Skip to main content
SpringerLink
Log in

Is the interaction between rabbit hemorrhagic disease and hyperpredation by raptors a major cause of the red-legged partridge decline in Spain?

  • Original Paper
  • Published:
European Journal of Wildlife Research Aims and scope Submit manuscript

Abstract

Hyperpredation can be described as a restrictive case of apparent competition where an increased number of primary prey species indirectly induces the decrease of the secondary prey species through numerical response of predators to the primary prey dynamics. It has been proposed that rabbit hemorrhagic disease (RHD), which decimated populations of European wild rabbit (Oryctolagus cuniculus) in Spain, led to prey switching by raptors towards red-legged partridges (Alectoris rufa) causing declines in their populations as a peculiar case of hyperpredation.

We have reviewed field studies that disagree with estimates (based on bag records) of recent increases of rabbit and partridge numbers in Spain. Because of an increase in releases of farm-reared animals, there is doubt about the use of bag records to accurately estimate population trends in recent decades. We also provide new data and discuss some analytical considerations related to the temporal and spatial scales that might affect the interpretation of data. Finally, we discuss why studies associated with raptor food habits, predator population dynamics and predator distribution suggest that diet data are not sufficient to link patterns and processes. Although we agree that the RHD outbreak has markedly affected rabbit populations, which has indirectly affected many other species in the Iberian Peninsula, we consider that hyperpredation mediated by raptors has not been clearly demonstrated. In contrast, endorsing the hypothesis of raptor-mediated hyperpredation without sufficient proof may have conflictive consequences if we consider the increased persecution of raptors in recent decades in Spain.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Angulo E (2003) Factores que Afectan a la Distribución y Abundancia del Conejo en Andalucía. PhD Thesis, Universidad Complutense de Madrid.

  • Arroyo, B. & Beja, P. (2002) Impact of hunting management practices on biodiversity. Report on Workpackage 2 of the European Project REGHAB No. EKV–2000–00637.

  • Blanco-Aguiar JA (2007) Variación Espacial en la Biología de la Perdiz Roja (Alectoris rufa): Una Aproximación Multidisciplinar. PhD Thesis, Universidad Complutense de Madrid.

  • Blanco-Aguiar JA, Virgós E, Villafuerte R (2004) Perdiz roja, Alectoris rufa. In: Madroño A, González C, Atienza JC (eds), Libro Rojo de las Aves de España. Dirección General para la Biodiversidad-SEO/Birdlife, pp. 182–185.

  • Blanco-Aguiar JA, González-Jara P, Ferrero ME, Sánchez-Barbudo I, Virgós E, Villafuerte R, Dávila JA (2008) Assessment of game restocking contributions to anthropogenic hybridization: the case of the Iberian red-legged partridge. Anim Conserv 11:535–545

    Article  Google Scholar 

  • Buenestado FJ, Ferreras P, Delibes-Mateos M, Tortosa FS, Blanco-Aguiar JA, Villafuerte R (2008) Habitat selection and home range size of red-legged partridges in Spain. Agric Ecosyst Environ 126:158–162

    Article  Google Scholar 

  • Buenestado FJ, Ferreras P, Blanco-Aguiar JA, Tortosa FS, Villafuerte R (2009) Survival and causes of mortality among wild red-legged partridges Alectoris rufa in southern Spain: Implications for conservation. Ibis 151:720–730

    Article  Google Scholar 

  • Carneiro M, Blanco-Aguiar JA, Villafuerte R, Ferrand N, Nachman MW (2010) Speciation in the european rabbit (Oryctolagus cuniculus): islands of differentiation on the X chromosome and autosomes. Evolution 64:3443–3460

    Article  PubMed  Google Scholar 

  • Casas F, Viñuela J (2010) Agricultural practices or game management: which is the key to improve red-legged partridge nesting success in agricultural landscapes? Environ Conserv 37:177–186

    Article  Google Scholar 

  • Cattadori IM, Haydon DT, Thirgood SJ, Hudson PJ (2003) Are indirect measures of abundance a useful index of population density? The case of red grouse harvesting. Oikos 100:439–446

    Article  Google Scholar 

  • Courchamp F, Langlais M, Sugihara G (2000) Rabbits killing birds: modelling the hyperpredation process. J Anim Ecol 69:154–164

    Article  Google Scholar 

  • 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 

  • Delibes-Mateos M, Fernandez de Simón J, Villafuerte R, Ferreras P (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 

  • Delibes-Mateos M, Ferreras P, Villafuerte R (2008c) Rabbit populations and game management: the situation after 15 years of rabbit haemorrhagic disease in central-southern Spain. Biodivers Conserv 17:559–574

    Article  Google Scholar 

  • Delibes-Mateos M, Farfán MA, Olivero J, Márquez AL, Vargas JM (2009a) Long-term changes in game species over a long period of transformation in the Iberian Mediterranean Landscape. Environ Manag 43:1256–1268

    Article  Google Scholar 

  • Delibes-Mateos M, Ferreras P, Villafuerte R (2009b) European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula. Mamm Rev 39:124–140

    Article  Google Scholar 

  • Díaz-Sánchez S., Mateo Moriones A, Casas F. and Höfle U. (2011) Prevalence of Escherichia coli, Salmonella sp. and Campylobacter sp. in the intestinal flora of farm-reared, restocked and wild red-legged partridges (Alectoris rufa): is restocking using farm-reared birds a risk? Eur J Wildl Res DOI: 10.1007/s10344-011-0547-5

  • Fernández C (1993) Effect of the viral haemorrhagic pneumonia of the wild rabbit on the diet and breeding success of the golden eagle Aquila chrysaetos (L.). Rev Ecol Terre Vie 48:323–329

    Google Scholar 

  • Ferreira C, Paupério J, Alves PC (2010) The usefulness of field data and hunting statistics in the assessment of wild rabbit (Oryctolagus cuniculus) status in Portugal. Wildl Res 37:223–229

    Article  Google Scholar 

  • Ferrero ME, Blanco-Aguiar JA, Lougheed SC, Sánchez-Barbudo I, De Nova PJG, Villafuerte R, Dávila JA (2011) Phylogeography and genetic structure of the red-legged partridge (Alectoris rufa): more evidence for refugia within the Iberian glacial refugium. Mol Ecol 20:2628–2642

    Article  PubMed  Google Scholar 

  • Fewster RM, Buckland ST, SiriwardenaGM BSR, Wilson JD (2000) Analysis of population trends for farmland birds using generalized additive models. Ecology 81:1970–1984

    Article  Google Scholar 

  • Gobierno de Navarra (2006) Memoria de Actividades 2006: Seguimiento Caza y Pesca. Departamento de Desarrollo Rural y Medio Ambiente, Gobierno de Navarra

    Google Scholar 

  • Gortázar C, Villafuerte R, Martín M (2000) Success of traditional restocking of red-legged partridge for hunting purposes in areas of low density of northeast Spain Aragon. Z Jagdwiss 46:23–30

    Article  Google Scholar 

  • Gregory RD, Strien AV, Vorisek P, Meyling AWG, Noble DG, Foppen RPB, Gibbons DW (2005) Developing indicators for European birds. Phil Trans R Soc B Biol Sci 360:269–288

    Article  Google Scholar 

  • Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Margalida A, Gonzalez LM, Sanchez R, Oria J, Prada L, Caldera J, Aranda A, Molina JI (2007) A long-term large-scale study of the breeding biology of the Spanish imperial eagle (Aquila adalverti). J Ornithol 148:309–322

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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 

  • Moleón M, Almaraz P, Sánchez-Zapata JA (2008) An emerging infectious disease triggering large-scale hyperpredation. PLoS One 3:e2307. doi:10.1371/journal.pone.0002307

    Article  PubMed  Google Scholar 

  • Newton I (1998) Population limitation in birds. Academic Press, London

    Google Scholar 

  • 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 

  • SEO/BIRDLIFE (2006) Monitoring common breeding birds in Spain. The SACRE Programme Report 1996–2005. SEO/BIRDLIFE

  • Serrano D (2000) Relationship between raptors and rabbits in the diet of eagle owls in southwestern Europe: competition removal or food stress? J Raptor Res 34:305–310

    Google Scholar 

  • Sinclair ARE, Pech RP (1996) Density dependence, stochasticity, compensation and predator regulation. Oikos 75:164–173

    Article  Google Scholar 

  • Smith AP, Quin DG (1996) Patterns and causes of extinction and decline in Australian conilunire rodents. Biol Conser 77:243–267

    Article  Google Scholar 

  • Tella JL, Mañosa S (1993) Eagle owl predation on Egyptian vulture and northern goshawk—possible effect of a decrease in European rabbit availability. J Raptor Res 27:111–112

    Google Scholar 

  • Valkama J, Korpimäki E, Arroyo B, Beja P, Bretagnolle V, Bro E, Kenward R, Mañosa S, Redpath SM, Thirgood S, Viñuela J (2005) Birds of prey as limiting factors of gamebird populations in Europe: a review. Biol Rev 80:171–203

    Article  PubMed  Google Scholar 

  • van Strien AJ, Pannekoek J, Gibbons DW (2001) Indexing European bird population trends using results of national monitoring schemes: a trial of a new method. Bird Study 48:200–213

    Article  Google Scholar 

  • Villafuerte R, Viñuela J, Blanco JC (1998) Extensive predator persecution caused by population crash in a game species: the case of red kites and rabbits in Spain. Biol Conserv 84:181–188

    Article  Google Scholar 

  • Villanúa D, Pérez-Rodríguez L, Casas F, Alzaga V, Acevedo P, Viñuela J, Gortázar C (2008) Sanitary risks of red-legged partridge releases: introduction of parasites. Eur J Wildl Res 54:199–204

    Article  Google Scholar 

  • Viñuela J, Veiga JP (1992) Importance of rabbits in the diet and reproductive success of black kites in southwestern Spain. Ornis Scandinavica 23:132–138

    Article  Google Scholar 

  • Virgós E, Cabezas-Díaz S, Lozano J (2007) Is the wild rabbit (Oryctolagus cuniculus) a threatened species in Spain? Sociological constraints in the conservation of species. Biodivers Conserv 16:3489–3504

    Article  Google Scholar 

  • Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397

    Article  Google Scholar 

Download references

Acknowledgements

J.A. Blanco-Aguiar was supported by Fundação para a Ciência e a Tecnologia (SFRH/BPD/65464/2009) grant. M. Delibes-Mateos was supported by a Juan de la Cierva research contract awarded by the Ministerio de Ciencia e Innovación—Fondo European Social Fund. F. Casas was supported by a postdoctoral grant of the Junta de Comunidades de Castilla la Mancha (JCCM). We thank the comments provided by Drs. E. Fernández-Juricic M. Moleón, G. Nugent, and anonymous reviewers on previous versions of this manuscript.

Author information

Authors and Affiliations

  1. Instituto de Investigación en Recursos Cinegéticos (IREC, CSIC-UCLM-JCCM), Ronda de Toledo s/n, E-13071, Ciudad Real, Spain

    José A. Blanco-Aguiar, Miguel Delibes-Mateos, Beatriz Arroyo, Pablo Ferreras, Fabián Casas, Rafael Villafuerte & Javier Viñuela

  2. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661, Vairao, Portugal

    José A. Blanco-Aguiar

  3. Departamento de Biología Animal, Facultad de Ciencias, Universidad de Málaga, 29071, Málaga, Spain

    Raimundo Real & J. Mario Vargas

  4. School of Biological Sciences, University of Aberdeen Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, Scotland, United Kingdom

    Fabián Casas

Authors
  1. José A. Blanco-Aguiar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miguel Delibes-Mateos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beatriz Arroyo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pablo Ferreras
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabián Casas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Raimundo Real
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Mario Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rafael Villafuerte
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Javier Viñuela
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José A. Blanco-Aguiar.

Additional information

Communicated by C. Gortázar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blanco-Aguiar, J.A., Delibes-Mateos, M., Arroyo, B. et al. Is the interaction between rabbit hemorrhagic disease and hyperpredation by raptors a major cause of the red-legged partridge decline in Spain?. Eur J Wildl Res 58, 433–439 (2012). https://doi.org/10.1007/s10344-011-0593-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10344-011-0593-z

Keywords

Search

Navigation