The response of social and non-social rodents to owl attack

  • Chen Rabi
  • Pazit Zadicario
  • Yael Mazon
  • Naama Wagner
  • David EilamEmail author
Original Article


Studies with individual rodents have revealed that they display protean (unpredictable) behavior when attacked by an owl. Other studies have revealed that voles in groups reduce behavioral variability a short time after owl attack, as if adopting the behavior of the higher-mass and perhaps older and more experienced, individuals. Here, we tested groups of rodents under owl attack in order to track the behavior of individuals within the group and compare between the behaviors of social and non-social species. We found differential behavior between species, between groups of the same species, among individuals in the same group, and among the various phases of the owl attack. We also found that upon being exposed to an owl, social rodents tended to huddle together whereas solitary rodents tended to scatter across the available space. Other non-social but perhaps not necessarily solitary rodent species displayed a mixed spacing, with some huddling and some scattering. The findings of the present study shed light on the defensive dynamics of small groups of social and non-social rodent species when they were under owl attack.

Significance statement

Freezing and fleeing are defensive responses that span the animal kingdom, and rodents display various combinations of these in order to prevent predators from predicting their response. Groups of six voles or six spiny mice that were attacked by a barn owl differentially displayed these responses during various phases of the owl attack. Responses also varied among individuals of the same group and among different groups. Finally, we show that when exposed to an owl and displayed freeze response, individuals of social species tended to huddle together, whereas individuals of solitary species scattered over the arena.


Freezing Fleeing Protean behavior Anti-predator behavior Defensive behavior 



We are grateful to Naomi Paz for language editing, and the anonymous reviewers for their thoughtful comments.

Compliance with ethical standards

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the Institutional Committee for Animal Experimentation at Tel-Aviv University (permit no. L-15-011).

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability

The datasets generated during the current study are available with no restriction, on request from the corresponding author.

Supplementary material

265_2017_2359_MOESM1_ESM.mp4 (2.2 mb)
ESM 1 (MP4 2213 kb).


  1. Abramsky Z, Rosenzweig ML, Brand S (1985) Habitat selection of Israel desert rodents—comparison of a traditional and a new method of analysis. Oikos 45:79–88CrossRefGoogle Scholar
  2. Alagaili AN, Mohammed OB, Bennett NC, Oosthuizen MK (2012) Lights out, let’s move about: locomotory activity patterns of Wagner’s gerbil from the desert of Saudi Arabia. Afr Zool 47:195–202Google Scholar
  3. Bacigalupe LD, Rezende EL, Kenagy GJ, Bozinovic F (2003) Activity and space use by degus: a trade-off between thermal conditions and food availability? J Mammal 84:311–318CrossRefGoogle Scholar
  4. Bednekoff P, Lima S (1998) Randomness, chaos and confusion in the study of antipredator vigilance. Trends Ecol Evol 13:284–287CrossRefPubMedGoogle Scholar
  5. Berger J (1979) “Predator harassment” as a defensive strategy in ungulates. Am Midl Nat 102:197–199CrossRefGoogle Scholar
  6. Bertram BC (1978) Living in groups: predators and prey. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell, Oxford, pp 64–96Google Scholar
  7. Bodek S, Eilam D (2015) Revisiting the “visible burrow system”: the impact of the group, social rank, and gender on voles under owl attack. Physiol Behav 146:79–85CrossRefPubMedGoogle Scholar
  8. Boesch C (1991) The effects of leopard predation on grouping patterns in forest chimpanzees. Behaviour 117:220–241CrossRefGoogle Scholar
  9. Bowen MT, Kevin RC, May M, Staples LG, Hunt GE, McGregor IS (2013) Defensive aggregation (huddling) in Rattus norvegicus toward predator odor: individual differences, social buffering effects and neural correlates. PLoS One 8:e68483CrossRefPubMedPubMedCentralGoogle Scholar
  10. Charter M, Izhaki I, Shapira L, Leshem Y (2007) Diets of urban breeding barn owls (Tyto alba) in Tel Aviv, Israel. Wilson J Ornithol 119:484–485CrossRefGoogle Scholar
  11. Charter M, Izhaki I, Meyrom K, Motro Y, Leshem Y (2009) Diets of barn owls differ in the same agricultural region. Wilson J Ornithol 121:378–383CrossRefGoogle Scholar
  12. Coleman RA, Browne M, Theobalds T (2004) Aggregation as a defense: limpet tenacity changes in response to simulated predator attack. Ecology 85:1153–1159CrossRefGoogle Scholar
  13. Davis M (1998) Are different parts of the extended amygdala involved in fear versus anxiety? Biol Psychiatry 44:1239–1247CrossRefPubMedGoogle Scholar
  14. Dawkins R, Krebs JR (1978) Animal signals: information or manipulation. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Scientific Publications, London, pp 282–309Google Scholar
  15. Demirbaş Y, Pamukoğlu N (2008) The bioecology of Meriones tristrami Thomas, 1892 in Kirikkale province (Mammalia: Rodentia). Int J Nat Eng Sci 2:39–44Google Scholar
  16. Domenici P, Blagburn JM, Bacon JP (2011a) Animal escapology I: theoretical issues and emerging trends in escape trajectories. J Exp Biol 214:2463–2473CrossRefPubMedPubMedCentralGoogle Scholar
  17. Domenici P, Blagburn JM, Bacon JP (2011b) Animal escapology II: escape trajectory case studies. J Exp Biol 214:2474–2494CrossRefPubMedPubMedCentralGoogle Scholar
  18. Dugatkin LA, Godin J-GJ (1992) Prey approaching predators: a cost-benefit perspective. Ann Zool Fenn 29:233–252Google Scholar
  19. Dutour M, Lena J-P, Lengagne T (2016) Mobbing behaviour varies according to predator dangerousness and occurrence. Anim Behav 119:119–124CrossRefGoogle Scholar
  20. Edut S, Eilam D (2003) Rodents in open space adjust their behavioral response to the different risk levels during barn-owl attack. BMC Ecol 3:10CrossRefPubMedPubMedCentralGoogle Scholar
  21. Edut S, Eilam D (2004) Protean behavior under barn-owl attack: voles alternate between freezing and fleeing and spiny mice flee in alternating patterns. Behav Brain Res 155:207–216CrossRefPubMedGoogle Scholar
  22. Eilam D (2005) Die hard: a blend of freezing and fleeing as a dynamic defense—implications for the control of defensive behavior. Neurosci Biobehav Rev 29:1181–1191CrossRefPubMedGoogle Scholar
  23. Eilam D, Izhar R, Mort J (2011) Threat detection: behavioral consequences in animals and humans. Neurosci Biobehav Rev 35:999–1006CrossRefPubMedGoogle Scholar
  24. Eilam D, Zadicario P, Genossar T, Mort J (2012) The anxious vole: the impact of group and gender on collective behavior under life-threat. Behav Ecol Sociobiol 66:959–968CrossRefGoogle Scholar
  25. Elgar MA (1989) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33CrossRefPubMedGoogle Scholar
  26. Gliwicz ZM, Maszczyk P, Jablonski J, Wrzosek D (2013) Patch exploitation by planktivorous fish and the concept of aggregation as an antipredation defense in zooplankton. Limnol Oceanogr 58:1621–1639CrossRefGoogle Scholar
  27. Gromov VS, Krasnov BR, Shenbrot GI (2001) Behavioural correlates of spatial distribution in Wagner’s gerbil Gerbillus dasyurus (Rodentia, Gerbillinae). Mammalia 65:111–120Google Scholar
  28. Hamilton W (1971) Geometry for the selfish herd. J Theor Biol 31:295–311CrossRefPubMedGoogle Scholar
  29. Handegard NO, Boswell KM, Ioannou CC, Leblanc SP, Tjostheim DB, Couzin ID (2012) The dynamics of coordinated group hunting and collective information transfer among schooling prey. Curr Biol 22:1213–1217CrossRefPubMedGoogle Scholar
  30. Haughton CL, Gawriluk TR, Seifert AW (2016) The biology and husbandry of the African spiny mouse (Acomys cahirinus) and the research uses of a laboratory colony. J Am Assoc Lab Anim Sci 55:9–17PubMedPubMedCentralGoogle Scholar
  31. Hausmann L, Plachta DT, Singheiser M, Brill S, Wagner H (2008) In-flight corrections in free-flying barn owls (Tyto alba) during sound localization tasks. J Exp Biol 211:2976–2988CrossRefPubMedGoogle Scholar
  32. Holand O, Weladji RB, Gjostein H, Kumpula J, Smith ME, Nieminen M, Roed KH (2004) Reproductive effort in relation to maternal social rank in reindeer (Rangifer tarandus). Behav Ecol Sociobiol 57:69–76CrossRefGoogle Scholar
  33. Humphries D, Driver P (1970) Protean defence by prey animals. Oecologia 5:285–302CrossRefPubMedGoogle Scholar
  34. Ilany A, Eilam D (2008) Wait before running for your life: defensive tactics of spiny mice (Acomys cahirinus) in evading barn owl (Tyto alba) attack. Behav Ecol Sociobiol 62:923–933CrossRefGoogle Scholar
  35. Izhar R, Eilam D (2010) Together they stand: a life-threatening event reduces individual behavioral variability in groups of voles. Behav Brain Res 208:282–285CrossRefPubMedGoogle Scholar
  36. Jaksić FM, Yáñez JL (1979) The diet of the barn owl in central Chile and its relation to the availability of prey. Auk 96:619–621Google Scholar
  37. Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc B 361:2215–2228CrossRefGoogle Scholar
  38. Kleiman M, Bodek S, Eilam D (2014) Who are the bosses? Group influence on the behavior of voles following owl attack. Behav Process 108:183–190CrossRefGoogle Scholar
  39. Knudsen EI (2002) Instructed learning in the auditory localization pathway of the barn owl. Nature 417(6886):322–328CrossRefPubMedGoogle Scholar
  40. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  41. Lay DM (1967) A study of the mammals of Iran: resulting from the street expedition of 1962–63. Field Museum of Natural History, ChicagoGoogle Scholar
  42. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  43. Maksimović N, Žujović M, Hristov S, Petrović M, Stanković B, Tomić Z, Stanišić N (2012) Association between the social rank, body mass, testicular circumference and linear body measures of rams. Biotechnol Anim Husb 28:253–261CrossRefGoogle Scholar
  44. Mandelik Y (1999) Foraging microhabitat use and foraging efficiencies of the common spiny mouse, Acomys cahirinus. Master’s dissertation, Tel Aviv UniversityGoogle Scholar
  45. Mendelssohn H, Yom-Tov Y (1999) Fauna palaestina: mammalia of israel. Keterpress Enterprises, JerusalemGoogle Scholar
  46. Pelletier F, Festa-Bianchet M (2006) Sexual selection and social rank in bighorn rams. Anim Behav 71:649–655CrossRefGoogle Scholar
  47. Pusey AE, Packer C (1997) The ecology of relationships. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 4th edn. Wiley, NY, pp 254–283Google Scholar
  48. Ritz D (1994) Social aggregation in pelagic invertebrates. Adv Mar Biol 30:155–216CrossRefGoogle Scholar
  49. Roulin A (2004) Covariation between plumage colour polymorphism and diet in the barn owl Tyto alba. Ibis 146:509–517CrossRefGoogle Scholar
  50. Shargal E, Kronfeld-Schor N, Dayan T (2000) Population biology and spatial relationships of coexisting spiny mice (Acomys) in Israel. J Mammal 81:1046–1052CrossRefGoogle Scholar
  51. Shifferman E, Eilam D (2004) Movement and direction of movement of a simulated prey affect the success rate in barn owl Tyto alba attack. J Avian Biol 35:111–116CrossRefGoogle Scholar
  52. Sillen-Tullberg B, Leimar O (1988) The evolution of gregariousness in distasteful insects as a defense against predators. Am Nat 132:723–734CrossRefGoogle Scholar
  53. Szulkin M, Dawidowicz P, Dodson SI (2006) Behavioural uniformity as a response to cues of predation risk. Anim Behav 71:1013–1019CrossRefGoogle Scholar
  54. Taillon J, Cote SD (2006) The role of previous social encounters and body mass in determining social rank: an experiment with white-tailed deer. Anim Behav 72:1103–1110CrossRefGoogle Scholar
  55. Vine I (1973) Detection of prey flocks by predators. J Theor Biol 40:207–210CrossRefPubMedGoogle Scholar
  56. Vulinec K (1990) Collective security: aggregation by insects as a defense. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, pp 251–288Google Scholar
  57. Wilson EO (2000) Sociobiology. Harvard University Press, NYGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Chen Rabi
    • 1
  • Pazit Zadicario
    • 1
  • Yael Mazon
    • 1
  • Naama Wagner
    • 1
  • David Eilam
    • 1
    Email author
  1. 1.School of ZoologyTel-Aviv UniversityRamat-AvivIsrael

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