Long-term changes in the breeding period diet of Bonelli’s eagle (Aquila fasciata) in Sicily, Italy
M. Di Vittorio A B , M. Lo Valvo C , E. Di Trapani B D , A. Sanguinetti E , A. Ciaccio B , S. Grenci B , M. Zafarana B , G. Giacalone B D , N. Patti B , S. Cacopardi B , P. Rannisi B , A. Scuderi B , L. Luiselli F G , G. La Grua B , G. Cortone A , S. Merlino B , A. Falci B , G. Spinella B and P. López-López
H I
A Ecologia Applicata Italia, Via Jevolella 2, 90018 Termini Imerese (PA), Italy.
B Gruppo Tutela Rapaci Sicilia, Via Mameli 3, 95030 Pedara (CT), Italy.
C Dipartimento di Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, Laboratorio di Zoologia applicata, University of Palermo, Via Archirafi 18, I 90123 Palermo, Italy.
D Cooperativa Silene, Via Dondes Regio 8/a, 90127 Palermo, Sicily, Italy.
E Via E. Notabartolo 60, 90145 Palermo, Italy.
F IDECC – Institute for Development, Ecology, Conservation and Cooperation, Via G. Tomasi di Lampedusa 33, I-00144 Rome, Italy.
G Niger Delta Ecology and Biodiversity Conservation Unit, Department of Applied and Environmental Biology, Rivers State University of Science and Technology, PMB 5080, Port Harcourt, Rivers State, Nigeria.
H Cavanilles Institute of Biodiversity and Evolutionary Biology, Terrestrial Vertebrates Group, University of Valencia, C/ Catedrático José Beltrán 2, E-46980 Paterna, Valencia, Spain.
I Corresponding author. Email: Pascual.Lopez@uv.es
Wildlife Research 46(5) 409-414 https://doi.org/10.1071/WR18081
Submitted: 9 May 2018 Accepted: 15 April 2019 Published: 1 August 2019
Abstract
Context: Dietary analyses are essential to achieve a better understanding of animal ecology. In the case of endangered species, assessing dietary requirements is crucial to improve their management and conservation. The Bonelli’s eagle (Aquila fasciata) has experienced a severe decline throughout its breeding range in Europe and, in Italy, fewer than 50 pairs remain, and only in Sicily. This species is subject to major threats, including changes in landscape composition and, consequently, prey availability, which is further aggravated by the occurrence of viral diseases in the case of rabbits.
Aims: To provide current data on the diet of the Bonelli’s eagle in Sicily during the breeding period and to examine dietary shifts with regard to previous studies conducted in the same study area. To discuss possible implications for conservation of the Italian population of this endangered species.
Methods: We used a combination of three methods, including pellet analysis, collection of prey remains, and imagery from camera-traps installed at nests, to examine the diet of 12 breeding pairs of Bonelli’s eagle from 2011 to 2017. We compared this information with data collected between 1993 and 1998 in the same study area.
Key results: In number, birds were the most frequently predated items (61.6%), followed by mammals (36.88%) and reptiles (1.52%). However, in terms of biomass, mammals were the main prey (65.71%), followed by birds (34.12%) and reptiles (0.17%). There was a decrease over the course of the current decade in the consumption of European wild rabbit (Oryctolagus cuniculus), which was compensated for with an increase in both dietary diversity and breadth in bird consumption, a trend not observed in the earlier study in the same region.
Conclusions: Here, we provide an updated assessment of diet composition of Bonelli’s eagle during the breeding period. Interestingly, we found significant differences within the study period (2011–2017) in terms of frequency of occurrence, percentage of biomass, dietary diversity and dietary breadth in a species at risk. Furthermore, we found significant differences between the two study periods in both frequency and percentage of biomass, with significant changes in the consumption of lagomorphs and birds.
Implications: Our results indicated that shifts in the diet are linked to changes in prey abundance, which may be contributing to population declines in the Bonelli’s eagle population in Sicily. Overall, measures aimed at increasing main dietary prey should be promoted to favour occupation of new territories and enhance vital demographic parameters (i.e. breeding success and survival rate) of Bonelli’s eagle across the species range. This would be particularly important for small isolated populations such as the Sicilian one.
Additional keywords: camera-trap, conservation, dietary composition, food, pellets.
References
AA.VV (2008). ‘Atlante della Biodiversità della Sicilia: Vertebrati Terrestri.’ (Arpa Sicilia: Palermo, Sicily, Italy.)Balbontín, J., Penteriani, V., and Ferrer, M. (2003). Variations in the age of mates as an early warning signal of changes in population trends? The case of Bonelli’s eagle in Andalusia. Biological Conservation 109, 417–423.
| Variations in the age of mates as an early warning signal of changes in population trends? The case of Bonelli’s eagle in Andalusia.Crossref | GoogleScholarGoogle Scholar |
BirdLife International (2016). ‘Species Factsheet: Aquila fasciata.’ Available at http://www.birdlife.org [11 December 2016].
Blanco, G. (2006). Natural selection and the risks of artificial selection in the wild: nestling quality or quantity from supplementary feeding in the Spanish imperial eagle. Ardeola 53, 341–351.
Cadahía, L., López-López, P., Urios, V., and Negro, J. J. (2010). Satellite telemetry reveals individual variation in juvenile Bonelli’s eagle dispersal areas. European Journal of Wildlife Research 56, 923–930.
| Satellite telemetry reveals individual variation in juvenile Bonelli’s eagle dispersal areas.Crossref | GoogleScholarGoogle Scholar |
Camarda, A., Pugliese, N., Cavadini, P., Circella, E., Capucci, L., Caroli, A., Legretto, M., Mallia, E., and Lavazza, A. (2014). Detection of the new emerging rabbit haemorrhagic disease type 2 virus (RHDV2) in Sicily from rabbit (Oryctolagus cuniculus) and Italian hare (Lepus corsicanus). Research in Veterinary Science 97, 642–645.
| Detection of the new emerging rabbit haemorrhagic disease type 2 virus (RHDV2) in Sicily from rabbit (Oryctolagus cuniculus) and Italian hare (Lepus corsicanus).Crossref | GoogleScholarGoogle Scholar | 25458493PubMed |
Caro, J., Ontiveros, D., and Pleguezuelos, J. M. (2011). The feeding ecology of Bonelli’s eagle (Aquila fasciata) floaters in southern Spain: implications for conservation. European Journal of Wildlife Research 57, 729–736.
| The feeding ecology of Bonelli’s eagle (Aquila fasciata) floaters in southern Spain: implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Carrete, M., Sánchez Zapata, J. A., Martínez, J. E., Sánchez, M. A., and Calvo, J. F. (2002). Factors influencing the decline of Bonelli’s eagle Hieraaetus fasciatus in southern Spain: demografy, habitat or competition? Biodiversity and Conservation 11, 975–985.
| Factors influencing the decline of Bonelli’s eagle Hieraaetus fasciatus in southern Spain: demografy, habitat or competition?Crossref | GoogleScholarGoogle Scholar |
Cheylan, G. (1977). La place trophique de l’aigle de Bonelli (Hieraaetus fasciatus) dans les biocenoses mediterraneennes. Alauda 45, 1–15.
Cohen, A., and Serjeantson, D. (1986). ‘A Manual for the Identification of Bird Bones from Archaeological Stes.’ (Archetype Publications Ltd: London.)
Cortone, P., and Mirabelli, P. (1987). Situazione dei rapaci in Calabria dal 1964 al 1984. Supplemento Ricerche Biologia della Selvaggina 12, 57–65.
Demerdzhiev, D. A., Gradev, G. Zh., Stoychev, S. A., Ivanov, I. I., Petrov, T. Hr., and Marin, S. A. (2011). Increase of the population of the eastern imperial eagle (Aquila heliaca) in Bulgaria. Acta Zool. Bulg. , 41–54.
Desse, J., Chaix, L., and Desse-Berset, N. (1986). ‘oSTEo: Base Réseau de Données Ostéométriques pour l’Archéozoologie.’ (CNRS: Paris, France.)
Di Vittorio, M., Grenci, S., and Campobello, D. (2001). Nuovi dati sulla biologia alimentare dell’aquila di Bonelli (Hieraaetus fasciatus) durante il periodo riproduttivo. Rivista Italiana di Ornitologia 1, 3–7.
Di Vittorio, M., López-López, P., and Sarà, M. (2012). Habitat preference of Bonelli’s eagle (Aquila fasciata) in Sicily. Bird Study 59, 207–217.
| Habitat preference of Bonelli’s eagle (Aquila fasciata) in Sicily.Crossref | GoogleScholarGoogle Scholar |
Di Vittorio, M., Rannisi, G., Di Trapani, E., Falci, A., Ciaccio, A., Rocco, M., Giacalone, G., Zafarana, M., Grenci, S., La Grua, G., Scuderi, A., Palazzolo, F., Cacopardi, S., Luiselli, L., Merlino, S., Lo Valvo, M., and López-López, P. (2018). Positive demographic effects of nest surveillance campaigns to counter illegal harvest of the Bonelli’s eagle in Sicily (Italy). Animal Conservation 21, 120–126.
| Positive demographic effects of nest surveillance campaigns to counter illegal harvest of the Bonelli’s eagle in Sicily (Italy).Crossref | GoogleScholarGoogle Scholar |
Ferguson-Lees, J., and Christie, D. A. (2001). ‘Raptors: Birds of Prey of the World.’ (A & C. Black: London.)
Fernández-Olalla, M., Martinez-Jauregui, M., Guil, F., and San Miguel-Ayanz, A. (2010). Provision of artificial warrens as a means to enhance native wild rabbit populations: what type of warren and where should they be sited? European Journal of Wildlife Research 56, 829–837.
| Provision of artificial warrens as a means to enhance native wild rabbit populations: what type of warren and where should they be sited?Crossref | GoogleScholarGoogle Scholar |
Ferrer, M., Newton, I., and Muriel, R. (2013). Rescue of a small declining population of Spanish imperial eagles. Biological Conservation 159, 32–36.
| Rescue of a small declining population of Spanish imperial eagles.Crossref | GoogleScholarGoogle Scholar |
Ferrer, M., Morandini, V., Baguena, G., and Newton, I. (2018). Reintroducing endangered raptors: a case study of supplementary feeding and removal of nestlings from wild populations Journal of Applied Ecology 55, 1360–1367.
| Reintroducing endangered raptors: a case study of supplementary feeding and removal of nestlings from wild populationsCrossref | GoogleScholarGoogle Scholar |
García-Salgado, G., Rebollo, S., Pérez-Camacho, L., Martínez-Hesterkamp, S., Navarro, A., and Fernández-Pereira, J. M. (2015). Evaluation of trail-cameras for analyzing the diet of nesting raptors using the Northern Goshawk as a model. PLoS One 10, e0127585.
| Evaluation of trail-cameras for analyzing the diet of nesting raptors using the Northern Goshawk as a model.Crossref | GoogleScholarGoogle Scholar | 25992956PubMed |
Gasc, J. P. (1997). ‘Atlas of Amphibians and Reptiles in Europe.’ (SEH and MNHN: Paris.)
Gil-Sánchez, J. M. (1998). Selección de presa por el águila-azor perdicera (Hieraaetus fasciatus) durante el periodo de nidificación en la provincia de Granada (SE de España). Ardeola 45, 151–160.
González, L. M., Margalida, A., Sánchez, R., and Oria, J. (2006). Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial eagle (Aquila adalberti). Biological Conservation 129, 477–486.
| Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial eagle (Aquila adalberti).Crossref | GoogleScholarGoogle Scholar |
Gotelli, N. J., and Ellison, A. M. (2004). ‘A Primer of Ecological Statistics.’ (Sinauer Associates, Inc.: Sunderland, MA.)
Gotelli, N. J., and Ellison, A. M. (2013). ‘EcoSimR 1.00.’ Available at http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html [Verified 22 May 2019].
Gotelli N.J., Graves G.R. (1996). ‘Null Models in Ecology.’ (Smithsonian Institution Press: Washington, DC.)
Guil, F., Higuero, R., and Moreno-Opo, R. (2014). European wild rabbit (Oryctolagus cuniculus) restocking: effects on abundance and spatial distribution. Wildlife Society Bulletin 38, 524–529.
| European wild rabbit (Oryctolagus cuniculus) restocking: effects on abundance and spatial distribution.Crossref | GoogleScholarGoogle Scholar |
Hagemeijer, W. J. M., and Blair, M. J. (1997). ‘The EBCC Atlas of European Breeding Birds.’ (T.&A.D. Poyser: London.)
Lewis, S. B., Fuller, M. R., and Titus, K. (2004). A comparison of 3 methods for assessing raptor diet during the breeding season. Wildlife Society Bulletin 32, 373–385.
| A comparison of 3 methods for assessing raptor diet during the breeding season.Crossref | GoogleScholarGoogle Scholar |
Litvaitis, J. A. (2000). Investigating food habits of terrestrial vertebrates. In ‘Research Techniques in Animal Ecology. Controversies and Consequences’. (Eds L. Boitani, T. K. Fuller.) pp. 165–190. (Columbia University Press: New York.)
Lo Valvo M., Massa B., and Sarà M. (1993). ‘Uccelli e Paesaggio in Sicilia alle Soglie del Terzo Millennio. Naturalista Sicil. 17 (Suppl.).’ (Luxograph Ed.: Palermo, Italy.)
Lo Valvo, M., La Scala, A., and Scalisi, M. (2014). Biometric characterisation and taxonomic considerations of European rabbit Oryctolagus cuniculus (Linnaeus 1758) in Sicily (Italy). World Rabbit Science 22, 207–214.
| Biometric characterisation and taxonomic considerations of European rabbit Oryctolagus cuniculus (Linnaeus 1758) in Sicily (Italy).Crossref | GoogleScholarGoogle Scholar |
Lo Valvo, M., Russo, R., Mascuso, F. P., and Palla, F. (2017). mtDNA diversity in a rabbit population from Sicily (Italy). Turkish Journal of Zoology 41, 645–653.
| mtDNA diversity in a rabbit population from Sicily (Italy).Crossref | GoogleScholarGoogle Scholar |
López-López, P., and Urios, P. (2010). Use of digital trail cameras to study Bonelli’s eagle’s diet during the nestling season. The Italian Journal of Zoology 77, 289–295.
| Use of digital trail cameras to study Bonelli’s eagle’s diet during the nestling season.Crossref | GoogleScholarGoogle Scholar |
López-López, P., Verdejo, J., and Barba, E. (2009). The role of pigeon consumption in the population dynamics and breeding performance of a peregrine falcon (Falco peregrinus) population: conservation implications. European Journal of Wildlife Research 55, 125–132.
| The role of pigeon consumption in the population dynamics and breeding performance of a peregrine falcon (Falco peregrinus) population: conservation implications.Crossref | GoogleScholarGoogle Scholar |
López-López, P., Sarà, M., and Di Vittorio, M. (2012). Living on the edge: assessing the extinction risk of critically endangered Bonelli’s eagle in Italy. PLoS One 7, e37862.
| Living on the edge: assessing the extinction risk of critically endangered Bonelli’s eagle in Italy.Crossref | GoogleScholarGoogle Scholar | 22768314PubMed |
Magurran, A. E. (2003). ‘Ecological Diversity and its Measurements.’ (Princeton University Press: Princeton, NJ.)
Marti, C. D. (1987). Raptor food habits studies. In ‘Raptor Management Tehniques Manual’. (Eds B. A. Giron Pendleton, B. A. Millsap, K. W. Cline, and D. M. Bird.) pp. 67–80. (National Wildlife Federation: Washington, DC.)
Massa, B. (1981). La régime alimentaire de quatorze espèces de rapaces en Sicilie: papaces Mèditerranèennes. Annales du C.R.O.P. Aix–en Provence 1, 119–129.
Mersmann, T. J., Buehler, D. A., Fraser, J. D., and Seegar, J. K. D. (1992). Assessing bias in studies of bald eagle food habits. The Journal of Wildlife Management 56, 73–78.
| Assessing bias in studies of bald eagle food habits.Crossref | GoogleScholarGoogle Scholar |
Milchev, B., Spassov, N., and Popov, V. (2012). Diet of the Egyptian vulture (Neophron percnopterus) after livestock reduction in eastern Bulgaria. North-Western Journal of Zoology 8, 315–323.
Moleón, M., Gil-Sánchez, J. M., Real, J., Sánchez-Zapata, J. A., Bautista, J., and Sánchez-Clemot, F. J. (2007). Non-breeding feeding ecology of territorial Bonelli’s eagles Hieraaetus fasciatus in the Iberian Peninsula. Ardeola 54, 135–143.
Moleón, M., Sánchez-Zapata, J. A., Real, J., García-Charton, J. A., Gil-Sánchez, J. M., Palma, L., Bautista, J., and Bayle, P. (2009). Large-scale spatio-temporal shifts in the diet of a predator mediated by an emerging infectious disease of its main prey. Journal of Biogeography 36, 1502–1515.
| Large-scale spatio-temporal shifts in the diet of a predator mediated by an emerging infectious disease of its main prey.Crossref | GoogleScholarGoogle Scholar |
Moleón, M., Sánchez-Zapata, J. A., Gil-Sánchez, J. M., Ballesteros-Duperón, E., Barea-Azcón, J. M., and Virgós, E. (2012). Predator–prey relationships in a Mediterranean vertebrate system: Bonelli’s eagles, rabbits and partridges. Oecologia 168, 679–689.
| Predator–prey relationships in a Mediterranean vertebrate system: Bonelli’s eagles, rabbits and partridges.Crossref | GoogleScholarGoogle Scholar | 21947548PubMed |
Newton, I. (1979). ‘Population Ecology of Raptors.’ (T & AD Poyser: London.)
Ontiveros, D., and Pleguezuelos, J. M. (2000). Influence of prey densities in the distribution and breeding success of Bonelli’s eagle (Hieraaetus fasciatus): management implications. Biological Conservation 93, 19–25.
| Influence of prey densities in the distribution and breeding success of Bonelli’s eagle (Hieraaetus fasciatus): management implications.Crossref | GoogleScholarGoogle Scholar |
Ontiveros, D., Real, J., Balbontín, J., Carrete, M., Ferrero, E., Ferrer, M., Mañosa, S., Pleguezuelos, J. M., and Sánchez-Zapata, J. A. (2004). Biología de la conservación del águila-azor perdicera Hieraaetus fasciatus en España: investigación científica y gestión. Ardeola 51, 459–468.
Oro, D., and Tella, J. L. (1995). A comparison of 2 methods for studying the diet of the Peregrine falcon. The Journal of Raptor Research 29, 207–210.
Real, J. (1996). Biases in diet study methods in the Bonelli’s eagle. The Journal of Wildlife Management 60, 632–638.
| Biases in diet study methods in the Bonelli’s eagle.Crossref | GoogleScholarGoogle Scholar |
Resano-Mayor, J., Hernández-Matías, A., Real, J., Moleón, M., Parés, F., Inger, R., and Bearhop, S. (2014). Multi-scale effects of nestling diet on breeding performance in a terrestrial top predator inferred from stable isotope analysis. PLoS One 9, e95320.
| Multi-scale effects of nestling diet on breeding performance in a terrestrial top predator inferred from stable isotope analysis.Crossref | GoogleScholarGoogle Scholar | 24743233PubMed |
Resano‐Mayor, J., Real, J., Moleón, M., Sánchez‐Zapata, J. A., Palma, L., and Hernández‐Matías, A. (2016). Diet–demography relationships in a long‐lived predator: from territories to populations. Oikos 125, 262–270.
| Diet–demography relationships in a long‐lived predator: from territories to populations.Crossref | GoogleScholarGoogle Scholar |
Rollan, À., Hernández-Matías, A., and Real, J. (2016). ‘Guidelines for the Conservation of Bonelli’s Eagle Populations.’ (Universitat de Barcelona. Barcelona, Spain.) Available at http://hdl.handle.net/2445/69446 [verified 22 May 2019].
Rondinini, C., Battistoni, A., Peronace, V., and Teofili, C. (2013). ‘Lista Rossa IUCN dei Vertebrati Italiani.’ (Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare: Roma.)
Rosenberg, K. V., and Cooper, R. J. (1990). Approaches to avian diet analysis. Studies in Avian Biology 13, 80–90.
Salvo, G. (1988). Dati preliminari sull’alimentazione dell’Aquila del Bonelli, Hieraaetus fasciatus, in Sicilia. Atti IV Convegno Italiano di Ornitologia, Pantelleria 12, 119–120.
Simeon, D., and Wilhelm, J. L. (1988). Essai sur l’alimentation annuelle de l’aigle de Bonelli (Hieraaetus fasciatus) en Provence. Alauda 56, 226–237.
Steenhof, K., and Kochert, M. N. (1985). Dietary shifts of sympatric buteos during a prey decline. Oecologia 66, 6–16.
| Dietary shifts of sympatric buteos during a prey decline.Crossref | GoogleScholarGoogle Scholar | 28310806PubMed |
Villafuerte, R., Calvete, C., Blanco, J. C., and Lucientes, J. (1995). Incidence of viral hemorrhagic disease in wild rabbit populations in Spain. Mammalia 59, 651–659.
| Incidence of viral hemorrhagic disease in wild rabbit populations in Spain.Crossref | GoogleScholarGoogle Scholar |
