Skip to main content
Log in

European rabbits recognise conspecifics in their predators’ diets

acta ethologica Aims and scope Submit manuscript

Abstract

Rabbits can successfully avoid their enemies by evaluating the risk of predation. They have various defensive strategies, such as morphological adaptations and behaviours patterns, which enable them to perceive their predators and thus reduce the risk of predation. It is well documented that rabbits recognise the scats of terrestrial predators and avoid those areas in which they are present. However, few studies show whether the prey species can recognise the presence of congeners in carnivores’ scats, which would allow them to identify their predators in a more efficient manner. We have carried out a comparative analysis of the use of space made by rabbits on plots on which a neutral odour (water) or the odours of the ferrets’ scats that had consumed either rabbit or another mammal (beef) were applied. Our results showed a lower number of rabbit pellets on those plots containing predator odours than on the control plots. During the first 6 days after applying the first odour, the number of rabbit pellets was lower on plots on which rabbit had been included in the diet when compared with scats obtained from a beef diet. However, no differences between the two experimental plots were recorded during the third visit (9 days after applying the first odour). Our results suggest that rabbits may be able to detect congeners in their predators’ scats, thus leading them to, in the short term, avoid areas in which their terrestrial predators’ diet is based on conspecifics, probably as the result of them perceiving a higher risk of predation.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144

    Article  PubMed  Google Scholar 

  • Apfelbach R, Soini HA, Vasilieva NY, Novotny MV (2015) Behavioral responses of predator-naïve dwarf hamsters (Phodopus campbelli) to odor cues of the European ferret fed with different prey species. Physiol Behav 146:57–66

    Article  PubMed  CAS  Google Scholar 

  • Barreto GR, Macdonald D (1999) The response of water voles, Arvicola terrestris, to the odours of predators. Anim Behav 57:1107–1112

    Article  PubMed  CAS  Google Scholar 

  • Barrio IC, Bueno CG, Tortosa FS (2010a) Alternative food and rabbit damage in vineyards of southern Spain. Agric Ecosyst Environ 138:51–54

    Article  Google Scholar 

  • Barrio IC, Bueno CG, Banks PB, Tortosa FS (2010b) Prey naiveté in an introduced prey species: the wild rabbit in Australian. Behav Ecol 21:986–991

    Article  Google Scholar 

  • Beja P, Pais M, Palma L (2007) Rabbit Oryctolagus Cuniculus habitats in Mediterranean scrubland: the role of scrub structure and composition. Wildl Biol 13:28–37

    Article  Google Scholar 

  • Beltran JF (1991) Temporal abundance pattern of the wild rabbit in Doñana, SW Spain. Mammalia 55:591–599

    Article  Google Scholar 

  • Caine NG, Weldon PJ (1989) Responses by red-bellied tamarins (Saguinus labiatus) to fecal scents of predatory and nonpredatory neotropical mammals. Biotropica 21:186–189

    Article  Google Scholar 

  • Carpio AJ, Soriano MA, Guerrero-Casado J, Prada LM, Tortosa FS, Lora Á, Gómez JA (2017) Evaluation of an unpalatable species (Anthemis arvensis L.) as an alternative cover crop in olive groves under high grazing pressure by rabbits. Agric Ecosyst Environ 246:48–54

    Article  Google Scholar 

  • Cox TE, Murray PJ, Hall GP, Li X (2010) Pest responses to odors from predators fed a diet of target species conspecifics and heterospecifics. JWM 74:1737–1744

    Article  Google Scholar 

  • Cremona T, Crowther MS, Webb JK (2014) Variation of prey responses to cues from a mesopredator and an apex predator. Aust Ecol 39:749–754

    Article  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 

  • Díaz M, Torre I, Peris A, Tena L (2005) Foraging behavior of wood mice as related to presence and activity of genets. J Mammal 86:1178–1185

    Article  Google Scholar 

  • Diete RL, Meek PD, Dickman CR, Lisle A, Leung LKP (2017) Diel activity patterns of northern Australian small mammals: variation, fixity, and plasticity. J Mammal 98:848–857

    Article  Google Scholar 

  • Fernandez-de-Simon J, Díaz-Ruiz F, Cirilli F, Tortosa FS, Villafuerte R, Delibes-Mateos M, Ferreras P (2011) Towards a standardized index of European rabbit abundance in Iberian Mediterranean habitats. Eur J Wildl Res 57(5):1091–1100

    Article  Google Scholar 

  • Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ, Datta SR, Spehr M, Fendt M, Liberles SD (2011) Detection and avoidance of a carnivore odour by prey. Proc Natl Acad Sci U S A 108:11235–11240

    Article  PubMed  PubMed Central  Google Scholar 

  • Guerrero-Casado J, Ruiz-Aizpurua L, Tortosa FS (2013) The short-term effect of total predation exclusion on wild rabbit abundance in restocking plots. Acta Theriol 58:415–418

    Article  Google Scholar 

  • Guerrero-Casado J, Carpio AJ, Prada LM, Tortosa FS (2015) Short communication. The role of rabbit density and the diversity of weeds in the development of cover crops in olive groves. Span J Agric Res 13:e03SC01

    Article  Google Scholar 

  • Hettyey A, Thonhauser KE, Bókony V, Penn DJ, Hoi H, Griggio M (2016) Naive tadpoles do not recognize recent invasive predatory fishes as dangerous. Ecology 97:2975–2985

    Article  PubMed  Google Scholar 

  • Jedrzejewski W, Jedrzejewska B (1990) Effect of a predator’s visit on the spatial distribution of bank voles: experiments with weasels. Can J Zool 68:660–666

    Article  Google Scholar 

  • Johnson-Delaney CA (2014) Ferret nutrition. Vet Clin North Am Exot Anim Pract 17:449–470

    Article  PubMed  Google Scholar 

  • Lima SL, Bednekoff P (1999) Temporal variation in danger drives antipredator behavior: thepredation risk allocation hypothesis. Am Nat 153:649–659

    Article  PubMed  Google Scholar 

  • McPhee ME, Segal A, Johnston RE (2010) Hamsters use predator odors as indirect cues of predation risk. Ethology 116:517–523

    Article  Google Scholar 

  • Monclús R, Rödel HG, Von Holstet D, De Miguel J (2005) Behavioural and physiological responses of naïve European rabbits to predator odour. Anim Behav 70:753–761

    Article  Google Scholar 

  • Monclús R, Palomares F, Tablado Z, Martínez-Fontúrbel A, Palme R (2009) Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 158:615–623

    Article  PubMed  Google Scholar 

  • Nersesian CL, Banks PB, McArthur C (2011) Behavioural responses to indirect and direct predator cues by a mammalian herbivore, the common brushtail possum. Behav Ecol Sociobiol 66:47–55

    Article  Google Scholar 

  • Parsons MH, Apfelbach R, Banks PB, Cameron EZ, Dickman CR, Frank ASK, Jones ME, McGregor IS, McLean S, Müller-Schwarze D, Sparrow EE, Blumstein DT (2018) Biologically meaningful scents: a framework for understanding predator–prey research across disciplines. Biol Rev 93:98–114

    Article  PubMed  Google Scholar 

  • Pereira RT, Leutz JDACM, Valença-Silva G, Barcellos LJG, Barreto RE (2017) Ventilation responses to predator odors and conspecific chemical alarm cues in the frillfin goby. Physiol Behav 179:319–323

    Article  PubMed  CAS  Google Scholar 

  • Pillay N, Alexander GJ, Lazenby SL (2003) Responses of striped mice, Rhabdomys pumilio, to faeces of a predatory snake. Behaviour 140:125–135

    Article  Google Scholar 

  • Preston DB, Forstner MR (2015) Houston toad (Bufo (Anaxyrus) houstonensis) tadpoles decrease their activity in response to chemical cues produced from the predation of conspecifics and congeneric (Bufo (Incilius) nebulifer) tadpoles. J Herpetol 49:170–175

    Article  Google Scholar 

  • Reichard U (1998) Sleeping sites, sleeping places, and presleep behavior of gibbons (Hylobates lar.). Am J Primatol 46:35–62

    Article  PubMed  CAS  Google Scholar 

  • Ríos-Saldaña CA, Delibes-Mateos M, Castro F, Martínez E, Vargas JM, Cooke BD, Villafuerte R (2013) Control of the European rabbit in Central Spain. Eur J Wildl Res 59:573–580

    Article  Google Scholar 

  • Rödel HG, Monclús R, Von Holst D (2006) Behavioral styles in European rabbits: social interactions and responses to experimental stressors. Physiol Behav 89:180–188

    Article  PubMed  CAS  Google Scholar 

  • Rosen JB, Asok A, Chakraborty T (2015) The smell of fear: innate threat of 2, 5-dihydro-2, 4, 5-trimethylthiazoline, a single molecule component of a predator odor. Front Neurosci 9:292

    PubMed  PubMed Central  Google Scholar 

  • Rouco C, Santoro S, Delibes-Mateos M, Villafuerte R (2016) Optimization and accuracy of faecal pellet count estimates of population size: the case of European rabbits in extensive breeding nuclei. Ecol Indic 64:212–216

    Article  Google Scholar 

  • Santilli F, Bagliacca M (2010) Habitat use by the European wild rabbit (Oryctolagus cuniculus) in a coastal sandy dune ecosystem of Central Italy. Hystrix. Ital J Mammal 21:57–64

    Google Scholar 

  • Scherer AE, Smee DL (2016) A review of predator diet effects on prey defensive responses. Chemoecology 26:83–100

    Article  CAS  Google Scholar 

  • Shaffery HM, Relyea RA (2015) Dissecting the smell of fear from conspecific and heterospecific prey: investigating the processes that induce anti-predator defenses. Oecologia 180:55–65

    Article  PubMed  Google Scholar 

  • Stankowich T, Haverkamp PJ, Caro T (2014) Ecological drivers of antipredator defenses in carnivores. Evolution 68:415–1425

    Article  Google Scholar 

  • Tortosa FS, Barrio IC, Carthey A, Banks P (2015) No longer naïve? Generalized responses of rabbits to marsupial predators in Australia. Behav Ecol Sociobiol 69:1649–1655

    Article  Google Scholar 

  • Vilhunen S, Hirvonen H (2003) Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet. Behav Ecol Sociobiol 55:1–10

    Article  Google Scholar 

  • Viota M, Rodríguez A, López-Vao JV, Palomares F (2012) Shift in microhabitat use as a mechanism allowing the coexistence of victim and killer carnivore predators. Open J Ecol 2:115–120

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the landowners that allowed us to work in their fields. We are indebted to A. J. Carpio and our others partners for their help during the fieldwork and to the farmers for their cooperation. Two anonymous reviewers provided useful comments that greatly improved the manuscript.

Funding

This work was supported by the AGL2012–40128-C03–01 project and EU-FEDER funds from the Spanish government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Guerrero-Casado.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prada, L.M., Guerrero-Casado, J. & Tortosa, F.S. European rabbits recognise conspecifics in their predators’ diets. acta ethol 21, 163–168 (2018). https://doi.org/10.1007/s10211-018-0295-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10211-018-0295-6

Keywords

Navigation