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.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Bates E, Camaioni L, Volterra V (1975) The acquisition of performatives prior to speech. Merrill-Palmer Q Behav Dev 21(3):205–226
Bates E, Benigni L, Bretherton I, Camaioni L, Volterra V (1979) The emergence of symbols: cognition and communication in infancy. Academic Press, New York
Birke L (2007) Learning to speak horse: the culture of natural horsemanship. Soc Anim 15(3):217–239
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 87:121–128
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):239–250
Call JE, Tomasello ME (2007) The gestural communication of apes and monkeys. Taylor & Francis Group/Lawrence Erlbaum Associates, New York
Canteloup C, Bovet D, Meunier H (2015) Intentional gestural communication and discrimination of human attentional states in rhesus macaques (Macaca mulatta). Anim cogn 18:875–883
Cartmill EA, Byrne RW (2007) Orangutans modify their gestural signaling according to their audience’s comprehension. Curr Biol 17:1345–1348
Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosc Biobehav R 24(6):581–604
Gaunet F (2010) How do guide dogs and pet dogs (Canis familiaris) ask their owners for their toy and for playing? Anim Cogn 13:311–323
Gaunet F, Deputte BL (2011) Functionally referential and intentional communication in the domestic dog: effects of spatial and social contexts. Anim Cogn 14:849–860
Hanggi EB (1999) Categorization learning in horses (Equus caballus). J Comp Psychol 1113:243–252
Hare B, Call J, Tomasello M (1998) Communication of food location between human and dog (Canis familiaris). Evolution of communication 2(1):137–159
Hobaiter C, Byrne RW (2011) The gestural repertoire of the wild chimpanzee. Anim Cogn 14(5):745–767
Kaminski J, Marshall-Pescini S (2014) The social dog: behaviour and cognition. Academic Press/Elsevier, San Diego (CA)
Krueger K (2007) Behaviour of horses in the “round pen technique”. Appl Anim Behav Sci 104(1):162–170
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
Krueger K, Farmer K, Heinze J (2014) The effects of age, rank and neophobia on social learning in horses. Anim Cogn 17(3):645–655
Leavens DA (2004) Manual deixis in apes and humans. Interact Stud 5:387–408
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):291–306
Lesimple C, Sankey C, Richard MA, Hausberger M (2012) Do horses expect humans to solve their problems? Front Psyc 3:306
Maros K, Gácsi M, Miklósi Á (2008) Comprehension of human pointing gestures in horses (Equus caballus). Anim Cogn 11:457–466
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 3:159–166
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
Petrazzini MEM (2014) Trained quantity abilities in horses (Equus caballus): a Preliminary Investigation. Behav Sci 4(3):213–225
Pika S (2012) The case of referential gestural signaling. Where next? Commun Integr Biol 5(6):578–582
Pika S, Bugnyar T (2011) The use of referential gestures in ravens (Corvus corax) in the wild. Nat Commun 2:56
Pika S, Mitani J (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol 16(6):R191–R192
Proops L, McComb K (2010) Attributing attention: the use of human-given cues by domestic horses (Equus caballus). Anim Cogn 13:197–205
Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). Proc Natl Acad Sci USA 106:947–951
Roberts AI, Vick SJ, Roberts SGB, Menzel CR (2014) Chimpanzees modify intentional gestures to coordinate a search for hidden food. Nat Commun 5:3088
Rubenstein DI, Wrangham RW (1986) Ecological aspects of social evolution: birds and mammals, 1st edn. Princeton University Press, Princeton (NJ)
Sankey C, Henry S, André N, Richard-Yris M, Hausberger M (2011) Do horses have a concept of person? Plos One 6:e18331
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):e108003
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–E5669
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 120:169–175
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 103–130
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 506–524
Tomasello M, Kruger A, Ratner H (1993) Cultural learning. Behav Brain Sci 16:495–552
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):675–691
Vail AL, Manica A, Bshary R (2013) Referential gestures in fish collaborative hunting. Nat Commun 4:1765
Waring G (2003) Horse behavior, 2nd edn. Noyes Publications/William Andrew Publishing, Norwich (NY)
Warneken F, Chen F, Tomasello M (2006) Cooperative activities in young children and chimpanzees. Child Dev 77:640–663
Wathan J, McComb K (2014) The eyes and ears are visual indicators of attention in domestic horses. Curr Biol 24(15):R677–R679
Xitco MJ, Gory JD, Ii SAK (2004) Dolphin pointing is linked to the attentional behavior of a receiver. Anim Cogn 7:231–238
We wish to thank EquiLuna A.S.D. for granting us the permission to use their facilities and involve in this research the horses they host. In particular, we thank Laura Ascione, Claudio Saba, Andrea Montagnani and Lesley Moore for the help provided, and all those volunteered in this research. Our warmest thanks go to Christian Postiglione, our camera operator and technical assistant. We are grateful to Christian Postiglione, Elisabetta Visalberghi, Ian Couzin and Corsin Müller for helpful discussions and statistical consultation, to Debbie Kelly and Amelia Wein for improving the English and to Alan McElligott for his invaluable help at the very beginning of this project. This research was supported exclusively by private funding.
Authors declare not to have any source of funding.
RM conceived of the study, designed the study, collected field data, participated in data analyses and in statistical analyses and contributed to draft the manuscript; LH participated in data analyses and in statistical analyses and contributed to draft the manuscript. Both authors gave final approval for publication.
Conflict of interest
The authors declare that they have no conflict of interest. All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Electronic supplementary material
Below is the link to the electronic supplementary material.
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)
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)
About this article
Cite this article
Malavasi, R., Huber, L. Evidence of heterospecific referential communication from domestic horses (Equus caballus) to humans. Anim Cogn 19, 899–909 (2016) doi:10.1007/s10071-016-0987-0
- Domestic horse
- Referential communication
- Human–animal communication
- Intentional communication
- Referential gesture