Animal Cognition

, Volume 19, Issue 5, pp 899–909 | Cite as

Evidence of heterospecific referential communication from domestic horses (Equus caballus) to humans

Original Paper

Abstract

Referential communication occurs when a sender elaborates its gestures to direct the attention of a recipient to its role in pursuit of the desired goal, e.g. by pointing or showing an object, thereby informing the recipient what it wants. If the gesture is successful, the sender and the recipient focus their attention simultaneously on a third entity, the target. Here we investigated the ability of domestic horses (Equus caballus) to communicate referentially with a human observer about the location of a desired target, a bucket of food out of reach. In order to test six operational criteria of referential communication, we manipulated the recipient’s (experimenter) attentional state in four experimental conditions: frontally oriented, backward oriented, walking away from the arena and frontally oriented with other helpers present in the arena. The rate of gaze alternation was higher in the frontally oriented condition than in all the others. The horses appeared to use both indicative (pointing) and non-indicative (nods and shakes) head gestures in the relevant test conditions. Horses also elaborated their communication by switching from a visual to a tactile signal and demonstrated perseverance in their communication. The results of the tests revealed that horses used referential gestures to manipulate the attention of a human recipient so to obtain an unreachable resource. These are the first such findings in an ungulate species.

Keywords

Domestic horse Referential communication Human–animal communication Intentional communication Referential gesture 

Supplementary material

10071_2016_987_MOESM1_ESM.jpg (778 kb)
Online Resource 1. Pictures of the different phases of the trials. The horse is handled by the experimenter into the arena from one of two entrances (1). It is shown a baited bucket at the opposite side of the arena (2) and taken back at the entrance (3), where it is shown the other baited bucket (4). The horse is then handled at the release point (5) and released (6). During the experimental condition ‘Forward’, the experimenter remains in the same position at the release point, whereas she is faced away from the arena in the condition ‘Backward’ (7a), and walks away from the arena in the condition ‘Walk-away’ (7b, the white circle shows the experimenter). During the condition ‘Many’, two helpers show the horse the baited buck, and remain behind the bucket until the end of the trial (7c). (JPEG 777 kb)

Online Resource 2. The video shows samples of the experimental conditions and coded behaviours. The target (bucket of food) is on the other side of the visible fence. The first two samples show gaze alternation between the horse and the experimenter during the condition ‘Forward’ (the experimenter was frontally oriented towards the center of the arena). In both samples, the experimenter stayed about in the direction of the video camera. The third sample shows a horse pointing to the bucket while at the same time performing a head gesture (very quick movement of the head along the sagittal plane). The fourth sample shows a horse elaborating its communication from visual to tactile during the condition ‘Forward’: while close to the target, she first pointed at it and used some head gestures, then walked back to the experimenter, touched her and again to the target. When she stopped close to it, she alternated her gaze between the walking experimenter and the target. The fifth sample shows another case of elaboration of communication, this time during the condition ‘Backward’ (the experimenter faced away from the gates, i.e. her back was oriented to the center of the arena). The horse walked back to the experimenter and touched her. (MP4 70,313 kb)

10071_2016_987_MOESM3_ESM.jpg (315 kb)
Online Resource 3. The first and the third trial of each condition, and the first and the last trial regardless of condition, were compared for each coded behaviour to test for learning during the experiment. In the figure, the medians of the absolute numbers of the coded behaviours are shown, with whiskers extending to the 25 % and 75 % quartile. The abbreviations on the x-axis refer to the different experimental conditions: M = Many, WA = Walk-away, F = Forward, B = Backward; the number next to each condition refers to the trial (1 = first, 3 = third). 1st and Last refer to the first and last trial regardless of condition. Under each tested pair, the z and p values of the two-sample Wilcoxon Signed-rank test. (JPEG 315 kb)

References

  1. Bates E, Camaioni L, Volterra V (1975) The acquisition of performatives prior to speech. Merrill-Palmer Q Behav Dev 21(3):205–226Google Scholar
  2. Bates E, Benigni L, Bretherton I, Camaioni L, Volterra V (1979) The emergence of symbols: cognition and communication in infancy. Academic Press, New YorkGoogle Scholar
  3. Birke L (2007) Learning to speak horse: the culture of natural horsemanship. Soc Anim 15(3):217–239CrossRefGoogle Scholar
  4. Bourjade M, Meguerditchian A, Maille A, Gaunet F, Vauclair J (2014) Olive baboons, Papio anubis, adjust their visual and auditory intentional gestures to the visual attention of others. Anim Behav 87:121–128CrossRefGoogle Scholar
  5. Bourjade M, Canteloup C, Meguerditchian A, Vauclair J, Gaunet F (2015) Training experience in gestures affects the display of social gaze in baboons’ communication with a human. Anim Cogn 18(1):239–250CrossRefPubMedGoogle Scholar
  6. Call JE, Tomasello ME (2007) The gestural communication of apes and monkeys. Taylor & Francis Group/Lawrence Erlbaum Associates, New YorkGoogle Scholar
  7. Canteloup C, Bovet D, Meunier H (2015) Intentional gestural communication and discrimination of human attentional states in rhesus macaques (Macaca mulatta). Anim cogn 18:875–883CrossRefPubMedGoogle Scholar
  8. Cartmill EA, Byrne RW (2007) Orangutans modify their gestural signaling according to their audience’s comprehension. Curr Biol 17:1345–1348CrossRefPubMedGoogle Scholar
  9. Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosc Biobehav R 24(6):581–604CrossRefGoogle Scholar
  10. Gaunet F (2010) How do guide dogs and pet dogs (Canis familiaris) ask their owners for their toy and for playing? Anim Cogn 13:311–323CrossRefPubMedGoogle Scholar
  11. Gaunet F, Deputte BL (2011) Functionally referential and intentional communication in the domestic dog: effects of spatial and social contexts. Anim Cogn 14:849–860CrossRefPubMedGoogle Scholar
  12. Hanggi EB (1999) Categorization learning in horses (Equus caballus). J Comp Psychol 1113:243–252CrossRefGoogle Scholar
  13. Hare B, Call J, Tomasello M (1998) Communication of food location between human and dog (Canis familiaris). Evolution of communication 2(1):137–159CrossRefGoogle Scholar
  14. Hobaiter C, Byrne RW (2011) The gestural repertoire of the wild chimpanzee. Anim Cogn 14(5):745–767CrossRefPubMedGoogle Scholar
  15. Kaminski J, Marshall-Pescini S (2014) The social dog: behaviour and cognition. Academic Press/Elsevier, San Diego (CA)Google Scholar
  16. Krueger K (2007) Behaviour of horses in the “round pen technique”. Appl Anim Behav Sci 104(1):162–170CrossRefGoogle Scholar
  17. Krueger K, Flauger B, Farmer K, Maros K (2011) Horses (Equus caballus) use human local enhancement cues and adjust to human attention. Anim Cogn 14:187–201CrossRefPubMedGoogle Scholar
  18. Krueger K, Farmer K, Heinze J (2014) The effects of age, rank and neophobia on social learning in horses. Anim Cogn 17(3):645–655CrossRefPubMedGoogle Scholar
  19. Leavens DA (2004) Manual deixis in apes and humans. Interact Stud 5:387–408Google Scholar
  20. Leavens DA, Russell JL, Hopkins WD (2005) Intentionality as measured in the persistence and elaboration of communication by chimpanzees (Pan troglodytes). Child Dev 76(1):291–306CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lesimple C, Sankey C, Richard MA, Hausberger M (2012) Do horses expect humans to solve their problems? Front Psyc 3:306Google Scholar
  22. Maros K, Gácsi M, Miklósi Á (2008) Comprehension of human pointing gestures in horses (Equus caballus). Anim Cogn 11:457–466CrossRefPubMedGoogle Scholar
  23. Miklósi Á, Polgárdi R, Topál J, Csányi V (2000) Intentional behaviour in dog-human communication: an experimental analysis of showing behaviour in the dog. Anim Cogn 3:159–166CrossRefGoogle Scholar
  24. Murphy J, Hall C, Arkins S (2009) What horses and humans see: a comparative review. Intl J Zool 2009:721798. doi:10.1155/2009/721798 CrossRefGoogle Scholar
  25. Petrazzini MEM (2014) Trained quantity abilities in horses (Equus caballus): a Preliminary Investigation. Behav Sci 4(3):213–225CrossRefGoogle Scholar
  26. Pika S (2012) The case of referential gestural signaling. Where next? Commun Integr Biol 5(6):578–582CrossRefPubMedPubMedCentralGoogle Scholar
  27. Pika S, Bugnyar T (2011) The use of referential gestures in ravens (Corvus corax) in the wild. Nat Commun 2:56CrossRefGoogle Scholar
  28. Pika S, Mitani J (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol 16(6):R191–R192CrossRefPubMedGoogle Scholar
  29. Proops L, McComb K (2010) Attributing attention: the use of human-given cues by domestic horses (Equus caballus). Anim Cogn 13:197–205CrossRefPubMedGoogle Scholar
  30. Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). Proc Natl Acad Sci USA 106:947–951CrossRefPubMedGoogle Scholar
  31. Roberts AI, Vick SJ, Roberts SGB, Menzel CR (2014) Chimpanzees modify intentional gestures to coordinate a search for hidden food. Nat Commun 5:3088CrossRefPubMedPubMedCentralGoogle Scholar
  32. Rubenstein DI, Wrangham RW (1986) Ecological aspects of social evolution: birds and mammals, 1st edn. Princeton University Press, Princeton (NJ)Google Scholar
  33. Sankey C, Henry S, André N, Richard-Yris M, Hausberger M (2011) Do horses have a concept of person? Plos One 6:e18331CrossRefPubMedPubMedCentralGoogle Scholar
  34. Savalli C, Ades C, Gaunet F (2014) Are dogs able to communicate with their owners about a desirable food in a referential and intentional way? Plos One 9(9):e108003CrossRefPubMedPubMedCentralGoogle Scholar
  35. Schubert M, Jónsson H, Chang D, Der Sarkissian C, Ermini L, Ginolhac A et al (2014) Prehistoric genomes reveal the genetic foundation and cost of horse domestication. P Natl Acad Sci 111(52):E5661–E5669CrossRefGoogle Scholar
  36. Schwab C, Huber L (2006) Obey or not obey? Dogs (Canis familiaris) behave differently in response to attentional states of their owners. J Comp Psychol 120:169–175CrossRefPubMedGoogle Scholar
  37. Tomasello M (1995) Joint attention as social cognition. In: Moore C, Dunham PJ (eds) Joint attention: its origin and role in development. Erlbaum, Hillsdale (NJ), pp 103–130Google Scholar
  38. Tomasello M (2006) Why don’t apes point? In: Enfield NJ, Levinson SC (eds) Roots of human sociality: culture, cognition and interaction. Berg, Oxford, pp 506–524Google Scholar
  39. Tomasello M, Kruger A, Ratner H (1993) Cultural learning. Behav Brain Sci 16:495–552CrossRefGoogle Scholar
  40. Tomasello M, Carpenter M, Call J, Behne T, Moll H (2005) Understanding and sharing intentions: the origins of cultural cognition. Behav Brain Sci 28(05):675–691PubMedGoogle Scholar
  41. Vail AL, Manica A, Bshary R (2013) Referential gestures in fish collaborative hunting. Nat Commun 4:1765CrossRefPubMedGoogle Scholar
  42. Waring G (2003) Horse behavior, 2nd edn. Noyes Publications/William Andrew Publishing, Norwich (NY)Google Scholar
  43. Warneken F, Chen F, Tomasello M (2006) Cooperative activities in young children and chimpanzees. Child Dev 77:640–663CrossRefPubMedGoogle Scholar
  44. Wathan J, McComb K (2014) The eyes and ears are visual indicators of attention in domestic horses. Curr Biol 24(15):R677–R679CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xitco MJ, Gory JD, Ii SAK (2004) Dolphin pointing is linked to the attentional behavior of a receiver. Anim Cogn 7:231–238CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Study Center for Ethical EquitationEquiluna A.S.D.Moncigoli Di FivizzanoItaly
  2. 2.Comparative Cognition, Messerli Research Institute, University of Veterinary Medicine Vienna, Medical University of ViennaUniversity of ViennaViennaAustria

Personalised recommendations