I, Shore RF, Wyllie I et al (1999) Empirical evidence of side-effects of rodenticides on some predatory birds and mammals. In: Cowan DP, Feare CJ (eds) Advances in vertebrate pest management. Filander, Fürth, pp 347–367
O’Rourke K (2002) Euthanized animals can poison wildlife: veterinarians receive fines. J Am Vet Med Assoc 220:146–147
Oaks JL, Gilbert M, Virani MZ et al (2004) Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427:630–633
Ogada DL (2014) The power of poison: pesticide poisoning of Africa’s wildlife. Ann N Y Acad Sci 1322:1–20
Ogada DL, Torchin ME, Kinnaird MF, Ezenwa VO (2012) Effects of vulture declines on facultative scavengers and potential implications for mammalian disease transmission. Conserv Biol 26(3):453–460
Ogada D, Botha A, Shaw P (2016b) Ivory poachers and poisons; drivers of Africa’s declining vulture populations. Oryx 50:593–596
Ogada D, Shaw P, Beyers RL et al (2016a) Another continental vulture crisis: Africa’s vultures collapsing toward extinction. Conserv Lett 9:89–97
Olea PP, Mateo-Tomás P (2009) The role of traditional farming practices in ecosystem conservation: the case of transhumance and vultures. Biol Conserv 142(8):1844–1853
Olea PP, Sánchez-Barbudo IS, Viñuela J et al (2009) Lack of scientific evidence and precautionary principle in massive release of rodenticides threatens biodiversity: old lessons need new reflections. Environ Conserv 36(01):1–4
Oro D, Margalida A, Carrete M et al (2008) Testing the goodness of supplementary feeding to enhance population viability in an endangered vulture. PLoS One 3(12):e408
Oro D, Genovart M, Tavecchia G et al (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16:1501–1514
Pain DJ, Cunningham AA, Donald PF et al (2003) Causes and effects of temporospatial declines of Gyps Vultures in Asia. Conserv Biol 17(3):661–671
Pain DJ, Fisher IJ, Thomas VG (2009) A global update of lead poisoning in terrestrial birds from ammunition sources. In: Richard T, Watson RT, Pokras M, Hunt G (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans, May 2008. The Peregrine Fund, Boise, ID, pp 99–118
Parmar G, Bratt H, Moore R, Batten PL (1987) Evidence for a common binding- site in vivo for the retention of anticoagulants in rat liver. Hum Toxicol 6:431–432
Pattee OH, Wiemeyer SN, Mulhern BM et al (1981) Experimental lead-shot poisoning in bald eagles. J Wildl Manag 45:806–810
Payne J, Farris R, Parker G et al (2015) Quantification of sodium pentobarbital residues from equine mortality compost piles. J Anim Sci 93(4):1824–1829
Piper SE (2004) Vulture restaurants-conflict in the midst of plenty. In: Chancellor RD, Meyburg B-U (eds) Raptors worldwide. WWGBP/MME, Budapest, pp 341–349
Piper SE (2005) Supplementary feeding programs: how necessary are they for the maintenance of numerous and healthy vultures populations? In: Houston DC, Piper SE (eds) Proceedings of the international conference on conservation and management of vulture populations. Natural History Museum of Crete & WWF Greece, Thessaloniki, pp 41–50
Piper SE, Boshoff AF, Scott HA (1999) Modelling survival rates in the Cape Griffon Gyps coprotheres, with emphasis on the effects of supplementary feeding. Bird Study 46(S1):S230–S238
Pokras MA, Kneeland MK (2009) Understanding lead uptake and effects across species lines: a conservation medicine approach. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, ID. https://doi.org/10.4080/ilsa.2009.0101
Prakash V (1999) Status of vultures in Keoladeo National Park, Bharatpur, Rajasthan, with special reference to population crash in Gyps species. J Bombay Nat Hist Soc 96:365–378
Rattner BA, Lazarus RS, Elliott JE et al (2014) Adverse outcome pathway and risks of anticoagulant rodenticides to predatory wildlife. Environ Sci Technol 48(15):8433–8445
Richards N (ed) (2012) Carbofuran and wildlife poisoning: global perspectives and forensic approaches. Wiley, Chichester
Richards NL, Ogada D (2014) The relative risks of veterinary agents and toxic compounds to avian scavengers and other wildlife within the European Union and Africa. Royal Society of Chemistry Bulletin September Issue
Richards N, Hall S, Scott K, Harrison N (2011a) First detection of an NSAID, flunixin, in sheep’s wool using GC/MS. Environ Pollut 159(5):1446–1450
Richards NL, Cook G, Simpson V et al (2011b) Qualitative detection of the NSAIDs diclofenac and ibuprofen in the hair of Eurasian otters (Lutra lutra) occupying UK waterways with GC-MS. Eur J Wildl Res 57(5):1107–1114
Richards NL, Hall SW, Harrison NM et al (2014) Merging wildlife and environmental monitoring approaches with forensic principles: application of unconventional and non-invasive sampling in eco-pharmacovigilance. J. Forensic Res 5:228
Richards NL, Gilbert M, Taggart M, Naidoo V (2018) A cautionary tale: diclofenac and its profound impact on vultures. In: Dellasala DA, Goldstein MI (eds) Encyclopedia of the Anthropocene. Elsevier, Oxford, pp. 247–255
Ruiz-Suárez N, Boada LD, Henríquez-Hernández LA et al (2015) Continued implication of the banned pesticides carbofuran and aldicarb in the poisoning of domestic and wild animals of the Canary Islands (Spain). Sci Total Environ 505:1093–1099
Ruxton GD, Houston DC (2004) Obligate vertebrate scavengers must be large soaring fliers. J Theor Biol 228:431–436
Sage M, Fourel I, Coeurdassier M et al (2010) Determination of bromadiolone residues in fox faeces by LC/ESI-MS in relationship with toxicological data and clinical signs after repeated exposure. Environ Res 110(7):664–674
Sánchez-Barbudo IS, Camarero PR, Mateo R (2012) Primary and secondary poisoning by anticoagulant rodenticides of non-target animals in Spain. Sci Total Environ 420:280–288
Sarrazin F, Bagnolini C, Pinna JL et al (1994) High survival estimates of griffon vultures (Gyps fulvus fulvus) in a reintroduced population. Auk 111(4):853–862
Scheuhammer AM, Templeton DM (1998) The use of stable isotope ratios to distinguish sources of lead exposure in wild birds. Ecotoxicology 7:37–42
Sharma P (2012) Aceclofenac as a potential threat to critically endangered vultures in India: a review. J Raptor Res 46(3):314–318
Sieg R, Sullivan KA, Parish CN (2009) Voluntary lead reduction efforts within the northern Arizona range of the California Condor. In: Watson RT, Fuller M, Pokras M et al (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise
Sileo L, Fefer S (1987) Paint chip poisoning of Laysan albatross at Midway Atoll. J Wildl Dis 23:432–437
Smith RH (1999) Population biology and non-target effects of rodenticides: trying to put the eco into ecotoxicology. In: Cowan DP, Feare CJ (eds) Advances in vertebrate pest management. Filander, Furth, pp 331–346
St John FAV, Keane AM, Edwards-Jones G et al (2011) Identifying indicators of illegal behaviour: carnivore killing in human-managed landscapes. Proc R Soc Lond B Biol Sci 279:804–812
Stone WB, Okoniewski JC, Stedelin JR (1999) Poisoning of wildlife with anticoagulant rodenticides in New York. J Wildl Dis 35(2):187–193
Stone WB, Okoniewski JC, Stedelin JR (2003) Anticoagulant rodenticides and raptors: recent findings from New York, 1998-2001. Bull Environ Contam Toxicol 70:34–40
Swarup DPRC, Patra RC, Prakash V et al (2007) Safety of meloxicam to critically endangered Gyps vultures and other scavenging birds in India. Anim Conserv 10(2):192–198
Taggart MA, Richards NL, Kinney CA (2015) Impacts of pharmaceuticals on terrestrial wildlife. In: Hester RE, Harrison RM (eds) Pharmaceuticals in the environment. Royal Society of Chemistry, pp 216–254
Tavares J (2013) Overview of the main threats to vultures in Europe today. In: Papazoglou C, Charalambous C (eds) Proceedings of the Griffon Vulture conference. BirdLife Cyrpus, Nicosia, pp 77–88
Tella JL (2001) Action is needed now, or BSE crisis could wipe out endangered birds of prey. Nature 410(6827):408–408
Thévenot M, Bergier P, Beaubrun P (1985) Present distribution and status of raptors in Morocco. In: Newton I, Chancellor RD (eds) Conservation studies on raptors. International Council for Bird Preservation, Cambridge, pp 83–101
Thévenot M, Vernon R, Bergier P (2003) The birds of Morocco. British Ornithologist’s Union. p 594
Thomas VG (2013) Lead-free hunting rifle ammunition: product availability, price, effectiveness, and role in global wildlife conservation. Ambio 42(6):737–745
Thomas PJ, Mineau P, Shore RF et al (2011) Second generation anticoagulant rodenticides in predatory birds: probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada. Environ Int 37(5):914–920
Tingay RE, McAdam D, Taylor MJ (2012) Perspectives on wildlife poisoning by carbofuran in the United Kingdom and Republic of Ireland–With a particular focus on Scotland. In: Carbofuran and wildlife poisoning: global perspectives and forensic approaches, pp 171–188
Tixier T, Blanckenhorn WU, Lahr J et al (2015) A four-country ring test of non-target effects of ivermectin residues on the function of coprophilous communities of arthropods in breaking down livestock dung. Environ Toxicol Chem 35(8):1953–1958
Toure O (1988) The pastoral environment of northern Senegal. Rev Afr Polit Econ 15(42):32–39
U.S. Environmental Protection Agency (USEPA) (1989) Carbofuran—special review technical support document. Office of Pesticides and Toxic Substances, Washington, DC
U.S. Environmental Protection Agency (USEPA) (2016a) Biological evaluation chapters for Chlorpyrifos. Biological evaluation chapters for chlorpyrifos. www.epa.gov/endangered-species/biological-evaluation-chapters-chlorpyrifos. Accessed 9 Apr 2016
U.S. Environmental Protection Agency (USEPA) (2016b) Biological evaluation chapters for diazinon. www.epa.gov/endangered-species/biological-evaluation-chapters-diazinon. Accessed 9 Apr 2016
U.S. Environmental Protection Agency (USEPA) (2016c) Biological evaluation chapters for malathion. www.epa.gov/endangered-species/biological-evaluation-chapters-malathion. Accessed 9 Apr 2016
Van Hoof N, De Wasch K, Poelmans S et al (2004) Multi-residue liquid chromatography /tandem mass spectrometry method for the detection of non-steroidal anti-inflammatory drugs in bovine muscle: optimisation of ion trap parameters. Rapid Commun Mass Spectrom 18(23):2823–2829
Varian-Ramos CW, Swaddle JP, Cristol DA (2014) Mercury reduces avian reproductive success and imposes selection: an experimental study with adult- or lifetime-exposure in zebra finch. PLoS One 9(4):e95674
Verdú JR, Cortez V, Ortiz AJ et al (2015) Low doses of ivermectin cause sensory and locomotor disorders in dung beetles. Sci Rep 5:13912
Verma K, Paul R (2013) Assessment of post mortem interval, (PMI) from forensic entomotoxicological studies of larvae and flies. Entomol Ornithol Herpetol 2:104–108
Verschuren J (1975) Wildlife in zaire. Oryx 13:149–163
Walker LA, Turk A, Long SM et al (2008) Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Sci Total Environ 392(1):93–98
Wells K, Butterworth A, Richards NL (2019) A review of secondary pentobarbital poisoning in wild, domestic and captive carnivores. J Veterinary Forensic Sci (Inaugural Issue). In Press
Whitfield DP, McLeod DR, Watson J et al (2003) The association of grouse moor in Scotland with the illegal use of poisons to control predators. Biol Conserv 114(2):157–163
Whitfield DP, Fielding AH, McLeod DRA, Haworth PF (2004) Modelling the effects of persecution on the population dynamics of golden eagles in Scotland. Biol Conserv 119(3):319–333
Wilbur SR, Carrier WD, Borneman JC (1974) Supplemental feeding program for California condors. J Wildl Manag 38(2):343–346
Yarnell RW, Phipps WL, Dell S et al (2015) Evidence that vulture restaurants increase the local abundance of mammalian carnivores in South Africa. Afr J Ecol 53(3):287–294
Zorrilla I, Taggart M, Martinez R, Richards NL (2015) Suspected flunixin poisoning of a wild Eurasian Griffon Vulture from Spain. Conserv Biol 29(2):587–592
Zorrilla I, Richards NL, Benítez JR et al (2018) Case study: detection of two non-steroidal anti-inflammatory drugs (NSAIDs) in the eggs of captive-reared Bearded Vultures at a breeding centre in southern Spain. J Wildlife Rehab. 38(1):15–27.
Acknowledgements
SB thanks Dr. Todd Katzner for his helpful review. We appreciate all those working to protect our vultures and scavengers, whether through research or careful policy-making.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Ogada, D., Richards, N., Behmke, S. (2019). What Makes Carrion Unsafe for Scavengers? Considerations for Appropriate Regulatory Policies and Sound Management Practices. In: Olea, P., Mateo-Tomás, P., Sánchez-Zapata, J. (eds) Carrion Ecology and Management. Wildlife Research Monographs, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-030-16501-7_9
Download citation
DOI: https://doi.org/10.1007/978-3-030-16501-7_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-16499-7
Online ISBN: 978-3-030-16501-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)