How do horses (Equus caballus) learn from observing human action?

Abstract

A previous study demonstrated that horses can learn socially from observing humans, but could not draw any conclusions about the social learning mechanisms. Here we develop this by showing horses four different human action sequences as demonstrations of how to press a button to open a feed box. We tested 68 horses aged between 3 and 12 years. 63 horses passed the habituation phase and were assigned either to the group Hand Demo (N = 13) for which a kneeling person used a hand to press the button, Head Demo (N = 13) for which a kneeling person used the head, Mixed Demo (N = 12) for which a squatting person used both head and hand, Foot Demo (N = 12) in which a standing person used a foot, or No Demo (N = 13) in which horses did not receive a demonstration. 44 horses reached the learning criterion of opening the feeder twenty times consecutively, 40 of these were 75% of the Demo group horses and four horses were 31% of the No Demo group horses. Horses not reaching the learning criterion approached the human experimenters more often than those who did. Significantly more horses used their head to press the button no matter which demonstration they received. However, in the Foot Demo group four horses consistently preferred to use a hoof and two switched between hoof and head use. After the Mixed Demo the horses’ actions were more diverse. The results indicate that only a few horses copy behaviours when learning socially from humans. A few may learn through observational conditioning, as some appeared to adapt to demonstrated actions in the course of reaching the learning criterion. Most horses learn socially through enhancement, using humans to learn where, and which aspect of a mechanism has to be manipulated, and by applying individual trial and error learning to reach their goal.

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References

  1. Blackmore TL, Foster TM, Sumpter CE, Temple W (2008) An investigation of colour discrimination with horses (Equus caballus). Behav Process 78:387–396. https://doi.org/10.1016/j.beproc.2008.02.003

    CAS  Article  Google Scholar 

  2. Brubaker L, Udell MAR (2016) Cognition and learning in horses (Equus caballus): what we know and why we should ask more. Behav Process 126:121–131. https://doi.org/10.1016/j.beproc.2016.03.017

    Article  Google Scholar 

  3. Byrne RW (1994) The evolution of intelligence. In: Slater PJB, Halliday TR (eds) Behaviour and evolution. Cambridge University Press, Cambridge, pp 223–265

    Google Scholar 

  4. Byrne RW (2002) Imitation of novel complex actions: what does the evidence from animals mean? In: Snowdon CT, Roper TJ (eds) Advances in the study of behavior. Academic Press, San Diego, pp 77–105

    Google Scholar 

  5. Byrne RW (2009) Animal imitation. Curr Biol 19:R111–R114. https://doi.org/10.1016/j.cub.2008.11.027

    CAS  Article  PubMed  Google Scholar 

  6. Byrne R, Whiten A (1988) Machiavellian intelligence. Oxford Univ Press, Oxford

    Google Scholar 

  7. Carroll J, Murphy CJ, Neitz M, Hoeve JN, Neitz J (2001) Photopigment basis for dichromatic color vision in the horse. J Vis 1:80–87. https://doi.org/10.1167/1.2.2

    CAS  Article  PubMed  Google Scholar 

  8. Cook M, Mineka S, Wolkenstein B, Laitsch K (1985) Observational conditioning of snake fear in unrelated rhesus monkeys. J Abnorm Psychol 94:591–610

    CAS  Article  Google Scholar 

  9. Custance D, Whiten A, Fredman T (1999) Social learning of an artificial fruit task in capuchin monkeys (Cebus apella). J Comp Psychol 113:13–23. https://doi.org/10.1037/0735-7036.113.1.13

    Article  Google Scholar 

  10. Deutsche Reiterliche Vereinigung e.V (2014) Pferde verstehen—Umgang und Bodenarbeit. FN Verlag der deutschen Reiterlichen Vereinigung GmbH, Warendorforey

    Google Scholar 

  11. d’Ingeo S, Quaranta A, Siniscalchi M, Stomp M, Coste C, Bagnard C et al (2019) Horses associate individual human voices with the valence of past interactions: a behavioural and electrophysiological study. Sci Rep 9:11568. https://doi.org/10.1038/s41598-019-47960-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Dorey NR, Conover AM, Udell MAR (2014) Interspecific communication from people to horses (Equus ferus caballus) is influenced by different horsemanship training styles. J Comp Psychol 128(4):337–342. https://doi.org/10.1037/a0037255

    Article  PubMed  Google Scholar 

  13. Feh C, de Mazières J (1993) Grooming at a preferred site reduces heart rate in horses. Anim Behav 46:1191–1194. https://doi.org/10.1006/anbe.1993.1309

    Article  Google Scholar 

  14. Flannery B (1997) Relational discrimination learning in horses. Appl Anim Behav Sci 54:267–280. https://doi.org/10.1016/S0168-1591(97)00006-3

    Article  Google Scholar 

  15. Galef BG (1989) Enduring social enhancement of rats’ preferences for the palatable and the piquant. Appetite 13:81–92. https://doi.org/10.1016/0195-6663(89)90106-2

    Article  PubMed  Google Scholar 

  16. Greco BJ, Brown TK, Andrews JRM, Swaisgood RR, Caine NG (2013) Social learning in captive African elephants (Loxodonta africana africana). Anim Cogn 16:459–469. https://doi.org/10.1007/s10071-012-0586-7

    Article  PubMed  Google Scholar 

  17. Hall CA, Cassaday HJ, Derrington AM (2003) The effect of stimulus height on visual discrimination in horses. J Anim Sci 81(7):1715–1720

    CAS  Article  Google Scholar 

  18. Healy SD, Jones CM (2002) Animal learning and memory: an integration of cognition and ecology. Zoology 105:321–327. https://doi.org/10.1078/0944-2006-00071

    Article  PubMed  Google Scholar 

  19. Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231. https://doi.org/10.1111/j.1469-185X.1994.tb01506.x

    CAS  Article  PubMed  Google Scholar 

  20. Hopewell L, Leaver L, Lea S, Wills A (2010) Grey squirrels (Sciurus carolinensis) show a feature-negative effect specific to social learning. Anim Cogn 13:219–227. https://doi.org/10.1007/s10071-009-0259-3

    Article  PubMed  Google Scholar 

  21. Hoppitt W, Laland KN (2008) Social processes influencing learning in animals: a review of the evidence. Adv Study Behav 38:105–165. https://doi.org/10.1016/S0065-3454(08)00003-X

    Article  Google Scholar 

  22. Irving-Pease EK, Ryan H, Jamieson A, Dimopoulos EA, Larson G, Frantz LAF (2019) Paleogenomics of animal domestication. In: Lindqvist C, Rajora OP (eds) Paleogenomics: genome-scale analysis of ancient DNA. Springer International Publishing, Cham, pp 225–272

    Google Scholar 

  23. Krueger K, Heinze J (2008) Horse sense: social status of horses (Equus caballus) affects their likelihood of copying other horses` behavior. Anim Cogn 11:431–439. https://doi.org/10.1007/s10071-007-0133-0

    Article  PubMed  Google Scholar 

  24. Krueger K, Flauger B, Farmer K, Maros K (2011) Horses (Equus caballus) use human local enhancement cues and adjust to human attention. Anim Cogn 14:187–201. https://doi.org/10.1007/s10071-010-0352-7

    Article  PubMed  Google Scholar 

  25. Krueger K, Farmer K, Heinze J (2014) The effects of age, rank and neophobia on social learning in horses. Anim Cogn 17:645–655. https://doi.org/10.1007/s10071-013-0696-x

    Article  PubMed  Google Scholar 

  26. Kubinyi E, Topál J, Miklósi Á, Csányi V (2003) Dogs (Canis familiaris) learn their owners via observation in a manipulation task. J Comp Psychol 117:156–165. https://doi.org/10.1037/0735-7036.117.2.156

    Article  PubMed  Google Scholar 

  27. Lamp JF, Andre J (2012) Cross-modal recognition of human individuals in domestic horses (Equus caballus). Anim Cogn 15:623–630. https://doi.org/10.1007/s10071-012-0490-1

    Article  Google Scholar 

  28. Leadbeater E, Dawson EH (2017) A social insect perspective on the evolution of social learning mechanisms. Proc Natl Acad Sci USA 114:7838–7845

    CAS  Article  Google Scholar 

  29. Lesimple C, Sankey C, Richard M-A, Hausberger M (2012) Do horses expect humans to solve their problems? Front Psychol 3:306. https://doi.org/10.3389/fpsyg.2012.00306

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Lovrovich P, Sighieri C, Baragli P (2015) Following human-given cues or not? Horses (Equus caballus) get smarter and change strategy in a delayed three choice task. Appl Anim Behav Sci 166:80–88. https://doi.org/10.1016/j.applanim.2015.02.017

    Article  Google Scholar 

  31. Malavasi R, Huber L (2016) Evidence of heterospecific referential communication from domestic horses (Equus caballus) to humans. Anim Cogn 19:899–909. https://doi.org/10.1007/s10071-016-0987-0

    Article  PubMed  Google Scholar 

  32. Maros K, Gácsi M, Miklósi Á (2008) Comprehension of human pointing gestures in horses (Equus caballus). Anim Cogn 11:457–466. https://doi.org/10.1007/s10071-008-0136-5

    Article  PubMed  Google Scholar 

  33. McDonnell SM, Haviland JCS (1995) Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 43:147–188. https://doi.org/10.1016/0168-1591(94)00550-X

    Article  Google Scholar 

  34. Mejdell CM, Buvik T, Jørgensen GHM, Bøe KE (2016) Horses can learn to use symbols to communicate their preferences. Appl Anim Behav Sci 184:66–73. https://doi.org/10.1016/j.applanim.2016.07.014

    Article  Google Scholar 

  35. Mersmann D, Tomasello M, Call J, Kaminski J, Taborsky M (2011) Simple mechanisms can explain social learning in domestic dogs (Canis familiaris). Ethology 117:675–690. https://doi.org/10.1111/j.1439-0310.2011.01919.x

    Article  Google Scholar 

  36. Miklósi Á, Soproni K (2006) A comparative analysis of animals’ understanding of the human pointing gesture. Anim Cogn 9:81–93. https://doi.org/10.1007/s10071-005-0008-1

    Article  PubMed  Google Scholar 

  37. Mills DS, McDonnell SM (2005) The domestic horse. Cambridge University Press, Camebridge

    Google Scholar 

  38. Nicol CJ (2002) Equine learning: progress and suggestions for future research. Appl Anim Behav Sci 78:193–208. https://doi.org/10.1016/S0168-1591(02)00093-X

    Article  Google Scholar 

  39. Pfungst O (1907) Der Kluge Hans. Ein Beitrag zur nichtverbalen Kommunikation. Frankfurter Fachbuchhandlung für Psychologie, Frankfurt am Main

    Google Scholar 

  40. Pongrácz P, Miklósi Á, Kubinyi E, Gurobi K, Topál J, Csányi V (2001) Social learning in dogs: the effect of a human demonstrator on the performance of dogs in a detour task. Anim Behav 62:1109–1117. https://doi.org/10.1006/anbe.2001.1866

    Article  Google Scholar 

  41. Pongrácz P, Miklósi Á, Timár-Geng K, Csányi V (2004) Verbal attention getting as a key factor in social learning between dog and human. J Comp Psychol 118:375–383

    Article  Google Scholar 

  42. Pongrácz P, Miklósi Á, Vida V, Csányi V (2005) The pet dogs ability for learning from a human demonstrator in a detour task is independent from the breed and age. Appl Anim Behav Sci 90:309–323. https://doi.org/10.1016/j.applanim.2004.08.004

    Article  Google Scholar 

  43. Proops L, McComb K (2010) Attributing attention: the use of human-given cues by domestic horses (Equus caballus). Anim Cogn 13:197–205. https://doi.org/10.1007/s10071-009-0257-5

    Article  PubMed  Google Scholar 

  44. Proops L, McComb K (2012) Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans. Proc R Soc B 279:3131–3138. https://doi.org/10.1098/rspb.2012.0626

    Article  PubMed  Google Scholar 

  45. Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). Proc Natl Acad Sci USA 106:947–951. https://doi.org/10.1073/pnas.0809127105

    CAS  Article  PubMed  Google Scholar 

  46. Proops L, Walton M, McComb K (2010) The use of human-given cues by domestic horses, Equus caballus, during an object choice task. Anim Behav 79:1205–1209. https://doi.org/10.1016/j.anbehav.2010.02.015

    Article  Google Scholar 

  47. Proops L, Rayner J, Taylor AM, McComb K (2013) The responses of young domestic horses to human-given cues. PLoS One. https://doi.org/10.1371/journal.pone.0067000

    Article  PubMed  PubMed Central  Google Scholar 

  48. R Development Core Team (2019) R: a language and environment for statistical computing. http://www.R-project.org

  49. Rescorla RA, Holland PC (1982) Behavioral Studies of Associative Learning in Animals. Ann Rev Psychol 33:265–308

    Article  Google Scholar 

  50. Ringhofer M, Yamamoto S (2017) Domestic horses send signals to humans when they face with an unsolvable task. Anim Cogn 20:397–405. https://doi.org/10.1007/s10071-016-1056-4

    Article  PubMed  Google Scholar 

  51. Rørvang MV, Ahrendt LP, Christensen JW (2015) A trained demonstrator has a calming effect on naïve horses when crossing a novel surface. Appl Anim Behav Sci 171:117–120. https://doi.org/10.1016/j.applanim.2015.08.008

    Article  Google Scholar 

  52. Sankey C, Henry S, André N, Richard-Yris M-A, Hausberger M (2011) Do horses have a concept of person? PLoS One. https://doi.org/10.1371/journal.pone.0018331

    Article  PubMed  PubMed Central  Google Scholar 

  53. Schuetz A, Farmer K, Krueger K (2017) Social learning across species: horses (Equus caballus) learn from humans by observation. Anim Cogn 20:567–573. https://doi.org/10.1007/s10071-016-1060-8

    Article  PubMed  Google Scholar 

  54. Shettleworth SJ (1998) Cognition, evolution and behaviour. Oxford University Press, Oxford

    Google Scholar 

  55. Smith AV, Proops L, Grounds K, Wathan J, McComb K (2016) Functionally relevant responses to human facial expressions of emotion in the domestic horse (Equus caballus). Biol Lett. https://doi.org/10.1098/rsbl.2015.0907

    Article  PubMed  PubMed Central  Google Scholar 

  56. Thorpe WH (1963) Learning and instinct in animals. Methuen, London

    Google Scholar 

  57. Tomasello M (1990) Cultural transmission in the tool use and communicatory signalling of chimpanzees? In: Parker ST, Gibson KR (eds) Language and intelligence in monkeys and apes. Cambridge University Press, Cambridge, pp 274–311

    Google Scholar 

  58. Topál J, Miklósi A, Csányi V (1997) Dog-human relationship affects problem solving be-havior in the dog. Anthrozoos 10:214–224

    Article  Google Scholar 

  59. Whalen A, Cownden D, Laland K (2015) The learning of action sequences through social transmission. Anim Cogn 18:1093–1103. https://doi.org/10.1007/s10071-015-0877-x

    Article  PubMed  Google Scholar 

  60. Whiten A, Ham R (1992) On the nature and evolution of imitation in the animal kingdom: reappraisal of a century of research. Adv Study Behav 21:239–283

    Article  Google Scholar 

  61. Whiten A, Horner V, Litchfield CA, Marshall-Pescini S (2004) How do apes ape? Learn Behav 32:36–52. https://doi.org/10.3758/BF03196005

    Article  PubMed  Google Scholar 

  62. Zajonc RB (1965) Social facilitation. Science 149:269–274. https://doi.org/10.1126/science.149.3681.269

    CAS  Article  PubMed  Google Scholar 

  63. Zentall TR (2006) Imitation: definitions, evidence, and mechanisms. Anim Cogn 9:335–353. https://doi.org/10.1007/s10071-006-0039-2

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Richard Byrne, Ádam Miklósi and many others for discussing the data, many persons for assisting in the experiments, several horse owners for supplying the experiment with their horses and three anonymous referees and the editor for helping to improve the manuscript.

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This study was not funded.

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Correspondence to Konstanze Krueger.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed and approved by the animal welfare board of Nürtingen-Geislingen University. All procedures performed in the study involving human participants were in accordance with the ethical standards of the ethics committee of Nürtingen-Geislingen University and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Bernauer, K., Kollross, H., Schuetz, A. et al. How do horses (Equus caballus) learn from observing human action?. Anim Cogn 23, 1–9 (2020). https://doi.org/10.1007/s10071-019-01310-0

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Keywords

  • Copying
  • Equus caballus
  • Human demonstrator
  • Interspecies specific social learning
  • Social learning
  • Social enhancement