Functional responses to changes in rabbit abundance: is the eagle owl a generalist or a specialist predator?

Abstract

How foraging behaviour of predators is influenced by prey abundance is often not clear. Predators may behave as generalist or specialist depending on the relationship between the predator feeding behaviour and prey abundance, known as functional response. The European rabbit (Oryctolagus cuniculus) is a key species for most Iberian vertebrate predators, especially for large raptors such as the eagle owl (Bubo bubo). The eagle owl functional response was analysed in central Iberian Peninsula by fitting different models (null, linear, two asymptotic and two sigmoidal models) between rabbit abundance and rabbit consumption by the eagle owl. Rabbit consumption increased as did its abundance until reaching an asymptote. Rabbit-consumed biomass better fitted to a type II functional response (convex, typical of specialist predators), whereas rabbit frequency in eagle owl diet better fitted to a type III functional response (sigmoidal, typical of generalist predators). Trophic diversity increased as rabbit abundance decreased. The consumption of other prey, such as Iberian hare (Lepus granatensis) and medium-size birds (mainly galliformes and columbiformes), increased as rabbit abundance decreased. The eagle owl is highly dependent on rabbits in central Spain, even at low rabbit abundance. In this situation, the eagle owl diversifies its diet, making it difficult to define the eagle owl as a specialist or as a generalist predator. Therefore, the eagle owl in the centre of the Iberian Peninsula should be rather considered as a facultative predator on wild rabbits.

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References

  1. Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai, Kiado, Budapest, Hungary, pp 267–281

    Google Scholar 

  2. Andersson M, Erlinge S (1977) Influence of predation on rodent populations. Oikos 29:591–597

    Article  Google Scholar 

  3. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer–Verlag, New York

    Google Scholar 

  4. Crawley MJ (2007) The R book. Wiley, Chichester

    Google Scholar 

  5. Day MG (1966) Identification of hair and feather remains in the gut and faeces of stoats and weasels. J Zool 148:201–217

    Article  Google Scholar 

  6. 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

    Article  Google Scholar 

  7. Delibes-Mateos M, Delibes M, Ferreras P, Villafuerte R (2008a) Key role of European rabbits in the conservation of the western Mediterranean basin hotspot. Conserv Biol 22:1106–1117

    Article  PubMed  Google Scholar 

  8. Delibes-Mateos M, Fernandez-de-Simon J, Ferreras P, Villafuerte R (2008b) Feeding responses of the red fox (Vulpes vulpes) to different wild rabbit (Oryctolagus cuniculus) densities: a regional approach. Eur J Wildl Res 54:71–78

    Article  Google Scholar 

  9. Díaz-Ruiz F, Buenestado F, Fernandez-de-Simon J, Ferreras P (2010) First record of rabbit carrion consumption by Eurasian eagle-owl (Bubo bubo) on the Iberian Peninsula. J Raptor Res 44:78–79

    Article  Google Scholar 

  10. Donázar J (1989) Variaciones geográficas y estacionales en la dieta del búho real (Bubo bubo) en Navarra. Ardeola 36:25–39

    Google Scholar 

  11. Donázar J, Ceballos O (1989) Selective predation by eagle owls Bubo bubo on rabbits Oryctolagus cuniculus: age and sex preferences. Ornis Scand 20:117–122

    Article  Google Scholar 

  12. Donázar J, Hiraldo F, Delibes M, Estrella RR (1989) Comparative food habits of the eagle owl Bubo bubo and the great horned owl Bubo virginianus in six Palearctic and Nearctic biomes. Ornis Scand 20:298–306

    Article  Google Scholar 

  13. Dunning JB (1993) CRC handbook of avian body masses. CRC Press, Boca Raton, FL

    Google Scholar 

  14. Fedriani JM, Ferreras P, Delibes M (1998) Dietary response of the Eurasian badger, Meles meles, to a decline of its main prey in the Doñana national park. J Zool 245:214–218

    Google Scholar 

  15. Fernandez-de-Simon J, Díaz-Ruiz F, Villafuerte R, Delibes-Mateos M, Ferreras P (2011a) Assessing predictors of pellet persistence in European rabbits Oryctolagus cuniculus: towards reliable population estimates from pellet counts. Wildl Biol 17:317–325

    Article  Google Scholar 

  16. Fernandez-de-Simon J, Díaz-Ruiz F, Cirilli F, Sánchez-Tortosa F, Villafuerte R, Delibes-Mateos M, Ferreras P (2011b) Towards a standardized index of European rabbit abundance in Iberian Mediterranean habitats. Eur J Wildl Res 57:1091–1100

    Article  Google Scholar 

  17. Fernandez-de-Simon J, Díaz-Ruiz F, Cirilli F, Sánchez-Tortosa F, Villafuerte R, Ferreras P (2014) Role of prey and intraspecific density dependence on the population growth of an avian top predator. Acta Oecol 60:1–6

    Article  Google Scholar 

  18. Ferrer M, Negro JJ (2004) The near extinction of two large European predators: super specialists pay a price. Conserv Biol 18:344–349

    Article  Google Scholar 

  19. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  20. Gallego L, Alemany A (1985) Vertebrados Ibéricos, 6. Roedores y lagomorfos. Antigua Imprenta Soler, Palma de Mallorca

    Google Scholar 

  21. Gurnell J, Flowerdew JR (2006) Live trapping small mammals: a practical guide. The Mammal Society, London

    Google Scholar 

  22. Herrera CM, Hiraldo F (1976) Food-niche and trophic relationships among European owls. Ornis Scand 7:29–41

    Article  Google Scholar 

  23. Hiraldo F, Andrada J, Parreño FF (1975) Diet of the eagle owl (Bubo bubo) in Mediterranean Spain. Doñana Acta Vertebr 2:161–177

    Google Scholar 

  24. Hiraldo F, Parreño FF, Andrada V, Amores F (1976) Variations in the food habits of the European eagle owl (Bubo bubo). Doñana Acta Vertebr 3:137–156

    Google Scholar 

  25. Holling CS (1959) The functional components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can Entomol 91:293–320

    Article  Google Scholar 

  26. Hughes RN (1979) Optimal diets under the energy maximization premise: the effects of recognition time and learning. Am Nat 209–221

  27. Krebs CJ (1989) Ecological methodology. Harper and Row, New York, USA

    Google Scholar 

  28. Lourenço OR (2006) The food habits of Eurasian eagle owl in southern Portugal. J Raptor Res 40:297–300

    Article  Google Scholar 

  29. Lourenço R, Santos SM, Rabaça JE, Penteriani V (2011) Superpredation patterns in four large European raptors. Popul Ecol 53:175–185

    Article  Google Scholar 

  30. Mañosa S (1994) Goshawk diet in a Mediterranean area of northeaestern Spain. J Raptor Res 28:84–94

    Google Scholar 

  31. Marchesi L, Pedrini P, Sergio F (2002) Biases associated with diet study methods in the eagle owl. J Raptor Res 36:11–16

    Google Scholar 

  32. Martínez JA, Zuberogoitia I (2001) The response of the eagle owl (Bubo bubo) to an outbreak of the rabbit haemorrhagic disease. J Ornithol 142:204–211

    Article  Google Scholar 

  33. MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:611–617

    Article  Google Scholar 

  34. Mikkola H (1983) Owls of Europe. Poyser, Berkhamsted

    Google Scholar 

  35. 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

    Article  PubMed  Google Scholar 

  36. Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 335–354

  37. O’Donoghue M, Boutin S, Krebs CJ, Zuleta G, Murria DL, Hofer EJ (1998) Functional responses of coyotes and lynx to the snowshoe hare cycle. Ecology 79:1193–1208

    Article  Google Scholar 

  38. Olsson V (1979) Studies on a population of eagle owls. Viltrevy 11:1–99

    Google Scholar 

  39. Ontiveros D, Pleguezuelos JM, Caro J (2005) Prey density, prey detectability and food habits: the case of Bonelli’s eagle and the conservation measures. Biol Conserv 123:19–25

    Article  Google Scholar 

  40. Ortego J (2007) Consequences of eagle owl nest-site habitat preference for breeding performance and territory stability. Ornis Fenn 84:78–90

    Google Scholar 

  41. Penteriani V, Sergio F, Delgado MM, Gallardo M, Ferrer M (2005) Biases in population diet studies due to sampling in heterogeneous environments: a case study with the eagle owl. J Field Ornithol 76:237–244

    Article  Google Scholar 

  42. Penteriani V, Delgado MDM, Bartolommei P, Maggio C, Alonso-Alvarez C, Holloway GJ (2008) Owls and rabbits: predation against substandard individuals of an easy prey. J Avian Biol 39:215–221

    Article  Google Scholar 

  43. Pérez-Mellado V (1980) Alimentación del búho real (Bubo bubo L.) en España Central. Ardeola 25:93–112

    Google Scholar 

  44. Purroy F, Varela J (2003) Guía de los mamíferos de España. Península, Baleares y Canarias. Lynx Edicions

  45. R Development Core Team (2012) R: a language and environment for statistical computing. Austria R Foundation for Statistical Computing, Vienna

    Google Scholar 

  46. Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer Science & Business Media, New York

    Google Scholar 

  47. Schluter D (1981) Does the theory of optimal diets apply in complex environments?. Am Nat 139–147

  48. Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404

    Article  Google Scholar 

  49. Serrano D (1998) Diferencias interhabitat en la alimentación del búho real (Bubo bubo) en el valle medio del Ebro (NE de España): efecto de la disponibilidad de conejo (Oryctolagus cuniculus). Ardeola 45:47–53

    Google Scholar 

  50. Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18:1–35

    Article  Google Scholar 

  51. Soriguer RC (1981) Estructura de sexos y edades de una población de conejo (Oryctolagus cuniculus) de Andalucía occidental. Doñana Acta Vertebr 8:225–236

    Google Scholar 

  52. Steenhof K, Kochert MN (1988) Dietary responses of three raptor species to changing prey densities in a natural environment. J Anim Ecol 37–48

  53. Teerink BJ (1991) Hair of west-European mammals. Cambridge University Press, Cambridge

    Google Scholar 

  54. Terraube J, Arroyo B, Madders M, Mougeot F (2010) Diet specialization and foraging efficiency under fluctuating vole abundance: a comparison between generalist and specialist avian predators. Oikos 120:234–244

    Article  Google Scholar 

  55. Trexler JC, McCulloch CE, Travis J (1988) How can the functional response best be determined? Oecologia 76:206–214

    Article  Google Scholar 

  56. Turchin P (2003) Complex population dynamics: a theoretical/empirical synthesis. Princeton University Press, Princeton, New York

    Google Scholar 

  57. Villafuerte R, Viñuela J (1999) Size of rabbits consumed by black kites increased after rabbit epizootic. Mammal Rev 29:261–264

    Article  Google Scholar 

  58. Williams RL, Goodenough AE, Stafford R (2012) Statistical precision of diet diversity from scat and pellet analysis. Ecol Inform 7:30–34

    Article  Google Scholar 

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Acknowledgments

This study is a partial result of CGL2005–02340, CGL2009–10741, and CGL2013-43197 projects, from I+D National Plan funded by the Spanish Ministry of Science and Innovation and EU–FEDER funds. J. Fernandez-de-Simon benefitted from a FPI PhD scholarship (BES–2006–12562) funded by the Spanish Ministry of Science and Innovation and the European Social Fund. J. Fernandez-de-Simon and F. Diaz-Ruiz are currently holding a postdoctoral fellowship from Junta de Castilla-La Mancha and the European Social Fund (Operational Programme FSE 2007/2013). We are indebted to the landowners of estates where field work was carried out and to the staff of Lagunas de Ruidera Natural Park, especially Manolo López for his support during field work. We thank Pedro Peiro for providing rabbit biometric data for body weight estimation of rabbit remains in owl pellets. We are indebted with many people that helped in field work, being mainly F. Buenestado, A. Camarero, J. Cañadilla, F. Castro, M. Delibes-Mateos, C. Ferreira, J.L. García-Moreno, L.E. Mínguez, E. Ramírez and C.A. Ríos-Saldaña, and C. Rouco. R.P. Pech, G. Forrester and C. Jones (Landcare Research, NZ) provided useful knowledge for fitting non-linear models in R.

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Correspondence to Jorge Tobajas.

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Tobajas, J., Fernandez-de-Simon, J., Díaz-Ruiz, F. et al. Functional responses to changes in rabbit abundance: is the eagle owl a generalist or a specialist predator?. Eur J Wildl Res 62, 85–92 (2016). https://doi.org/10.1007/s10344-015-0976-7

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Keywords

  • Alternative prey
  • Bubo bubo
  • Diet analysis
  • Feeding behaviour
  • Oryctolagus cuniculus
  • Predator-prey relationships