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Human-Mediated Carrion: Effects on Ecological Processes

  • Rubén Moreno-Opo
  • Antoni Margalida
Chapter
Part of the Wildlife Research Monographs book series (WIREMO, volume 2)

Abstract

Humans play an essential role as modulators of energy flow within food webs in terrestrial and marine ecosystems. This is especially relevant given their capacity to generate large amounts of carrion as a result of anthropogenic activities. These trophic subsidies have increased since the twentieth century due to uses related to livestock management, hunting, waste disposal and sea fishing, changing the way in which food resources are available for scavenging species. Knowledge about the management of anthropogenic carrion is key to understanding the supply and demand mechanisms of this resource for necrophagous animals and the associated effects. Thus, changes in carrion occurrence patterns are happening at a global scale. Carrion has shifted from a pulsed random resource from carcasses of wild animals, to a more predictable resource in its appearance at certain times and locations depending on human activities. These changes have occurred in a short period of time, mainly in industrialized countries with large human populations. As a result, some wild scavengers have been forced to adapt their diet and their manner of obtaining food, modulating their biological fitness, including fertility, survival, morphology, and space use. To these individual effects, different population implications have been added, including demographic (increases or decreases in population size and density-dependence phenomena), behavioral (intra- and interspecific competition and migration), and chorological (modulation of distribution range). At the community level, anthropogenic carrion subsidies have also produced alterations, especially in food web performance, in predator-prey relationships, in aspects like species richness and even in characteristics of the landscape. This determinant influence of humans on carrion-related ecological processes also requires an analysis from the point of view of conservation biology. In this sense, it is necessary to avoid negative effects leading to the extinction of certain species or populations as well as to ensure that carrion provisions in the wild is provided following natural patterns.

Keywords

Animal by-products Carcasses Fishing discards Food subsidies Livestock management Rubbish dumps Scavengers 

Notes

Acknowledgements

We are indebted to several colleagues involved in the projects performed to assess the role of avian scavengers and carrion consumption: L. M. González, R. Casanovas, D. García, J. Caldera, A. Aranda, A. Trujillano, J. J. García, A. Arredondo, R. Higuero. We also thank the editors for the opportunity in taking part of this book and the reviews of drafts of our manuscript. This research was supported by project CGL2015-66966-C2-2-R2.

References

  1. Allen B (2016) Animals in religion: devotion, symbol and ritual. Reaktion Books, LondonGoogle Scholar
  2. Barton PS, Cunningham SA, Lindenmayer DB, Manning AD (2013a) The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171(4):761–772PubMedPubMedCentralCrossRefGoogle Scholar
  3. Barton PS, Cunningham SA, Macdonald BC et al (2013b) Species traits predict assemblage dynamics at ephemeral resource patches created by carrion. PLoS One 8(1):e53961PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287(1):1–23CrossRefGoogle Scholar
  6. Bellan SE, Turnbull PCB, Beyer W, Getz WM (2013) Effects of experimental exclusion of scavengers from carcasses of anthrax-infected herbivores on Bacillus anthracis sporulation, survival, and distribution. Appl Environ Microbiol 79:3756–3761PubMedPubMedCentralCrossRefGoogle Scholar
  7. Benbow ME, Tomberlin JK, Tarone AM (2016) Carrion ecology, evolution and their applications. CRC Press, Taylor and Francis Group, Boca RatonGoogle Scholar
  8. Benskin CM, Wilson K, Jones K, Hartley IR (2009) Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev 84(3):349–373PubMedCrossRefPubMedCentralGoogle Scholar
  9. 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 118:71–82PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bicknell AW, Oro D, Camphuysen KC, Votier SC (2013) Potential consequences of discard reform for seabird communities. J Appl Ecol 50(3):649–658CrossRefGoogle Scholar
  11. Bignal EM, McCracken DI (2000) The nature conservation value of European traditional farming systems. Environ Rev 8:149–171CrossRefGoogle Scholar
  12. Blázquez M, Sánchez-Zapata JA (2009) The role of wild ungulates as a resource for the community of vertebrate scavengers. In: Donázar JA, Margalida A, Campión D (eds) Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology, Munibe 29 (Suppl). Sociedad de Ciencias Aranzadi San Sebastián, Spain, pp 308–327Google Scholar
  13. Blázquez M, Sánchez-Zapata JA, Botella F, Carrete M, Eguía S (2009) Spatio-temporal segregation of facultative avian scavengers at ungulate carcasses. Acta Oecol 35:645–650CrossRefGoogle Scholar
  14. Blench R (2000) Extensive pastoral livestock systems: issues and options for the future. FAO-Japan Cooperative Project “Collection of Information on Animal Production and Health”. FAO, RomeGoogle Scholar
  15. Bodey TW, Jessopp MJ, Votier SC et al (2014) Seabird movement reveals the ecological footprint of fishing vessels. Curr Biol 24:R514–R515PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bozzano A, Sarda F (2002) Fishery discard consumption rate and scavenging activity in the northwestern Mediterranean Sea. ICES J Mar Sci 59(1):15–28CrossRefGoogle Scholar
  17. Brashares JS, Arcese P, Sam MK et al (2004) Bushmeat hunting, wildlife declines, and fish supply in West Africa. Science 306(5699):1180–1183PubMedCrossRefPubMedCentralGoogle Scholar
  18. Breck SW, Kluever BM, Panasci M et al (2011) Domestic calf mortality and producer detection rates in the Mexican wolf recovery area: implications for livestock management and carnivore compensation schemes. Biol Conserv 144(2):930–936CrossRefGoogle Scholar
  19. Brown CJ, Plug I (1990) Food choice and diet of the bearded vulture Gypaetus barbatus in southern Africa. S Afr J Zool 25(3):169–177CrossRefGoogle Scholar
  20. Buechley ER, Şekercioğlu ÇH (2016) The avian scavenger crisis: looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biol Conserv 198:220–228CrossRefGoogle Scholar
  21. Carrasco-García R, Barroso P, Montoro V et al (2018) Consumption of big game remains by scavengers: a potential risk as regards disease transmission in Central Spain. Front Vet Sci 5:4PubMedPubMedCentralCrossRefGoogle Scholar
  22. Carrete M, Donázar JA (2005) Application of central-place foraging theory shows the importance of Mediterranean dehesas for the conservation of the cinereous vulture, Aegypius monachus. Biol Conserv 126(4):582–590CrossRefGoogle Scholar
  23. Carrete M, Donázar JA, Margalida A (2006) Density-dependent productivity depression in pyrenean bearded vultures: implications for conservation. Ecol Appl 16(5):1674–1682PubMedCrossRefGoogle Scholar
  24. 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 557:620–626PubMedCrossRefGoogle Scholar
  25. Catchpole TL, Elliott S, Peach D, Mangi SC, Gray TS (2017) How to deal with the EU landing obligation: lessons from an English discard ban sea trial. ICES J Mar Sci 75(1):270–278CrossRefGoogle Scholar
  26. Chamberlain CP, Waldbauer JR, Fox-Dobbs K et al (2005) Pleistocene to recent dietary shifts in California condors. Proc Natl Acad Sci U S A 102:16707–16711PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chapron G, Kaczensky P, Linnell J et al (2014) Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346:1517–1519PubMedCrossRefGoogle Scholar
  28. Coleman FC, Williams SL (2002) Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends Ecol Evol 17(1):40–44CrossRefGoogle Scholar
  29. Condie HM, Grant A, Catchpole TL (2014) Incentivising selective fishing under a policy to ban discards; lessons from European and global fisheries. Mar Policy 45:287–292CrossRefGoogle Scholar
  30. Cooper SM, Ginnett TF (2000) Potential effects of supplemental feeding of deer on nest predation. Wildl Soc Bull 28:660–666Google Scholar
  31. Cortés-Avizanda A, Carrete M, Serrano D, Donázar JA (2009) Carcasses increase the probability of predation of ground-nesting birds: a caveat regarding the conservation value of vulture restaurants. Anim Conserv 12(1):85–88CrossRefGoogle Scholar
  32. Cortés-Avizanda A, Carrete M, Donázar JA (2010) Managing supplementary feeding for avian scavengers: guidelines for optimal design using ecological criteria. Biol Conserv 143(7):1707–1715CrossRefGoogle Scholar
  33. Cortés-Avizanda A, Jovani R, Carrete M, Donázar JA (2012) Resource unpredictability promotes species diversity and coexistence in an avian scavenger guild: a field experiment. Ecology 93(12):2570–2579CrossRefGoogle Scholar
  34. Cortés-Avizanda A, Jovani R, Donázar JA, Grimm V (2014) Bird sky networks: how do avian scavengers use social information to find carrion. Ecology 95:1799–1808CrossRefGoogle Scholar
  35. 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):191–199CrossRefGoogle Scholar
  36. Costillo E, Corbacho C, Morán R, Villegas A (2007a) Diet plasticity of Cinereous Vulture Aegypius monachus in different colonies in the Extremadura (SW Spain). Ardea 95(2):201–211CrossRefGoogle Scholar
  37. Costillo E, Corbacho C, Morán R, Villegas A (2007b) The diet of the black vulture Aegypius monachus in response to environmental changes in Extremadura (1970–2000). Ardeola 54:197–204Google Scholar
  38. Côté SD, Rooney TP, Tremblay JP et al (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–147CrossRefGoogle Scholar
  39. Darimont CT, Fox CH, Bryan HM, Reimchen TE (2015) The unique ecology of human predators. Science 349(6250):858–860PubMedCrossRefGoogle Scholar
  40. Darimont CT, Codding BF, Hawkes K (2017) Why men trophy hunt. Biol Lett 13:20160909PubMedPubMedCentralCrossRefGoogle Scholar
  41. Davies RWD, Cripps SJ, Nickson A, Porter G (2009) Defining and estimating global marine fisheries bycatch. Mar Policy 33(4):661–672CrossRefGoogle Scholar
  42. Davis SE, Nager RG, Furness RW (2005) Food availability affects adult survival as well as breeding success of parasitic jaegers. Ecology 86(4):1047–1056CrossRefGoogle Scholar
  43. Deinet S, Ieronymidou C, McRae L et al (2013) Wildlife comeback in Europe. The recovery of selected mammal and bird species. ZSL, BirdLife International and the European Bird Census Council, LondonGoogle Scholar
  44. Delibes-Mateos M, Farfán MA, Olivero J et al (2009) Long-term changes in game species over a long period of transformation in the Iberian Mediterranean landscape. Environ Manag 43:1256–1268CrossRefGoogle Scholar
  45. DeVault TL, Rhodes OE Jr, Shivik JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102(2):225–234CrossRefGoogle Scholar
  46. Deygout C, Gault A, Duriez O et al (2010) Impact of food predictability on social facilitation by foraging scavengers. Behav Ecol 21(6):1131–1139CrossRefGoogle Scholar
  47. Di Minin E, Leader-Williams N, Bradshaw CJ (2016) Banning trophy hunting will exacerbate biodiversity loss. Trends Ecol Evol 31(2):99–102PubMedCrossRefGoogle Scholar
  48. Domínguez-Rodrigo M (2001) A study of carnivore competition in riparian and open habitats of modern savannas and its implications for hominid behavioral modelling. J Hum Evol 40:77–98PubMedCrossRefGoogle Scholar
  49. Domínguez-Rodrigo M, Pickering TR (2003) Early hominid hunting and scavenging: a zooarcheological review. Evol Anthropol 12(6):275–282CrossRefGoogle Scholar
  50. Donázar JA (1992) Muladares y basureros en la biología y conservación de las aves en España. Ardeola 39(2):29–40Google Scholar
  51. Donázar JA (1993) Los buitres ibéricos: biología y conservación. JM Reyero, MadridGoogle Scholar
  52. Donázar JA, Fernández C (1990) Population trends of Griffon Vultures (Gyps fulvus) in northern Spain between 1969 and 1989 in relation to conservation measures. Biol Conserv 53:83–91Google Scholar
  53. Donázar JA, Naveso MA, Tella JL, Campión D (1997) Extensive grazing and raptors in Spain. In: Pain D, Pienkowski M (eds) Farming and birds in Europe: the common agricultural policy and it’s implications for bird conservation. Academic, London, pp 117–149Google Scholar
  54. Donázar JA, Margalida A, Campión D (2009) Vultures, feedings stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology, Munibe 29 (Suppl). Sociedad de Ciencias Aranzadi San Sebastián, SpainGoogle Scholar
  55. Donázar JA, Cortés-Avizanda A, Carrete M (2010) Dietary shifts in two vultures after the demise of supplementary feeding stations: consequences of the EU sanitary legislation. Eur J Wildl Res 56(4):613–621CrossRefGoogle Scholar
  56. Donázar JA, Cortés-Avizanda A, Fargallo JA et al (2016) Roles of raptors in a changing world: from flagships to providers of key ecosystem services. Ardeola 63(1):181–234CrossRefGoogle Scholar
  57. Dubois S, Fraser D (2013) A framework to evaluate wildlife feeding in research, wildlife management, tourism and recreation. Animals 3:978–994PubMedCrossRefGoogle Scholar
  58. FAO (2016) The State of World Fisheries and Aquaculture 2016. Contributing to food security and nutrition for all. Food and Agriculture Organization-United Nations, RomeGoogle Scholar
  59. Fernández-Giménez ME, Fillat F (2012) Pyrenean pastoralists’ ecological knowledge: documentation and application to natural resource management and adaptation. Hum Ecol 40(2):287–300CrossRefGoogle Scholar
  60. 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):810–819CrossRefGoogle Scholar
  61. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131(3):421–432CrossRefGoogle Scholar
  62. Flanders F, Gillespie JR (2015) Modern livestock and poultry production. Cengage Learning, BostonGoogle Scholar
  63. Fryxell JM (1991) Forage quality and aggregation by large herbivores. Am Nat 138(2):478–498CrossRefGoogle Scholar
  64. Gangoso L, Álvarez-Lloret P, Rodríguez-Navarro AA et al (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157(2):569–574PubMedCrossRefPubMedCentralGoogle Scholar
  65. Gangoso L, Agudo R, Anadón JD et al (2013) Reinventing mutualism between humans and wild fauna: insights from vultures as ecosystem services providers. Conserv Lett 6(3):172–179CrossRefGoogle Scholar
  66. Ganz HH, Karaoz U, Getz WM et al (2012) Diversity and structure of soil bacterial communities associated with vultures in an African savanna. Ecosphere 3(6):47CrossRefGoogle Scholar
  67. García-Heras MS, Cortés-Avizanda A, Donázar JA (2013) Who are we feeding? Asymmetric individual use of surplus food resources in an insular population of the endangered Egyptian vulture Neophron percnopterus. PLoS One 8(11):e80523PubMedPubMedCentralCrossRefGoogle Scholar
  68. García-Tarrasón M, Bécares J, Bateman S et al (2015) Sex-specific foraging behavior in response to fishing activities in a threatened seabird. Ecol Evol 5:2348–2358PubMedPubMedCentralCrossRefGoogle Scholar
  69. Garthe S, Camphuysen K, Furness RW (1996) Amounts of discards by commercial fisheries and their significance as food for seabirds in the North Sea. Mar Ecol Progr Ser 136:1–11CrossRefGoogle Scholar
  70. Gavashelishvili A, McGrady MJ (2006) Breeding site selection by bearded vulture (Gypaetus barbatus) and Eurasian griffon (Gyps fulvus) in the Caucasus. Anim Conserv 9:159–170CrossRefGoogle Scholar
  71. Gompper ME, Vanak AT (2008) Subsidized predators, landscapes of fear and disarticulated carnivore communities. Anim Conserv 11(1):13–14CrossRefGoogle Scholar
  72. González LM, Margalida A, Sánchez R, Oria J (2006) Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial eagle (Aquila adalberti). Biol Conserv 129(4):477–486CrossRefGoogle Scholar
  73. Gortazar C, Diez-Delgado I, Barasona JA et al (2015) The wild side of disease control at the wildlife-livestock-human interface: a review. Front Vet Sci 1:27PubMedPubMedCentralCrossRefGoogle Scholar
  74. Green RE, Newton IAN, Shultz S et al (2004) Diclofenac poisoning as a cause of vulture population declines across the Indian subcontinent. J Appl Ecol 41:793–800CrossRefGoogle Scholar
  75. Guil F, Fernández-Olalla M, Moreno-Opo R et al (2011) Minimising mortality in endangered raptors due to power lines: the importance of spatial aggregation to optimize the application of mitigation measures. PLoS One 6(11):e28212PubMedPubMedCentralCrossRefGoogle Scholar
  76. Gunson KE, Mountrakis G, Quackenbush LJ (2011) Spatial wildlife-vehicle collision models: a review of current work and its application to transportation mitigation projects. J Environ Manag 92(4):1074–1082CrossRefGoogle Scholar
  77. Hahn GL (1981) Housing and management to reduce climatic impacts on livestock. J Anim Sci 52:175–186PubMedCrossRefPubMedCentralGoogle Scholar
  78. Heath MR, Cook RM, Cameron AI et al (2014) Cascading ecological effects of eliminating fishery discards. Nature 5:3893Google Scholar
  79. Hernández M, Margalida A (2008) Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 17(4):264–272PubMedCrossRefPubMedCentralGoogle Scholar
  80. Hernández M, Margalida A (2009a) Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ Res 109(7):837–842PubMedCrossRefPubMedCentralGoogle Scholar
  81. Hernández M, Margalida A (2009b) Poison-related mortality effects in the endangered Egyptian vulture (Neophron percnopterus) population in Spain. Eur J Wildl Res 55(4):415–423CrossRefGoogle Scholar
  82. Hernández M, Colomer MA, Pizarro M, Margalida A (2018) Changes in eggshell thickness and ultrastructure in the Bearded Vulture (Gypaetus barbatus): a long-term analysis. Sci Total Environ 624:713–721Google Scholar
  83. Herrero M, Havlík P, Valin H et al (2013) Biomass use, production, feed efficiencies, and greenhouse gas emissions from global livestock systems. Proc Natl Acad Sci U S A 110(52):20888–20893PubMedPubMedCentralCrossRefGoogle Scholar
  84. Hertel F (1994) Diversity in body size and feeding morphology within past and present vulture assemblages. Ecology 75(4):1074–1084CrossRefGoogle Scholar
  85. Hobbs RJ, Higgs E, Harris JA (2009) Novel ecosystems: implications for conservation and restoration. Trends Ecol Evol 24(11):599–605PubMedCrossRefPubMedCentralGoogle Scholar
  86. Houston DC, Cooper JE (1975) The digestive tract of the white-back griffon vulture and its role in disease transmission among wild ungulates. J Wildl Dis 11:306–313CrossRefGoogle Scholar
  87. Hulme-Beaman A, Dobney K, Cucchi T, Searle JB (2016) An ecological and evolutionary framework for commensalism in anthropogenic environments. Trends Ecol Evol 31(8):633–645PubMedCrossRefPubMedCentralGoogle Scholar
  88. Jackson AL, Ruxton GD, Houston DC (2008) The effect of social facilitation on foraging success in vultures: a modelling study. Biol Lett 4(3):311–313CrossRefGoogle Scholar
  89. Jayathilakan K, Sultana K, Radhakrishna K, Bawa AS (2012) Utilization of byproducts and waste materials from meat, poultry and fish processing industries: a review. J Food Sci Technol 49:278–293PubMedCrossRefPubMedCentralGoogle Scholar
  90. Kane A, Healy K, Guillerme T et al (2017) A recipe for scavenging in vertebrates–the natural history of a behaviour. Ecography 40(2):324–334CrossRefGoogle Scholar
  91. Kelleher K (2005) Discards in the world’s marine fisheries. An update. FAO Fisheries Technical Paper. No. 470. FAO, RomeGoogle Scholar
  92. Kelly TR, Grantham J, George D et al (2014) Spatiotemporal patterns and risk factors for lead exposure in endangered California condors during 15 years of reintroduction. Conserv Biol 28:1721–1730PubMedCrossRefPubMedCentralGoogle Scholar
  93. Kendall CJ (2013) Alternative strategies in avian scavengers: how subordinate species foil the despotic distribution. Behav Ecol Sociobiol 67(3):383–393CrossRefGoogle Scholar
  94. Kendall CJ, Virani MZ, Hopcraft JGC et al (2014) African vultures don’t follow migratory herds: scavenger habitat use is not mediated by prey abundance. PLoS One 9(1):e83470PubMedPubMedCentralCrossRefGoogle Scholar
  95. Lagos L, Bárcena F (2015) EU sanitary regulation on livestock disposal: implications for the diet of wolves. Environ Manag 56(4):890–902CrossRefGoogle Scholar
  96. Lambertucci SA, Speziale KL, Rogers TE, Morales JM (2009a) How do roads affect the habitat use of an assemblage of scavenging raptors? Biodivers Conserv 18(8):2063–2074CrossRefGoogle Scholar
  97. Lambertucci SA, Trejo A, Di Martino S et al (2009b) Spatial and temporal patterns in the diet of the Andean condor: ecological replacement of native fauna by exotic species. Anim Conserv 12(4):338–345CrossRefGoogle Scholar
  98. Leff JW, Jones SE, Prober SM et al (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci U S A 112:10967–10972PubMedPubMedCentralCrossRefGoogle Scholar
  99. Lindsey P, Roulet P, Romanach S (2007) Economic and conservation significance of the trophy hunting industry in sub-Saharan Africa. Biol Conserv 134:455–469CrossRefGoogle Scholar
  100. López-López P, Benavent-Coral J, García-Ripollés C, Urios V (2013) Scavengers on the move: behavioural changes in foraging search patterns during the annual cycle. PLoS One 8(1):e54352PubMedPubMedCentralCrossRefGoogle Scholar
  101. López-López P, García-Ripollés C, Urios V (2014) Food predictability determines space use of endangered vultures: implications for management of supplementary feeding. Ecol Appl 24(5):938–949PubMedCrossRefGoogle Scholar
  102. Loss SR, Will T, Loss SS, Marra PP (2014a) Bird–building collisions in the United States: estimates of annual mortality and species vulnerability. Condor 116(1):8–23CrossRefGoogle Scholar
  103. Loss SR, Will T, Marra PP (2014b) Refining estimates of bird collision and electrocution mortality at power lines in the United States. PLoS One 9(7):e101565PubMedPubMedCentralCrossRefGoogle Scholar
  104. Lucas RE (2003) The industrial revolution. Federal Reserve Bank of MinneapolisGoogle Scholar
  105. Margalef R (1997) Our biosphere. Ecology Institute, Oldendorf/LuheGoogle Scholar
  106. Margalida A (2008) Bearded vultures (Gypaetus barbatus) prefer fatty bones. Behav Ecol Sociobiol 63(2):187–193CrossRefGoogle Scholar
  107. 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 Wildl Res 56(4):673–678CrossRefGoogle Scholar
  108. Margalida A (2012) Baits, budget cuts: a deadly mix. Science 338(6104):192–192PubMedCrossRefGoogle Scholar
  109. Margalida A, Colomer MA (2012) Modelling the effects of sanitary policies on European vulture conservation. Sci Rep 2:753PubMedPubMedCentralCrossRefGoogle Scholar
  110. Margalida A, Moleón M (2016) Toward carrion-free ecosystems? Front Ecol Environ 14(4):183–184CrossRefGoogle Scholar
  111. Margalida A, Mañosa S, Bertran J, Garcia D (2007) Biases in studying the diet of the Bearded Vulture. J Wildl Manag 71(5):1621–1625CrossRefGoogle Scholar
  112. Margalida A, Bertran J, Heredia R (2009) Diet and food preferences of the endangered Bearded Vulture Gypaetus barbatus: a basis for their conservation. Ibis 151(2):235–243Google Scholar
  113. 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):931–935CrossRefGoogle Scholar
  114. Margalida A, Campión D, Donázar JA (2011a) European vultures’ altered behaviour. Nature 480:457PubMedCrossRefPubMedCentralGoogle Scholar
  115. Margalida A, Colomer MA, Sanuy D (2011b) Can wild ungulate carcasses provide enough biomass to maintain avian scavenger populations? An empirical assessment using a bio-inspired computational model. PLoS One 6(5):e20248PubMedPubMedCentralCrossRefGoogle Scholar
  116. Margalida A, Carrete M, Hegglin D et al (2013) Uneven large-scale movement patterns in wild and reintroduced pre-adult bearded vultures: conservation implications. PLoS One 8(6):e65857PubMedPubMedCentralCrossRefGoogle Scholar
  117. Margalida A, Bogliani G, Bowden CG et al (2014a) One Health approach to use of veterinary pharmaceuticals. Science 346(6215):1296–1298CrossRefGoogle Scholar
  118. Margalida A, Colomer MA, Oro D (2014b) Man-induced activities modify demographic parameters in a long-lived species: effects of poisoning and health policies. Ecol Appl 24(3):436–444PubMedCrossRefPubMedCentralGoogle Scholar
  119. Margalida A, Campión D, Donázar JA (2014c) Vultures vs. livestock: conservation relationships in an emerging conflict between humans and wildlife. Oryx 48(02):172–176CrossRefGoogle Scholar
  120. Margalida A, Pérez-García JM, Afonso I, Moreno-Opo R (2016) Spatial and temporal movements in Pyrenean bearded vultures (Gypaetus barbatus): integrating movement ecology into conservation practice. Sci Rep 6:35746Google Scholar
  121. Margalida A, Martínez JM, Gómez de Segura A et al (2017a) Supplementary feeding and young extraction from the wild are not a sensible alternative to captive breeding for reintroducing bearded vultures Gypaetus barbatus. J Appl Ecol 54:334–340CrossRefGoogle Scholar
  122. Margalida A, Pérez-García JM, Moreno-Opo R (2017b) European policies on livestock carcasses management did not modify the foraging behavior of a threatened vulture. Ecol Indic 80:66–83CrossRefGoogle Scholar
  123. Margalida A, Oliva-Vidal P, Llamas A, Colomer, MA (2018) Bioinspired models for assessing the importance of transhumance and transboundary management in the conservation of European avian scavengers. Biol Conserv 228:321–330CrossRefGoogle Scholar
  124. Martínez-Abraín A, Tavecchia G, Regan HM et al (2012) Effects of wind farms and food scarcity on a large scavenging bird species following an epidemic of bovine spongiform encephalopathy. J Appl Ecol 49:109–117CrossRefGoogle Scholar
  125. Martín-Vega D, Baz A (2011) Could the ‘vulture restaurants’ be a lifeboat for the recently rediscovered bone-skippers (Diptera: Piophilidae)? J Insect Conserv 15(5):747CrossRefGoogle Scholar
  126. Massé S, Dussault C, Dussault C, Ibarzabal J (2014) How artificial feeding for tourism-watching modifies black bear space use and habitat selection. J Wildl Manag 78:1228–1238CrossRefGoogle Scholar
  127. Massei G, Kindberg J, Licoppe A et al (2015) Wild boar populations up, numbers of hunters down? A review of trends and implications for Europe. Pest Manag Sci 71(4):492–500PubMedCrossRefPubMedCentralGoogle Scholar
  128. Mateo-Tomás P, Olea PP (2010) When hunting benefits raptors: a case study of game species and vultures. Eur J Wildl Res 56:519–528CrossRefGoogle Scholar
  129. 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. J Appl Ecol 49:376–385CrossRefGoogle Scholar
  130. 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 21:913–924CrossRefGoogle Scholar
  131. Mateo-Tomás P, Olea PP, Jiménez-Moreno M et al (2016) Mapping the spatio-temporal risk of lead exposure in apex species for more effective mitigation. Proc R Soc Lond B Biol Sci 283:20160662CrossRefGoogle Scholar
  132. Mithen S (1999) The hunter-gatherer prehistory of human-animal interactions. Anthrozoös 12:195–204CrossRefGoogle Scholar
  133. Moleón M, Sánchez-Zapata JA, Margalida A et al (2014) Humans and scavengers: the evolution of interactions and ecosystem services. Bioscience 64:394–403CrossRefGoogle Scholar
  134. Monsarrat S, Benhamou S, Sarrazin F et al (2013) How predictability of feeding patches affects home range and foraging habitat selection in avian social scavengers? PLoS One 8:e53077PubMedPubMedCentralCrossRefGoogle Scholar
  135. Morales-Reyes Z, Martín-López B, Moleón M et al (2018) Farmer perceptions of the ecosystem services provided by scavengers: what, who, and to whom. Conserv Lett 11(2):e12392CrossRefGoogle Scholar
  136. Мorelle K, Lehaire F, Lejeune P (2013) Spatio-temporal patterns of wildlife-vehicle collisions in a region with a high-density road network. Nat Conserv 5:53–73CrossRefGoogle Scholar
  137. Moreno-Opo R, Margalida A (2013) Carcasses provide resources not exclusively to scavengers: patterns of carrion exploitation by passerine birds. Ecosphere 4(8):1–15CrossRefGoogle Scholar
  138. Moreno-Opo R, Margalida A, Garcia 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 21:1673–1685CrossRefGoogle Scholar
  139. Moreno-Opo R, Trujillano A, Arredondo A et al (2015a) Manipulating size, amount and appearance of food inputs to optimize supplementary feeding programs for European vultures. Biol Conserv 181:27–35CrossRefGoogle Scholar
  140. Moreno-Opo R, Trujillano A, Margalida A (2015b) Optimization of supplementary feeding programs for European vultures depends on environmental and management factors. Ecosphere 6(7):1–15CrossRefGoogle Scholar
  141. Moreno-Opo R, Trujillano A, Margalida A (2016) Behavioral coexistence and feeding efficiency drive niche partitioning in European avian scavengers. Behav Ecol 27:1041–1052CrossRefGoogle Scholar
  142. Mundy P, Butchart D, Ledger J, Piper S (1992) The vultures of Africa. Academic, LondonGoogle Scholar
  143. Nardone A, Ronchi B, Lacetera N et al (2010) Effects of climate changes on animal production and sustainability of livestock systems. Livest Sci 130:57–69CrossRefGoogle Scholar
  144. Neumann W, Ericsson G, Dettki H et al (2012) Difference in spatiotemporal patterns of wildlife road-crossings and wildlife-vehicle collisions. Biol Conserv 145(1):70–78CrossRefGoogle Scholar
  145. Newsome TM, Dellinger JA, Pavey CR et al (2015) The ecological effects of providing resource subsidies to predators. Glob Ecol Biogeogr 24(1):1–11CrossRefGoogle Scholar
  146. Oaks JL, Gilbert M, Virani MZ et al (2004) Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427(6975):630–633CrossRefGoogle Scholar
  147. Ogada DL, Keesing F, Virani MZ (2012) Dropping dead: causes and consequences of vulture population declines worldwide. Ann N Y Acad Sci 1249(1):57–71PubMedPubMedCentralCrossRefGoogle Scholar
  148. Ogada D, Botha A, Shaw P (2016a) Ivory poachers and poison: drivers of Africa’s declining vulture populations. Oryx 50(4):593–596CrossRefGoogle Scholar
  149. Ogada D, Shaw P, Beyers RL et al (2016b) Another continental vulture crisis: Africa’s vultures collapsing toward extinction. Conserv Lett 9(2):89–97CrossRefGoogle Scholar
  150. 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):1844–1853CrossRefGoogle Scholar
  151. Oro D, Genovart X, Ruiz X et al (1996) Differences in diet, population size and reproductive performance between two colonies of Audouin’s Gull Larus audouinii affected by a trawling moratorium. J Avian Biol 27(3):245–251CrossRefGoogle Scholar
  152. 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):e4084PubMedPubMedCentralCrossRefGoogle Scholar
  153. Oro D, Genovart M, Tavecchia G et al (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16(12):1501–1514PubMedPubMedCentralCrossRefGoogle Scholar
  154. Parra J, Tellería JL (2004) The increase in the Spanish population of Griffon Vulture Gyps fulvus during 1989–1999: effects of food and nest site availability. Bird Conserv Int 14(1):33–41CrossRefGoogle Scholar
  155. Peris J (2003) Feeding in urban refuse dumps: ingestion of plastic objects by the White Stork (Ciconia ciconia). Ardeola 50:81–84Google Scholar
  156. Plaza PI, Lambertucci SA (2017) How are garbage dumps impacting vertebrate demography, health, and conservation? Glob Ecol Conserv 12:9–20CrossRefGoogle Scholar
  157. Ponce C, Alonso JC, Argandoña G et al (2010) Carcass removal by scavengers and search accuracy affect bird mortality estimates at power lines. Anim Conserv 13(6):603–612CrossRefGoogle Scholar
  158. Pons JM (1992) Effects of changes in the availability of human refuse on breeding parameters in a herring gull. Ardea 80:143–150Google Scholar
  159. Pons JM, Migot P (1995) Life-history strategy of the herring gull: changes in survival and fecundity in a population subjected to various feeding conditions. J Anim Ecol 64:592–599CrossRefGoogle Scholar
  160. Prakash V, Pain DJ, Cunningham AA et al (2003) Catastrophic collapse of Indian white-backed Gyps bengalensis and long-billed Gyps indicus vulture populations. Biol Conserv 109(3):381–390CrossRefGoogle Scholar
  161. Prugh LR, Stoner CJ, Epps CW et al (2009) The rise of the mesopredator. Bioscience 59(9):779–791CrossRefGoogle Scholar
  162. Pulido F (2007) The genetics and evolution of avian migration. Bioscience 57:165–174CrossRefGoogle Scholar
  163. Real E, Oro D, Martínez-Abraín A et al (2017) Predictable anthropogenic food subsidies, density-dependence and socio-economic factors influence breeding investment in a generalist seabird. J Avian Biol 48(11):1462–1470CrossRefGoogle Scholar
  164. Rioux S, Savard JPL, Gerick AA (2013) Avian mortalities due to transmission line collisions: a review of current estimates and field methods with an emphasis on applications to the Canadian electric network. Avian Conserv Ecol 8(2):7Google Scholar
  165. Ripple WJ, Newsome TM, Wolf C et al (2015) Collapse of the world’s largest herbivores. Sci Adv 1:e140010CrossRefGoogle Scholar
  166. Robb GN, McDonald RA, Chamberlain DE, Bearhop S (2008) Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front Ecol Environ 6:476–484CrossRefGoogle Scholar
  167. Ruiz M, Ruiz JP (1986) Ecological history of transhumance in Spain. Biol Conserv 37:73–86CrossRefGoogle Scholar
  168. Ruxton GD, Houston DC (2004) Obligate vertebrate scavengers must be large soaring fliers. J Theor Biol 228(3):431–436CrossRefGoogle Scholar
  169. Rytwinski T, Soanes K, Jaeger JA et al (2016) How effective is road mitigation at reducing road-kill? A meta-analysis. PLoS One 11(11):e0166941PubMedPubMedCentralCrossRefGoogle Scholar
  170. Sardà F, Coll M, Heymans JJ, Stergiou KI (2015) Overlooked impacts and challenges of the new European discard ban. Fish Fish 16:175–180CrossRefGoogle Scholar
  171. Sarrazin F, Lecomte J (2016) Evolution in the Anthropocene. Science 351(6276):922–923PubMedCrossRefGoogle Scholar
  172. Sarrazin F, Bagnolin C, Pinna JL et al (1994) High survival estimates of griffon vultures (Gyps fulvus fulvus) in a reintroduced population. Auk 111(4):853–862CrossRefGoogle Scholar
  173. Schutgens M, Shaw JM, Ryan PG (2014) Estimating scavenger and search bias for collision fatality surveys of large birds on power lines in the Karoo, South Africa. Ostrich 85(1):39–45CrossRefGoogle Scholar
  174. Selva N, Fortuna MA (2007) The nested structure of a scavenger community. Proc R Soc Lond B Biol Sci 274(1613):1101–1108CrossRefGoogle Scholar
  175. Sesé J A, Antor RJ, Alcántara M, Ascaso JC, Gil JA (2005) La alimentación suplementaria en el quebrantahuesos: estudio de un comedero del Pirineo occidental aragonés. Biología de la conservación del Quebrantahuesos Gypaetus barbatus en España. Organismo Autónomo Parques Nacionales, Madrid, pp 279–304Google Scholar
  176. Shester GG, Micheli F (2011) Conservation challenges for small-scale fisheries: bycatch and habitat impacts of traps and gillnets. Biol Conserv 144(5):1673–1681CrossRefGoogle Scholar
  177. Sigurðardóttir S, Stefánsdóttir EK, Condie H et al (2015) How can discards in European fisheries be mitigated? Strengths, weaknesses, opportunities and threats of potential mitigation methods. Mar Policy 51:366–374CrossRefGoogle Scholar
  178. Skov H, Durinck J (2001) Seabird attraction to fishing vessels is a local process. Mar Ecol Progr Ser 214:289–298CrossRefGoogle Scholar
  179. Stara K, Sidiropoulos L, Tsiakiris R (2016) Bound eagles, evil vultures and cuckoo horses. Preserving the bio-cultural diversity of carrion eating birds. Hum Ecol 44(6):751–764CrossRefGoogle Scholar
  180. Stephens DW, Brown JS, Ydenberg RC (eds) (2007) Foraging: behavior and ecology. University of Chicago Press, ChicagoGoogle Scholar
  181. Strickland MS, Wickings K (2016) Carrion effects on belowgrounds communities and consequences for soil processes. In: Benbow ME, Tomberlin JK, Tarone AM (eds) Carrion ecology, evolution and their applications. CRC Press, Boca RatónGoogle Scholar
  182. Tauler-Ametller H, Hernández-Matías A, Pretus JL, Real J (2017) Landfills determine the distribution of an expanding breeding population of the endangered Egyptian Vulture Neophron percnopterus. Ibis 159:757–768CrossRefGoogle Scholar
  183. Teixeira FZ, Coelho AVP, Esperandio IB, Kindel A (2013) Vertebrate road mortality estimates: effects of sampling methods and carcass removal. Biol Conserv 157:317–323CrossRefGoogle Scholar
  184. Thiollay J (2006) The decline of raptors in West Africa: long-term assessment and the role of protected areas. Ibis 148(2):240–254CrossRefGoogle Scholar
  185. Thoma VG (2013) Lead-free hunting rifle ammunition: product availability, price, effectiveness, and role in global wildlife conservation. Ambio 42(6):737–745CrossRefGoogle Scholar
  186. Tortosa FS, Caballero JM, Reyes-López J (2002) Effect of rubbish dumps on breeding success in the white stork in southern Spain. Waterbirds 25(1):39–43CrossRefGoogle Scholar
  187. Vicente J, Carrasco R, Acevedo P, Montoro V, Gortazar C (2011) Big game waste production: sanitary and ecological implications. In: Integrated waste management—volume II. IntechOpen, RijekaGoogle Scholar
  188. Virani MZ, Kendall C, Njoroge P, Thomsett S (2011) Major declines in the abundance of vultures and other scavenging raptors in and around the Masai Mara ecosystem, Kenya. Biol Conserv 144:746–752CrossRefGoogle Scholar
  189. Votier SC, Furness RW, Bearhop S et al (2004) Changes in fisheries discard rates and seabird communities. Nature 427(6976):727–730PubMedCrossRefGoogle Scholar
  190. Votier SC, Bearhop S, Witt MJ et al (2010) Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J Appl Ecol 47:487–497CrossRefGoogle Scholar
  191. Wilmers CC, Stahler DR, Crabtree RL, Smith DW, Getz WM (2003) Resource dispersion and consumer dominance: scavenging at wolf- and hunter-killed carcasses in Greater Yellowstone, USA. Ecol Lett 11:993–1006Google Scholar
  192. Wilson EE, Wolkovich EM (2011) Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol 26(3):129–135PubMedPubMedCentralCrossRefGoogle Scholar
  193. 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 53:287–294CrossRefGoogle Scholar
  194. Yom-Tov Y (2003) Body sizes of carnivores commensal with humans have increased over the past 50 years. Funct Ecol 17:323–327CrossRefGoogle Scholar
  195. Zorrilla I, Martinez R, Taggart MA, Richards N (2015) Suspected flunixin poisoning of a wild Eurasian Griffon Vulture from Spain. Conserv Biol 29(2):587–592PubMedCrossRefGoogle Scholar
  196. Zuberogoitia I, Martínez JE, Margalida A et al (2010) Reduced food availability induces behavioural changes in Griffon Vulture Gyps fulvus. Ornis Fennica 87(2):52Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Rubén Moreno-Opo
    • 1
    • 2
  • Antoni Margalida
    • 3
    • 4
  1. 1.Ministry for the Ecological TransitionMadridSpain
  2. 2.Evolution and Conservation Biology Research GroupUniversity Complutense of MadridMadridSpain
  3. 3.Department of Animal Science, Faculty of Life Sciences and EngineeringUniversity of LleidaLleidaSpain
  4. 4.Institute for Game and Wildlife Research, IREC (CSIC-UCLM-JCCM)Ciudad RealSpain

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