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

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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.

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Notes

  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

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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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.

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Authors and Affiliations

  1. Laboratoire d’éthologie animale et humaine, UMR 6552 CNRS, Université de Rennes 1, Station Biologique, 35380, Paimpont, France

    Carol Sankey, Séverine Henry, Carole Fureix & Martine Hausberger

  2. Laboratoire d’éthologie animale et humaine—UMR 6552, Université de Rennes 1/CNRS, Avenue du Général Leclerc, Campus de Beaulieu, 35042, Rennes Cedex, France

    Marie-Annick Richard-Yris, Carole Fureix, Fouad Nassur & Martine Hausberger

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  1. Carol Sankey
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  2. Marie-Annick Richard-Yris
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  3. Séverine Henry
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  4. Carole Fureix
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  5. Fouad Nassur
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  6. Martine Hausberger
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Correspondence to Carol Sankey.

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Sankey, C., Richard-Yris, MA., 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

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  • DOI: https://doi.org/10.1007/s10071-010-0326-9

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