Abstract
The survival rate is a key parameter for population management and the monitoring of populations. Thus, an analysis of survival rate variations and the factors influencing the same is essential for understanding population dynamics. Here, we study the factors determining the survival and the causes of mortality of the Eurasian eagle owl (Bubo bubo) in two Spanish Mediterranean populations (Murcia and Seville) where the species has a high population density and breeding success; yet its survival rates and the factors that affect them are unknown. Between 2003 and 2010, 63 breeding owls were captured and radio-tracked. Three monthly (quarterly) survival rates were estimated using known-fate models in the program MARK. The mean overall annual survival rate was 0.776 (95 % CI: 0.677, 0.875). We observed survival differences between sexes, and between the breeding and non-breeding periods, although no overwhelming support was found for any particular model. We concluded that (i) females have a lower survival rate than males, probably due to their larger home ranges, which increase the risk of mortality; (ii) the survival rates of both sexes were lower during the non-breeding period; and (iii) the causes of mortality differed significantly between the two populations, gunshot being the main cause in Seville and electrocution in Murcia.
Similar content being viewed by others
References
Altwegg R, Roulin A, Kestenholz M, Jenni L (2003) Variation and covariation in survival, dispersal, and population size in barn owls (Tyto alba). J Anim Ecol 72:391–399
Angelier F, Weimerskirch H, Dano S, Chastel O (2007) Age, experience and reproductive performance in a long-lived bird: a hormonal perspective. Behav Evol Sociobiol 61:611–621
Barrientos R, Ponce C, Palacín C, Martín CA, Martín B, Alonso JC (2012) Wire marking results in a small but significant reduction in avian mortality at power lines: a BACI designed study. PLoS ONE 7:e32569
Beltrán JF (1991) Temporal abundance pattern of the wild rabbit in Doñana, SW Spain. Mammalia 55:591–599
Boano G, Silvano F (2015) Adult survival probability in a recovered population of Scops Owls Otus scops. Ardea 103:145–153
Borda de Água L, Grilo C, Pereira HM (2014) Modeling the impact of road mortality on barn owl (Tyto alba) populations using age-structured models. Ecol Model 276:29–37
Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn, A practical information—theoretic approach. Springer, New York
Campioni L, Delgado MM, Lourenço R, Bastianelli G, Fernández N, Penteriani V (2013) Individual and spatio-temporal variations in the home range behaviour of a long-lived, territorial species. Oecologia 172:371–385
Cooch E, White GC (2016) Program MARK, 16th edn, A gentle introduction. Colorado State University, Fort Collins, http://www.cnr.colostate.edu/~gwhite/mark/mark.htm
Daunt F, Wanless S, Harris MP, Money L, Monaghan P (2007) Older and wiser: improvements in breeding success are linked to better foraging performance in European shags. Funct Ecol 21:561–567
Delgado MM, Penteriani V (2004) Gender determination of Eurasian eagle-owls (Bubo bubo) by morphology. J Raptor Res 38:375–377
Delibes-Mateos M, Redpath SM, Angulo E, Ferreras P, Villafuerte R (2007) Rabbits as a keystone species in southern Europe. Biol Conserv 137:149–156
Dinsmore SJ, Collazo JA (2003) The influence of body condition on local apparent survival of spring migrant sanderlings in coastal North Carolina. Condor 105:465–473
Donald PF (2007) Adult sex ratios in wild bird populations. Ibis 149:671–692
Dugger KM, Wagner F, Anthony RG, Olson GS (2005) The relationship between habitat characteristics and demographic performance of northern spotted owls in southern Oregon. Condor 107:863–878
Dugger KM, Forsman ED, Davis RJ et al (2016) The effects of habitat, climate and barred owls on the long-term population demographics of northern spotted owls. Condor 118:57–116
Fargallo JA, Martínez-Padilla J, Viñuela J, Blanco G, Torre I, Vergara P, De Neve L (2009) Kestrel-prey dynamic in a Mediterranean region: the effect of generalist predation and climatic factors. PLoS ONE 4:e4311
Ferrer M, Hiraldo F (1992) Man-induced sex-biased mortality in the Spanish imperial eagle. Biol Conserv 60:57–60
Fox J, Weisberg S (2011) An {R} Companion to applied regression, 2nd edn. Sage, Thousand Oaks CA
Francis CM, Saurola P (2004) Estimating components of variance in demographic parameters of tawny owls, (Strix aluco). Anim Biodivers Conserv 27:489–502
Franklin AB, Anderson DR, Gutiérrez RJ, Burnham KP (2000) Climate, habitat quality, and fitness in northern spotted owl populations in northwestern California. Ecol Monogr 70:539–590
Grande JM, Serrano D, Tavecchia G, Carrete M, Ceballos O, Díaz-Delgado R, Tella JL, Donázar JA (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
Grayson KL, Mitchell NJ, Monks JM, Keall SN, Wilson JN, Nelson NJ (2014) Sex ratio bias and extinction risk in an isolated population of tuatara (Sphenodon punctatus). PLoS ONE 9:e94214
Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
Grilo C, Sousa J, Ascensäo F, Matos H, Leitão I, Pinheiro P, Costa M, Bernardo J, Reto D, Lourenço R, Santos-Reis M, Revilla E (2012) Individual spatial responses towards roads: implications for mortality risk. PLoS ONE 7:e43811
Hakkarainen H, Korpimäki E, Laaksonen T, Nikula A, Suorsa P (2008) Survival of male tengmalm’s owls increases with cover of old forest in their territory. Oecologia 155:479–486
Hernández-Matías A, Real J, Pradel R, Ravayrol A, Vincent-Martin N (2011) Effects of age, territoriality and breeding on survival of Bonelli’s eagle Aquila fasciata. Ibis 153:846–857
Hylton RA, Frederick PC, De La Fuente TE, Spalding MG (2006) Effects of nestling health on postfledging survival of woods storks. Condor 108:97–106
Karell P, Ahola K, Karstinen T, Zolei A, Brommer JE (2009) Population dynamics in a cyclic environment: consequences of cyclic food abundance on tawny owl reproduction and survival. J Anim Ecol 78:1050–1062
Kenward RE (2001) A manual for wildlife radio tagging, 2nd edn. Academic, London
Korpimäki E (1992) Fluctuating food abundance determines the lifetime reproductive success of male tengmalm’s owls. J Anim Ecol 61:103–111
Lambertucci SA, Carrete M, Donázar JA, Hiraldo F (2012) Large-scale age-dependent skewed sex ratio in a sexually dimorphic avian scavenger. PLoS ONE 7:e46347
Le Gouar PJ, Schekkerman H, van der Jeugd HP, Boele A, van Harxen R, Fuchs P, Stroeken P, Van Noordwijk A (2011) Long-term trends in survival of a declining population: the case of the little owl (Athene noctua) in the Netherlands. Oecologia 166:369–379
Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypothesis using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118
Lehikoinen A, Ranta E, Pietiäinen H, Byholm P, Saurola P, Valkama J, Huitu O, Henttonen H, Korpimäki E (2011) The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species. Oecologia 165:349–355
León-Ortega M, González-Wangüemert M, Martínez JE, Calvo JF (2014) Spatial patterns of genetic diversity in Mediterranean eagle owl Bubo bubo populations. Ardeola 61:45–62
Leyrer J, Lok T, Brugge M, Spaans B, Sandercock BK, Piersma T (2013) Mortality within the annual cycle: seasonal survival patterns in Afro-Siberian red knots Calidris canutus canutus. J Ornithol 154:933–943
Liker A, Székely T (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59:890–897
Liker A, Freckleton RP, Székely T (2014) Divorce and infidelity are associated with skewed adult sex ratios in birds. Curr Biol 24:880–884
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
Lourenço R (2006) The food habits of Eurasian eagle owls in Southern Portugal. J Raptor Res 40:297–300
Marchesi L, Sergio F, Pedrini P (2002) Costs and benefits of breeding in human-altered landscapes for the eagle owl Bubo bubo. Ibis 144:E164–E177
Margalida A, Colomer MA, 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
Martín CA, Alonso JC, Alonso JA, Palacín C, Magaña M, Martín B (2007) Sex-biased juvenile survival in a bird with extreme size dimorphism, the great bustard Otis tarda. J Avian Biol 38:335–346
Martínez JE, Calvo JF (2001) Diet and breeding success of eagle owl in southeastern Spain: effect of rabbit haemorrhagic disease. J Raptor Res 35:259–262
Martínez JA, Zuberogoitia I, Alonso R (2002) Rapaces nocturnas. Guía para la determinación de la edad y el sexo en las estrigiformes ibéricas. Monticola, Madrid
Martínez JA, Martínez JE, Mañosa S, Zuberogoitia I, Calvo JF (2006) How to manage human-induced mortality in the eagle owl Bubo bubo. Bird Conserv Int 16:265–278
Martínez-Fernández J, Esteve MA, Calvo JF (2000) Environmental and socioeconomic interactions in the evolution of traditional irrigated lands: a dynamic system model. Hum Ecol 28:279–299
Martínez-Fernández J, Esteve MA, Baños I, Carreño F, Moreno A (2013) Dynamics and sustainability of Mediterranean traditional irrigated lands. In: Quaddus MA, Siddique MAB (eds) Handbook of sustainable development planning, 2nd edn. Edward Elgar, Cheltenham, UK, pp 245–274
Moleón M, Bautista J, Garrido JR, Martín-Jaramillo J, Ávila E, Madero A (2007) La corrección de tendidos eléctricos en áreas de dispersión de Águila-azor perdicera: efectos potenciales positivos sobre la comunidad de rapaces. Ardeola 54:319–325
Moleón M, Sánchez-Zapata JA, Gil-Sánchez JM, Ballesteros-Duperón E, Barea-Azcón JM, Virgós E (2012) Predator–prey relationships in a Mediterranean vertebrate system: bonelli’s eagles, rabbits and partridges. Oecologia 168:679–689
Mora O, Delgado MM, Penteriani V (2010) Secondary sex ratio in Eurasian eagle-owls: early-breeding females produce more daughters. J Raptor Res 44:62–65
Moyes K, Coulson T, Morgan BJT, Donald A, Morris SJ, Clutton-Brock TH (2006) Cumulative reproduction and survival costs in female red deer. Oikos 115:241–252
Newton I, McGrady MJ, Oli MK (2016) A review of survival estimates for raptors and owls. Ibis 158:227–248
Olsson V (1997) Breeding success, dispersal, and long-term changes in a population of eagle owls Bubo bubo in southeastern Sweden 1952-1996. Ornis Svec 7:49–60
Pavón-Jordán D, Karell P, Ahola K, Kolunen H, Pietiäinen H, Karstinen T, Brommer JE (2013) Environmental correlates of annual survival differ between two ecologically similar and congeneric owls. Ibis 155:823–834
Penteriani V, Gallardo M, Roche P (2002) Landscape structure and food supply affect Eurasian eagle owl (Bubo bubo) density and breeding performance: a case of intra-population heterogeneity. J Zool 257:365–372
Penteriani V, Delgado MM, Maggio C, Aradis A, Sergio F (2005) Development of chicks and pre-dispersal behaviour of young in the Eagle owl Bubo bubo. Ibis 147:155–168
Penteriani V, Delgado MM, Alonso-Álvarez C, Sergio F (2007) The importance of visual cues for nocturnal species: eagle owls signal by badge brightness. Behav Ecol 18:143–147
Penteriani V, Delgado MM, Pérez-García JM, Botella F, García S, Sánchez-Zapata JA, León-Ortega M, Martínez JE, Calvo JF, Ortego J, Penteriani G, Melletti M, Krugersberg I, Talavera OM (2010) Sex allocation from an owl perspective: clutch order could determine brood sex to reduce sibling aggression in the eagle owl Bubo bubo. Ornis Fenn 87:135–143
Penteriani V, Kuparinen A, Delgado MM, Lourenço R, Campioni L (2011) Individual status, foraging effort and need for conspicuousness shape behavioural responses of a predator to moon phases. Anim Behav 82:413–420
Pollock KH, Winterstein SR, Bunck CM, Curtis PD (1989) Survival analysis in telemetry studies: the staggered entry design. J Wildl Manag 53:7–15
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Available at: http://www.R-project.org/
Robinson RA, Kew JJ, Kew AJ (2010) Survival of suburban blackbirds Turdus merula varies seasonally but not by sex. J Avian Biol 41:83–87
Rubolini D, Bassi E, Bogliani G, Galeotti P, Garavaglia R (2001) Eagle owl Bubo bubo and power line interactions in the Italian Alps. Bird Conserv Int 11:319–324
Rutz C, Bijlsma RB (2006) Food limitation in a generalist predator. Proc R Soc B 273:2069–2076
Rymešová D, Šmilauer P, Šálek M (2012) Sex- and age-biased mortality in wild grey partridge Perdix perdix populations. Ibis 154:815–824
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
Seamans ME, Gutiérrez RJ, May CA (2002) Mexican spotted owl (Strix occidentalis) population dynamics: influence of climatic variation on survival and reproduction. Auk 119:321–334
Sergio F, Marchesi L, Pedrini P, Ferrer M, Penteriani V (2004) Electrocution alters the distribution and density of a top predator, the eagle owl Bubo bubo. J Appl Ecol 41:836–845
Severinghaus LL, Rothery P (2001) The survival rate of lanyu scops owls (Otus elegans botelensis). Ibis 143:540–546
Sibly RM, Hone J (2002) Population growth rate and its determinants: an overview. Philos Trans R Soc Lond B Biol Sci 357:1153–1170
Smith JG, Griffiths AD, Brook BW (2010) Survival estimation in a long-lived lizarz: radio-tracking of Varanus mertensi. Popul Ecol 52:243–247
Smith JB, Jenks JA, Grovenburg TW, Klaver RW (2014) Disease and predation: sorting out causes of a bighorn sheep (Ovis canadiensis) decline. PLoS ONE 92:e88271
Sunde P (2005) Predators control post-fledging mortality in tawny owls (Strix aluco). Oikos 110:461–472
Székely T, Liker A, Freckleton RP, Fitchel C, Kappeler PM (2014) Sex-biased survival predict adult sex ratio variation in wild birds. Proc R Soc B 281:20140342
Tavecchia G, Pradel R, Boy V, Johnson AR, Cezilly F (2001) Sex- and age-related variation in survival and cost of first reproduction in greater flamingos. Ecology 82:165–174
Tenan S, Adrover J, Muñoz-Navarro A, Sergio F, Tavecchia G (2012) Demographic consequences of poison-related mortality in a threatened bird of prey. PLoS ONE 7:e49187
Thorup K, Pedersen D, Sunde P, Jacobsen LB, Rahbek C (2013) Seasonal survival rates and causes of mortality of little owls in Denmark. J Ornithol 154:183–190
Valkama J, Saurola P, Lehikoinen A, Lehikoinen E, Piha M, Sola P, Velmala W (2015) The Finnish Bird Ringing Atlas, Volume II / Suomen Rengastusatlas II. Finnish Museum of Natural History, Helsinki
Varmer DM, Hepp GR, Bielefeld RR (2014) Annual and seasonal survival of adult female Mottled Ducks in southern Florida, USA. Condor 116: 134–143
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–138
Wisdom MJ, Mills LS, Doak DF (2000) Life stage simulation analysis: estimating vital-rate effects on population growth for conservation. Ecology 81:628–641
Acknowledgments
We are very grateful to Eloy Peréz, José Alfonso Lacalle, Letizia Campioni, Chiara Bettega, Rui Lourenço and other collaborators for their help on the field work. We thank Encarni Montoya, María Victoria Jiménez-Franco and Silvia Villaverde for their unconditional support and comments. The suggestions and comments of Jari Valkama and two anonymous reviewers considerably helped to improve the manuscript. The Asociación de Naturalistas del Sureste (ANSE) is also acknowledged for partial financial support in the Murcia area. The Spanish Ministry of Economy and Competitiveness (CGL2012–33240; FEDER co-financing) funded this study in the Seville area. The research adheres to the legal requirements of the country where it has been carried out.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
León-Ortega, M., Delgado, M., Martínez, J.E. et al. Factors affecting survival in Mediterranean populations of the Eurasian eagle owl. Eur J Wildl Res 62, 643–651 (2016). https://doi.org/10.1007/s10344-016-1036-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10344-016-1036-7