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Can widespread generalist predators affect keystone prey? A case study with red foxes and European rabbits in their native range

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Population Ecology

Abstract

Widespread generalist predators may affect declining keystone prey populations. However, this phenomenon is not well understood. In this paper, we assessed whether the abundance and population growth of European rabbits Oryctolagus cuniculus, a keystone prey species in Mediterranean Iberia, was related to the abundance and diet of red foxes, Vulpes vulpes, a widespread generalist predator. In a locality in central Spain, where rabbit population abundance declined, we estimated rabbit abundance during almost 3 years and determined fox abundance and diet during two concurrent years. We calculated a fox predation index (percentage of consumed rabbit biomass × fox abundance) to assess the importance of rabbits to foxes. We employed a multi–model approach to explain rabbit abundance and population growth. Foxes consumed between 60 and 99 % rabbit biomass in their diets, and this was independent of rabbit abundance. Periods of higher fox predation index coincided with lower rabbit density and vice versa. Two models best explained rabbit abundance and four rabbit population growth. They included the fox predation index and its interaction with rabbit abundance during the previous month. Altogether, fox predation, intraspecific density dependence, and their interaction partly explained rabbit population dynamics. We conclude that in order to propel the recovery of the rabbit in Iberia, it is essential to better understand the role of these factors in driving the abundance of the species.

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References

  • Allen BL, Leung LKP (2014) The (non)effects of lethal population control on the diet of Australian dingoes. PLoS One 9(9):e108251

    Article  PubMed Central  PubMed  Google Scholar 

  • Allen BL, Allen LR, Engeman RM, Leung LKP (2014) Sympatric prey responses to lethal top-predator control: predator manipulation experiments. Front Zool 11:56

    Article  Google Scholar 

  • Banks PB (2000) Can foxes regulate rabbit populations? J Wildl Manag 64:401–406

    Article  Google Scholar 

  • Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford

    Google Scholar 

  • Breusch TS (1979) Testing for autocorrelation in dynamic linear models. Aust Econ Pap 17:334–355

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Calzada J (2000) Impacto de la depredación y selección de presa del lince y el zorro sobre el conejo. PhD thesis, Universidad de León, León (in Spanish)

  • Delibes M, Hiraldo F (1981) The rabbit as prey in the Iberian Mediterranean ecosystem. In: Myers K, MacInnes CD (eds) Proceedings of the World Lagomorph Conference. Univ Guelph, Guelph, pp 614–622

    Google Scholar 

  • 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 

  • 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, Ferreras P, Villafuerte R (2008b) 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, Fernandez de Simon J, Ferreras P, Villafuerte R (2008c) 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 (2009) European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula. Mamm Rev 39:124–140

    Article  Google Scholar 

  • Delibes-Mateos M, Díaz-Fernández S, Ferreras P, Viñuela J, Arroyo B (2013) The role of economic and social factors driving predator control in small game estates in central Spain. Ecol Soc 18(2):28

    Google Scholar 

  • Delibes-Mateos M, Ferreira C, Carro F, Escudero MA, Gortázar C (2014a) Ecosystem effects of variant rabbit hemorrhagic disease virus, Iberian Peninsula. Emerg Infect Dis 20:2166–2168

    Article  PubMed Central  PubMed  Google Scholar 

  • Delibes-Mateos M, Ferreira C, Rouco C, Villafuerte R, Barrio IC (2014b) Conservationists, hunters and farmers: the European rabbit Oryctolagus cuniculus management conflict in the Iberian peninsula. Mamm Rev 44:190–203

    Article  Google Scholar 

  • Development Core Team R (2013) R: A language and environment for statistical computing. Austria R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Díaz-Ruiz F, Ferreras P (2013) Conocimiento científico sobre la gestión de depredadores generalistas en España: el caso del zorro (Vulpes vulpes) y la urraca (Pica pica). Ecosistemas 22:40–47 (in Spanish with English abstract)

    Article  Google Scholar 

  • Díaz-Ruiz F, Delibes-Mateos M, García-Moreno JL, López–Martín JM, Ferreira C, Ferreras P (2013) Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian peninsula. Mamm Rev 43:59–70

    Article  Google Scholar 

  • Fernandez-de-Simon J (2013) Predation and the recovery of European rabbit populations in central–southern Iberian peninsula. An assessment of the predator pit hypothesis. PhD thesis, Universidad de Castilla–La Mancha, Ciudad Real

  • 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 

  • Fernandez-de-Simon J, Díaz-Ruiz F, Cirilli F, Tortosa FS, 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 

  • Ferreira C, Touza J, Rouco C, Díaz-Ruiz F, Fernandez-de-Simon J, Ríos-Saldaña CA, Ferreras P, Villafuerte R, Delibes-Mateos M (2014) Habitat management as a generalized tool to boost European rabbit Oryctolagus cuniculus populations in the Iberian peninsula: a cost-effectiveness analysis. Mamm Rev 44:30–43

    Article  Google Scholar 

  • 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 

  • Gálvez L, Belliure J, Rebollo S (2009) European rabbits as ecosystem engineers: warrens increase lizard density and diversity. Biodivers Conserv 18:869–885

    Article  Google Scholar 

  • Godfrey LG (1978) Testing against general autoregressive and moving average error models when the regressors include lagged dependent variables. Econometrica 46:1293–1302

    Article  Google Scholar 

  • Gómez-Sal A, Rey-Benayas JM, López-Pintor A, Rebollo S (1999) Role of disturbance in maintaining a savanna-like pattern in Mediterranean Retama sphaerocarpa shrubland. J Veg Sci 10:365–370

    Article  Google Scholar 

  • Korpimäki E, Norrdahl K, Rinta-Jaskari T (1991) Responses of stoats and least weasels to fluctuating food abundances: is the low phase of the vole cycle due to mustelid predation? Oecologia 88:552–561

    Article  Google Scholar 

  • Lombardi L, Fernández N, Moreno S, Villafuerte R (2003) Habitat–related differences in rabbit (Oryctolagus cuniculus) abundance, distribution, and activity. J Mammal 84:26–36

    Article  Google Scholar 

  • Macdonald DW, Reynolds JC (2004) Red fox Vulpes vulpes Linnaeus, 1758. In: Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan, IUCN/SSC Canid Specialist Group, Gland and Cambridge, pp 129–136

    Google Scholar 

  • Moreno S, Beltrán JF, Cotilla I, Kuffner B, Laffite R, Jordán G, Ayala J, Quintero C, Jiménez A, Castro F, Cabezas S, Villafuerte R (2007) Long-term decline of the European wild rabbit (Oryctolagus cuniculus) in south-western Spain. Wildl Res 34:652–658

    Article  Google Scholar 

  • Norbury G, Jones C (2015) Pests controlling pests: does predator control lead to greater European rabbit abundance in Australasia? Mamm Rev 45:79–87

    Article  Google Scholar 

  • Pech RP, Sinclair ARE, Newsome AE, Catling PC (1992) Limits to predator regulation of rabbits in Australia: evidence from predator-removal experiments. Oecologia 89:102–112

    Article  Google Scholar 

  • Reynolds J, Aebischer N (1991) Comparison and quantification of carnivore diet by faecal analysis: a critique with recommendations based on a study of the fox Vulpes vulpes. Mamm Rev 21:97–122

    Article  Google Scholar 

  • Reynolds JC, Tapper SC (1995) The ecology of the red fox Vulpes vulpes in relation to small game in rural southern England. Wildl Biol 1:105–119

    Google Scholar 

  • Ruiz-Azpurua L, Guerrero-Casado J, Carpio AJ, Tortosa FS (2014) High rabbit abundance proves detrimental to the population growth rate in European rabbit (Oryctolagus cuniculus L.) extensive breeding enclosures. World Rabbit Sci 22:179–186

    Article  Google Scholar 

  • Sarmento P (1996) Feeding ecology of the European wildcat Felis silvestris in Portugal. Acta Theriol 41:409–414

    Article  Google Scholar 

  • Saunders G, Gentle MN, Dickman CR (2010) The impacts and management of foxes Vulpes vulpes in Australia. Mamm Rev 40:181–211

    Article  Google Scholar 

  • Sinclair ARE, Krebs CJ (2002) Complex numerical responses to top–down and bottom–up processes in vertebrate populations. Philos Trans R Soc B Biol Sci 357:1221–1231

    Article  CAS  Google Scholar 

  • Sinclair ARE, Pech RP, Dickman CR, Hik D, Mahon P, Newsome AE (1998) Predicting effects of predation on conservation of endangered prey. Conserv Biol 12:564–575

    Article  Google Scholar 

  • Sinclair ARE, Fryxell JM, Caughley G (2006) Wildlife ecology, conservation, and management, 2nd edn. Blackwell, Oxford

    Google Scholar 

  • Sobrino R, Acevedo P, Escudero MA, Marco J, Gortázar C (2009) Carnivore population trends in Spanish agrosystems after the reduction in food availability due to rabbit decline by rabbit haemorrhagic disease and improved waste management. Eur J Wildl Res 55:161–165

    Article  Google Scholar 

  • Tapper SC, Potts GR, Brockless MH (1996) The effect of an experimental reduction in predation pressure on the breeding success and population density of grey partridges Perdix perdix. J Appl Ecol 33:965–978

    Article  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 

  • Verdú JR, Galante E (2004) Behavioural and morphological adaptations for a low-quality resource in semi-arid environments: dung beetles (Coleoptera, Scarabaeoidea) associated with the European rabbit (Oryctolagus cuniculus L.). J Nat Hist 38:705–715

    Article  Google Scholar 

  • Villafuerte R, Delibes-Mateos M (2007) Oryctolagus cuniculus (Linnaeus, 1758). In: Palomo LJ, Gisbert J, Blanco JC (eds) Atlas y libro rojo de los mamíferos terrestres de España. Dirección General para la Biodiversidad–SECEM–SECEMU, Madrid, pp 490–491 (in Spanish)

  • Villafuerte R, Luco DF, Gortázar C, Blanco JC (1996) Effect on red fox litter size and diet after rabbit haemorrhagic disease in north-eastern Spain. J Zool 240:764–767

    Article  Google Scholar 

  • Wagner SC (2012) Keystone species. Nature Education Knowledge 3(10):51

    Google Scholar 

  • Webbon C, Baker P, Harris S (2004) Faecal density counts for monitoring changes in red fox numbers in rural Britain. J Appl Ecol 41:768–779

    Article  Google Scholar 

  • Williams D, Acevedo P, Gortázar C, Escudero MA, Labarta JL, Marco J, Villafuerte R (2007) Hunting for answers: rabbit (Oryctolagus cuniculus) population trends in northeastern Spain. Eur J Wildl Res 53:19–28

    Article  Google Scholar 

  • Willot SJ, Miller AJ, Incoll LD, Compton SG (2000) The contribution of rabbits (Oryctolagus cuniculus L.) to soil fertility in semi-arid Spain. Biol Fertil Soils 31:379–384

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York

    Book  Google Scholar 

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Acknowledgments

This is a partial result from the I+D National Plan Projects CGL2005-02340, CGL2009-10741 and CGL2013-43197, funded by the Spanish Ministry of Science and Innovation and EU FEDER funds. JFdS 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. Díaz-Ruiz are currently holding a postdoctoral fellowship from Junta de Castilla-La Mancha and the European Social Fund (Operational Programme FSE 2007/2013). M. Delibes-Mateos is currently funded by Junta de Andalucía and the EU FP7, under grant agreement 267226. The authors had the necessary licences and permits (dated 1 February 2004) for the activities described in the paper and took into account the welfare of animals. We are indebted to landowners and personnel of the study area. We thank many people who kindly collaborated with us. Prof. J. E. Fa carefully revised the English text. In addition, F.S. Tortosa, F. Cirilli, B. Arroyo, M. Delibes, P.C. Alves, C. Johnson, B. Allen, T. Saitoh, and three anonymous reviewers provided helpful suggestions in earlier drafts of the manuscript.

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Correspondence to Javier Fernandez-de-Simon.

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Fernandez-de-Simon, J., Díaz-Ruiz, F., Rodríguez-de la Cruz, M. et al. Can widespread generalist predators affect keystone prey? A case study with red foxes and European rabbits in their native range. Popul Ecol 57, 591–599 (2015). https://doi.org/10.1007/s10144-015-0510-5

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