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Movement ecology of pre-adult Cinereous Vultures Aegypius monachus: insights from a reintroduced population

Published online by Cambridge University Press:  21 May 2024

Jorge Tobajas*
Affiliation:
Universidad de Córdoba, Departamento de Botánica, Ecología y Fisiología Vegetal, 14071, Córdoba, Spain
Juan José Iglesias-Lebrija
Affiliation:
Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat (GREFA), 28220 Majadahonda, Madrid, Spain
Émilie Delepoulle
Affiliation:
Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat (GREFA), 28220 Majadahonda, Madrid, Spain
Ernesto Álvarez
Affiliation:
Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat (GREFA), 28220 Majadahonda, Madrid, Spain
Pilar Oliva-Vidal
Affiliation:
Institute for Game and Wildlife Research IREC (CSIC-UCLM-JCCM), 13005 Ciudad Real, Spain University of Lleida, Department of Animal Science, School of Agrifood and Forestry Engineering and Veterinary Mediccine (ETSEA), 25198 Lleida, Spain
Antoni Margalida
Affiliation:
University of Lleida, Department of Animal Science, School of Agrifood and Forestry Engineering and Veterinary Mediccine (ETSEA), 25198 Lleida, Spain Pyrenean Institute of Ecology (CSIC), 22700 Jaca, Spain
*
Corresponding author: Jorge Tobajas; Emails: [email protected]; [email protected]

Summary

Understanding the movement ecology of threatened species is fundamental to improving management and conservation actions for their protection, mainly during the pre-adult stage and particularly when a species is subject to population reinforcement or reintroduction projects. An example is the case of the Cinereous Vulture Aegypius monachus on the Iberian Peninsula, an endangered species that has been reintroduced in different regions during the last two decades. Here, we explore differences between the spatial ecology of reintroduced pre-adult Cinereous Vultures, according to age-class, sex, and season (breeding and non-breeding). We used GPS-tag data from 51 pre-adult individuals reintroduced into Catalonia (north-east Spain) to describe their use of space, i.e. home-range size, core area, and minimum convex polygon (MCP) and movement patterns, i.e. cumulative distance, maximum displacement, maximum daily dispersal, and maximum annual dispersal. Our study showed significant variation in the use of space and movement patterns among pre-adult birds and the influences of age, sex, and season. Age was the most influential factor, determining range areas and movement patterns. Similar to other vulture species, home range and core areas increase with age, with subadult vultures exhibiting larger ranges than young first year, juveniles, and immature birds, but the MCP measures were larger for juveniles. Movement patterns were also influenced by age-class, with juveniles making longer movements, followed by immatures and subadults (with similar values), and shorter movements for birds during their first year of life. Overall, males made shorter movements and explored smaller foraging areas than females. Season had an important effect on movement patterns, and the daily and dispersal movements were longer during the breeding period (February–August). Our findings fill a knowledge gap regarding the dispersal behaviours of Cinereous Vultures, information that will enable the improvement of management and conservation decisions.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of BirdLife International

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Footnotes

*

Equal contribution

References

Alarcón, P.A. and Lambertucci, S.A. (2018). A three-decade review of telemetry studies on vultures and condors. Movement Ecology 6, 13.CrossRefGoogle ScholarPubMed
Álvarez, M., Gálvez, M., Millet, A., Marco, X., Alvarez, E., Rafa, M. et al. (2011). “Vulturnet” conectividad de las poblaciones de buitre negro europeas: el programa de rentroducción del buitre negro en Cataluña. In Zuberogoitia, I. and Martínez, J.E. (eds), Ecología y Conservación de las Rapaces Forestales Europeas. Bilbao: Provincial Council of Biscay, pp. 356361.Google Scholar
Arrondo, E., García‐Alfonso, M., Blas, J., Cortes‐Avizanda, A., De la Riva, M., Devault, T. L. et al. (2021). Use of avian GPS tracking to mitigate human fatalities from bird strikes caused by large soaring birds. Journal of Applied Ecology 58, 14111420.CrossRefGoogle Scholar
Berger-Tal, O., Polak, T., Oron, A., Lubin, Y., Kotler, B.P. and Saltz, D. (2011). Integrating animal behavior and conservation biology: a conceptual framework. Behavioral Ecology 22, 236239.CrossRefGoogle Scholar
Blumstein, D.T. and Fernandez-Juricic, E. (2010). A Primer of Conservation Behavior. Sunderland, MA: Sinauer Associates Inc. Publishers.Google Scholar
Bohrer, G., Brandes, D., Mandel, J.T., Bildstein, K.L., Miller, T.A., Lanzone, M. et al. (2012). Estimating updraft velocity components over large spatial scales: contrasting migration strategies of golden eagles and turkey vultures. Ecology Letters 15, 96103.CrossRefGoogle ScholarPubMed
Bridge, E.S., Thorup, K., Bowlin, M.S., Chilson, P.B., Diehl, R.H., Fléron, R.W. et al. (2011). Technology on the move: recent and forthcoming innovations for tracking migratory birds. BioScience 61, 689698.CrossRefGoogle Scholar
Burnham, K. and Anderson, D.R. (2002). Model Selection and Multimodel Inference – A Practical Information-Theoretic Approach. New York: Springer Publishing.Google Scholar
Carrete, M. and Donázar, J.A. (2005). Application of central-place foraging theory shows the importance of Mediterranean dehesas for the conservation of the cinereous vulture, Aegypius monachus. Biological Conservation 126, 582590.CrossRefGoogle Scholar
Cerecedo-Iglesias, C., Bartumeus, F., Cortés-Avizanda, A., Pretus, J.L., Hernández-Matías, A. and Real, J. (2023). Resource predictability modulates spatial-use networks in an endangered scavenger species. Movement Ecology 11, 22.CrossRefGoogle Scholar
Clark, W.S. (2004). Wave moult of the primaries in accipitrid raptors, and its use in ageing immatures. In Chancellor, R.D. and Meyburg, B.-U. (eds), Raptors Worldwide: Proceedings of the V World Conference on Birds of Prey. Berlin: World Working Group on Birds of Prey, pp. 795804.Google Scholar
Cooke, S.J., Hinch, S.G., Wikelski, M., Andrews, R.D., Kuchel, L.J., Wolcott, T.G. et al. (2004). Biotelemetry: a mechanistic approach to ecology. Trends in Ecology & Evolution 19, 334343.CrossRefGoogle ScholarPubMed
De la Puente, J. and Elorriaga, J. (2012). Primary moult and its application to ageing in the black vulture Aegypius monachus. In Dobado, P.M. and Arenas, R. (eds), The Black Vulture: Status, Conservation and Studies. Córdoba: Ministry of the Environment, Junta de Andalucía, pp. 259269.Google Scholar
Del Moral, J.C. (ed.). (2019). El Buitre Negro en España, Población Reproductora en 2017 y Método de Censo. Madrid: SEO/BirdLife.Google Scholar
Delepoulle, E., Plana, G. and García-Ferré, D. (2017). Censo de la población del buitre negro en Cataluña en 2017. In Del Moral, J.C. (ed.), El Buitre Negro en España, Población Reproductora en 2017 y Método de Censo. Madrid: SEO/BirdLife, pp. 4851.Google Scholar
Delgado-Gonzalez, A., Cortés-Avizanda, A., Serrano, D., Arrondo, E., Duriez, O., Margalida, A. et al. (2022). Apex scavengers from different European populations converge at threatened savannah landscapes. Scientific Reports 12, 2500.CrossRefGoogle ScholarPubMed
Deygout, C., Gault, A., Sarrazin, F. and Bessa-Gomes, C. (2009). Modeling the impact of feeding stations on vulture scavenging service efficiency. Ecological Modelling 220, 18261835.CrossRefGoogle Scholar
Donázar, J.A., Margalida, A., Carrete, M. and Sánchez-Zapata, J.A. (2009). Too sanitary for vultures. Science 326, 664.CrossRefGoogle ScholarPubMed
Fluhr, J., Benhamou, S., Peyrusque, D. and Duriez, O. (2021). Space use and time budget in two populations of Griffon Vultures in contrasting landscapes. The Journal of Raptor Research 55, 425437.CrossRefGoogle Scholar
Fozzi, I., Brogi, R., Cavazza, S., Chirichella, R., De Rosa, D., Aresu, M. et al. (2023). Insights on the best release strategy from post-release movements and mortality patterns in an avian scavenger. iScience 26, 106699.CrossRefGoogle Scholar
García, V., Iglesias‐Lebrija, J.J. and Moreno‐Opo, R. (2021). Null effects of the Garcelon harnessing method and transmitter type on soaring raptors. Ibis 163, 899912.CrossRefGoogle Scholar
García-Jiménez, R., Pérez-García, J.M. and Margalida, A. (2018). Drivers of daily movement patterns affecting an endangered vulture flight activity. BMC Ecology 18, 115.CrossRefGoogle ScholarPubMed
García-Macía, J., Álvarez, E., Galán, M., Iglesias-Lebrija, J.J., Gálvez, M., Plana, G. et al. (2024). Age, season and sex influence juvenile dispersal in the Iberian cinereous vultures (Aegypius monachus). Journal of Ornithology 165, 325335.CrossRefGoogle Scholar
Gavashelishvili, A., McGrady, M., Ghasabian, M. and Bildstein, K.L. (2012). Movements and habitat use by immature Cinereous Vultures (Aegypius monachus) from the Caucasus. Bird Study 59, 449462.CrossRefGoogle Scholar
González, L.M., Oria, J., Margalida, A., Sánchez, R., Prada, L., Caldera, J. et al. (2006). Effective natal dispersal and age of maturity in the threatened Spanish Imperial Eagle Aquila adalberti: Conservation implications. Bird Study 53, 285293.CrossRefGoogle Scholar
Grande, J.M., Serrano, D., Tavecchia, G., Carrete, M., Ceballos, O., Díaz-Delgado, R. et al. (2009). Survival in a long-lived territorial migrant: effects of life-history traits and ecological conditions in wintering and breeding areas. Oikos 118, 580590.CrossRefGoogle Scholar
Guido, J.M., Cecchetto, N.R., Plaza, P.I., Donázar, J.A. and Lambertucci, S.A. (2023). The influence of age, sex and season on Andean condor ranging behavior during the immature stage. Animals 13, 1234.CrossRefGoogle ScholarPubMed
Hernández, M. and Margalida, A. (2008). Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 17, 264272.CrossRefGoogle ScholarPubMed
Herrero-Villar, M., Delepoulle, É., Suárez-Regalado, L., Solano-Manrique, C., Juan-Sallés, C., Iglesias-Lebrija, J.J. et al. (2021). First diclofenac intoxication in a wild avian scavenger in Europe. Science of the Total Environment 782, 146890.CrossRefGoogle Scholar
Hiraldo, F. and Donázar, J.A. (1990). Foraging time in the Cinereous Vulture (Aegypius monachus): seasonal and local variations and influence of weather. Bird Study 37, 128132.CrossRefGoogle Scholar
Holland, A.E., Byrne, M.E., Bryan, A.L., DeVault, T.L., Rhodes, O.E. and Beasley, J.C. (2017). Fine-scale assessment of home ranges and activity patterns for resident black vultures (Coragyps atratus) and turkey vultures (Cathartes aura). PLOS ONE 12, e0179819.CrossRefGoogle ScholarPubMed
Iglesias-Lebrija, J.J., Peragón, I., Galán, M. and Álvarez, E. (2015). Seguimiento telemétrico (GPS) de tres generaciones de milanos reales (Milvus milvus) en el noroeste de la Comunidad de Madrid. El papel de nuevas técnicas de recuperación aplicadas a fauna salvaje. Chronica Naturae 5, 3544.Google Scholar
Jiménez, J. and González, L.M. (2012). Patrones de movimiento y uso del espacio en la dispersión juvenil del buitre negro (Aegypius monachus). Ecología 24, 7393.Google Scholar
Jouventin, P. and Weimerskirch, H. (1990). Satellite tracking of wandering albatrosses. Nature 343, 746748.CrossRefGoogle Scholar
Jung, K., Kim, Y., Lee, H. and Kim, J.T. (2009). Aspergillus fumigatus infection in two wild Eurasian black vultures (Aegypius monachus Linnaeus) with carbofuran insecticide poisoning: a case report. Veterinary Journal 179, 307312.CrossRefGoogle ScholarPubMed
Kang, J.H., Hyun, B.R., Kim, I.K., Lee, H., Lee, J.K., Hwang, H.S. et al. (2019). Movement and home range of cinereous vulture Aegypius monachus during the wintering and summering periods in East Asia. Turkish Journal of Zoology 43, 305313.CrossRefGoogle Scholar
Katzner, T.E. and Arlettaz, R. (2020). Evaluating contributions of recent tracking-based animal movement ecology to conservation management. Frontiers in Ecology and Evolution 7, 519.CrossRefGoogle Scholar
Krüger, S., Reid, T. and Amar, A. (2014). Differential range use between age classes of Southern African Bearded Vultures Gypaetus barbatus. PLOS ONE 9, e114920.CrossRefGoogle ScholarPubMed
Mandel, J.T., Bildstein, K.L., Bohrer, G. and Winkler, D.W. (2008). Movement ecology of migration in turkey vultures. Proceedings of the National Academy of Sciences – PNAS 105, 1910219107.CrossRefGoogle ScholarPubMed
Margalida, A., Carrete, M., Hegglin, D., Serrano, D., Arenas, R. and Donázar, J.A. (2013). Uneven large-scale movement patterns in wild and reintroduced pre-adult bearded vultures: conservation implications. PLOS ONE 8, e65857.CrossRefGoogle ScholarPubMed
Margalida, A., García, D., Bertran, J. and Heredia, R. (2003). Breeding biology and success of the Bearded Vulture (Gypaetus barbatus) in the eastern Pyrenees. Ibis 145, 244252.CrossRefGoogle Scholar
Margalida, A., Jiménez, J., Martínez, J.M., Sesé, J.A., Llamas, A., García, D. et al. (2020). An assessment of population size and demographic drivers of the Bearded Vulture using integrated population models. Ecological Monographs 90, e01414.CrossRefGoogle Scholar
Margalida, A., Oliva-Vidal, P., Llamas, A. and Colomer, M.A. (2018). Bioinspired models for assessing the importance of transboundaring management and transhumance in the conservation of avian scavengers. Biological Conservation 228, 321330.CrossRefGoogle Scholar
Margalida, A., Pérez-García, J.M., Afonso, I. and Moreno-Opo, R. (2016). Spatial and temporal movements in Pyrenean bearded vultures (Gypaetus barbatus): Integrating movement ecology into conservation practice. Scientific Reports 6, 35746.CrossRefGoogle ScholarPubMed
McClure, C.J., Westrip, J.R., Johnson, J.A., Schulwitz, S.E., Virani, M.Z., Davies, R. et al. (2018). State of the world’s raptors: Distributions, threats, and conservation recommendations. Biological Conservation 227, 390402.CrossRefGoogle Scholar
Monsarrat, S., Benhamou, S., Sarrazin, F., Bessa-Gomes, C., Bouten, W. and Duriez, O. (2013). How predictability of feeding patches affects home range and foraging habitat selection in avian social scavengers? PLOS ONE 8, e53077.CrossRefGoogle ScholarPubMed
Morant, J., Arrondo, E., Cortés-Avizanda, A., Moleón, M., Donázar, J.A., Sánchez-Zapata, J.A. et al. (2023a). Large-scale quantification and correlates of ungulate carrion production in the Anthropocene. Ecosystems 26, 383396.CrossRefGoogle Scholar
Morant, J., Arrondo, E., Sánchez‐Zapata, J.A., Donázar, J.A., Cortés‐Avizanda, A., De La Riva, M. et al. (2023b). Large‐scale movement patterns in a social vulture are influenced by seasonality, sex, and breeding region. Ecology and Evolution 13, e9817.CrossRefGoogle Scholar
Morant, J., Arrondo, E., Sánchez-Zapata, J.A., Donázar, J.A., Margalida, A., Carrete, M. et al. (2024). Fine-scale collision risk mapping and validation with long-term mortality data reveal current and future wind energy development impact on sensitive species. Environmental Impact Assessment Review 104, 107399.CrossRefGoogle Scholar
Moreno-Opo, R., Fernández-Olalla, M., Margalida, A. Arredondo, A. and Guil, F. (2012). Effect of methodological and ecological approaches on results of habitat selection of a long-lived vulture. PLOS ONE 7, e33469.CrossRefGoogle ScholarPubMed
Moreno-Opo, R. and Margalida, A. (2014). Conservation of the Cinereous Vulture Aegypius monachus in Spain (1966–2011): a bibliometric review of threats, research and adaptive management. Bird Conservation International 24, 178191.CrossRefGoogle Scholar
Moreno-Opo, R., Trujillano, A. and Margalida, A. (2015). Optimization of supplementary feeding programs for European vultures depends on environmental and management factors. Ecosphere 6, 115.CrossRefGoogle Scholar
Moreno-Opo, R., Trujillano, A. and Margalida, A. (2020). Larger size and older age confer competitive advantage: dominance hierarchy within European vulture guild. Scientific Reports 10, 2430.CrossRefGoogle ScholarPubMed
Morrison, J.L. and Wood, P.B. (2009). Broadening our approaches to studying dispersal in raptors. Journal of Raptor Research 43, 8189.CrossRefGoogle Scholar
Nathan, R., Getz, W.M., Revilla, E., Holyoak, M., Kadmon, R., Saltz, D. et al. (2008). A movement ecology paradigm for unifying organismal movement research. Proceedings of the National Academy of Sciences – PNAS 105, 1905219059.CrossRefGoogle ScholarPubMed
Oliva-Vidal, P., Martínez, J.M., Sánchez-Barbudo, I.S., Camarero, P.R., Colomer, M.À., Margalida, A. et al. (2022a). Second-generation anticoagulant rodenticides in the blood of obligate and facultative European avian scavengers. Environmental Pollution 315, 120385.CrossRefGoogle ScholarPubMed
Oliva‐Vidal, P., Sebastián‐González, E. and Margalida, A. (2022b). Scavenging in changing environments: woody encroachment shapes rural scavenger assemblages in Europe. Oikos 12. e09310.CrossRefGoogle Scholar
Pérez-García, J.M., Morant, J., Arrondo, E., Sebastián-González, E., Lambertucci, S.A., Santangeli, A. et al. (2022). Priority areas for conservation alone are not a good proxy for predicting the impact of renewable energy expansion. Proceedings of the National Academy of Sciences – PNAS 119, e2204505119.CrossRefGoogle Scholar
R Core Team (2020). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Ramírez, J., Elorriaga, J. and de la Cruz, A. (2022). Cinereous Vulture Aegypius monachus movements between Europe and Africa show a pattern across the Strait of Gibraltar. Ostrich 93, 151156.CrossRefGoogle Scholar
Reading, R.P., Azua, J., Garrett, T., Kenny, D., Lee, H., Paek, W.K. et al. (2020). Differential movement of adult and juvenile Cinereous Vultures (Aegypius monachus) (Accipitriformes: Accipitridae) in Northeast Asia. Journal of Asia-Pacific Biodiversity 13, 156161.CrossRefGoogle Scholar
Rivers, J.W., Johnson, J.M., Haig, S.M., Schwarz, C.J., Burnett, L.J., Brandt, J. et al. (2014). An analysis of monthly home range size in the critically endangered California Condor Gymnogyps californianus. Bird Conservation International 24, 492504.CrossRefGoogle Scholar
Rousteau, T., Duriez, O., Pradel, R., Sarrazin, F., David, T., Herniquet, S. et al. (2022). High long-term survival and asymmetric movements in a reintroduced metapopulation of Cinereous vultures. Ecosphere 13, e03862.CrossRefGoogle Scholar
Safford, R., Andevski, J., Botha, A., Bowden, C.G., Crockford, N., Garbett, R. et al. (2019). Vulture conservation: the case for urgent action. Bird Conservation International 29, 19.CrossRefGoogle Scholar
Serrano, D. (2018). Dispersal in raptors. In Sarasola, J.H., Grande, J.M. and Negro, J.J. (eds), Birds of Prey: Biology and Conservation in the XXI Century. Cham: Springer, pp. 95121.CrossRefGoogle Scholar
Serrano, D., Cortés-Avizanda, A., Zuberogoitia, I., Blanco, G., Benítez, J.R., Ponchon, C. et al. (2021). Phenotypic and environmental correlates of natal dispersal in a long-lived territorial vulture. Scientific Reports 11, 5424.CrossRefGoogle Scholar
Serrano, D., Margalida, A., Pérez-García, J.M., Juste, J., Traba, J., Valera, F. et al. (2020). Renewables in Spain threaten biodiversity. Science 370, 12821283.CrossRefGoogle ScholarPubMed
Serrano, D. and Tella, J.L. (2003). Dispersal within a spatially structured population of lesser kestrels: the role of spatial isolation and conspecific attraction. Journal of Animal Ecology 72, 400410.CrossRefGoogle Scholar
Van Overveld, T., Blanco, G., Moleón, M., Margalida, A., Sánchez-Zapata, J.A., de la Riva, M. et al. (2020). Integrating vulture social behavior into conservation practice. The Condor 122, 120.CrossRefGoogle Scholar
Vasilakis, D.P., Whitfield, D.P., Schindler, S., Poirazidis, K.S. and Kati, V. (2016). Reconciling endangered species conservation with wind farm development: Cinereous vultures (Aegypius monachus) in south-eastern Europe. Biological Conservation 196, 1017.CrossRefGoogle Scholar
Whitfield, D.P., Fielding, A.H., Anderson, D., Benn, S., Dennis, R., Grant, J. et al. (2022). Age of first territory settlement of Golden Eagles Aquila chrysaetos in a variable competitive landscape. Frontiers in Ecology and Evolution 10, 743598.CrossRefGoogle Scholar
Wink, M., Sauer-Gürth, H., Martinez, F., Doval, G., Blanco, G. and Hatzofe, O. (1998). The use of (GACA)4 PCR to sex Old World vultures (Aves: Accipitridae). Molecular Ecology 7, 779782.CrossRefGoogle Scholar
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