Functionally relevant responses to human facial expressions of emotion in the domestic horse (Equus caballus).
Abstract: Whether non-human animals can recognize human signals, including emotions, has both scientific and applied importance, and is particularly relevant for domesticated species. This study presents the first evidence of horses' abilities to spontaneously discriminate between positive (happy) and negative (angry) human facial expressions in photographs. Our results showed that the angry faces induced responses indicative of a functional understanding of the stimuli: horses displayed a left-gaze bias (a lateralization generally associated with stimuli perceived as negative) and a quicker increase in heart rate (HR) towards these photographs. Such lateralized responses towards human emotion have previously only been documented in dogs, and effects of facial expressions on HR have not been shown in any heterospecific studies. Alongside the insights that these findings provide into interspecific communication, they raise interesting questions about the generality and adaptiveness of emotional expression and perception across species.
© 2016 The Author(s).
Publication Date: 2016-02-13 PubMed ID: 26864784PubMed Central: PMC4780548DOI: 10.1098/rsbl.2015.0907Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research paper presents a study on horses’ ability to distinguish between human emotions, displaying the first evidence of horses discriminating between happy and angry human facial expressions. The study showed that when horses were presented with angry faces, they displayed a left-gaze bias and increased heart rate – a reaction associated with perceiving negative stimuli.
Objective of Research
- The study aimed to explore if non-human animals, specifically horses, can recognize human emotional signals given it has significant implications in both scientific and applied fields.
- The research focused on horses’ ability to discriminate between positive (happy) and negative (angry) expressions on human faces using photographs.
Results of the study
- The study found that horses exhibited functional comprehension of the negative emotion presented in the photographs. They displayed a left-gaze bias and a rapid increase in heart rate when faced with photographs of angry human faces. This indicates that horses perceived angry faces as negative stimuli.
- This left-gaze bias towards negative stimuli was previously only documented in dogs, making this the first observed instance in horses.
- The effect of facial expressions on heart rate, a biological measure of emotional response, has not been observed in any heterospecific (different species) studies prior to this.
Significance and Implications of Findings
- These findings provide valuable insights into interspecies communication, suggesting that horses can interpret emotional cues from humans. They contribute to a more robust understanding of animal cognition and emotions.
- The study results also invite further research into the generality and adaptability of emotional expression and perception across different species, highlighting the unexplored complexity of emotional intelligence in animals.
Cite This Article
APA
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, 12(2), 20150907.
https://doi.org/10.1098/rsbl.2015.0907 Publication
Researcher Affiliations
- Mammal Vocal Communication and Cognition Research Group, School of Psychology, University of Sussex, Brighton BN1 9QH, UK a.v.smith@sussex.ac.uk.
- Mammal Vocal Communication and Cognition Research Group, School of Psychology, University of Sussex, Brighton BN1 9QH, UK.
- Mammal Vocal Communication and Cognition Research Group, School of Psychology, University of Sussex, Brighton BN1 9QH, UK.
- Mammal Vocal Communication and Cognition Research Group, School of Psychology, University of Sussex, Brighton BN1 9QH, UK.
- Mammal Vocal Communication and Cognition Research Group, School of Psychology, University of Sussex, Brighton BN1 9QH, UK karenm@sussex.ac.uk.
MeSH Terms
- Animals
- Avoidance Learning
- Emotions
- Facial Expression
- Female
- Heart Rate
- Horses / physiology
- Horses / psychology
- Humans
- Male
- Pattern Recognition, Visual
Grant Funding
- BB/F016808/1 / Biotechnology and Biological Sciences Research Council
References
This article includes 13 references
- Waller BM, Micheletta J. Facial expression in nonhuman animals. Emot. Rev. 2013;5:54–59.
- Mendl M, Burman OHP, Parker RMA, Paul ES. Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Appl. Anim. Behav. Sci. 2009;118:161–181.
- Merola I, Lazzaroni M, Marshall-Pescini S, Prato-Previde E. Social referencing and cat-human communication.. Anim Cogn 2015 May;18(3):639-48.
- Nagasawa M, Murai K, Mogi K, Kikusui T. Dogs can discriminate human smiling faces from blank expressions.. Anim Cogn 2011 Jul;14(4):525-33.
- Racca A, Guo K, Meints K, Mills DS. Reading faces: differential lateral gaze bias in processing canine and human facial expressions in dogs and 4-year-old children.. PLoS One 2012;7(4):e36076.
- Müller CA, Schmitt K, Barber AL, Huber L. Dogs can discriminate emotional expressions of human faces.. Curr Biol 2015 Mar 2;25(5):601-5.
- Leliveld LMC, Langbein J, Puppe B. The emergence of emotional lateralization: evidence in non-human vertebrates and implications for farm animals. Appl. Anim. Behav. Sci. 2013;145:1–14.
- De Boyer Des Roches A, Richard-Yris MA, Henry S, Ezzaouïa M, Hausberger M. Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value.. Physiol Behav 2008 Jun 9;94(3):487-90.
- Keeling LJ, Jonare L, Lanneborn L. Investigating horse-human interactions: the effect of a nervous human.. Vet J 2009 Jul;181(1):70-1.
- Wathan J, Burrows AM, Waller BM, McComb K. EquiFACS: The Equine Facial Action Coding System.. PLoS One 2015;10(8):e0131738.
- Wathan J. Social communication in domestic horses: the production and perception of facial expressions. .
- Proops L, McComb K. Attributing attention: the use of human-given cues by domestic horses (Equus caballus).. Anim Cogn 2010 Mar;13(2):197-205.
- Merola I, Prato-Previde E, Lazzaroni M, Marshall-Pescini S. Dogs' comprehension of referential emotional expressions: familiar people and familiar emotions are easier.. Anim Cogn 2014 Mar;17(2):373-85.
Citations
This article has been cited 67 times.- Albuquerque N, Savalli C, Belli M, Varella AC, Felício B, França J, Izar P. The shape of lipsmacking: socio-emotional regulation in bearded capuchin monkeys (Sapajus libidinosus).. Evol Hum Sci 2023;5:e16.
- Jardat P, Liehrmann O, Reigner F, Parias C, Calandreau L, Lansade L. Horses discriminate between human facial and vocal expressions of sadness and joy.. Anim Cogn 2023 Sep;26(5):1733-1742.
- Lazzaroni M, Schär J, Baxter E, Gratalon J, Range F, Marshall-Pescini S, Dale R. Village dogs match pet dogs in reading human facial expressions.. PeerJ 2023;11:e15601.
- Pahl A, König von Borstel U, Brucks D. Llamas use social information from conspecifics and humans to solve a spatial detour task.. Anim Cogn 2023 Sep;26(5):1623-1633.
- Tomberg C, Petagna M, de Selliers de Moranville LA. Horses (Equus caballus) facial micro-expressions: insight into discreet social information.. Sci Rep 2023 May 27;13(1):8625.
- Wilson VAD, Bethell EJ, Nawroth C. The use of gaze to study cognition: limitations, solutions, and applications to animal welfare.. Front Psychol 2023;14:1147278.
- Liehrmann O, Cosnard C, Riihonen V, Viitanen A, Alander E, Jardat P, Koski SE, Lummaa V, Lansade L. What drives horse success at following human-given cues? An investigation of handler familiarity and living conditions.. Anim Cogn 2023 Jul;26(4):1283-1294.
- Kappel S, Ramirez Montes De Oca MA, Collins S, Herborn K, Mendl M, Fureix C. Do you see what I see? Testing horses' ability to recognise real-life objects from 2D computer projections.. Anim Cogn 2023 Jul;26(4):1147-1159.
- Jardat P, Destrez A, Damon F, Menard-Peroy Z, Parias C, Barrière P, Keller M, Calandreau L, Lansade L. Horses discriminate human body odors between fear and joy contexts in a habituation-discrimination protocol.. Sci Rep 2023 Feb 25;13(1):3285.
- Pérez Fraga P, Morvai B, Gerencsér L, Lehoczki F, Andics A. Out-of-reach rewards elicit human-oriented referential communicative behaviours in family dogs but not in family pigs.. Sci Rep 2023 Jan 23;13(1):811.
- Schubert CL, Ryckewaert B, Pereira C, Matsuzawa T. Garrano Horses Perceive Letters of the Alphabet on a Touchscreen System: A Pilot Study.. Animals (Basel) 2022 Dec 12;12(24).
- Wilson C, Campbell K, Petzel Z, Reeve C. Dogs can discriminate between human baseline and psychological stress condition odours.. PLoS One 2022;17(9):e0274143.
- Merkies K, Sudarenko Y, Hodder AJ. Can Ponies (Equus Caballus) Distinguish Human Facial Expressions?. Animals (Basel) 2022 Sep 7;12(18).
- Kovács G, van Dijke A, Leontjevas R, Enders-Slegers MJ. The Relevance of Internal Working Models of Self and Others for Equine-Assisted Psychodynamic Psychotherapy.. Int J Environ Res Public Health 2022 Aug 30;19(17).
- Wiśniewska A, Janczarek I, Tkaczyk E, Wilk I, Janicka W, Próchniak T, Kaczmarek B, Pokora E, Łuszczyński J. Minimizing the Effects of Social Isolation of Horses by Contact with Animals of a Different Species: The Domestic Goat as an Example.. Animals (Basel) 2022 Sep 2;12(17).
- Choińska AM, Bajer W, Żurek A, Gieysztor E. The Effect of Contact with a Horse During a Three-day Hippotherapy Session on Physiotherapy Students' Emotions.. Psychol Res Behav Manag 2022;15:1385-1396.
- Krueger K, Schwarz S, Marr I, Farmer K. Laterality in Horse Training: Psychological and Physical Balance and Coordination and Strength Rather Than Straightness.. Animals (Basel) 2022 Apr 16;12(8).
- Jardat P, Calandreau L, Ferreira V, Gouyet C, Parias C, Reigner F, Lansade L. Pet-directed speech improves horses' attention toward humans.. Sci Rep 2022 Mar 11;12(1):4297.
- Wolfsberger WW, Ayala NM, Castro-Marquez SO, Irizarry-Negron VM, Potapchuk A, Shchubelka K, Potish L, Majeske AJ, Oliver LF, Lameiro AD, Martínez-Cruzado JC, Lindgren G, Oleksyk TK. Genetic diversity and selection in Puerto Rican horses.. Sci Rep 2022 Jan 11;12(1):515.
- Jardat P, Lansade L. Cognition and the human-animal relationship: a review of the sociocognitive skills of domestic mammals toward humans.. Anim Cogn 2022 Apr;25(2):369-384.
- Brubaker L, Schroeder K, Sherwood D, Stroud D, Udell MAR. Horse Behavior towards Familiar and Unfamiliar Humans: Implications for Equine-Assisted Services.. Animals (Basel) 2021 Aug 11;11(8).
- Watanabe S, Masuda S, Shinozuka K, Borlongan C. Preference and discrimination of facial expressions of humans, rats, and mice by C57 mice.. Anim Cogn 2022 Apr;25(2):297-306.
- Baragli P, Scopa C, Felici M, Reddon AR. Horses show individual level lateralisation when inspecting an unfamiliar and unexpected stimulus.. PLoS One 2021;16(8):e0255688.
- Merkies K, Franzin O. Enhanced Understanding of Horse-Human Interactions to Optimize Welfare.. Animals (Basel) 2021 May 9;11(5).
- Picó A, Gadea M. When animals cry: The effect of adding tears to animal expressions on human judgment.. PLoS One 2021;16(5):e0251083.
- Hockenhull J, Bell C, White J, Rogers S. Response of UK Horse, Pony and Donkey Owners to the Early Stages of the COVID-19 Pandemic.. Animals (Basel) 2021 Apr 23;11(5).
- Ricci-Bonot C, Romero T, Nicol C, Mills D. Social buffering in horses is influenced by context but not by the familiarity and habituation of a companion.. Sci Rep 2021 Apr 23;11(1):8862.
- Ragonese G, Baragli P, Mariti C, Gazzano A, Lanatà A, Ferlazzo A, Fazio E, Cravana C. Interspecific two-dimensional visual discrimination of faces in horses (Equus caballus).. PLoS One 2021;16(2):e0247310.
- Hartmann E, Rehn T, Christensen JW, Nielsen PP, McGreevy P. From the Horse's Perspective: Investigating Attachment Behaviour and the Effect of Training Method on Fear Reactions and Ease of Handling-A Pilot Study.. Animals (Basel) 2021 Feb 9;11(2).
- Prato-Previde E, Cannas S, Palestrini C, Ingraffia S, Battini M, Ludovico LA, Ntalampiras S, Presti G, Mattiello S. What's in a Meow? A Study on Human Classification and Interpretation of Domestic Cat Vocalizations.. Animals (Basel) 2020 Dec 14;10(12).
- Mott RO, Hawthorne SJ, McBride SD. Blink rate as a measure of stress and attention in the domestic horse (Equus caballus).. Sci Rep 2020 Dec 8;10(1):21409.
- Rault JL, Waiblinger S, Boivin X, Hemsworth P. The Power of a Positive Human-Animal Relationship for Animal Welfare.. Front Vet Sci 2020;7:590867.
- Lansade L, Colson V, Parias C, Reigner F, Bertin A, Calandreau L. Human Face Recognition in Horses: Data in Favor of a Holistic Process.. Front Psychol 2020;11:575808.
- Humphrey T, Proops L, Forman J, Spooner R, McComb K. The role of cat eye narrowing movements in cat-human communication.. Sci Rep 2020 Oct 5;10(1):16503.
- Törmälehto E, Korkiamäki R. The Potential of Human-Horse Attachment in Creating Favorable Settings for Professional Care: A Study of Adolescents' Visit to a Farm.. Animals (Basel) 2020 Sep 21;10(9).
- Quaranta A, d'Ingeo S, Amoruso R, Siniscalchi M. Emotion Recognition in Cats.. Animals (Basel) 2020 Jun 28;10(7).
- Kido N, Tanaka S, Omiya T, Kamite Y, Sawada K, Komatsu Y, Shoji Y, Senzaki M, Hanzawa S, Ando M, Suto I. Emotion estimation using a wearable heart rate monitoring device in Asian elephants (Elephas maximus) during veterinary clinical procedures.. J Vet Med Sci 2020 Jun 30;82(6):856-860.
- Marr I, Preisler V, Farmer K, Stefanski V, Krueger K. Non-invasive stress evaluation in domestic horses (Equus caballus): impact of housing conditions on sensory laterality and immunoglobulin A.. R Soc Open Sci 2020 Feb;7(2):191994.
- Calvi E, Quassolo U, Massaia M, Scandurra A, D'Aniello B, D'Amelio P. The scent of emotions: A systematic review of human intra- and interspecific chemical communication of emotions.. Brain Behav 2020 May;10(5):e01585.
- Schrimpf A, Single MS, Nawroth C. Social Referencing in the Domestic Horse.. Animals (Basel) 2020 Jan 18;10(1).
- White-Lewis S. Equine-assisted therapies using horses as healers: A concept analysis.. Nurs Open 2020 Jan;7(1):58-67.
- Scopa C, Contalbrigo L, Greco A, Lanatà A, Scilingo EP, Baragli P. Emotional Transfer in Human-Horse Interaction: New Perspectives on Equine Assisted Interventions.. Animals (Basel) 2019 Nov 26;9(12).
- Semin GR, Scandurra A, Baragli P, Lanatà A, D'Aniello B. Inter- and Intra-Species Communication of Emotion: Chemosignals as the Neglected Medium.. Animals (Basel) 2019 Oct 31;9(11).
- Trösch M, Cuzol F, Parias C, Calandreau L, Nowak R, Lansade L. Horses Categorize Human Emotions Cross-Modally Based on Facial Expression and Non-Verbal Vocalizations.. Animals (Basel) 2019 Oct 24;9(11).
- Robins A, Berthoux G, Santurtun E, Navarro G, Phillips CJC. Sheep Quickstep while the Floor Rock and Rolls: Visuomotor Lateralization during Simulated Sea Travel.. Animals (Basel) 2019 Sep 18;9(9).
- Baba C, Kawai M, Takimoto-Inose A. Are Horses (Equus caballus) Sensitive to Human Emotional Cues?. Animals (Basel) 2019 Aug 29;9(9).
- Baciadonna L, Briefer EF, Favaro L, McElligott AG. Goats distinguish between positive and negative emotion-linked vocalisations.. Front Zool 2019;16:25.
- Henriksson J, Sauveroche M, Roth LSV. Effects of size and personality on social learning and human-directed behaviour in horses (Equus caballus).. Anim Cogn 2019 Nov;22(6):1001-1011.
- Krueger K, Esch L, Byrne R. Animal behaviour in a human world: A crowdsourcing study on horses that open door and gate mechanisms.. PLoS One 2019;14(6):e0218954.
- Mendonça RS, Ringhofer M, Pinto P, Inoue S, Hirata S. Feral horses' (Equus ferus caballus) behavior toward dying and dead conspecifics.. Primates 2020 Jan;61(1):49-54.
- Amici F. Memories of emotional expressions in horses.. Learn Behav 2019 Sep;47(3):191-192.
- Nawroth C, Albuquerque N, Savalli C, Single MS, McElligott AG. Goats prefer positive human emotional facial expressions.. R Soc Open Sci 2018 Aug;5(8):180491.
- Smith AV, Proops L, Grounds K, Wathan J, Scott SK, McComb K. Domestic horses (Equus caballus) discriminate between negative and positive human nonverbal vocalisations.. Sci Rep 2018 Aug 29;8(1):13052.
- Farmer K, Krüger K, Byrne RW, Marr I. Sensory laterality in affiliative interactions in domestic horses and ponies (Equus caballus).. Anim Cogn 2018 Sep;21(5):631-637.
- Nakamura K, Takimoto-Inose A, Hasegawa T. Cross-modal perception of human emotion in domestic horses (Equus caballus).. Sci Rep 2018 Jun 21;8(1):8660.
- Burla JB, Siegwart J, Nawroth C. Human Demonstration Does Not Facilitate the Performance of Horses (Equus caballus) in a Spatial Problem-Solving Task.. Animals (Basel) 2018 Jun 13;8(6).
- Kiley-Worthington M. The Mental Homologies of Mammals. Towards an Understanding of Another Mammals World View.. Animals (Basel) 2017 Nov 23;7(12).
- Bellegarde LGA, Erhard HW, Weiss A, Boissy A, Haskell MJ. Valence of Facial Cues Influences Sheep Learning in a Visual Discrimination Task.. Front Vet Sci 2017;4:188.
- Smith AV, Wilson C, McComb K, Proops L. Domestic horses (Equus caballus) prefer to approach humans displaying a submissive body posture rather than a dominant body posture.. Anim Cogn 2018 Mar;21(2):307-312.
- Li Y, Dai Q, Hou R, Zhang Z, Chen P, Xue R, Feng F, Chen C, Liu J, Gu X, Zhang Z, Qi D. Giant pandas can discriminate the emotions of human facial pictures.. Sci Rep 2017 Aug 16;7(1):8437.
- Battarbee R. Research papers, gender bias and peer-review.. Biol Lett 2017 Aug;13(8).
- Maréchal L, Levy X, Meints K, Majolo B. Experience-based human perception of facial expressions in Barbary macaques (Macaca sylvanus).. PeerJ 2017;5:e3413.
- Baragli P, Demuru E, Scopa C, Palagi E. Are horses capable of mirror self-recognition? A pilot study.. PLoS One 2017;12(5):e0176717.
- Huber A, Barber ALA, Faragó T, Müller CA, Huber L. Investigating emotional contagion in dogs (Canis familiaris) to emotional sounds of humans and conspecifics.. Anim Cogn 2017 Jul;20(4):703-715.
- Smith AV, Proops L, Grounds K, Wathan J, McComb K. Horses give functionally relevant responses to human facial expressions of emotion: a response to Schmoll (2016).. Biol Lett 2016 Sep;12(9).
- Schmoll T. Can horses read emotional cues from human faces? Re-analysis of Smith et al. (2016).. Biol Lett 2016 Sep;12(9).
- Anderson R, Waayers R, Knight A. Orca Behavior and Subsequent Aggression Associated with Oceanarium Confinement.. Animals (Basel) 2016 Aug 18;6(8).
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists