Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

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

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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Notes

  1. 1.

    Training was performed by a skilled ethologist, well versed in learning theory and experienced in horse training (C. Sankey, woman, dark hair, see also Sankey et al. 2010) and moreover supervised by a 30 years experienced university teacher on learning rules (M-A Richard-Yris) and a research scientist with more than 30 years of experience in horse training (M. Hausberger).

References

  1. Altman J (1974) Observational study of behaviour: sampling methods. Behav 49:227–267

  2. Bisaz R, Conboy L, Sandi C (2009) Learning under stress: a role for the neural cell adhesion molecule NCAM. Neurobiol Learn Mem 91:333–342

  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 75:2892–2898

  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 112:158–173

  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):487–490

  6. De Passillé AM, Rushen J, Ladewig J, Petherick JC (1996) Dairy calves’ discrimination of people based on previous handling. J Anim Sci 74:969–974

  7. Domjan M (2003) The principles of learning and behaviour, 5th edn. Wadsworth-Thomson Learning, Belmont

  8. Fureix C, Jego P, Sankey C, Hausberger M (2009) How horses (Equus caballus) see the world: humans as significant “objects”. Anim Cogn 12:643–654

  9. Ghirlanda S, Jansson L, Enquist M (2002) Chickens prefer beautiful humans. Hum Nat—Interdiscip Biosoci persp 13(3):383–389

  10. Hanggi EB (2003) Discrimination learning based on relative size concepts in horses (Equus caballus). Appl Anim Behav Sci 83:201–213

  11. Hanggi EB, Ingersoll JF (2009) Long-term memory for categories and concepts in horses (Equus caballus). Anim Cogn 12(3):451–462

  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 76:339–344

  13. Hausberger M, Roche H, Henry S, Visser E (2008) A review of the human-horse relationship. Appl Anim Behav Sci 109:1–24

  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):213–222

  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):245–252

  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 30:61–72

  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 40:129–142

  18. Hemsworth PH, Price EO, Borgwardt R (1996) Behavioural responses of domestic pigs and cattle to human kind novel stimuli. Appl Anim Behav Sci 50:43–56

  19. Henry S, Hemery D, Richard MA, Hausberger M (2005) Human-mare relationships and behaviour of foals toward humans. Appl Anim Behav Sci 93:341–362

  20. Herd JA (1991) Cardiovascular response to stress. Physiol Rev 71(1):305–330

  21. Hinde R (1979) Towards understanding relationships. Academic Press, London

  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 40:144–149

  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):357–368

  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):1–11

  25. Jones RB (1994) Regular handling and the domestic chick’s fear of human beings: generalisation of response. Appl Anim Behav Sci 42:129–143

  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):69–115

  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 73:45–58

  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):492–508

  29. Larose C, Rogers L, Richard-Yris M-A, Hausberger M (2006) Laterality of horses associated with emotionality in novel situations. Lat 11(4):355–367

  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):163–173

  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 78:1213–1218

  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 78:1219–1226

  33. Marinier SL, andand Alexander AJ (1994) The use of a maze in testing learning and memory in horse. Appl Anim Behav Sci 39:177–182

  34. Maros K, Gácsi M, Miklósi A (2008) Comprehension of human pointing gestures in horses. Anim Cogn 11(3):457–466

  35. McDonnell SM (2000) How to rehabilitate horses with injection shyness (or any procedure non-compliance). AEEP Procee 46:168–172

  36. McDonnell S, Haviland J (1995) Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 43:147–188

  37. McDonnell S, Poulin A (2002) Equid play ethogram. Appl Anim Behav Sci 78:263–290

  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 196–211

  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):209–220

  40. McKinley J, Sambrook TD (2000) Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim Cogn 3:13–22

  41. Mendl M (1999) Performing under pressure: stress and cognitive function. Appl Anim Behav Sci 65:221–244

  42. Miklósi Á, Polgárdi R, Topál J, Csányi V (1998) Use of experimenter-given cues in dogs. Anim Cogn 1:113–121

  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):179–186

  44. Miklósi Á, Soproni K (2006) A comparative analysis of animals’ understanding of the human pointing gesture. Anim Cogn 9:81–93

  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 80:1106–1112

  46. Oliveira N (1991) L’art équestre. Ed Crépin Leblond, Paris

  47. Prescott MJ, Buchanan-Smith HM (2003) Training non-human primates using positive reinforcement techniques. J Appl Anim Wel Sci 6(3):157–161

  48. Reinhardt V (1991) Training adult male rhesus monkeys to actively cooperate during in-homecage venipuncture. Anim Tech 42:11–17

  49. Ridgway K, Harman J (1999) Equine back rehabilitation. Vet Clinics North Amer: equine practice 15:263–280

  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 79:869–875

  51. Shors T (2004) Learning during stressful times. Learn Mem 11:137–144

  52. Skinner BF (1938) The behaviour of organisms. Appleton-Century-Crofts, New-York

  53. Skinner BF (1981) Selection by consequences. Sci 213:501–504

  54. Søndergaard E, Halekoh U (2003) Young horses’ reactions to humans in relation to handling and social environment. Appl Anim Behav Sci 84:265–280

  55. Tanida H, Miura A, Tanaka T, Yoshimoto T (1995) Behavioural response to humans in individually handled weanling pigs. Appl Anim Behav Sci 42:249–259

  56. Tanida H, Nagano Y (1998) The ability of miniature pigs to discriminate between a stranger and their familiar handler. Appl Anim Behav Sci 56:149–159

  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 76:289–296

  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 116:228–236

  59. von Uexküll J (1965) Monde animaux et monde humain, suivi de la théorie de la signifcation, Ed: Denoël, Paris

  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 101:185–242

  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 184–195

  62. Waring GH (2003) Horse behaviour. Noyes Publications, William Andrew Publishing, New York

  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 16:481–488

  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 46:137–143

Download references

Acknowledgments

The authors are grateful to Mr. S. Gicqueau from the ‘‘Lycée agricole La Touche’’ in Ploermel and Mr. F. Reyé from the ‘‘CFA de Pommerit Jaudy’’ (France) for allowing us to use their ponies and facilities and all the staff for their help and understanding. We are grateful to Hélène Leroy, Anne Ouvrard and Xavier Comparé for their help filming the animals’ training. Thanks to Marine Grandgeorge who was the unfamiliar experimenter. Carol Sankey was supported by a PhD grant of the “Haras Nationaux” and the “Region Bretagne”. This study, which was funded by the COST of the “Haras Nationaux”, complies with the French laws concerning the use of animals in research.

Author information

Correspondence to Carol Sankey.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sankey, C., Richard-Yris, M., Henry, S. et al. Reinforcement as a mediator of the perception of humans by horses (Equus caballus). Anim Cogn 13, 753–764 (2010). https://doi.org/10.1007/s10071-010-0326-9

Download citation

Keywords

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