Subtle cues of predation risk: Starlings respond to a predator's direction of eye-gaze

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1644, 2008, Pages 1709-1715

  Carter, Julia ^a   Lyons, Nicholas J ^a   Cole, Hannah L ^a   Goldsmith, Arthur R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Anti predator vigilance; European starlings Sturnus vulgaris; Eye gaze direction; Predation risk; Predator orientation; Starvation predation trade off

Indexed keywords

BEHAVIORAL RESPONSE; ENVIRONMENTAL CUE; PASSERINE; PREDATION RISK; PREDATOR-PREY INTERACTION; STARVATION; TRADE-OFF; VIGILANCE;

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; FEEDING; FEMALE; FOOD INTAKE; GAZE; MALE; NONHUMAN; PREDATION RISK; PREDATOR; PREDATOR PREY INTERACTION; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; STARLING;

ANIMALIA; AVES; STURNIDAE; STURNUS VULGARIS;

EID: 45249113919     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0095     Document Type: Article

References (48)

1. Bednekoff, P. A. & Lima, S. L. 1998 Randomness, chaos and confusion in the study of antipredator vigilance. Trends Ecol. Evol. 13, 284-287. (doi:10.1016/S0169-5347(98)01327-5)
2. Bouskila, A. & Blumstein, D. T. 1992 Rules of thumb for predation hazard assessment: predictions from a dynamic model. Am. Nat. 139, 161-176. (doi:10.1086/285318)
3. Bräuer, J., Call, J. & Tomasello, M. 2005 All great ape species follow gaze to distant locations and around barriers. J. Comp. Psychol. 119, 145-154. (doi:10.1037/0735-7036.119.2.145)
4. Bugnyar, T., Stöwe, M. & Heinrich, B. 2004 Ravens, Corvus corax, follow gaze direction of humans around obstacles. Proc. R. Soc. B 271, 1331-1336. (doi:10.1098/rspb.2004.2738)
5. Burger, J. & Gochfeld, M. 1981 Discrimination of the threat of direct versus tangential approach to the nest by incubating herring and great black-backed gulls. J. Comp. Physiol. Psychol. 95, 676-684. (doi:10.1037/h0077811)
6. Burger, J. & Gochfeld, M. 1990 Risk discrimination of direct versus tangential approach by basking black iguanas (Ctenosaura similis): variation as a function of human exposure. J. Comp. Psychol. 104, 388-394. (doi:10.1037/0735-7036.104.4.388)
7. Campbell, F. M., Heyes, C. M. & Goldsmith, A. R. 1999 Stimulus learning and response learning by observation in the European starling, in a two-object/two-action test. Anim. Behav. 58, 151-158. (doi:10.1006/anbe.1999.1121)
8. Carlile, P. A., Peters, R. A. & Evans, C. S. 2006 Detection of a looming stimulus by the Jacky dragon: selective sensitivity to characteristics of an aerial predator. Anim. Behav. 72, 553-562. (doi:10.1016/j.anbehav.2005.10.027)
9. Carpenter, R. H. S. 1977 Movements of the eyes. London, UK: Pion.
10. Cowlishaw, G., Lawes, M. J., Lightbody, M., Martin, A., Pettifor, R. & Rowcliffe, J. M. 2004 A simple rule for the costs of vigilance: empirical evidence from a social forager. Proc. R. Soc. B 271, 27-33. (doi:10.1098/rspb.2003.2522)
11. Cramp, S. & Perrins, C. M. (eds) 1994 Sturnus vulgaris starling. In Handbook of the birds of Europe, the Middle East and North Africa: the birds of the Western Palearctic, vol. 8 crows to finches. Oxford, UK: Oxford University Press.
12. Cresswell, W., Quinn, J. L., Whittingham, M. J. & Butler, S. 2003 Good foragers can also be good at detecting predators. Proc. R. Soc. B 270, 1069-1076. (doi:10.1098/rspb.2003.2353)
13. Curio, E. 1993 Proximate and developmental aspects of antipredator behaviour. Adv. Study Behav. 22, 135-238.
14. Devereux, C. L., Whittingham, M. J., Fernández-Juricic, E., Vickery, J. A. & Krebs, J. R. 2006 Predator detection and avoidance by starlings under differing scenarios of predation risk. Behav. Ecol. 17, 303-309. (doi:10.1093/beheco/arj032)
15. Emery, N. J. 2000 The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci. Biobehav. Rev. 24, 581-604. (doi:10.1016/S0149-7634(00)00025-7)
16. Fawcett, T. W., Skinner, A. M. J. & Goldsmith, A. R. 2002 A test of imitative learning in starlings using a two-action method with an enhanced ghost control. Anim. Behav. 64, 547-556. (doi:10.1006/anbe.2002.3092)
17. Feare, C. 1984 The starling. Oxford, UK: Oxford University Press.
18. Gallup, G. G., Nash, R. F. & Ellison, A. L. 1971 Tonic immobility as a reaction to predation: artificial eyes as a fear stimulus for chickens. Psychon. Sci. 23, 79-80.
19. Gallup, G. G., Cummings, W. H. & Nash, R. F. 1972 Experimenter as an independent variable in studies of animal hypnosis in chickens (Gallus gallus). Anim. Behav. 20, 166-169. (doi:10.1016/S0003-3472(72)80187- 8)
20. Hampton, R. R. 1994 Sensitivity to information specifying the line of gaze of humans in sparrows (Passer domesticus). Behaviour 130, 41-51. (doi:10.1163/156853994X00136)
21. Hawkins, P. et al. 2001 Laboratory birds: refinements in husbandry and procedures. Lab. Anim. 35, S1-S163. (doi:10.1258/ 0023677011911967)
22. Hegner, R. E. 1985 Dominance and anti-predator behavior in blue tits (Parus caeruleus). Anim. Behav. 33, 762-768. (doi:10.1016/S0003- 3472(85)80008-7)
23. Helfman, G. S. 1989 Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav. Ecol. Sociobiol. 24, 47-58. (doi:10.1007/BF00300117)
24. Heyes, C. M. 1998 Theory of mind in nonhuman primates. Behav. Brain Sci. 21, 101-148. (doi:10.1017/S0140525X98000703)
25. Hurlbert, S. H. 1984 Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187-211. (doi:10.2307/1942661)
26. Inglis, I. R., Huson, L. W., Marshall, M. B. & Neville, P. A. 1983 The feeding behaviour of starlings (Sturnus vulgaris) in the presence of eyes. Z. Tierpsychol. J. Comp. Ethol. 62, 181-208.
27. Jones, R. B. 1980 Reactions of male domestic chicks to two-dimensional eye-like shapes. Anim. Behav. 28, 212-218. (doi:10.1016/S0003- 3472(80)80025-X)
28. Kaminski, J., Call, J. & Tomasello, M. 2004 Body orientation and face orientation: two factors controlling apes' begging behavior from humans. Anim. Cogn. 7, 216-223. (doi:10.1007/s10071-004-0214-2)
29. Kavaliers, M. & Choleris, E. 2001 Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci. Biobehav. Rev. 25, 577-586. (doi:10.1016/S0149-7634(01) 00042-2)
30. Kobayashi, H. & Kohshima, S. 2001 Unique morphology of the human eye and its adaptive meaning: comparative studies on external morphology of the primate eye. J. Hum. Evol. 40, 419-435. (doi:10.1006/jhev.2001. 0468)
31. Koops, M. A. & Giraldeau, L. A. 1996 Producer-scrounger foraging games in starlings: a test of rate-maximizing and risk-sensitive models. Anim. Behav. 51, 773-783. (doi:10.1006/anbe.1996.0082)
32. Lima, S. L. 1998 Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv. Study Behav. 27, 215-290.
33. Lima, S. L. & Bednekoff, P. A. 1999 Back to the basics of antipredatory vigilance: can nonvigilant animals detect attack? Anim. Behav. 58, 537-543. (doi:10.1006/anbe.1999.1182)
34. Lima, S. L. & Dill, L. M. 1990 Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619-640.
35. Ottoni, E. B. 2000 ETHOLOG 2.2: a tool for the transcription and timing of behavior observation sessions. Behav. Res. Methods Instrum. Comput. 32, 446-449.
36. Quinn, J. L. & Cresswell, W. 2005a Escape response delays in wintering redshank, Tringa totanus, flocks: perceptual limits and economic decisions. Anim. Behav. 69, 1285-1292. (doi:10.1016/j.anbehav.2004.10.007)
37. Quinn, J. L. & Cresswell, W. 2005b Personality, antipredation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142, 1377-1402. (doi:10.1163/156853905774539391)
38. Ristau, C. A. 1991 Aspects of the cognitive ethology of an injury-feigning bird, the piping plover. In Cognitive ethology: the minds of other animals (ed. C. A. Ristau), pp. 91-126. Hillsdale, NJ: Lawrence Erlbaum.
39. Scaife, M. 1976 Response to eye-like shapes by birds 2: importance of staring, pairedness and shape. Anim. Behav. 24, 200-206. (doi:10.1016/S0003-3472(76)80116-9)
40. Schiff, W., Caviness, J. A. & Gibson, J. J. 1962 Persistent fear responses in rhesus monkeys to the optical stimulus of looming. Science 136, 982-983. (doi:10.1126/science.136.3520.982)
41. Smitha, B., Thakar, J. & Watve, M. 1999 Do bee eaters have theory of mind? Curr. Sci. 76, 574-577.
42. Stankowich, T. & Blumstein, D. T. 2005 Fear in animals: a meta-analysis and review of risk assessment. Proc. R. Soc. B 272, 2627-2634. (doi:10.1098/rspb.2005.3251)
43. Stevens, M., Hopkins, E., Hinde, W., Adcock, A., Connolly, Y., Troscianko, T. & Cuthill, I. C. 2007 Field experiments on the effectiveness of 'eyespots' as predator deterrents. Anim. Behav. 74, 1215-1227. (doi:10.1016/j.anbehav.2007.01.031)
44. Templeton, J. J. & Giraldeau, L. A. 1995 Public information cues affect the scrounging decisions of starlings. Anim. Behav. 49, 1617-1626. (doi:10.1016/0003-3472(95)90084-5)
45. Wang, Y. & Frost, B. J. 1992 Time to collision is signalled by neurons in the nucleus rotundus of pigeons. Nature 356, 236-238. (doi:10.1038/356236a0)
46. Watve, M., Thakar, J., Kale, A., Puntambekar, S., Shaikh, I., Vaze, K., Jog, M. & Paranjape, S. 2002 Bee-eaters (Merops orientalis) respond to what a predator can see. Anim. Cogn. 5, 253-259. (doi:10.1007/s10071-002-0155-6)
47. Woolnough, A. P., Lowe, T. J. & Rose, K. 2006 Can the Judas technique be applied to pest birds? Wildl. Res. 33, 449-455. (doi:10.1071/WR06009)
48. Ydenberg, R. C. & Dill, L. M. 1986 The economics of fleeing from predators. Adv. Study Behav. 16, 229-249.