Animal Cognition

, Volume 14, Issue 2, pp 279–290 | Cite as

Cattle discriminate between familiar and unfamiliar conspecifics by using only head visual cues

  • Marjorie Coulon
  • Claude Baudoin
  • Yvan Heyman
  • Bertrand L. Deputte
Original Paper

Abstract

Faces have features characteristic of the identity, age and sex of an individual. In the context of social communication and social recognition in various animal species, facial information is relevant for discriminating between familiar and unfamiliar individuals. Here, we present two experiments aimed at testing the ability of cattle (Bos taurus) to visually discriminate between heads (including face views) of familiar and unfamiliar conspecifics represented as 2D images. In the first experiment, we observed the spontaneous behaviour of heifers when images of familiar and unfamiliar conspecifics were simultaneously presented. Our results show that heifers were more attracted towards the image of a familiar conspecific (i.e., it was chosen first, explored more, and given more attention) than towards the image of an unfamiliar one. In the second experiment, the ability to discriminate between images of familiar and unfamiliar conspecifics was tested using a food-rewarded instrumental conditioning procedure. Eight out of the nine heifers succeeded in discriminating between images of familiar and unfamiliar conspecifics and in generalizing on the first trial to a new pair of images of familiar and unfamiliar conspecifics, suggesting a categorization process of familiar versus unfamiliar conspecifics in cattle. Results of the first experiment and the observation of ear postures during the learning process, which was used as an index of the emotional state, provided information on picture processing in cattle and lead us to conclude that images of conspecifics were treated as representations of real individuals.

Keywords

Social familiarity Instrumental conditioning Cattle Spontaneous behavioural choice Simultaneous discrimination task 2D images of head 

References

  1. Bouissou MF, Andrieu S (1978) Etablissement des relations préférentielles chez les bovins domestiques. Behaviour 64:148–157CrossRefGoogle Scholar
  2. Bouissou MF, Porter RH, Boyle L, Ferreira G (1996) Influence of a conspecific image of own vs. different breed on fear reactions of ewes. Behav Process 38:37–44CrossRefGoogle Scholar
  3. Bovet D, Vauclair J (2000) Picture recognition in animals and humans. Behav Brain Res 109:143–165CrossRefPubMedGoogle Scholar
  4. Charrier I, Mathevon N, Jouventin P (2001) Mother’s voice recognition by seal pups. Nature 412:87CrossRefGoogle Scholar
  5. Coulon M, Deputte BL, Heyman Y, Richard C, Delatouche L, Baudoin C (2007) Visual discrimination by heifers (Bos taurus) of their own species. J Comp Psychol 121:198–204CrossRefPubMedGoogle Scholar
  6. Coulon M, Deputte BL, Heyman Y, Baudoin C (2009) Individual recognition in domestic cattle (Bos taurus): evidence from 2D-images of heads from different breeds. PLoS ONE 4(2):e4441CrossRefPubMedGoogle Scholar
  7. Coulon M, Baudoin C, Abdi H, Heyman Y, Deputte BL (2010) Social behavior and kin discrimination in a mixed group of cloned and non cloned heifers (Bos taurus). Theriogenology 74:1596–1603CrossRefPubMedGoogle Scholar
  8. Cummins KA (1991) Olfactory and visual cues. Individual recognition and social aggression in lactating cows. J Dairy Sci 74:301CrossRefGoogle Scholar
  9. Dasser V (1987) Slides of group members as representations of real animals (Macaca fascicularis). Ethology 76:65–73CrossRefGoogle Scholar
  10. Dawkins MS (1996) Distance and social recognition in hens: implication for the use of photographs as social stimuli. Behaviour 133:663–680CrossRefGoogle Scholar
  11. Deputte BL (2000) Primate socialization revisited: theoretical and practical issues in social ontogeny. In: Slater PJB, Rosenblatt JS, Snowdon CT, Roper TJ (eds) Advances in the study of behaviour. Academic Press, San Diego, pp 99–157Google Scholar
  12. Deputte BL (2010) Communication, perception et expression du chien. In: Bedossa T, Deputte BL (eds) Comportement et éducation du chien. Educagri Editions, Dijon, pp 355–424Google Scholar
  13. Deputte BL, Pelletier S, Barbe S (2001) Visual categorization of natural and abstract items in forest monkeys and humans. Behav Process 55:51–64CrossRefGoogle Scholar
  14. Entsu S, Dohi H, Yamada A (1992) Visual acuity of cattle determined by the method of discrimination learning. Appl Anim Behav Sci 34:1–10CrossRefGoogle Scholar
  15. Fagot J (2000) Picture perception in animals. Psychology Press, HoveGoogle Scholar
  16. Fagot J, Thompson RKR, Parron C (2010) How to read a picture: lessons from nonhuman primates. Proc Natl Acad Sci 107:519–520CrossRefPubMedGoogle Scholar
  17. Farah MJ, Wilson KD, Drain M, Tanaka JN (1998) What is “special” about face perception? Psychol Rev 105:482–498CrossRefPubMedGoogle Scholar
  18. Ferreira G, Keller M, Saint-Dizier H, Perrin G, Lévy F (2004) Transfer between views of conspecific faces at different ages or in different orientations by sheep. Behav Process 67:491–499CrossRefGoogle Scholar
  19. Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2001) Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291:312–316CrossRefPubMedGoogle Scholar
  20. Gheusi G, Bluthé RM, Goodall G, Dantzer R (1994) Social and individual recognition in rodents: methodological aspects and neurobiological bases. Behav Process 33:59–88CrossRefGoogle Scholar
  21. Gothard KM, Erickson CA, Amaral DG (2003) How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? Anim Cogn 7:25–36CrossRefPubMedGoogle Scholar
  22. Gothard KM, Brooks KN, Peterson MA (2009) Multiple perceptual strategies used by macaque monkeys for face recognition. Anim Cogn 12:155–167CrossRefPubMedGoogle Scholar
  23. Hagen K, Broom DM (2003) Cattle discriminate between individual familiar herd members in a learning experiment. Appl Anim Behav Sci 82:13–28CrossRefGoogle Scholar
  24. Herrnstein RJ (1990) Levels of stimulus control: a functional approach. Cognition 37:133–166CrossRefPubMedGoogle Scholar
  25. Hirata S, Fuwa K, Sugama K, Kusunoki K, Fujita S (2010) Facial perception of conspecifics: chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes. Anim Cogn 13:679–688CrossRefPubMedGoogle Scholar
  26. Houpt KA (2005) Domestic animal behavior for veterinarians and animal scientists. Blackwell, OxfordGoogle Scholar
  27. Isingrini M, Lenoir A, Jaisson P (1985) Preimaginal learning as a basis of colony-brood recognition cues in the ant Cataglyphis cursor. Proc Natl Acad Sci 82:8545–8547CrossRefPubMedGoogle Scholar
  28. Kendrick KM (1998) Intelligent perception. Appl Anim Behav Sci 57:213–231CrossRefGoogle Scholar
  29. Kendrick KM, Baldwin BA (1987) Cells in temporal cortex of conscious sheep can respond preferentially to the sight of faces. Science 236:448–450CrossRefPubMedGoogle Scholar
  30. Kendrick KM, Atkins K, Hinton MR, Broad KD, Fabre-Nys C, Keverne B (1995) Facial and vocal discrimination in sheep. Anim Behav 49:1665–1676CrossRefGoogle Scholar
  31. Kendrick KM, Atkins K, Hinton MR, Heavens P, Keverne B (1996) Are faces special for sheep? Evidence from facial and object discrimination learning tests showing effects of inversion and social familiarity. Behav Process 38:19–35CrossRefGoogle Scholar
  32. Kendrick KM, Leigh AE, Peirce JW (2001) Behavioural and neural correlates of mental imagery in sheep using face recognition paradigms. Anim Welf 10:89–101Google Scholar
  33. Lacreuse A, Martin-Malivel J, Lange HS, Herndon JG (2007) Effects of the menstrual cycle on looking preferences for faces in female rhesus monkeys. Anim Cogn 10:105–115CrossRefPubMedGoogle Scholar
  34. Lensink J, Leruste H, Tillie M (2006) L’observation du troupeau bovin : voir, interpréter, agir. France agricole, ParisGoogle Scholar
  35. Lewkowicz DJ, Sowinski R, Place S (2008) The decline of cross-species intersensory perception in human infants: underlying mechanisms and its developmental persistence. Brain Res 1242:291–302CrossRefPubMedGoogle Scholar
  36. Marsh HL, MacDonald SE (2008) The use of perceptual features in categorization by orangutans (Pongo abelli). Anim Cogn 11:569–585CrossRefPubMedGoogle Scholar
  37. Moe RO, Bakken M, Kittilsen S, Kingsley-Smith H, Spruijt BM (2006) A note on reward-related behaviour and emotional expressions in farmed silver foxes (Vulpes vulpes) _Basis for a novel tool to study animal welfare. Appl Anim Behav Sci 101:362–368CrossRefGoogle Scholar
  38. Neiworth JJ, Hassett JM, Sylvester CJ (2007) Face processing in humans and new world monkeys: the influence of experiential and ecological factors. Anim Cogn 10:125–134CrossRefPubMedGoogle Scholar
  39. Parr LA, Heintz M (2008) Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle. Anim Cogn 11:467–474CrossRefPubMedGoogle Scholar
  40. Parr LA, Winslow JT, Hopkins WD (1999) Is the inversion effect in rhesus monkeys face-specific? Anim Cogn 2:123–129CrossRefGoogle Scholar
  41. Parr LA, Winslow JT, Hopkins WD, de Waal FBM (2000) Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol 114:47–60CrossRefPubMedGoogle Scholar
  42. Parron C, Call J, Fagot J (2008) Behavioural responses to photographs by pictorially naïve baboons (Papio anubis), gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes). Behav Process 78:351–357CrossRefGoogle Scholar
  43. Pascalis O, de Haan M, Nelson CA (2002) Is face processing species specific during the first year of life? Science 296:1321–1323CrossRefPubMedGoogle Scholar
  44. Peirce JW, Kendrick KM (2000) Configurational coding, familiarity and the right hemisphere advantage for face recognition in sheep. Neuropsychologia 38:475–483CrossRefPubMedGoogle Scholar
  45. Phillips C (2002) Cattle behaviour. Farming Press, IpswichCrossRefGoogle Scholar
  46. Pokorny JJ, de Waal FDM (2009) Monkeys recognize the faces of group mates in photographs. Proc Natl Acad Sci 106:21539–21543CrossRefPubMedGoogle Scholar
  47. Porter RH, Bouissou MF (1999) Discriminative responsiveness by lambs to visual images of conspecifics. Behav Process 48:101–110CrossRefGoogle Scholar
  48. Racca A, Amadei E, Ligout S, Guo K, Meints K, Mills D (2010) Discrimination of human and dog faces and inversion responses in domestic dogs (Canis familiaris). Anim Cogn 13:525–533CrossRefPubMedGoogle Scholar
  49. Reefmann N, Wechsler B, Gygax L (2009) Behavioural and physiological assessment of positive and negative emotion in sheep. Anim Behav 78:651–659CrossRefGoogle Scholar
  50. Rehkämper G, Görlach A (1997) Visual discrimination in adult dairy bulls. J Dairy Sci 80:1613–1621CrossRefPubMedGoogle Scholar
  51. Rosenfeld SA, Van Hoesen GW (1979) Face recognition in rhesus monkey. Neuropsychology 17:503–509CrossRefGoogle Scholar
  52. Sato S, Yoshikawa C (1996) Estimation of cognition pattern of cattle by the visual attention to photograph and movie images. Animal Sci Technol 67:36–42Google Scholar
  53. Tate AJ, Fisher H, Leigh A, Kendrick KM (2006) Behavioural and neurophysiological evidence for face identity and face emotion processing in animals. Phys Trans R Soc B 361:2155–2172CrossRefGoogle Scholar
  54. Taylor AA, Davis H (1998) Individual humans as discriminative stimuli for cattle (Bos taurus). Appl Anim Behav Sci 58:13–21CrossRefGoogle Scholar
  55. Thom MD, Hurst JL (2004) Individual recognition by scent. Ann Zool Fenn 41:765–787Google Scholar
  56. Thompson RKR (1995) Natural and relational concepts in animals. In: Roitblat HL, Meyer JA (eds) Comparative approaches to cognitive science. MIT Press, Cambridge, pp 175–224Google Scholar
  57. Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. Proc R Soc Lond B 269:1423–1428CrossRefGoogle Scholar
  58. Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22:529–537CrossRefPubMedGoogle Scholar
  59. Van der Velden J, Zheng Y, Patullo BW, Macmillan DL (2008) Crayfish recognize the faces of fight opponents. PLoS ONE 3:e1695CrossRefPubMedGoogle Scholar
  60. Vauclair J, Fagot J (1996) Categorization of alphanumeric characters by Guinea baboons: within- and between-class stimulus discrimination. Curr Psychol Cogn 15:449–462Google Scholar
  61. Waring GH (2003) Horse behaviour. Noyes Publications, NorwichGoogle Scholar
  62. Wasserman EA, Kiedinger RE, Bhatt RS (1988) Conceptual behavior in pigeons: categories, subcategories, and pseudocategories. J Exp Psychol Anim Behav Process 14:235–246CrossRefGoogle Scholar
  63. Weiss DJ, Kralik JD, Hauser MD (2001) Face processing in cotton-top tamarins (Saguinus oedipus). Anim Cogn 4:191–205CrossRefGoogle Scholar
  64. Zangenehpour S, Ghazanfar AA, Lewkowicz DJ, Zatorre RJ (2009) Heterochrony and cross-species intersensory matching by infant vervet Monkeys. PLoS ONE 4(1):e4302CrossRefPubMedGoogle Scholar
  65. Zayan R (1994) Mental representations in the recognition of conspecific individuals. Behav Process 33:233–246CrossRefGoogle Scholar
  66. Zayan R, Vauclair J (1998) Categories as paradigms for comparative cognition. Behav Process 42:7–99CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Marjorie Coulon
    • 1
    • 2
  • Claude Baudoin
    • 1
  • Yvan Heyman
    • 2
  • Bertrand L. Deputte
    • 1
    • 3
  1. 1.Laboratoire d’Ethologie Expérimentale et ComparéeUniversité Paris 13VilletaneuseFrance
  2. 2.UMR 1198 Biologie du Développement et ReproductionINRAJouy-en-JosasFrance
  3. 3.Département d’EthologieEcole Nationale Vétérinaire d’AlfortMaisons-AlfortFrance

Personalised recommendations