Who are we feeding? Asymmetric individual use of surplus food resources in an insular population of the endangered Egyptian vulture Neophron percnopterus

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  García Heras, Marie Sophie ^a,b   Cortés Avizanda, Ainara ^a,c   Donázar, José Antonio ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c UNIVERSITY OF LISBON   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; BREEDING; ENDANGERED SPECIES; FEEDING BEHAVIOR; FLEDGLING; FOOD ASSISTANCE; FOOD AVAILABILITY; FORAGING BEHAVIOR; GENERAL CONDITION; NEOPHRON PERCNOPTERUS; NONHUMAN; POPULATION ABUNDANCE; RESOURCE MANAGEMENT; SEASONAL VARIATION; SPECIES CONSERVATION; SPECIES HABITAT; VULTURE (BIRD); ANIMAL; ENVIRONMENTAL PROTECTION; FALCONIFORMES; POPULATION DYNAMICS;

ANIMALS; CONSERVATION OF NATURAL RESOURCES; FALCONIFORMES; POPULATION DYNAMICS;

EID: 84892727462     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080523     Document Type: Article

References (69)

1. Monsarrat S, Benhamou S, Sarrazin F, Bessa-Gomes C, Bouten W et al. (2013) How predictability of feeding patches affects home range and foraging habitat selection in avian social scavengers? PLOS ONE 8 (1): e53077. doi:10.1371/journal.pone.0053077. PubMed: 23301024.
2. Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can J Zool 68: 203-220. doi:10.1139/z90-031.
3. Marzluff J, Millspaugh JJ, Hurvitz P, Handcock MS (2004) Relating resources to a probabilistic measure of space use: forest fragments and Steller's Jays. Ecology 85: 1411-1427. doi:10.1890/03-0114.
4. Blanco G (2006) Natural selection and the risk of artificial selection in the wild: nestling quality or quantity from supplementary feeding in the Spanish imperial eagle. Ardeola 53: 341-351.
5. 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: 476-484. doi:10.1890/060152.
6. Robb GN, Mcdonald RA, Chamberlain DE, Reynolds SJ, Harrison TJE et al. (2008) Winter feeding of birds increases productivity in the subsequent breeding season. Biol Lett 4: 220-223. doi:10.1098/rsbl.2007.0622. PubMed: 18252663.
7. López-Bao JV, Palomares F, Rodríguez A, Delibes M (2010) Effects of food supplementation on home-range size, reproductive success, productivity and recruitment in a small population of Iberian lynx. Anim Conserv 13: 35-42. doi:10.1111/j.1469-1795.2009.00300.x.
8. Harrison TJE, Smith JA, Martin GR, Chamberlain DE, Bearhop S et al. (2010) Does food supplementation really enhance productivity of breeding birds? Oecologia 164: 311-320. doi:10.1007/s00442-010-1645-x. PubMed: 20473622.
9. Cortés-Avizanda A, Carrete M, Donázar JA (2010) Managing supplementary feeding for avian scavengers: Guidelines for optimal design using ecological criteria. Biol Conserv 143: 1707-1715. doi: 10.1016/j.biocon.2010.04. 016.
10. Margalida A, Colomer MA, 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 (5): e20248. doi:10.1371/journal.pone.0020248. PubMed: 21629647.
11. Margalida A, Colomer MA (2012) Modelling the effects of sanitary policies on European vulture conservation. Sci Rep 2: 753. PubMed: 23082243.
12. Newton I (1979) Population ecology of raptors. Berkhamsted: T. & A.D. Poyser. 399 p.
13. Newton I (1991) Population limitation in birds of prey: a comparative approach. In: CM PerrinsJD LebretonTJM Hirons. Bird population studies. Oxf: Ornithol S: 3-21.
14. Newton I (1992) Experiments on the limitation of bird numbers by territorial behaviour. Biol Rev 67: 129-173. doi:10.1111/j.1469-185X.1992. tb01017.x.
15. Newton I (1998) Population limitation in birds. London: Academic Press Limited. 597 p.
16. 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 Conser 129: 477-486. doi:10.1016/j.biocon.2005.11.014.
17. Koenig R (2006) Vulture research soars as the scavenger's numbers decline. Science 312: 1591-1592. doi:10.1126/science.312.5780.1591. PubMed: 16778034.
18. Piper SE (2006) Supplementary feeding programs: how necessary are they for the maintenance of numerous and healthy vulture populations? In: DC HoustonSE Piper. Proceedings of the international conference on conservation and management of vulture populations. Thessaloniki: Natural History Museum of Crete and WWF Greece. pp. 41-50.
19. 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. doi: 10.1371/journal.pone. 0004084. PubMed: 19115009.
20. Benítez JR, Cortés-Avizanda A, Ávila E, García R (2009) Effects of the creation of a vulture restaurant for the conservation of an Egyptian vulture Neophron percnopterus population en Andalucía (Southern Spain). In: JA DonázarA MargalidaD Campión. Munibe supplement 29, Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology. San Sebastián: Sociedad de Ciencias Aranzadi. pp. 276-283.
21. Grande JM, Carrete M, Ceballos O, Tella JL, Donázar JA (2009) Relevance of vulture restaurants for the conservation of Egyptian vulture Neophron percnopterus in Spain. In: JA DonázarA MaragalidaD Campión. Munibe supplement 29, Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology. San Sebastián: Sociedad de Ciencias Aranzadi. pp. 254-267.
22. Carrete M, Donázar JA, Margalida A (2006) Density-dependent productivity depression in Pyrenean Bearbed vulture: implication for conservation. Ecol Appl 16: 1674-1682. doi: 10.1890/1051-0761(2006)016[1674: DPDIPB]2.0.CO;2. PubMed: 17069362.
23. 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: 85-88. doi:10.1111/j.1469-1795.2008.00231.x.
24. Cortés-Avizanda A, Selva N, Carrete M, Donázar JA (2009) Effects of carrion resources on herbivore spatial distribution are mediated by facultative scavengers. Basic Appl Ecol 10: 265-272.
25. Orians GH, Pearson NE (1979) On the theory of central place foraging. In: BJ HornGR StairsRD Mitchell. Analysis of Ecological Systems. Columbus: Ohio State University Press. pp. 155-177.
26. Renison D, Boersma D, Martella MB (2002) Winning and losing: causes for variability in outcome of fights in male Magellanic penguins (Spheniscus magellanicus). Behav Ecol 13: 462-466. doi:10.1093/beheco/13.4.462.
27. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79: 241-277. doi:10.1086/422893. PubMed: 15529965.
28. Dingemanse NJ, Wright J, Kazem JN, Thomas DK, Hickling R et al. (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76: 1128-1138. doi:10.1111/j.1365-2656.2007.01284.x. PubMed: 17922709.
29. Donázar JA, Negro JJ, Palacios CJ, Gangoso L, Godoy JA et al. (2002) Description of a new subspecies of the Egyptian vulture (Accipitridae: Neophron percnopterus) from the Canary Islands. J Raptor Res 36: 17-23.
30. Gangoso L (2006) Insularidad y conservación: el caso del alimoche (Neophron percnopterus) en Canarias. PhD-thesis. Universidad de Sevilla. 244 p.
31. Agudo R (2010) Conservation Genetics on Islands, a case of the Canarian Egyptian Vulture. PhD thesis Universidad Complutense: Madrid. 230 p.
32. Sergio F, Newton I (2003) Occupancy as a measure of territory quality. J Anim Ecol 72: 857-865. doi:10.1046/j.1365-2656.2003.00758.x.
33. Donázar JA, Palacios CJ, Gangoso L, Ceballos O, González MJ et al. (2002) Conservation status and limiting factors in the endangered population of Egyptian vulture (Neophron percnopterus) in the Canary Islands. Biol Conserv 107: 89-97. doi:10.1016/S0006-3207(02)00049-6.
34. Donázar JA (2004) Alimoche común Neophron percnopterus. In: A MadroñoC GonzálezJC Atienza. Libro Rojo de las Aves de España. Madrid: Dirección General para la Biodiversidad-SEO/ BirdLife. pp. 129-131.
35. BirdLife International (2008) Neophron percnopterus. In: IUCN Red List of Threatened Species.
36. Donázar JA, Gangoso L, Forero MG, Juste J (2002) Presence, richness and exctinction of birds of prey in the Mediterranean and Macaronesian island. J Biogeogr 32: 1701-1713.
37. Gangoso L, Palacios CJ (2005) Ground nesting by Egyptian vultures (Neophron percnopterus) in the Canary Islands. J Raptor Res 39: 186-187.
38. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for Mixed Models, Second Edition. Cary, NC: SAS Institute Inc. 814 p
39. Jovani R, Serrano D (2001) Feather mites (Astigmata) avoid moulting wing feathers of passerine birds. Anim Behav 62: 723-727. doi: 10.1006/anbe.2001. 1814.
40. Crawley MJ (1993) GLIM for Ecologists. Oxford: Blackwell Scientific Publishing House. 379 p.
41. Mendelssohn JM, Kemp AC, Biggs HC, Biggs R, Brown CJ (1989) Wing areas, wing loadings and wing spans of 66 species of African raptors. Ostrich 60: 35-42. doi:10.1080/00306525.1989.9634503.
42. Zajac T, Solarz W, Bielañski W (2008) Site-dependent population dynamics: the influence of spatial habitat heterogeneity on individual fitness in the sedge warbler Acrocephalus schoenobaenus. J Avian Biol 39: 206-214.
43. Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82: 1473-1483. doi: 10.1890/0012- 9658(2001)082[1473:MLRMOB]2.0.CO;2.
44. Peig J, Green A (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24: 1323-1332. doi:10.1111/j.1365-2435.2010.01751.x.
45. Donázar JA, Hiraldo F, Bustamante J (1993) Factors influencing nest site selection, breeding density and breeding success in the bearded vulture Gypaetus barbatus. J Appl Ecol 30: 500-514.
46. McCullagh P, Nelder JA (1989) Generalized Linear Models. London: Chapman and Hall. 532 pp.
47. Houston A, Mcnamara JM (1985) A general theory of central place foraging for single- prey loaders. Theor Popul Biol 28: 233-262. doi: 10.1016/0040-5809(85)90029-2.
48. Donázar JA, Ceballos O (1990) Post-Fledging dependence period and development of flight and foraging behaviour in the Egyptian Vulture Neophron percnopterus. Ardea 78: 387-394.
49. Donázar JA (1993) Los Buitres Ibéricos. Biología y Conservación. Madr J.M. Reyero: 256.
50. Marzluff JM, Kimsey BA, Schueck LS, McFadzen ME, Vekasy MS et al. (1997) The influence of habitat, prey abundance, sex, and breeding success on the ranging behavior of prairie falcons. Condor 99: 567-584. doi:10.2307/1370470.
51. Margalida A, Carrete M, Hegglin D, Serrano D, Arenas R et al. (2013) Uneven large-scale movement patterns in wild and reintroduced preadult bearded vultures: conservation implications. PLOS ONE (. (2013)) PubMed: 23776559.
52. Coulson JC (1968) Differences in the quality of birds nesting in the centre and on the edge of a colony. Nature 217: 478-479. doi: 10.1038/217478a0.
53. Winkler DW, Allen PE (1996) The seasonal decline in Tree Swallow clutch size: physiological constraint or strategic adjustment? Ecology 77: 922-932. doi:10.2307/2265512.
54. Rodenhouse NL, Sheery TW, Holmes RT (1997) Site dependent regulation of population size: a new synthesis. Ecology 78: 2025-2042. doi:10.1890/0012- 9658(1997)078[2025:SDROPS]2.0.CO;2.
55. Chamberlain DE, Fuller RJ (1999) Density-dependent habitat distribution in birds: issues of scale, habitat definition and habitat availability. J Avian Biol 30: 427-436.
56. Zajac T, Bielañski W, Solarz W (2011) Territory choice during the breeding tenure of male sedge. Behav Ecol Sociobiol 65: 2305-2317. doi:10.1007/s00265-011-1241-z. PubMed: 22162903.
57. Margalida M, Benítez JR, Sánchez-Zapata JA, Ávila E, Arenas R et al. (2012) Long-term relationships between diet and breeding success in a declining population of Egyptian Vultures Neophron percnopterus. Ibis 154: 184-188. doi:10.1111/j.1474-919X.2011.01189.x.
58. Whitfield DP, Reid R, Waworth PF, Madders M, Marquiss M et al. (2009) Diet specificity is not associated with increased productive performance of Golden Eagles Aquila chrysaetos in Western Scotland. Ibis 151: 255-264. doi:10.1111/j.1474-919X.2009.00924.x.
59. Reynolds SJ, Mänd R, Tilgar V (2004) Calcium supplementation of breeding birds: directions for future research. Ibis 146: 601-614. doi: 10.1111/j.1474-919x.2004.00298.x.
60. Richardson PRK, Mundy PJ, Plug I (1986) Bone crushing carnivores and their significance to osteodystrophy in griffon vulture chicks. J Zool 210: 23-43.
61. Carrete M, Donázar JA (2005) Application of central-place foraging theory shows the importance of Mediterranean dehesas for the conservation of the Cinereous Vulture. Biol Conserv 126: 582-590. doi: 10.1016/j.biocon.2005.06. 031.
62. 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: 613-621. doi:10.1007/s10344-009-0358-0.
63. Carrete M, Grande JM, Tella JL, Sánchez-Zapata JA, Donázar JA et al. (2007) Habitat, human pressure, and social behavior: Partialling out factors affecting large-scale territory extinction in an endangered vulture. Biol Conserv 136: 143-154. doi:10.1016/j.biocon.2006.11.025.
64. Deygout C, Gault A, Duriez O, Sarrazin F, Bessa-Gomes C (2010) Impact of food predictability on social facilitation by foraging scavengers. Behav Ecol 21: 1131-1139. doi:10.1093/beheco/arq120.
65. Schaffer SA, Weimerskircht H, Costa DP (2001) Functional significance of sexual dimorphism in wandering albatrosses Diomedea exulans. Funct Ecol 15: 203-210. doi:10.1046/j.1365-2435.2001.00514.x.
66. Gangoso L, Alvarez-LLoret P, Rodríguez-Navarro AA, Mateo R, Hiraldo F et al. (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157: 569-574. doi:10.1016/j.envpol.2008.09.015. PubMed: 18995938.
67. Margalida A, Donázar JA, Bustamante J, Hernández FJ, Romero-Pujante M (2008) Application of a predictive model to detect long-term changes in nest-site selection in the Bearded Vulture Gypaetus barbatus: conservation in relation to territory shrinkage. Ibis 150: 242-249.
68. Peterson C, Messmer TA (2007) Effects of winter-feeding on mule deer in Northern Utah. J Wildl Manage 71: 1440-1445. doi: 10.2193/2006-202.
69. Putman RJ, Staines BW (2004) Supplementary winter feeding of wild red deer Cervus elaphus in Europe and North America: justifications, feeding and effectiveness. Mamm Rev 34: 285-306. doi:10.1111/j.1365-2907.2004.00044.x.