Animal Cognition

, Volume 13, Issue 5, pp 753–764 | Cite as

Reinforcement as a mediator of the perception of humans by horses (Equus caballus)

  • Carol Sankey
  • Marie-Annick Richard-Yris
  • Séverine Henry
  • Carole Fureix
  • Fouad Nassur
  • Martine Hausberger
Original Paper

Abstract

A central question in the interspecific human/animal relationship is how domestic animals perceive humans as a significant element of their environment. In this study, we tested the hypothesis that the use of positive or negative reinforcement in horse training may have consequences on the animals’ perception of humans, as a positive, negative or neutral element. Two groups of ponies were trained to walk backwards in response to a vocal order using either positive or negative reinforcement. Heart rate monitors and behavioural observations were used to assess the animals’ perception of humans on the short (just after training) and long (5 months later) terms. The results showed that the type of reinforcement had a major effect on the subsequent animals’ perception of familiar and unfamiliar humans. Negative reinforcement was rapidly associated with an increased emotional state, as revealed by heart rate measurements and behavioural observations (head movements and ears laid back position). Its use led the ponies to seek less contact with humans. On the contrary, ponies trained with positive reinforcement showed an increased interest in humans and sought contact after training. This is especially remarkable as it was reached in a maximum of 5 sessions of 1 to 3 min (i.e. 5 to 15 min) and had lasting effects (visible after 5 months). Even learning was positively influenced by positive reinforcement. Overall, horses seem capable of associating humans to particular experiences and display extended long-term memory abilities.

Keywords

Perception of humans Human/animal relationship Positive reinforcement Negative reinforcement Equus caballus 

References

  1. Altman J (1974) Observational study of behaviour: sampling methods. Behav 49:227–267CrossRefGoogle Scholar
  2. Bisaz R, Conboy L, Sandi C (2009) Learning under stress: a role for the neural cell adhesion molecule NCAM. Neurobiol Learn Mem 91:333–342CrossRefPubMedGoogle Scholar
  3. Boivin X, Nowak R, Desprès G, Tournadre H, Le Neindre P (1997) Discrimination between shepherds by lambs reared under artificial conditions. J Anim Sci 75:2892–2898PubMedGoogle Scholar
  4. Cloutier S, Newberry RC (2008) Use of a conditioning technique to reduce stress associated with repeated intra-peritoneal injections in laboratory rats. Appl Anim Behav Sci 112:158–173CrossRefGoogle Scholar
  5. De Boyer Des Roches A, Richard-Yris M-A, Henry S, Ezzaouia M, Hausberger M (2008) Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects’ emotional value. Physiol Behav 94(3):487–490CrossRefPubMedGoogle Scholar
  6. De Passillé AM, Rushen J, Ladewig J, Petherick JC (1996) Dairy calves’ discrimination of people based on previous handling. J Anim Sci 74:969–974PubMedGoogle Scholar
  7. Domjan M (2003) The principles of learning and behaviour, 5th edn. Wadsworth-Thomson Learning, BelmontGoogle Scholar
  8. Fureix C, Jego P, Sankey C, Hausberger M (2009) How horses (Equus caballus) see the world: humans as significant “objects”. Anim Cogn 12:643–654CrossRefPubMedGoogle Scholar
  9. Ghirlanda S, Jansson L, Enquist M (2002) Chickens prefer beautiful humans. Hum Nat—Interdiscip Biosoci persp 13(3):383–389Google Scholar
  10. Hanggi EB (2003) Discrimination learning based on relative size concepts in horses (Equus caballus). Appl Anim Behav Sci 83:201–213CrossRefGoogle Scholar
  11. Hanggi EB, Ingersoll JF (2009) Long-term memory for categories and concepts in horses (Equus caballus). Anim Cogn 12(3):451–462CrossRefPubMedGoogle Scholar
  12. Hausberger M, Muller C (2002) A brief note on some possible factors involved in the reactions of horses to humans. Appl Anim Behav Sci 76:339–344CrossRefGoogle Scholar
  13. Hausberger M, Roche H, Henry S, Visser E (2008) A review of the human-horse relationship. Appl Anim Behav Sci 109:1–24CrossRefGoogle Scholar
  14. Heleski C, Bauson L, Bello N (2008) Evaluating the addition of positive reinforcement for learning a frightening task: a pilot study with horses. J Appl Anim Wel Sci 11(3):213–222CrossRefGoogle Scholar
  15. Hemsworth PH, Barnett JL, Hansen C (1987) The influence of inconsistent handling by humans on the behaviour, growth and corticosteroids of young pigs. Appl Anim Behav Sci 17(3–4):245–252CrossRefGoogle Scholar
  16. Hemsworth PH, Barnett JL (1991) The effect of aversively handling pigs, either individually or in groups, on their behaviour, growth and corticosteroids. Appl Anim Behav Sci 30:61–72CrossRefGoogle Scholar
  17. Hemsworth PH, Coleman GJ, Barnett JL (1994) Stimulus generalization: the inability of pigs to discriminate between humans on the basis of their previous handling experience. Appl Anim Behav Sci 40:129–142CrossRefGoogle Scholar
  18. Hemsworth PH, Price EO, Borgwardt R (1996) Behavioural responses of domestic pigs and cattle to human kind novel stimuli. Appl Anim Behav Sci 50:43–56CrossRefGoogle Scholar
  19. Henry S, Hemery D, Richard MA, Hausberger M (2005) Human-mare relationships and behaviour of foals toward humans. Appl Anim Behav Sci 93:341–362CrossRefGoogle Scholar
  20. Herd JA (1991) Cardiovascular response to stress. Physiol Rev 71(1):305–330PubMedGoogle Scholar
  21. Hinde R (1979) Towards understanding relationships. Academic Press, LondonGoogle Scholar
  22. Holden MD, Gregory J, Watkins V, Radford L (2006) Operant-conditioning programme for White rhinoceros and Indian or Greater one-horned Asian rhinoceros. Int Zoo Year Book 40:144–149CrossRefGoogle Scholar
  23. Innes L, McBride S (2008) Negative versus positive reinforcement: an evaluation of training strategies for rehabilitated horses. Appl Anim Behav Sci 112(3–4):357–368CrossRefGoogle Scholar
  24. Jezierski T, Jaworski Z, Gorecka A (1999) Effects of handling on behaviour and heart rate in konik horses: comparison of stable and forest reared youngstock. Appl Anim Behav Sci 62(1):1–11CrossRefGoogle Scholar
  25. Jones RB (1994) Regular handling and the domestic chick’s fear of human beings: generalisation of response. Appl Anim Behav Sci 42:129–143CrossRefGoogle Scholar
  26. Kiley-Worthington M (1976) The tail movements of ungulates, canids and felids with particular reference to their causation and function as displays. Behav LVI (1–2):69–115Google Scholar
  27. Koba Y, Tanida H (2001) How do miniature pigs discriminate between people? discrimination between people wearing coveralls of the same colour. Appl Anim Behav Sci 73:45–58CrossRefPubMedGoogle Scholar
  28. Lansade L, Bouissou M-F (2008) Reactivity to humans: a temperament trait of horses which is stable across time and situations. Appl Anim Behav Sci 114(3–4):492–508CrossRefGoogle Scholar
  29. Larose C, Rogers L, Richard-Yris M-A, Hausberger M (2006) Laterality of horses associated with emotionality in novel situations. Lat 11(4):355–367Google Scholar
  30. Laule GE, Bloomsmith MA, Scapiro SJ (2003) The use of positive reinforcement training techniques to enhance the care, management and welfare of primates in the laboratory. J Appl Anim Wel Sci 6(3):163–173CrossRefGoogle Scholar
  31. Lensink J, Boivin X, Pradel P, LeNeindre P, Veissier I (2000a) Reducing veal calves’ reactivity to people by providing additional human contact. J Anim Sci 78:1213–1218PubMedGoogle Scholar
  32. Lensink J, Fernandez X, Boivin X, Pradel P, LeNeindre P, Veissier I (2000b) The impact of gentle contacts on ease of handling, welfare, and growth of calves and on quality of veal meat. J Anim Sci 78:1219–1226PubMedGoogle Scholar
  33. Marinier SL, andand Alexander AJ (1994) The use of a maze in testing learning and memory in horse. Appl Anim Behav Sci 39:177–182CrossRefGoogle Scholar
  34. Maros K, Gácsi M, Miklósi A (2008) Comprehension of human pointing gestures in horses. Anim Cogn 11(3):457–466CrossRefPubMedGoogle Scholar
  35. McDonnell SM (2000) How to rehabilitate horses with injection shyness (or any procedure non-compliance). AEEP Procee 46:168–172Google Scholar
  36. McDonnell S, Haviland J (1995) Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 43:147–188CrossRefGoogle Scholar
  37. McDonnell S, Poulin A (2002) Equid play ethogram. Appl Anim Behav Sci 78:263–290CrossRefGoogle Scholar
  38. McGreevy P, McLean A (2005) Behavioural problems with the ridden horse. In: Mills DS, Mc Donnell SM (eds) The domestic horse: the origins, development and management of its behaviour. Cambridge University Press, Cambridge, pp 196–211Google Scholar
  39. McKinley J, Buchanan-Smith HM, Basset L (2003) Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: ease of training and time investment. J Appl Anim Wel Sci 6(3):209–220CrossRefGoogle Scholar
  40. McKinley J, Sambrook TD (2000) Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim Cogn 3:13–22CrossRefGoogle Scholar
  41. Mendl M (1999) Performing under pressure: stress and cognitive function. Appl Anim Behav Sci 65:221–244CrossRefGoogle Scholar
  42. Miklósi Á, Polgárdi R, Topál J, Csányi V (1998) Use of experimenter-given cues in dogs. Anim Cogn 1:113–121CrossRefGoogle Scholar
  43. Miklósi Á, Pongrácz P, Lakatos G, Topál J, Csányi V (2005) A comparative study of the use of visual communicative signals in interactions between dogs (Canis familiaris) and humans and cats (Felis catus) and humans. J Comp Psychol 119(2):179–186CrossRefPubMedGoogle Scholar
  44. Miklósi Á, Soproni K (2006) A comparative analysis of animals’ understanding of the human pointing gesture. Anim Cogn 9:81–93CrossRefPubMedGoogle Scholar
  45. Munksgaard L, De Passillé AM, Rushen J, Thodberg K, Jensen MB (1997) Discrimination of people by dairy cows based on handling. J Dairy Sci 80:1106–1112CrossRefPubMedGoogle Scholar
  46. Oliveira N (1991) L’art équestre. Ed Crépin Leblond, ParisGoogle Scholar
  47. Prescott MJ, Buchanan-Smith HM (2003) Training non-human primates using positive reinforcement techniques. J Appl Anim Wel Sci 6(3):157–161CrossRefGoogle Scholar
  48. Reinhardt V (1991) Training adult male rhesus monkeys to actively cooperate during in-homecage venipuncture. Anim Tech 42:11–17Google Scholar
  49. Ridgway K, Harman J (1999) Equine back rehabilitation. Vet Clinics North Amer: equine practice 15:263–280Google Scholar
  50. Sankey C, Richard-Yris M-A, Leroy H, Henry S, Hausberger M (2010) Training experience induces lasting memories of humans in horses, Equus caballus. Anim Behav 79:869–875CrossRefGoogle Scholar
  51. Shors T (2004) Learning during stressful times. Learn Mem 11:137–144CrossRefPubMedGoogle Scholar
  52. Skinner BF (1938) The behaviour of organisms. Appleton-Century-Crofts, New-YorkGoogle Scholar
  53. Skinner BF (1981) Selection by consequences. Sci 213:501–504CrossRefGoogle Scholar
  54. Søndergaard E, Halekoh U (2003) Young horses’ reactions to humans in relation to handling and social environment. Appl Anim Behav Sci 84:265–280CrossRefGoogle Scholar
  55. Tanida H, Miura A, Tanaka T, Yoshimoto T (1995) Behavioural response to humans in individually handled weanling pigs. Appl Anim Behav Sci 42:249–259CrossRefGoogle Scholar
  56. Tanida H, Nagano Y (1998) The ability of miniature pigs to discriminate between a stranger and their familiar handler. Appl Anim Behav Sci 56:149–159CrossRefGoogle Scholar
  57. Visser EK, van Reenen CG, van der Werf JTN, Schilder MBH, Knaap JH, Barneveld A, Blokhuis HJ (2002) Heart rate and heart rate variability during a novel object test and a handling test in young horses. Physiol Behav 76:289–296CrossRefPubMedGoogle Scholar
  58. Von Borstel UU, Heatly Duncan IJ, Shoveller AK, Merkies K, Keeling LJ, Millman ST (2009) Impact of riding in a coercively obtained Rollkur posture on welfare and fear of performance horses. Appl Anim Behav Sci 116:228–236CrossRefGoogle Scholar
  59. von Uexküll J (1965) Monde animaux et monde humain, suivi de la théorie de la signifcation, Ed: Denoël, ParisGoogle Scholar
  60. Waiblinger S, Boivin X, Pederson V, Tosi MV, Janczak A, Visser K, Jones RB (2006) Assessing the human-animal relationship in farmed species: a critical review. Appl Anim Behav Sci 101:185–242CrossRefGoogle Scholar
  61. Waran N, Casey R (2005) Horse training. In: Mills DS, Mc Donnell SM (eds) The domestic horse: the origins, development and management of its behaviour. Cambridge University Press, Cambridge, pp 184–195Google Scholar
  62. Waring GH (2003) Horse behaviour. Noyes Publications, William Andrew Publishing, New YorkGoogle Scholar
  63. Warren-Smith AK, McGreevy PD (2007) The use of blended positive and negative reinforcement in shaping the halt response of horses (Equus caballus). Anim Wel 16:481–488Google Scholar
  64. Wolff A, Hausberger M (1996) Learning and memorisation of two different tasks in horses: the effects of age, sex and sire. Appl Anim Behav Sci 46:137–143CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Carol Sankey
    • 1
  • Marie-Annick Richard-Yris
    • 2
  • Séverine Henry
    • 1
  • Carole Fureix
    • 1
    • 2
  • Fouad Nassur
    • 2
  • Martine Hausberger
    • 1
    • 2
  1. 1.Laboratoire d’éthologie animale et humaine, UMR 6552 CNRSUniversité de Rennes 1PaimpontFrance
  2. 2.Laboratoire d’éthologie animale et humaine—UMR 6552Université de Rennes 1/CNRSRennes CedexFrance

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