Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Landscape anthropization shapes the survival of a top avian scavenger


Events of non-natural mortality in human-dominated landscapes are especially challenging for populations of large vertebrates with K strategies. Among birds, vultures are one of the most threatened groups experiencing sharp population declines due to non-natural mortality. Factors causing non-natural mortality are usually studied separately. However, the potential use of an integrated index able to predict large-scale mortality risks of avian scavengers could be especially useful for planning conservation strategies. Here, we used the Human Footprint index to examine the impact of landscape anthropization on the survival rates of 66 GPS-tagged adult Eurasian griffon vultures (Gyps fulvus) in two Spanish regions. Foraging in more anthropized areas resulted in a significantly higher individual mortality risk mainly due to collisions with vehicles, poisonings, electrocutions and fatalities with wind turbines. Mean yearly survival rates were estimated at 0.817 ± 0.043 SE and 0.968 ± 0.018 SE for individuals from the more and less anthropized regions, respectively. Additional research should investigate whether some vulture populations could be acting as sinks unnoticed due to metapopulation dynamics. From a broader point of view, our study shows that a straightforward Human Footprint was a useful index to predict the survival of top scavengers and can be highly applicable to planning large-scale conservation measures.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3


  1. Angelov I, Hashim I, Oppel S (2013) Persistent electrocution mortality of Egyptian vultures Neophron percnopterus over 28 years in East Africa. Bird Conserv Int 23(1):1–6. https://doi.org/10.1017/S0959270912000123

  2. Apollonio M, Andersen R, Putman R (2010) European ungulates and their management in the 21st century. Cambridge University Press, Cambridge

  3. Arrondo E, Moleón M, Cortés-Avizanda A, Jiménez J, Beja P, Sánchez-Zapata JA, Donázar JA (2018) Invisible barriers: differential sanitary regulations constrain vulture movements across country borders. Biol Conserv 219:46–52

  4. Arrondo E, Morales-Reyes Z, Moleón M, Cortés-Avizanda A, Donázar JA, Sánchez-Zapata JA (2019) Rewilding traditional grazing areas affects scavenger assemblages and carcass consumption patterns. Basic Appl Ecol 41:56–66

  5. Badia-Boher JA, Sanz-Aguilar A, de la Riva M, Gangoso L, van Overveld T, García-Alfonso M, Luzardo OP, Suarez-Pérez A, Donázar JA (2019) Evaluating European LIFE conservation projects: improvements in survival of an endangered vulture. J Appl Ecol. https://doi.org/10.1111/1365-2664.13350

  6. Bennett RE, Rodewald AD, Rosenberg KV (2019) Overlooked sexual segregation of habitats exposes female migratory landbirds to threats. Biol Conservdulac 240:108266

  7. Bernardino J, Bevanger K, Barrientos R, Dwyer JF, Marques AT, Martins RC, Shaw JM, Silva JP, Moreira F (2018) Bird collisions with power lines: state of the art and priority areas for research. Biol Conserv 222:1–13

  8. Bevanger K (1994) Bird interactions with utility structures: collision and electrocution, causes and mitigating measures. Ibis 136(4):412–425

  9. Blanco G, Cortés-Avizanda A, Frías Ó, Arrondo E, Donázar JA (2019) Livestock farming practices modulate vulture diet-disease interactions. Glob Ecol Conserv 17:e00518

  10. Bosè M, Sarrazin F (2007) Competitive behaviour and feeding rate in a reintroduced population of griffon vultures Gyps fulvus. Ibis 149(3):490–501

  11. Bosè M, Duriez O, Sarrazin F (2012) Intra-specific competition in foraging griffon vultures Gyps fulvus: 1 Dynamics of group feeding. Bird Study 59(2):182–192

  12. Boshoff AF, Minnie JC, Tambling CJ, Michael MD (2011) The impact of power line-related mortality on the Cape Vulture Gyps coprotheres in a part of its range, with an emphasis on electrocution. Bird Conserv Int 21(3):311–327

  13. Boxall AB, Kolpin DW, Halling-Sørensen B, Tolls J (2003) Peer reviewed: are veterinary medicines causing environmental risks? Environ. Sci. Technol 37(15):286A–294A. https://doi.org/10.1021/es032519b

  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach (2nd edn). In: Ecological modelling. Springer Science & Business Media, New York

  15. Calenge C, and Fortmann-Roe S (2013) AdehabitatHR: home range estimation. R package version 0.4, 7

  16. Campos P, Caparrós A, Oviedo JL, Ovando P, Álvarez-Farizo B, Díaz-Balteiro L, Carranza J, Beguería S, Díaz M, Herruzo AC, Martínez-Peña F, de Fruto P, Aldea J, Almazána E, Concepción ED, Mesa B, Romero C, Serrano-Notivoli R, Fernández C, Torres-Porras J, Montero G (2019) Bridging the gap between national and ecosystem accounting application in andalusian forests, Spain. Ecol Econ 157:218–236

  17. 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):582–590

  18. Carrete M, Sánchez-Zapata JA, Benítez JR, Lobón M, Donázar JA (2009) Large scale risk-assessment of wind-farms on population viability of a globally endangered long-lived raptor. Biol Conserv 142(12):2954–2961

  19. Chantepie S, Teplitsky C, Pavard S, Sarrazin F, Descaves B, Lecuyer P, Robert A (2016) Age-related variation and temporal patterns in the survival of a long-lived scavenger. Oikos 125(2):167–178

  20. Cortés-Avizanda A, Donázar JA, Pereira HM (2015) Top scavengers in a wilder Europe. In: Rewilding European landscapes, Springer, Cham pp. 85–106

  21. Cramp S, Simmons KEL (1980) The birds of the western palearctic, 2nd edn. Oxford University Press, Oxford

  22. D'Amico, M., Román, J., De los Reyes, L., & Revilla, E. (2015) Vertebrate road-kill patterns in Mediterranean habitats: who, when and where. Biol Conserv 191:234–242

  23. De Lucas M, Ferrer M, Bechard MJ, Muñoz AR (2012) Griffon vulture mortality at wind farms in southern Spain: distribution of fatalities and active mitigation measures. Biol Conserv 147(1):184–189

  24. De Vault TL, Beasley JC, Olson ZH, Moleón M, Carrete M, Margalida A, Sánchez-Zapata JA (2016) Ecosystem services provided by avian scavengers. Why birds matter: avian ecological function and ecosystem services. University of Chicago Press, Chicago, pp 235–270

  25. Del Moral JC, y Molina B (eds) (2018) El buitre leonado en España, población reproductora en 2018 y método de censo. SEO/BirdLife, Madrid

  26. Dixon A, Maming R, Gunga A, Purev-Ochir G, Batbayar N (2013) The problem of raptor electrocution in Asia: case studies from Mongolia and China. Bird 23(4):520–529

  27. 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):613–621

  28. Dupont H, Mihoub JB, Bobbé 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

  29. Ferrer et al (2004) Density-dependent age of first reproduction as a buffer affecting persistence of small populations. Ecol Appl 14:616–624

  30. Fluhr J, Benhamou S, Riotte-Lambert L, Duriez O (2017) Assessing the risk for an obligate scavenger to be dependent on predictable feeding sources. Biol Conserv 215:92–98

  31. Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O'Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Seehan J, Siebert S, Tilman D, Zaks DPM (2011) Solutions for a cultivated planet. Nature 478(7369):337

  32. García-Barón I, Cortés-Avizanda A, Verburg PH, Marques TA, Moreno-Opo R, Pereira HM, Donázar JA (2018) How to fit the distribution of apex scavengers into land abandonment scenarios? The Cinereous vulture in the Mediterranean biome. Divers Distrib 24(7):1018–1031

  33. Green RE, Newton IAN, Shultz S, Cunningham AA, Gilbert M, Pain DJ, Prakash V (2004) Diclofenac poisoning as a cause of vulture population declines across the Indian subcontinent. J Appl Ecol 41(5):793–800

  34. Henriques M, Granadeiro JP, Monteiro H, Nuno A, Lecoq M, Cardoso P, Regalla A, Catry P (2018) Not in wilderness: African vulture strongholds remain in areas with high human density. PLoS ONE 13(1):e0190594

  35. Hernández-Matías A, Real J, Moleón M, Palma L, Sánchez-Zapata JA, Pradel R, Arroyo B, Fernández C, Vincent-Martin N, Ravayrol A, Benítez JR, Ferreiro E, García J (2013) From local monitoring to a broad-scale viability assessment: a case study for the Bonelli's Eagle in western Europe. Ecol Monogr. 83(2):239–261

  36. Ibisch PL, Hoffmann MT, Kreft S, Pe'er G, Kati V, Biber-Freudenberger L, DellaSala DA, Vale MM, Hobson P, Selva N (2016) A global map of roadless areas and their conservation status. Science 354(6318):1423–1427

  37. Le Gouar P, Robert A, Choisy JP, Henriquet S, Lecuyer P, Tessier C, Sarrazin F (2008) Roles of survival and dispersal in reintroduction success of griffon vulture (Gyps fulvus). Ecol Appl 18(4):859–872

  38. Lecina S, Playán E, Isidoro D, Dechmi F, Causapé J, Faci JM (2005) Irrigation evaluation and simulation at the irrigation district V of Bardenas (Spain). Agric Water Manag. 73(3):223–245

  39. Loss SR, Will T, Marra PP (2015) Direct mortality of birds from anthropogenic causes. Ann Rev Ecol Evol Syst 46:99–120

  40. Luna Á, Romero-Vidal P, Hiraldo F, Tella JL (2018) Cities favour the recent establishment and current spread of the Eurasian collared dove Streptopelia decaocto (Frivaldszky, 1838) in Dominican Republic. Bioinvasions Rec 7(1):95–99

  41. 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

  42. Margalida A, Colomer MÀ, Sanuy D (2011) Can wild ungulate carcasses provide enough biomass to maintain avian scavenger populations? An empirical assessment using a bio-inspired computational model. PLoS ONE 6:e20248

  43. 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 6:35746

  44. Martín-Queller E, Moreno-Mateos D, Pedrocchi C, Cervantes J, Martínez G (2010) Impacts of intensive agricultural irrigation and livestock farming on a semi-arid Mediterranean catchment. Environ Monit Assess 167(1–4):423–435

  45. McShane BB, Gal D, Gelman A, Robert C, Tackett JL (2019) Abandon statistical significance. Am Stat 73(1):235–245

  46. Millán J, López-Bao JV, García EJ, Oleaga Á, Llaneza L, Palacios V, de la Torre A, Rodriguez A, Dubovi EJ, Esperón F (2016) Patterns of exposure of Iberian wolves (Canis lupus) to canine viruses in human-dominated landscapes. EcoHealth 13(1):123–134

  47. Moleón M, Sanchez-Zapata JA, Margalida A, Carrete M, Owen-Smith N, Donazar JA (2014) Humans and scavengers: the evolution of interactions and ecosystem services. Biosci J. 64(5):394–403

  48. Monsarrat S, Benhamou S, Sarrazin F, Bessa-Gomes C, Bouten W, Duriez O (2013) How predictability of feeding patches affects home range and foraging habitat selection in avian social scavengers? PLoS ONE 8(1):e53077

  49. Morales-Reyes Z, Pérez-García JM, Moleón M, Botella F, Carrete M, Lazcano C, Sánchez-Zapata JA (2015) Supplanting ecosystem services provided by scavengers raises greenhouse gas emissions. Sci Rep 5:7811

  50. Morales-Reyes Z, Pérez-García JM, Moleón M, Botella F, Carrete M, Donázar JA, Cortés-Avizanda A, Arrondo E, Moreno-Opo R, Jiménez J, Margalida M (2017) Evaluation of the network of protection areas for the feeding of scavengers in Spain: from biodiversity conservation to greenhouse gas emission savings. J Appl Ecol 54(4):1120–1129

  51. Morales-Reyes M, Martín-López B, Moleón M, Mateo-Tomás P, Botella F, Margalida A, Donázar JA, Blanco G, Pérez I, Sánchez-Zapata JA (2018) Farmer perceptions of the ecosystem services provided by scavengers: what, who and to whom. Conserv Lett 11:e12392

  52. Navarro LM, Pereira HM (2015) Rewilding abandoned landscapes in Europe. Rewilding European landscapes. Springer, Cham, pp 3–23

  53. Ogada DL, Keesing F, Virani MZ (2012) Dropping dead: causes and consequences of vulture population declines worldwide. Ann N Y Acad Sci 1249(1):57–71

  54. Ogada D, Shaw P, Beyers RL, Buij R, Murn C, Thiollay JM, Krüger SC, Botha A, Virani MZ, Monadjem A, Sinclari ARE (2016) Another continental vulture crisis: Africa's vultures collapsing toward extinction. Cons Lett 9(2):89–97

  55. 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

  56. Oro D, Margalida A, Carrete M, Heredia R, Donázar JA (2008) Testing the goodness of supplementary feeding to enhance population viability in an endangered vulture. PLoS ONE 3(12):e4084

  57. Oro D, Genovart M, Tavecchia G, Fowler MS, Martínez-Abraín A (2013) Ecological and evolutionary implications of food subsidies from humans. Ecol Lett 16(12):1501–1514

  58. Owens IP, Bennett PM (2000) Ecological basis of extinction risk in birds: habitat loss versus human persecution and introduced predators. Proc Natl Acad Sci 97(22):12144–12148

  59. Payo-Payo A, Genovart M, Sanz-Aguilar A, Greño JL, García-Tarrasón M, Bertolero A, Picardo J, Oro D (2017) Colonisation in social species: the importance of breeding experience for dispersal in overcoming information barriers. Sci Rep 7:42866

  60. Pérez-García JM, DeVault T, Botella F, Sánchez-Zapata JA (2017) Using risk prediction models and species sensitivity maps for large-scale identification of infrastructure-related wildlife protection areas: the case of bird electrocution. Biol Conserv 210:334–342

  61. Perino A, Pereira HM, Navarro LM, Fernández N, Bullock JM, Ceauşu S, Cortés-Avizanda A, van Klink R, Kuemmerle T, Lomba A, Peer G, Plieninger T, Rey Benyas JM, Sandom CJ, Svenning JC, Wheeler HC (2019) Rewilding complex ecosystems. Science 364(6438):eaav5570

  62. Pitarch A, Gil C, Blanco G (2017) Oral mycoses in avian scavengers exposed to antibiotics from livestock farming. Sci Total Environ 605:139–146

  63. Plaza PI, Lambertucci SA (2017) How are garbage dumps impacting vertebrate demography, health, and conservation? Glob Ecol Conserv 12:9–20

  64. Popp A, Calvin K, Fujimori S, Havlik P, Humpenöder F, SteHuman Footprintest E, LeonBodirsky B, PhilippDietrich J, Doelmann JC, MykolaGusti M, Tomoko-Hasegawa T, Kyle P, Obersteiner M, Tabeau A, Takahashi K, Valin H, Waldhoff S, Weindl I, van Vuuren DP (2017) Land-use futures in the shared socio-economic pathways. Global Environ Chang 42:331–345

  65. Powell LA (2007) Approximating variance of demographic parameters using the delta method: a reference for avian biologists. Condor 109:949–954

  66. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org.

  67. Rebolo-Ifrán N, Tella JL, Carrete M (2017) Urban conservation hotspots: predation release allows the grassland-specialist burrowing owl to perform better in the city. Sci Rep 7(1):3527

  68. Sæther BE, Bakke Ø (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81(3):642–653

  69. Sánchez-Zapata JA, Clavero M, Carrete M, DeVault TL, Hermoso V, Losada MA, Polo MJ, Sánchez-Navarro S, Pérez-García JM, Botella F, Ibáñez C, Donázar JAC (2016) Effects of renewable energy production and infrastructure on wildlife. Current trends in Wildlife Research. Springer, Cham, pp 97–123

  70. Santangeli A, Girardello M, Buechley E, Botha A, Minin ED, Moilanen A (2019) Priority areas for conservation of Old World vultures. Conserv Lett. https://doi.org/10.1111/cobi.13282

  71. Sanz-Aguilar, A., De Pablo, F., & Donázar, J. A. (2015a). Age-dependent survival of island vs. mainland populations of two avian scavengers: delving into migration costs. Oecologia, 179(2), 405–414.

  72. Sanz-Aguilar A, Sánchez-Zapata JA, Carrete M, Benítez JR, Ávila E, Arenas R, Donázar JA (2015b) Action on multiple fronts, illegal poisoning and wind farm planning, is required to reverse the decline of the Egyptian Vulture in southern Spain. Biol Conserv 187:10–18

  73. Sanz-Aguilar A, Igual JM, Tavecchia G, Genovart M, Oro D (2016) When immigration mask threats: the rescue effect of a Scopoli's shearwater colony in the Western Mediterranean as a case study. Biol Conserv 198:33–36

  74. Sanz-Aguilar A, Cortés-Avizanda A, Serrano D, Blanco G, Ceballos O, Grande JM, Tella JL, Donázar JA (2017) Sex-and age-dependent patterns of survival and breeding success in a long-lived endangered avian scavenger. Sci Rep 7:40204

  75. Sarrazin FO, Bagnolini C, Pinna JL, Danchin E, Clobert J (1994) High survival estimates of griffon vultures (Gyps fulvus fulvus) in a reintroduced population. Auk 111(4):853–862

  76. Sarrazin F, Bagnolini C, Pinna JL, Danchin E (1996) Breeding biology during establishment of a reintroduced Griffon Vulture Gyps fulvus population. Ibis 138(2):315–325

  77. Schaub M, Aebischer A, Gimenez O, Berger S, Arlettaz R (2010) Massive immigration balances high anthropogenic mortality in a stable eagle owl population: lessons for conservation. Biol Conserv 143(8):1911–1918

  78. Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17(10):474–480

  79. Sebastián-González E, Barbosa JM, Pérez-García JM, Morales-Reyes Z, Botella P, Olea PP, Mateo-Tomás P, Moleón M, Hiraldo F, Arrondo E, Donázar JA, Cortés-Avizanda A, Selva N, Lambertucci SA, Bhattacharjee A, Brewer A, Anadón JD, Abernethy E, Rhodes OE, Turner K, Beasley JC, DeVault TL, Ordiz A, Wikenros C, Zimmermann B, Wabakken P, Wilmers CC, Smith JA, Kendall CJ, Ogada D, Buechley ER, Frehner E, Allen ML, Wittmer HU, Butler JRA, Toit JT, Read J, Wilson D, Jerina K, Krofel M, Kostecke R, Inger R, Samson A, Naves-Alegre L, Sánchez-Zapata JA (2019) Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale. Global Change Biology 25(9):3005–3017

  80. Sherub S, Fiedler W, Duriez O, Wikelski M (2017) Bio-logging, new technologies to study conservation physiology on the move: a case study on annual survival of Himalayan vultures. J Comp Physiol A 203(6–7):531–542

  81. 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(4):757–768

  82. van Overveld T, García-Alfonso M, Dingemanse NJ, Bouten W, Gangoso L, de la Riva M, Serrano D, Donázar JA (2018) Food predictability and social status drive individual resource specializations in a territorial vulture. Sci Rep 8(1):15155

  83. Venter O, Sanderson EW, Magrach A, Allan JR, Beher J, Jones KR, Possingham HP, Laurance WF, Wood P, Fekete BM, Levy MA, Watson JEM (2016) Global terrestrial Human Footprint maps for 1993 and 2009. Sci Data 3:160067

  84. Vidal-Vallés D, Rodríguez A, Pérez-Collazos E (2018) Bird roadkill occurences in Aragon Spain. Anim Biodiv Conserv 41(2):379–388

  85. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth's ecosystems. Science 277(5325):494–499

  86. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(1):S120–S139

  87. Wink M, Sauer-Gürth H, Martinez F, Doval G, Blanco G, Hatzofe O (1998) The use of (GACA) 4 PCR to sex Old World vultures (Aves: Accipitridae). Mol Ecol 7(6):779–782

  88. Xirouchakis SM, Poulakakis N (2008) Biometrics, sexual dimorphism and gender determination of griffon vultures Gyps fulvus from Crete. Ardea 96(1):91–98

  89. Zuberogoitia I, De La Puente J, Elorriaga J, Alonso R, Palomares LE, Martínez JE (2013) The flight feather molt of griffon vultures (Gyps fulvus) and associated biological consequences. J Raptor Res 47(3):292–304

Download references


This research was funded by the Project RNM-1925 (Junta de Andalucía), the Project CGL2015-66966-C2-1-2-R (Spanish Ministry of Economy and Competitiveness and EU/ERDF) and the Project RTI2018-099609-B-C21 (Spanish Ministry of Economy and Competitiveness and EU/ERDF). “Roads Less Travelled” project (DiversEarth, Trashumancia y Naturaleza and Yolda Initiative) also contributed to this research. EA was supported by La Caixa-Severo Ochoa International PhD Program 2015. ASA and ACA by a post-doctoral contract Viçent Mut (PD/003/2016 and PD/039/2017, respectiely) co-funded by the Govern Balear and European Social Funds. ASA was also supported by a Spanish Ramón y Cajal contract (RYC-2017-22796) funded by the Ministerio de Ciencia, Innovación y Universidades, the Agencia Estatal de Investigación and the European Social Found. JMPG was supported by a Juan de la Cierva research contract (FJCI-2015-25632).

Author information

Correspondence to Eneko Arrondo.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Karen E. Hodges.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (DOCX 22 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arrondo, E., Sanz-Aguilar, A., Pérez-García, J.M. et al. Landscape anthropization shapes the survival of a top avian scavenger. Biodivers Conserv (2020). https://doi.org/10.1007/s10531-020-01942-6

Download citation


  • Griffon
  • Vulture
  • Human footprint
  • Non-natural mortality
  • Anthropization