Diet shifting of tortoise-eating Golden Eagles (Aquila chrysaetos) in southeastern Bulgaria
DOI:
https://doi.org/10.51812/of.121253Keywords:
diet change, food niche breadth, Testudo, Erineceaus, predationAbstract
Top predators may adapt their diets to changes in prey availability where human-induced environmental changes are intense. This long-term study of the breeding-season diet of Golden Eagle (Aquila chrysaetos) in the Strandzha Mountains analyzed shifts in diet caused by the population decline in principal prey species, the tortoises (Testudo hermanni and T. graeca). Tortoises comprised 50.0% of the eagle diet by prey number in the 1990s, but that share collapsed to 5.8% in 2014–2021. During this later interval, Golden Eagles preyed more intensively on lighter-weight prey such as Northern White-breasted Hedgehog (Erinaceus roumanicus, an increrase of 28.2% by number) and Edible Dormouse (Glis glis, an increase of 14.9% by number). Hedgehogs predominated in the diet of an individual eagle nest site for the first time in 1998 and became the principal prey in 2014–2021. Differences in food niche breadth and proportions of mesopredators between tortoise- and hedgehog-dominated individual annual diets were not significant, corresponding to a low level of food stress. The only eagle with an annual diet dominated by Squamata (snakes and lizards) was an exception, having the widest food niche. Young domestic ungulates have almost completely disappeared from eagle diets at the same as the reduction of tortoises, corresponding to a concurrent decline of livestock farming. The results obtained here have relevance to conservation management of both predator and prey populations.
References
Bedrosian, G., Watson, J., Steenhof, K., Kochert, M., Preston, C., Woodbridge, B., Williams, G., Keller K. & Crandall, R. 2017: Spatial and Temporal Patterns in Golden Eagle Diets in the Western United States, with Implications for Conservation Planning. — Journal of Raptor Research 51: 347–367. https://doi.org/10.3356/JRR-16-38.1
Beshkov, V. 1984: On the distribution, relative abundance and protection of tortoises in Bulgaria. — Ecology, Sofiа 14: 14–34. (In Bulgarian)
Clouet, M. 1981: L’Aigle Royal Aquila chrysaetos dans les Pyrénées Francaises. Résultats de 5 ans d’observations. — La Revue française d’ornithologie 51: 89–100. (In French)
Clouet, M., Gonzalez, L., Laspreses, F. & Rebours, I. 2015: Le régime alimentaire de l’Aigle royal Aquila chrysaetos en période de reproduction dans le nord du Pays Basque. — Alauda 83: 1–6. (In French)
Collins, P. & Latta, B. 2009: Food habits of nesting Golden Eagles (Aquila chrysaetos) on Santa Cruz and Santa Rosa islands, California. — In Proceedings of the 7th California Islands Symposium. (ed Damiani, C. & Garcelon D.): 255–268. Institute for Wildlife Studies, Arcata, CA.
Collopy, M. 1983: A comparison of direct observations and collections of prey remains in determining the diet of Golden Eagles. — The Journal of Wildlife Management 47: 360–368. https://doi.org/10.2307/3808508
Demerdzhiev, D., Dobrev, D., Isfendiyaroǧlu, S., Boev, Z., Stoychev, S., Terziev, N. & Spasov, S. 2014: Distribution, abundance, breeding parameters, threats and prey preferences of the eastern Imperial Eagle (Aquila heliaca) in European Turkey. — Slovak Raptor Journal 8: 17–25. https://doi.org/10.2478/srj-2014-0004
Demerdzhiev, D., Dobrev, D., Arkumarev, V., Terziev, N. & Georgiev, G. 2019: Distribution, abundance and breeding performance of Lesser Spotted Eagle Clanga pomarina Brehm, 1831 (Aves: Accipitridae) in Southeast Bulgaria. — Acta Zoologica Bulgarica Suppl. 14: 15–33.
Fernàndez, C. 1993: Effect of the viral haemorrhagic pneumonia of the wild rabbit on the diet and breeding success of the Golden Eagle Aquila chrysaëtos (L.). — Revue d’Ecologie (La Terre et la Vie) 48: 323–329.
Fischer, W., Zenker, D. & Baumgart, W. 1975: Ein Beitrag zum Bestand und zur Ernährung des Steinadlers (Aquila chrysaetos) auf der Balkanhalbinsel. — Beiträge zur Vogelkunde 21: 275–287. (In German)
Georgiev, D. 2009. Diet of the Golden Eagle (Aquila chrysaetos) (Aves: Accipitridae) in Sarnena Sredna Gora mountains (Bulgaria). — Ecologia Balkanica 1: 95–98.
Glutz von Blotzheim, U. & Bauer, K. 1994: Handbuch der Vögel Mitteleuropas. vol. 9. — Wiesbaden, Germany: Akademische Verlagsgesellschaft. (In German)
Golemanski, V. (ed.) 2015: Red Data Book of Bulgaria. 2nd ed. — Bulgarian Academy of Sciences and Ministry of Environment and Waters of Bulgaria, Sofia, Bulgaria.
Görner, M. & Hackethal, H. 1987: Säugetiere Europas. — Neumann Verl., Leipzig-Radebeul. (In German)
Grubač, R. 1987: L’Aigle Royal en Macedone. — In L’Aigle Royal en Europe. (ed. Michel S.): 37–39. Actes du Premier Colloque International, Arvieux. (In French)
Haller, H. 1996: Die Steiadler in Graubünden. Langfristige Untersuchungen zur Popuationsökologie von Aquila chrysaetos im Zentrum der Alpen. — Der Ornithologische Beobachter, Beiheft 9: 1–167. (In German with English summary)
Hammer, Ø., Harper, D. & Ryan, P. 2001: PAST: Paleontological Statistics software package for education and data analysis. — Paleontologia Electronica 4: 1–9.
Heath, J., Kochert, M. & Steenhof, K. 2021: Golden Eagle dietary shifts following wildfire and shrub loss have negative consequences for nestling survivorship. — Ornithological Applications. 123: 1–14. https://doi.org/10.1093/ornithapp/duab034
Högström, S. & Wiss L.-E. 1992: Diet of the Golden Eagle Aquila chrysaetos (L.) in Gotland, Sweden during the breeding season. — Ornis Fennica 69: 39–44.
Horváth, M., Solti, B., Fatér, I., Juhász, T., Haraszthy, L., Szitta, T., Ballók, Z. & Pásztory-Kovács, S. 2018: Temporal changes in the diet composition of the Eastern Imperial Eagle (Aquila heliaca) in Hungary. — Ornis Hungarica 26: 1–26. https://doi.org/10.1515/orhu-2018-0001
Jackson, O. 1980: Weight and measurement data on tortoises (Testudo graeca and Testudo hermanni) and their relationship to health. — Journal of small animal practice 21: 409–416. https://doi.org/10.1111/j.1748-5827.1980.tb01269.x
Karyakin, I., Kovalenko, A., Levin, A. & Pazhenkov, A. 2011: Eagles of the Aral-Caspian Region, Kazakhstan. — Raptor Conservation 22: 92–152.
Lepš, J. & Šmilauer, P. 2003: Multivariate Analysis of Ecological Data using CANOCO. — Cambridge, UK: Cambridge University Press. https://doi.org/10.1017/CBO9780511615146
Levins, R. 1968: Evolution in Changing Environments. — Princeton, NJ, USA: Princeton University Press. https://doi.org/10.1515/9780691209418
Lourenço, R., Santos, S., Rabaça, J. & Penteriani, V. 2011: Superpredation patterns in four large European raptors. — Population Ecology 53: 175–185. https://doi.org/10.1007/s10144-010-0199-4
März, R. 1987: Gewöll- und Rupfungskunde. — Akademie-Verlag Berlin. (In German)
Mebs, T. & Schmidt, D. 2014: Die Greifvögel Europas, Nordafrikas und Vorderasiens. Biologie, Kennzeichen, Bestände. 2nd edn. — Franckh-Kosmos Verlag, Stuttgart. (In German)
Menzel, J. & Miltschev, B. 2001: Ein neues Vorkommen des Habichtskauzes Strix uralensis in Bulgarien. — Ornithologische Mitteilungen 53: 280–281. (In German)
Milchev, B. & Kovachev, A. 1995: A contribution to the migration of the White Stork (Ciconia ciconia (L.)) along the Bulgarian Black sea coast. — Annual University of Sofia “St. K. Ohridski” 86/87: 43–48.
Milchev, B. & Georgiev, V. 2014: Extinction of the globally endangered Egyptian vulture Neophron percnopterus breeding in SE Bulgaria. — North-Western Journal of Zoology 10: 266–272. art.141601 http://biozoojournals.ro/nwjz/index.html
Milchev, B. & Georgiev, V. 2020: Temporal and spatial dietary shifts of a generalist top predator: long-term study of an Eagle owl Bubo bubo population. — Forestry Ideas 26: 366–379.
Milchev, B. & Georgiev, V. 2021: The effect of Natura 2000 network on the Eurasian Eagle-owl (Bubo bubo) population in Southeast Bulgaria: implications for conservation. — Ornis Hungarica 29: 170–178. https://doi.org/10.2478/orhu-2021-0013
Miltschew, B. & Georgiewa, U. 1992: Eine Studie zum Bestand, zur Brutbiologie und Ernährung des Steinadlers, Aquila chrysaetos (L.) im Strandsha-Gebirge. — Beiträge zur Vogelkunde 38: 327–334. (In German)
Newton, I. 1979: Population ecology of raptors. — T & AD Poyser, Berkhamsted.
Nyström, J., Ekenstedt, J., Angerbjörn, A., Thulin, L., Hellström, P. & Dalén, L. 2006: Golden Eagles on the Swedish mountain tundra – diet and breeding success in relation to prey fluctuations. — Ornis Fennica 83:145–152.
Pedrini, P. & Sergio, F. 2002: Regional conservation priorities for a large predator: Golden eagles (Aquila chrysaetos) in the Alpine range. — Biological Conservation 103: 163–172. https://doi.org/10.1016/S0006-3207(01)00116-1
Penteriani, V. & Delgado, M. 2019: The Eagle Owl. — T & AD Poyser, London, Oxford, New York, New Delhi, Sydney
Peshev, C., Peshev, D. & Popov, V. 2004: Fauna Bulgarica. Vol. 27 Mammalia. — BAS, Sofia. (In Bulgarian with English summary).
Petrov, B., Beshkov, V., Popgeorgiev, G. & Plachijski, D. 2004: Action plan for the tortoises in Bulgaria: 2005-2014. — BSPB-NMNH-BFB, Plovdiv. (In Bulgarian)
Preston, C., Jones, R. & Horton, N. 2017: Golden Eagle diet breadth and reproduction in relation to fluctuations in primary prey abundance in Wyoming’s Bighorn Basin. — Journal of Raptor Research 51: 334–346. https://doi.org/10.3356/JRR-16-39.1
Popgeorgiev, G. 2008: The effects of a large-scale fire on the demographic structure of a population of Hermann’s (Testudo hermanni boettgeri Mojsisovics, 1889) and Spur- thighed (Testudo graeca ibera Pallas, 1814) tortoises in eastern Rhodopes Mountains, Bulgaria. — Historia naturalis bulgarica 19: 115-127.
Roemer, G. & Collins, P. 2019: Community reorganization revealed by exploring shifts in the diet of an apex predator, the Golden Eagle Aquila chrysaetos, with stable isotopes and prey remains. — Ibis 66 https://doi.org/10.1111/ibi.12734
Rutz, C. & Bijlsma. R. 2006. Food-limitation in a generalist predator. — Proceedings of the Royal Society of London, Series B 273: 2069–2076. doi: 10.1098/rspb.2006.3507
Scherzinger, W. & Mebs, T. 2020: Die Eulen Europas: Biologie, Kennzeichen, Bestände. — Franckh-Kosmos Verlag, Stuttgart. (In German)
Schluter, D. 1981: Does the theory of optimal diets apply in complex environments? — American Naturalist 118: 139–147. https://doi.org/10.1086/283810
Seguin, J.-F., Bayle, P., Thibault, J.-C. , Torre, J. & Vigne, J.-D. 1998: A comparison of methods to evaluate the diet of Golden Eagles in Corsica. — Journal of Raptor Research 32: 314–318.
Sidiropoulos, L., Whitfield, D., Astaras, C., Vasilakis, D., Alivizatos, H. & Kati, V. 2022: Pronounced seasonal diet diversity expansion of Golden Eagles (Aquila chrysaetos) in Northern Greece during the Non-Breeding Season: The Role of Tortoises. — Diversity 14, 135. https://doi.org/10.3390/d14020135
Steenhof, K. & Kochert, M. 1988: Dietary responses of three raptor species to changing prey densities in a natural environment. — Journal of Animal Ecology 57: 37–48. https://doi.org/10.2307/4761
Steenhof, K., Kochert, M., McIntyre, C. & Brown, J. 2017: Coming to terms about describing Golden Eagle reproduction. — Journal of Raptor Research 51: 378–390. https://doi.org/10.3356/JRR-16-46.1
Stojanov, A., Tzankov, N. & Naumov, B. 2011: Die Amphibien und Reptilien Bulgariens. — Frankfurt am Main, Germany: Edition Chimaira (in German).
Sulkava, S., Huhtala, K., Rajala, P. & Tornberg, R. 1998: Changes in the diet of the Golden Eagle Aquila chrysaetos and small game populations in Finland in 1957-96. — Ornis Fennica 76: 1–16.
Takeuchi, T., Shiraki, S., Nashimoto, M., Matsuki, R., Abe, S. & Yatake, H. 2006: Regional and temporal variations in prey selected by Golden eagle Aquila chrysaetos during the nestling period in Japan. — Ibis 148: 79–87. https://doi.org/10.1111/j.1474-919X.2006.00495.x
Taylor, I. 1994: Barn Owls: predator-prey relationships and conservation. — Cambridge, UK: Cambridge University Press.
ter Braak, C. 1995: Ordination. — In Data Analysis in Community and Landscape Ecology (ed. Jongman R., ter Braak C. & van Tongeren O.): 91–173 Cambridge, UK: Cambridge Univ. Press. https://doi.org/10.1017/CBO9780511525575.007
Tofft, J. 2002: Zur Einwanderung und Bestandsituation von Seeadler (Haliaeetus albicilla) und Steinadler (Aquila chrysaetos) in Dänemark. — Corax 19: 79–84. (In German with English summary)
Tzankov, N. & Milchev, B. 2014: Tortoises as prey of three bird species in Bulgaria: Implications for tortoise reintroduction programs. — Herpetozoa 26: 173-177.
Watson, J. 2010: The Golden Eagle. 2nd edn. — London: T. & A.D. Poyser.
Watson, J. W. & Davies R. 2015: Comparative diets of nesting Golden Eagles in the Columbia Basin between 2007–2013 and the late 1970s. — Northwestern Naturalist 96: 81–86. https://doi.org/10.1898/NWN13-31.1
Whitfield, D., Reid, R., Haworth, P., Madders, M., Marquiss, M., Tingay, R. & Fielding, A. 2009: Diet specificity is not associated with increased reproductive performance of Golden Eagles Aquila chrysaetos in Western Scotland. — Ibis 151: 255–264. https://doi.org/10.1111/j.1474-919X.2009.00924.x
Downloads
Additional Files
Published
Versions
- 2022-10-07 (2)
- 2022-09-02 (1)
Issue
Section
License
Copyright (c) 2022 Boyan P. Milchev
This work is licensed under a Creative Commons Attribution 4.0 International License.
