Skip to main content
Log in

Studying the demographic drivers of an increasing Imperial Eagle population to inform conservation management

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Assessing whether conservation management actions are effective requires a good understanding of the demographic parameters that contribute to the population growth rate. Among the key demographic parameters influencing a population, immigration is one of the most difficult to measure empirically but may mask or accentuate the effects of conservation measures. We use an integrated population model to assess whether a population increase of a large raptor species can be explained by high fecundity and survival resulting from local conservation measures, or whether immigration may have contributed to population growth. We monitored the Eastern Imperial Eagle (Aquila heliaca) population in Bulgaria from 1998 to 2014, and tracked juveniles using satellite transmitters to estimate survival probability over the first three years of life. We used intensive territory monitoring of breeding birds to estimate survival probabilities and fecundity of birds older than 3 years. The Imperial Eagle population in Bulgaria increased by about 11 % per year between 1998 and 2014 (λ = 1.111, 95 % credible interval 1.076–1.156). While local conservation measures have succeeded in reducing nest loss and the mortality of adults (adult survival = 0.924; 0.887–0.955), high mortality of juveniles during their first year of life resulted in only 12 % of fledglings surviving to adult age. Based on these survival probabilities and the estimated fecundity of breeding pairs in Bulgaria (1.063; 0.932–1.203), some immigration may have contributed to the population growth in Bulgaria. Because the integrated population model accounts for all the uncertainty associated with disparate data sources, the estimated immigration rate was too imprecise (0.143–2.862 young birds per breeding pair) to quantify the relative importance of immigration. Future conservation measures for Imperial Eagles need to focus on improving the survival of juvenile birds, particularly the reduction of electrocution risk in Eastern Europe and the Middle East.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abadi F, Gimenez O, Arlettaz R, Schaub M (2010a) An assessment of integrated population models: bias, accuracy, and violation of the assumption of independence. Ecology 91:7–14

    Article  PubMed  Google Scholar 

  • Abadi F, Gimenez O, Ullrich B, Arlettaz R, Schaub M (2010b) Estimation of immigration rate using integrated population models. J Appl Ecol 47:393–400

    Article  Google Scholar 

  • Altwegg R, Jenkins A, Abadi F (2014) Nestboxes and immigration drive the growth of an urban Peregrine falcon Falco peregrinus population. Ibis 156:107–115

    Article  Google Scholar 

  • Angelov I, Hashim I, Oppel S (2013) Persistent electrocution mortality of Egyptian Vultures Neophron percnopterus over 28 years in East Africa. Bird Conserv Int 23:1–6

    Article  Google Scholar 

  • Besbeas P, Freeman SN, Morgan BJT, Catchpole EA (2002) Integrating mark–recapture–recovery and census data to estimate animal abundance and demographic parameters. Biometrics 58:540–547

    Article  CAS  PubMed  Google Scholar 

  • BirdLife International (2014) Species factsheet: Aquila heliaca. In. BirdLife International (2014) IUCN Red List for birds. http://www.birdlife.org/datazone/species/factsheet/22696048

  • Bowman TD, Schempf PF, Bernatowicz JA (1995) Bald Eagle survival and population dynamics in Alaska after the “Exxon Valdez” oil spill. J Wildl Manag 59:317–324

    Article  Google Scholar 

  • Brooks SP, Gelman A (1998) General methods for monitoring convergence of iterative simulations. J Comput Graph Stat 7:434–455

    Google Scholar 

  • Brooks S, King R, Morgan B (2004) A Bayesian approach to combining animal abundance and demographic data. Anim Biodivers Conserv 27:515–529

    Google Scholar 

  • Buehler DA, Fraser JD, Seegar JK, Therres GD (1991) Survival rates and population dynamics of bald eagles on Chesapeake Bay. J Wildl Manag 55:608–613

    Article  Google Scholar 

  • Carrete M, Donazar JA, Margalida A (2006) Density-dependent productivity depression in Pyrenean Bearded Vultures: implications for conservation. Ecol Appl 16:1674–1682

    Article  PubMed  Google Scholar 

  • Clark JS, Bjørnstad ON (2004) Population time series: process variability, observation errors, missing values, lags, and hidden states. Ecology 85:3140–3150

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Danko Š et al (2011) Conservation of eastern imperial eagle in the Slovak part of the Carpathian Basin—Results of the EU LIFE-Nature project (2003–2007). Acta Zool Bulg Suppl 3:71–78

    Google Scholar 

  • De Valpine P (2003) Better inferences from population-dynamics experiments using Monte Carlo state-space likelihood methods. Ecology 84:3064–3077

    Article  Google Scholar 

  • del Hoyo J, Elliott A, Sargatal J (eds) (1994) Handbook of the birds of the world, Vol. 2 New World Vultures to Guineafowl. Lynx Edicions, Barcelona

  • Demerdzhiev D, Gradev G, Stoychev S, Ivanov I, Petrov TH, Marin S (2011a) Increase of the population of the Eastern Imperial Eagle (Aquila heliaca) in Bulgaria. Acta Zool Bulg Suppl. 3:41–54

    Google Scholar 

  • Demerdzhiev D, Horváth M, Kovács A, Stoychev S, Karyakin I (2011b) Status and population trend of the Eastern Imperial Eagle (Aquila heliaca) in Europe in the period 2000–2010. Acta Zool Bulg Suppl 3:5–14

    Google Scholar 

  • Demerdzhiev D, Stoychev S, Dobrev D, Spasov S, Terziev N (2014) Conservation measures undertaken to improve the population status of eastern imperial eagle (Aquila heliaca) in Bulgaria. Slovak Raptor J 8:27–39

    Google Scholar 

  • Ferrer M, Bisson I (2003) Age and territory-quality effects on fecundity in the Spanish Imperial Eagle (Aquila adalberti). Auk 120:180–186

    Article  Google Scholar 

  • Ferrer M, Calderón J (1990) The Spanish imperial eagle Aquila adalberti C. L. Brehm 1861 in Doñana National Park (South West Spain): a study of population dynamics. Biol Conserv 51:151–161

    Article  Google Scholar 

  • Ferrer M, Donazar JA (1996) Density-dependent fecundity by habitat heterogeneity in an increasing population of Spanish Imperial Eagles. Ecology 77:69–74

    Article  Google Scholar 

  • Ferrer M, Hiraldo F (1991) Evaluation of management techniques for the Spanish Imperial Eagle. Wildl Soc Bull:436–442

  • Ferrer M, Hiraldo F (1992) Man-induced sex-biased mortality in the Spanish imperial eagle. Biol Conserv 60:57–60

    Article  Google Scholar 

  • Ferrer M, Penteriani V (2007) Supplementary feeding and the population dynamic of the Spanish imperial eagle. Ardeola 54:359–363

    Google Scholar 

  • Ferrer M, Otalora F, GarcÍa-Ruiz JM (2004) Density-dependent age of first reproduction as a buffer affecting persistence of small populations. Ecol Appl 14:616–624

    Article  Google Scholar 

  • Ferrer M, Newton I, Muriel R (2013) Rescue of a small declining population of Spanish imperial eagles. Biol Conserv 159:32–36

    Article  Google Scholar 

  • González LM, Margalida A, Sánchez R, Oria J (2006a) Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial eagle (Aquila adalberti). Biol Conserv 129:477–486

    Article  Google Scholar 

  • González LM et al (2006b) Effective natal dispersal and age of maturity in the threatened Spanish Imperial Eagle Aquila adalberti: conservation implications. Bird Study 53:285–293

    Article  Google Scholar 

  • Gradev GG et al (2011) First results of the tracking of Eastern Imperial Eagles (Aquila heliaca) tagged with radio-transmitters in Bulgaria. Acta Zool Bulg Suppl 3:21–28

    Google Scholar 

  • Grande JM et al (2009) Survival in a long-lived territorial migrant: effects of life-history traits and ecological conditions in wintering and breeding areas. Oikos 118:580–590

    Article  Google Scholar 

  • Hernández-Matías A, Real J, Pradel R (2011) Quick methods for evaluating survival of age-characterizable long-lived territorial birds. J Wildl Manag 75:856–866

    Article  Google Scholar 

  • Horal D (2011) Eastern Imperial Eagle (Aquila heliaca) in the Czech Republic. Acta Zool Bulg Suppl 3:55–59

    Google Scholar 

  • Horvath M, Kovacs A (2009) Imperial eagle (Aquila heliaca Savigny, 1809). In: Csorgo T et al. (ed) Magyar madarvonulasi atlasz (Hungarian bird migration atlas) Kossuth Kiado, Budapest, pp 231–234

  • Horváth M et al (2011) Population dynamics of the Eastern Imperial Eagle (Aquila heliaca) in Hungary between 2001 and 2009. Acta Zool Bulg Suppl 3:61–70

    Google Scholar 

  • Karyakin I, Kovalenko A, Novikova L (2006) The Imperial Eagle in the Volga–Ural sands: results of researches in 2006. Raptors Conserv 6:39–47

    Google Scholar 

  • Karyakin IV, Nikolenko EN, Levin AS, Kovalenko AV (2011) Eastern Imperial Eagle in Russia and Kazakhstan: population status and trends. Acta Zool Bulg Suppl 3:95–104

    Google Scholar 

  • Katzner TE (2003) Ecology and behavior of four coexisting eagle species at Naurzum Zapovednik, Kazakhstan. PhD Dissertation. Arizona State University, Tempe

  • Katzner TE, Bragin EA, Milner-Gulland E (2006) Modelling populations of long-lived birds of prey for conservation: a study of imperial eagles (Aquila heliaca) in Kazakhstan. Biol Conserv 132:322–335

    Article  Google Scholar 

  • Katzner T, Milner-Gulland EJ, Bragin E (2007) Using modeling to improve monitoring of structured populations: are we collecting the right data? Conserv Biol 21:241–252

    Article  PubMed  Google Scholar 

  • Katzner TE, Ivy JAR, Bragin EA, Milner-Gulland EJ, DeWoody JA (2011) Conservation implications of inaccurate estimation of cryptic population size. Anim Conserv 14:328–332

    Article  Google Scholar 

  • Kenward R (2001) A manual for wildlife radio tagging. Academic Press, London

    Google Scholar 

  • Kéry M, Schaub M (2012) Bayesian population analysis using WinBUGS. Academic Press, Oxford

    Google Scholar 

  • Kovács A et al (2008) Current efforts to monitor and conserve the Eastern Imperial Eagle Aquila heliaca in Hungary. Ambio 37:457–459

    Article  PubMed  Google Scholar 

  • Lehman RN, Kennedy PL, Savidge JA (2007) The state of the art in raptor electrocution research: a global review. Biol Conserv 136:159–174

    Article  Google Scholar 

  • López-López P, Ferrer M, Madero A, Casado E, McGrady M (2011) Solving man-induced large-scale conservation problems: the Spanish Imperial Eagle and power lines. PLoS ONE 6:e17196

    Article  PubMed Central  PubMed  Google Scholar 

  • Lunn DJ, Thomas A, Best N, Spiegelhalter D (2000) WinBUGS—a Bayesian modelling framework: concepts, structure, and extensibility. Stat Comput 10:325–337

    Article  Google Scholar 

  • Margalida A, Oro D, Cortés-Avizanda A, Heredia R, Donázar JA (2011) Misleading population estimates: Biases and consistency of visual surveys and matrix modelling in the endangered Bearded Vulture. PLoS ONE 6:e26784

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Margalida A, Colomer MÀ, Oro D (2014) Man-induced activities modify demographic parameters in a long-lived species: effects of poisoning and health policies. Ecol Appl 24:436–444

    Article  PubMed  Google Scholar 

  • McIntyre CL, Collopy MW, Lindberg MS (2006) Survival probability and mortality of migratory juvenile Golden Eagles from interior Alaska. J Wildl Manag 70:717–722

    Article  Google Scholar 

  • Murray DL (2006) On improving telemetry-based survival estimation. J Wildl Manag 70:1530–1543

    Article  Google Scholar 

  • Newton I (2010) Population ecology of raptors. T. & A. D. Poyser, London

    Google Scholar 

  • Ogada DL, Keesing F, Virani MZ (2012) Dropping dead: causes and consequences of vulture population declines worldwide. Ann N Y Acad Sci 1249:57–71

    Article  PubMed  Google Scholar 

  • Oppel S et al (2014) Assessing population viability while accounting for demographic and environmental uncertainty. Ecology 95:1809–1818

    Article  PubMed  Google Scholar 

  • Ortega E, Mañosa S, Margalida A, Sánchez R, Oria J, González LM (2009) A demographic description of the recovery of the Vulnerable Spanish imperial eagle Aquila adalberti. Oryx 43:113–121

    Article  Google Scholar 

  • Peniche G, Vaughan-Higgins R, Carter I, Pocknell A, Simpson D, Sainsbury A (2011) Long-term health effects of harness-mounted radio transmitters in red kites (Milvus milvus) in England. Vet Rec 169:311

    Article  CAS  PubMed  Google Scholar 

  • Petrov T, Stoychev S (2002) National action plan for the Imperial Eagle (A. heliaca). In: Globally threatened birds in Bulgaria: national action plans for conservation vol Part 1. BSPB-MOSV, Sofia, pp 132–161

  • Powell LA (2007) Approximating variance of demographic parameters using the delta method: a reference for avian biologists. Condor 109:949–954

    Article  Google Scholar 

  • R Development Core Team (2014) R: A language and environment for statistical computing. Available at: http://www.R-project.org/, Accessed 10 June 2014

  • Richardson CT, Miller CK (1997) Recommendations for protecting raptors from human disturbance: a review. Wildl Soc Bull 25:634–638

    Google Scholar 

  • Roth T, Amrhein V (2010) Estimating individual survival using territory occupancy data on unmarked animals. J Appl Ecol 47:386–392

    Article  Google Scholar 

  • Rudnick JA, Katzner TE, Bragin EA, Rhodes OE, Dewoody JA (2005) Using naturally shed feathers for individual identification, genetic parentage analyses, and population monitoring in an endangered Eastern imperial eagle Aquila heliaca population from Kazakhstan. Mol Ecol 14:2959–2967

    Article  CAS  PubMed  Google Scholar 

  • Schaub M, Abadi F (2011) Integrated population models: a novel analysis framework for deeper insights into population dynamics. J Ornithol 152:227–237

    Article  Google Scholar 

  • Schaub M, Gimenez O, Sierro A, Arlettaz R (2007) Use of integrated modeling to enhance estimates of population dynamics obtained from limited data. Conserv Biol 21:945–955

    Article  PubMed  Google Scholar 

  • Schaub M, Aebischer A, Gimenez O, Berger S, Arlettaz R (2010) Massive immigration balances high anthropogenic mortality in a stable eagle owl population: lessons for conservation. Biol Conserv 143:1911–1918

    Article  Google Scholar 

  • Schaub M, Jakober H, Stauber W (2013) Strong contribution of immigration to local population regulation: evidence from a migratory passerine. Ecology 94:1828–1838

    Article  PubMed  Google Scholar 

  • Sekercioglu ÇH et al (2011) Turkey’s globally important biodiversity in crisis. Biol Conserv 144:2752–2769

    Article  Google Scholar 

  • Soutullo A, López-López P, 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

    Article  Google Scholar 

  • Steenhof K, Bates KK, Fuller MR, Kochert MN, McKinley JO, Lukacs PM (2006) Effects of radiomarking on prairie falcons: attachment failures provide insights about survival. Wildl Soc Bull 34:116–126

    Article  Google Scholar 

  • Stoychev S et al (2004) Status of the Eastern Imperial Eagle (Aquila heliaca) in Bulgaria between 1994 and 2002. In: Chancellor RD, Meyburg BU (eds) Raptors worldwide Proceedings of the VI world conference on birds of prey and owls. World Working Group on Birds of Prey and Owls/MME BirdLife Hungary, Budapest, pp 653–660

  • Stoychev S, Demerdzhiev D, Petrov T (2013) National action plan for the conservation of Imperial Eagle (A. heliaca) in Bulgaria 2013–2022. Ministry of Environment and Water, Sofia, 76

  • Stoychev S, Demerdzhiev D, Spasov S, Meyburg B-U, Dobrev D (2014) Survival rate and mortality of juvenile and immature Eastern Imperial eagles from Bulgaria studied by satellite telemetry. Slovak Raptor J 8:53–60

    Google Scholar 

  • Sturtz S, Ligges U, Gelman A (2005) R2WinBUGS: a package for running WinBUGS from R. J Stat Softw 12:1–16

    Google Scholar 

  • Thiollay J-M (2006) The decline of raptors in West Africa: long-term assessment and the role of protected areas. Ibis 148:240–254

    Article  Google Scholar 

  • Vili N, Szabó K, Kovács S, Kabai P, Kalmár L, Horváth M (2013) High turnover rate revealed by non-invasive genetic analyses in an expanding Eastern Imperial Eagle population. Acta Zool Acad Sci Hung 59:279–295

    Google Scholar 

  • Virani MZ, Kendall C, Njoroge P, Thomsett S (2011) Major declines in the abundance of vultures and other scavenging raptors in and around the Masai Mara ecosystem, Kenya. Biol Conserv 144:746–752

    Article  Google Scholar 

  • Wade PR (2000) Bayesian methods in conservation biology. Conserv Biol 14:1308–1316

    Article  Google Scholar 

Download references

Acknowledgments

Many BSPB/BirdLife volunteers assisted in monitoring and conservation efforts, and we are grateful for the assistance by Ivaylo Angelov, Petar Iankov, Hristo Hristov, Nikolai Terziev, Tzeno Petrov, Georgi Popgeorgiev, Prof. Zlatozar Boev, Vladimir Trifonov, Nedko Nedyalkov, Atanas Demerdzhiev, Krasimira Demerdzhieva, Georgi Georgiev, Dimitar Plachiyski, Georgi Gerdzhikov, Vladimir Dobrev, Ivayla Klimentova, Vera Dyulgerska, Kiril Metodiev, Vanyo Angelov, Petya Karpuzova, Yanko Yankov, Aleksandar Georgiev, Vasilena Chobanova, Girgina Daskalova, Marin Kurtev, Valentin Velev, Tatiana Veleva, Georgi Manolov, Nikolay Dolapchiev, Petya Kurteva, Volen Arkumarev, Ivan Lafchiev, Dimitar Aygatov, Kiril Mihalev, Emil Yordanov. We are grateful to Gradimir Gradev, Ivaylo Klisurov, Simeon Marin and all the colleagues from Green Balkans for sharing information and collaboration in implementing conservation activities. Márton Horváth, András Kovács, Tamás Szitta, Gabor Papp and Magyar Madártani és Természetvédelmi Egyesület (BirdLife in Hungary) shared their expertise on raptor ecology, tree climbing, and preliminary results of genetic analyses. Dimitris Vasilakis from WWF Greece and Richard Cuthbert and Guy Anderson from the RSPB (Birdlife in UK), and Bernd-Ulrich Meyburg assisted with satellite tagging. Fitsum Abadi shared valuable thoughts on the integrated population model and we appreciate his help. Miguel Ferrer and an anonymous reviewer provided valuable comments on a previous draft of the manuscript. This work was funded by the Bulgarian Ministry of Environment and Waters, by the Bulgaria-Turkey cross-border cooperation programme under the project “Strandzha-Sakar—the realm of the eagles”, and by the LIFE + Program of the European Union under the project „Conservation of Imperial Eagle and Saker Falcon in key Natura 2000 sites in Bulgaria” LIFE07 NAT/BG/000068.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dimitar Demerdzhiev.

Additional information

Communicated by Stephen Garnett.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Demerdzhiev, D., Stoychev, S., Dobrev, D. et al. Studying the demographic drivers of an increasing Imperial Eagle population to inform conservation management. Biodivers Conserv 24, 627–639 (2015). https://doi.org/10.1007/s10531-014-0841-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-014-0841-0

Keywords

Navigation