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Assessing the effects of different management scenarios on the conservation of small island vulture populations

Published online by Cambridge University Press:  16 March 2020

MAURO ARESU ,
ANDREA ROTTA ,
ALBERTO FOZZI ,
ALFONSO CAMPUS ,
MARCO MUZZEDDU ,
DIONIGI SECCI ,
ILARIA FOZZI ,
DAVIDE DE ROSA  and
FIAMMETTA BERLINGUER Open the ORCID record for FIAMMETTA BERLINGUER [Opens in a new window]
MAURO ARESU
Affiliation:
Via Crispi 5, 08015Macomer, Italy.
ANDREA ROTTA
Affiliation:
University of Sassari, Ufficio Gestione Centri e Consorzi, Largo Macao 32, 07100Sassari, Italy.
ALBERTO FOZZI
Affiliation:
CRiMM onlus, Centro Ricerca Mammiferi Marini, 07028Santa Teresa di Gallura, Italy.
ALFONSO CAMPUS
Affiliation:
Associazione Naturalistica L’altra Bosa, 09089Bosa (OR), Italy.
MARCO MUZZEDDU
Affiliation:
Agenzia forestale regionale per lo sviluppo del territorio e l’ambiente della Sardegna (Fo.Re.S.T.A.S.), Viale Luigi Merello, 86 - 09123Cagliari, Italy.
DIONIGI SECCI
Affiliation:
Agenzia forestale regionale per lo sviluppo del territorio e l’ambiente della Sardegna (Fo.Re.S.T.A.S.), Viale Luigi Merello, 86 - 09123Cagliari, Italy.
ILARIA FOZZI
Affiliation:
Centro Studi Fauna, Via Vincenzo Monti 19, 07046Porto Torres (SS), Italy. ARDEA-Associazione per la Ricerca, la Divulgazione e l’Educazione Ambientale, Via Ventilabro 6, 80126 Naples, Italy.
DAVIDE DE ROSA
Affiliation:
University of Sassari, Ufficio Gestione Centri e Consorzi, Largo Macao 32, 07100Sassari, Italy. ARDEA-Associazione per la Ricerca, la Divulgazione e l’Educazione Ambientale, Via Ventilabro 6, 80126 Naples, Italy.
FIAMMETTA BERLINGUER*
Affiliation:
University of Sassari, Department of Veterinary Medicine, Via Vienna 2, 07100 Sassari, Italy.
*
*Author for correspondence; email: [email protected]
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Summary

Although the population of Griffon Vulture Gyps fulvus is significantly increasing in Europe, in Italy the species is still on the Red List as ‘Critically Endangered’, with the last natural population persisting on the island of Sardinia. Several episodes of poisoning hampered the success of conservation actions implemented in the years 1987–1995. In 2005 there were estimated to be only 31–32 territorial pairs, with the population occupying the territories of Alghero and Bosa. We used a long-term dataset of reproductive records from the Sardinian Griffon Vulture populations to run a population viability analysis (PVA) to evaluate the extinction risk using the Vortex simulation software. The model estimated the probability of extinction over the next five generations (estimated generation time: 11 years, simulation time used: 55 years) as 96.4% for the Alghero population, and near-zero for the Bosa population. We used sensitivity analyses to understand how uncertainty about parameter values affect model outcomes. Population projections were evaluated under different management scenarios tackling the main threats (poisoning and human disturbance) and implementing conservation actions (supplementary feeding and restocking). Our results showed that population size is a critical factor in affecting the projections of population dynamics of Griffon Vultures. Sensitivity analyses highlighted the importance of poisoning events to population persistence and showed that juvenile and adult mortality rates had a secondary impact on population viability. The only conservation measure effective in significantly increasing stochastic growth rates in the Alghero population, whose initial population was set at five individuals, was the complete removal of poisoning events. When targeting the Bosa population (initial population size 94 individuals), supplementary feeding, mitigation of the risk of poisoning episodes, restocking, and mitigation of human disturbance in the reproductive sites significantly increased stochastic growth rate. A cost-effectiveness analysis should be performed to prioritise interventions.

Keywords

population viability analysisGriffon Vulturefeeding stationsrestockinghuman disturbance
Type
Research Article
Information
Bird Conservation International , Volume 31 , Issue 1 , March 2021 , pp. 111 - 128
Copyright
© BirdLife International, 2020

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References

Aresu, M and Schenk, H (2006) Il Grifone (Gyps fulvus) in Sardegna. WWF Italia, Alberto Perdisa Editore.Google Scholar
Arroyom, B., Ferreiro, E. and Garza, V. (1990) II censo nacional de Buitre leonado (Gyps fulvus). Poblacion, distribucion, demografıa y conservacion. Madrid, Spain: Coleccion tecnica.Google Scholar
Badia-Boher, J. A., Sanz-Aguilar, A., de la Riva, M., Gangoso, L., van Overveld, T., García-Alfonso, M., Luzardo, O. P., Suarez-Pérez, A. and Donázar, J. A. (2019) Evaluating European LIFE conservation projects: Improvements in survival of an endangered vulture. J. Appl. Ecol. 56: 1210–1219.CrossRefGoogle Scholar
Bamford, A. J., Monadjem, A. and Hardy, I. C. W. (2009) Nesting habitat preference of the African White-backed Vulture Gyps africanus and the effects of anthropogenic disturbance. Ibis. 151: 51–62.CrossRefGoogle Scholar
Bennett, P. M. and Ian, P. F. O. (1997) Variation in extinction risk among birds: Chance or evolutionary predisposition? Proc. Biol. Sci. 264: 401–408.CrossRefGoogle Scholar
Bennett, P. M. and Owens, I. P. F. (1997) Variation in extinction risk among birds: chance or evolutionary predisposition? Proc. Roy. Soc. B: Biol. Sci. 264: 401–408.CrossRefGoogle Scholar
, BirdLifeInternational (2018) State of the world’s birds: taking the pulse of the planet. Cambridge, UK: BirdLife International.Google Scholar
Botha, A. J., Andevski, J., Bowden, C., Gudka, G. R., Safford, M., Tavares, R. J. and Williams, N. P. (2017) Multi-species Action Plan to conserve African-Eurasian vultures. Abu Dhabi, United Arab Emirates: Coordinating Unit of the CMS Raptors MOU.Google Scholar
Bretagnolle, V., Inchausti, P., Seguin, J. F. and Thibault, J. C. (2004) Evaluation of the extinction risk and of conservation alternatives for a very small insular population: The bearded vulture Gypaetus barbatus in Corsica. Biol. Conserv. 120: 19–30.CrossRefGoogle Scholar
Buechley, E. R. and Şekercioğlu, T. H. (2016) The avian scavenger crisis: Looming extinctions, trophic cascades, and loss of critical ecosystem functions. Biol. Conserv. 198: 220–228.CrossRefGoogle Scholar
Campbell, M. O. N. (2015) Vultures: Their evolution, ecology and conservation. Boca Raton: CRC Press.CrossRefGoogle Scholar
Carrete, M., Donázar, J. A. and Margalida, A. (2006) Density-dependent productivity depression in Pyrenean Bearded Vultures: Implications for conservation. Ecol. Applic. 16: 1674–1682.CrossRefGoogle ScholarPubMed
Chiari, M., Cortinovis, C., Vitale, N., Zanoni, M., Faggionato, E., Biancardi, A. and Caloni, F. (2017) Pesticide incidence in poisoned baits: A 10-year report. Sci. Total Environ. 601-602: 285–292.CrossRefGoogle ScholarPubMed
Cortés-Avizanda, A., Carrete, M., Serrano, D. and Donázar, J. A. (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.CrossRefGoogle Scholar
Cortés-Avizanda, A., Jovani, R., Carrete, M. and Donázar, J. A. (2012) Resource unpredictability promotes species diversity and coexistence in an avian scavenger guild: A field experiment. Ecology 93: 2570–2579.CrossRefGoogle Scholar
Cortés-Avizanda, A., Blanco, G., DeVault, T. L., Markandya, A., Virani, M. Z., Brandt, J. and Donázar, J. A. (2016) Supplementary feeding and endangered avian scavengers: benefits, caveats, and controversies. Front. Ecol. Environ. 14: 191–199.CrossRefGoogle Scholar
Coulson, T,, Mace, G. M., Hudson, E. and Possingham, H. (2001) The use and abuse of population viability analysis. Trends Ecol. Evol. 16: 219–221.CrossRefGoogle ScholarPubMed
Deinet, S., Ieronymidou, C., McRae, L., Burfield, I., Foppen, R., Collen, B. and Böhm, M. (2013) Wildlife comeback in Europe - The recovery of selected mammal and bird species. London, UK: Zoological Society of London; Birdlife International; and the European Bird Census Council.Google Scholar
Demerdzhiev, D., Hristov, H., Dobrev, D., Angelov, I. and Kurtev, M. (2014) Long-term population status, breeding parameters and limiting factors of the Griffon Vulture (Gyps fulvus Hablizl, 1783) population in the Eastern Rhodopes, Bulgaria. Acta Zool. Bulgarica 66: 373–384.Google Scholar
DeVault, T. L., Rhodes, J., Olin, E.. and Shivik, J. A. (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102: 225–234.CrossRefGoogle Scholar
Deygout, C., Gault, A., Sarrazin, F. and Bessa-Gomes, C. (2009) Modeling the impact of feeding stations on vulture scavenging service efficiency. Ecol: Model. 220: 1826–1835.Google Scholar
Donazar, J., Margalida, A. and Campion, D. (2009) Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology. San Sebastian, Spain: Munibe.Google Scholar
Donázar, J. A., Margalida, A., Carrete, M. and Sánchez-Zapata, J. A. (2009) Too sanitary for vultures. Science 326: 664.CrossRefGoogle ScholarPubMed
García-Ripollés, C. and López-López, P. (2011) Integrating effects of supplementary feeding, poisoning, pollutant ingestion and wind farms of two vulture species in Spain using a population viability analysis. J. Ornithol. 152: 879–888.CrossRefGoogle Scholar
García-Ripollés, C., López-López, P., García-López, F., Aguilar, J. M. and Verdejo, J. (2005) Modelling nesting habitat preferences of Eurasian Griffon Vulture Gyps fulvus in eastern Iberian Peninsula. Ardeola 52: 287–304.Google Scholar
Gavashelishvili, A. and McGrady, M. J. (2006) Breeding site selection by bearded vulture (Gypaetus barbatus) and Eurasian griffon (Gyps fulvus) in the Caucasus. Anim. Conserv. 9: 159–170.CrossRefGoogle Scholar
González, L. M., Arroyo, B. E., Margalida, A., Sánchez, R. and Oria, J. (2006) Effect of human activities on the behaviour of breeding Spanish imperial eagles (Aquila adalberti): management implications for the conservation of a threatened species. Anim. Conserv. 9: 85–93.CrossRefGoogle Scholar
Green, R. E., Donázar, J. A., Sánchez-Zapata, J. A. and Margalida, A. (2016) Potential threat to Eurasian griffon vultures in Spain from veterinary use of the drug diclofenac. J. Appl. Ecol. 53: 993–1003.CrossRefGoogle Scholar
Hernández, M. and Margalida, A. (2008) Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus) population in Spain. Ecotoxicology 17: 264–272.CrossRefGoogle ScholarPubMed
Hernández, M. and Margalida, A. (2009) Poison-related mortality effects in the endangered Egyptian vulture (Neophron percnopterus) population in Spain. Eur. J. Wildl. Res. 55: 415–423.CrossRefGoogle Scholar
Hollander, M. and Wolfe, D. (1999) Nonparametric statistical methods. Chichester, UK: Wiley.Google Scholar
Lacy, R. and Pollak, J. (2014) Vortex: A stochastic simulation of the extinction process. Version 10.0. Brookfield, Illinois, USA: Chicago Zoological Society.Google Scholar
Lacy, R. and Pollak, J. (2017) MetaModel Manager. Users manual. Brookfield, Illinois, USA: Chicago Zoological Society.Google Scholar
Lacy, R., Miller, P. and Traylor-Holzer, K. (2017) Vortex 10 user’s Manual. Apple valley, Minnesota, USA: IUCN SSC Conservation Breeding Specialist Group, and Chicago Zoological Society.Google Scholar
Lacy, R. C. (1993) VORTEX: a computer simulation model for Population Viability Analysis. Wildl. Res. 20: 45–65.CrossRefGoogle Scholar
Lacy, R. C. (2000) Structure of the VORTEX simulation model for population viability analysis. Ecol. Bull. 48: 191–203.Google Scholar
Lande, R. (1987) Extinction thresholds in demographic models of territorial populations. Am. Nat. 130: 624–635.CrossRefGoogle Scholar
Le Gouar, P., Robert, A., Choisy, J. P., Henriquet, S., Lecuyer, P., Tessier, C. and Sarrazin, F. (2008) Roles of survival and dispersal in reintroduction success of Griffon vulture (Gyps fulvus). Ecol. Applic. 18: 859–872.CrossRefGoogle ScholarPubMed
López-López, P., Garcia-Ripolles, C. and Verdejo, J. (2004) Population status and reproductive performance of Eurasian Griffons (Gyps fulvus) in eastern Spain. J. Raptor Res. 38: 350–356.Google Scholar
Margalida, A. (2012) Baits, budget cuts: A deadly mix. Science 338: 192.CrossRefGoogle ScholarPubMed
Margalida, A. and Colomer, M., À. (2012) Modelling the effects of sanitary policies on European vulture conservation. Sci. Reports 2: 753.Google ScholarPubMed
Margalida, A. and Mateo, R. (2019) Illegal killing of birds in Europe continues. Science 363: 1161.Google ScholarPubMed
Margalida, A., Campión, D. and Donázar, J. A. (2014) Vultures vs livestock: conservation relationships in an emerging conflict between humans and wildlife. Oryx 48: 172–176.CrossRefGoogle Scholar
Margalida, A., Ogada, D. and Botha, A. (2019) Protect African vultures from poison. Science 365: 1089.Google ScholarPubMed
Margalida, A., Donázar, J. A., Carrete, M. and Sánchez-Zapata, J. A. (2010) Sanitary versus environmental policies: fitting together two pieces of the puzzle of European vulture conservation. J. Appl. Ecol. 47: 931–935.CrossRefGoogle Scholar
Margalida, A., Moreno-Opo, R., Arroyo, B. E. and Arredondo, A. (2011) Reconciling the conservation of endangered species with economically important anthropogenic activities: Interactions between cork exploitation and the cinereous vulture in Spain. Anim. Conserv. 14: 167–174.CrossRefGoogle Scholar
Margalida, A., Oliva-Vidal, P., Llamas, A. and Colomer, M. (2018) Bioinspired models for assessing the importance of transhumance and transboundary management in the conservation of European avian scavengers. Biol. Conserv. 228: 321–330.CrossRefGoogle Scholar
Martínez-Haro, M., Mateo, R., Guitart, R., Soler-Rodríguez, F., Pérez-López, M., María-Mojica, P. and García-Fernández, A. J. (2008) Relationship of the toxicity of pesticide formulations and their commercial restrictions with the frequency of animal poisonings. Ecotoxicol. Environ. Safety 69: 396–402.CrossRefGoogle ScholarPubMed
Moleón, M., Sánchez-Zapata, J. A., Margalida, A., Carrete, M., Owen-Smith, N. and Donázar, J. A. (2014) Humans and scavengers: The evolution of interactions and ecosystem services. BioScience 64: 394–403.CrossRefGoogle Scholar
Monadjem, A., Kane, A., Botha, A., Kelly, C. and Murn, C, (2018) Spatially explicit poisoning risk affects survival rates of an obligate scavenger. Sci. Reports 8.Google ScholarPubMed
Morales-Reyes, Z., Pérez-García, J. M., Moleón, M., Botella, F., Carrete, M., Lazcano, C., Moreno-Opo, R., Margalida, A., Donázar, J. A. and Sánchez-Zapata, J. A. (2015) Supplanting ecosystem services provided by scavengers raises greenhouse gas emissions. Sci. Rep. 5.CrossRefGoogle ScholarPubMed
Moreno-Opo, R., Trujillano, A., Arredondo, T., González, L. M. and Margalida, A. (2015) Manipulating size, amount and appearance of food inputs to optimize supplementary feeding programs for European vultures. Biol. Conserv. 181: 27–35.CrossRefGoogle Scholar
Murn, C. and Botha, A. (2018) A clear and present danger: Impacts of poisoning on a vulture population and the effect of poison response activities. Oryx 52: 552–558.CrossRefGoogle Scholar
O’Grady, J. J., Reed, D. H., Brook, B. W. and Frankham, R. (2008) Extinction risk scales better to generations than to years. Anim. Conserv. 11: 442–451.CrossRefGoogle Scholar
Ogada, D. L., Keesing, F. and Virani, M. Z. (2012) Dropping dead: causes and consequences of vulture population declines worldwide. Ann. NY Acad. Sci. 1249: 57–71.CrossRefGoogle ScholarPubMed
Oro, D., Margalida, A., Carrete, M., Heredia, R. and Donázar, J. A. (2008) Testing the goodness of supplementary feeding to enhance population viability in an endangered vulture. PLoS One 3: e4084–e4084.CrossRefGoogle Scholar
Ortega, E., Mañosa, S., Margalida, A., Sánchez, R., Oria, J. and Garcia, L (2009) A demographic description of the recovery of the vulnerable Spanish Imperial Eagle Aquila adalberti. Oryx 43: 113–121.CrossRefGoogle Scholar
Pavoković, G. and Sušić, G. (2006) Population Viability Analysis of (Eurasian) Griffon Vulture Gyps fulvus in Croatia. In International Conference on Conservation and Management of Vulture Populations, Thessaloniki, Greece, 14–16. 11. 2005.Google Scholar
Plaza, P. I., Martínez-López, E. and Lambertucci, S. A. (2019) The perfect threat: Pesticides and vultures. Sci. Total Environ. 687: 1207–1218.CrossRefGoogle ScholarPubMed
Reed, J. M. and McCoy, E. D. (2014) Relation of Minimum Viable Population size to biology, time frame, and objective. Conserv. Biol. 28: 867–870.CrossRefGoogle ScholarPubMed
Reed, J. M., Mills, L. S., Dunning, J. B. Jr., Menges, E. S., McKelvey, K. S., Frye, R., Beissinger, S. R., Anstett, M-C. and Miller, P. (2002) Emerging issues in Population Viability Analysis. Conserv. Biol. 16: 7–19.CrossRefGoogle Scholar
Robb, G. N., McDonald, R. A., Chamberlain, D. E. and Bearhop, S. (2008) Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front. Ecol. Environ. 6: 476–484.CrossRefGoogle Scholar
Rondinini, C., Battistoni, A., Peronace, V. and Teofili, C. (2013) Lista Rossa IUCN dei Vertebrati Italiani. Roma: Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare. http://www.iucn.it/scheda.php?id=-1607566788.Google Scholar
Safford, R., Andevski, J., Botha, A., Bowden, C. G. R., Crockford, N., Garbett, R., Margalida, A., Ramírez, I., Shobrak, M., Tavares, J. and Williams, N. P. (2019) Vulture conservation: The case for urgent action. Bird Conserv. Internatn. 29: 1–9.CrossRefGoogle Scholar
Santangeli, A., Arkumarev, V., Rust, N. and Girardello, M. (2016) Understanding, quantifying and mapping the use of poison by commercial farmers in Namibia – Implications for scavengers’ conservation and ecosystem health. Biol. Conserv. 204: 205–211.Google Scholar
Santangeli, A., Girardello, M., Buechley, E., Botha, A., Minin, E. D. and Moilanen, A. (2019) Priority areas for conservation of Old World vultures. Conserv. Biol. 33: 1056–1065.CrossRefGoogle ScholarPubMed
Schenk, H., Aresu, M. and Naitana, S. (2008) Proposta di un Piano d’Azione per il Grifone (Gyps fulvus) in Sardegna. Cagliari, Italy: Legambiente Sardegna.Google Scholar
Şekercioğlu, Ç,Daily, H., , G. C. and Ehrlich, P. R. (2004) Ecosystem consequences of bird declines. Proc. Natl. Ac. Sci. 101: 18042.CrossRefGoogle ScholarPubMed
Soutullo, A., López-López, P. and Urios, V. (2008) Incorporating spatial structure and stochasticity in endangered Bonelli’s eagle’s population models: Implications for conservation and management. Biol. Conserv. 141: 1013–1020.CrossRefGoogle Scholar
Tella, J. L. (2001) Action is needed now, or BSE crisis could wipe out endangered birds of prey. Nature 410: 408.CrossRefGoogle ScholarPubMed
Van Beest, F., Van Den Bremer, L., De Boer, W. F., Heitkönig, I. M. A. and Monteiro, A. E. (2008) Population dynamics and spatial distribution of Griffon Vultures (Gyps fulvus) in Portugal. Bird Conserv. Internatn. 18: 102–117.CrossRefGoogle Scholar
Xirouchakis, S. M. (2010) Breeding biology and reproductive performance of Griffon Vultures Gyps fulvus on the island of Crete (Greece). Bird Study 57: 213–225.CrossRefGoogle Scholar
Zorrilla, I., Martinez, R., Taggart, M. A. and Richards, N. (2015) Suspected flunixin poisoning of a wild Eurasian Griffon Vulture from Spain. Conserv. Biol. 29: 587–592.CrossRefGoogle ScholarPubMed
Zuberogoitia, I., Zabala, J., Martínez, J. E., González-Oreja, J. A. and López-López, P. (2014) Effective conservation measures to mitigate the impact of human disturbances on the endangered Egyptian vulture. Anim. Conserv. 17: 410–418.CrossRefGoogle Scholar
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