Vocal expression of emotional valence in Przewalski’s horses (Equus przewalskii).
Abstract: Vocal expression of emotions has been suggested to be conserved throughout evolution. However, since vocal indicators of emotions have never been compared between closely related species using similar methods, it remains unclear whether this is the case. Here, we investigated vocal indicators of emotional valence (negative versus positive) in Przewalski's horses, in order to find out if expression of valence is similar between species and notably among Equidae through a comparison with previous results obtained in domestic horse whinnies. We observed Przewalski's horses in naturally occurring contexts characterised by positive or negative valence. As emotional arousal (bodily activation) can act as a confounding factor in the search for indicators of valence, we controlled for its effect on vocal parameters using a behavioural indicator (movement). We found that positive and negative situations were associated with specific types of calls. Additionally, the acoustic structure of calls differed according to the valence. There were some similarities but also striking differences in expression of valence between Przewalski's and domestic horses, suggesting that vocal expression of emotional valence, unlike emotional arousal, could be species specific rather than conserved throughout evolution.
Publication Date: 2017-08-18 PubMed ID: 28821880PubMed Central: PMC5562828DOI: 10.1038/s41598-017-09437-1Google Scholar: Lookup
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Summary
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This research looks into whether different species of horses express emotion differently through vocal sounds. They particularly focused on the Przewalski’s horses, analyzing their vocal expressions during instances of both positive and negative valence. Their findings suggest that the expression of emotional valence, as opposed to emotional arousal, may not be evolutionary conserved, which contradicts previous assumptions.
Objectives and Methodology
- The aim of this research was to glean more information about whether the vocal indications of emotions in different species, particularly among Equidae, are conserved or varied.
- Przewalski’s horses were the main subjects of the study. Researchers observed these horses in organic contexts that were characterized by either positive or negative valence (the intrinsic attractiveness or averseness of an event, object, or situation).
- To limit the effects of confounding factors such as emotional arousal (body activation), controls for vocal parameters were established using a behavioural indicator – the horse’s movement.
Findings
- The researchers noted that positive and negative situations incited unique vocal responses from the horses.
- They observed that the horse’s calls’ acoustic structure altered based on the situation’s valence.
Comparison with Previous Research
- Upon comparison, results showed that while there were certain similarities, there were also striking differences in the expression of emotional valence between Przewalski’s horses and domestic horses. This suggests that the vocal indication of emotional valence may potentially be species-specific, rather than conserved through evolution.
Implications
- This research challenges previous assumptions about vocal expressions of emotions being conserved through evolution.
- It highlights the potential for different species to have unique, species-specific methods of vocalizing their emotional responses to positive or negative situations.
- This informs future studies about vocal expressions of emotion, hinting at the necessity to consider the possibility of species-specific vocalizations.
Cite This Article
APA
Maigrot AL, Hillmann E, Anne C, Briefer EF.
(2017).
Vocal expression of emotional valence in Przewalski’s horses (Equus przewalskii).
Sci Rep, 7(1), 8779.
https://doi.org/10.1038/s41598-017-09437-1 Publication
Researcher Affiliations
- Division of Animal Welfare, Veterinary Public Health Institute, Vetsuisse Faculty, University of Bern, Länggassstrasse 120, 3012, Bern, Switzerland. anne.maigrot@usys.ethz.ch.
- Ethology and Animal Welfare Unit, Institute of Agricultural Sciences, ETH Zürich, Universitätstrasse 2, 8092, Zurich, Switzerland. anne.maigrot@usys.ethz.ch.
- Ethology and Animal Welfare Unit, Institute of Agricultural Sciences, ETH Zürich, Universitätstrasse 2, 8092, Zurich, Switzerland.
- Ethology and Animal Welfare Unit, Institute of Agricultural Sciences, ETH Zürich, Universitätstrasse 2, 8092, Zurich, Switzerland.
- Ethology and Animal Welfare Unit, Institute of Agricultural Sciences, ETH Zürich, Universitätstrasse 2, 8092, Zurich, Switzerland.
Conflict of Interest Statement
The authors declare that they have no competing interests.
References
This article includes 58 references
- Špinka M. Social dimension of emotions and its implication for animal welfare. Appl. Anim. Behav. Sci. 2012;138:170–181.
- Mendl M, Burman OH, Paul ES. An integrative and functional framework for the study of animal emotion and mood.. Proc Biol Sci 2010 Oct 7;277(1696):2895-904.
- Russell JA. A circumplex model of affect. J. Pers. Soc. Psychol. 1980;39:1161–1178.
- Bradley MM, Codispoti M, Cuthbert BN, Lang PJ. Emotion and motivation I: defensive and appetitive reactions in picture processing.. Emotion 2001 Sep;1(3):276-98.
- Boissy A, Manteuffel G, Jensen MB, Moe RO, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, Bakken M, Veissier I, Aubert A. Assessment of positive emotions in animals to improve their welfare.. Physiol Behav 2007 Oct 22;92(3):375-97.
- Proctor HS, Carder G. Can ear postures reliably measure the positive emotional state of cows?. Appl. Anim. Behav. Sci. 2014;161:20–27.
- Proctor HS, Carder G. Measuring positive emotions in cows: Do visible eye whites tell us anything?. Physiol Behav 2015 Aug 1;147:1-6.
- Briefer EF, Tettamanti F, McElligott AG. Emotions in goats: mapping physiological, behavioural and vocal profiles. Anim. Behav. 2015;99:131–143.
- Forkman B, Boissy A, Meunier-Salaün MC, Canali E, Jones RB. A critical review of fear tests used on cattle, pigs, sheep, poultry and horses.. Physiol Behav 2007 Oct 22;92(3):340-74.
- Selye H. The stress of life. xvi (McGraw-Hill, 1956).
- Morton ES. On the Occurrence and Significance of Motivation-Structural Rules in Some Bird and Mammal Sounds. Am. Nat. 1977;111:855–869.
- Proctor HS, Carder G, Cornish AR. Searching for Animal Sentience: A Systematic Review of the Scientific Literature.. Animals (Basel) 2013 Sep 4;3(3):882-906.
- Briefer EF. Vocal expression of emotions in mammals: mechanisms of production and evidence. J. Zool. 2012;288:1–20.
- Zimmermann E, Leliveld LMC, Schehka S. Toward the evolutionary roots of affective prosody in human acoustic communication: A comparative approach to mammalian voices - Oxford Scholarship. (2013).
- von Borell E, Bünger B, Schmidt T, Horn T. Vocal-type classification as a tool to identify stress in piglets under on-farm conditions. Anim. Welf. 2009;18:407–416.
- Slocombe KE, Zuberbühler K. Chimpanzees modify recruitment screams as a function of audience composition.. Proc Natl Acad Sci U S A 2007 Oct 23;104(43):17228-33.
- Thomas TJ, Weary DM, Appleby MC. Newborn and 5-week-old calves vocalize in response to milk deprivation. Appl. Anim. Behav. Sci. 2001;74:165–173.
- Gogoleva SS, Volodina EV, Volodin IA, Kharlamova AV, Trut LN. The gradual vocal responses to human-provoked discomfort in farmed silver foxes.. Acta Ethol 2010 Oct;13(2):75-85.
- Sugiura H. Effects of proximity and behavioral context on acoustic variation in the coo calls of Japanese macaques.. Am J Primatol 2007 Dec;69(12):1412-24.
- Brudzynski SM. Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine-dopamine interaction and acoustic coding.. Behav Brain Res 2007 Sep 4;182(2):261-73.
- Yin S, McCowan B. Barking in domestic dogs: context specificity and individual identification. Anim. Behav. 2004;68:343–355.
- Coss RG, McCowan B, Ramakrishnan U. Threat-Related Acoustical Differences in Alarm Calls by Wild Bonnet Macaques (Macaca radiata) Elicited by Python and Leopard Models. Ethology 2007;113:352–367.
- Soltis J, Blowers TE, Savage A. Measuring positive and negative affect in the voiced sounds of African elephants (Loxodonta africana).. J Acoust Soc Am 2011 Feb;129(2):1059-66.
- Yeon SC, Kim YK, Park SJ, Lee SS, Lee SY, Suh EH, Houpt KA, Chang HH, Lee HC, Yang BG, Lee HJ. Differences between vocalization evoked by social stimuli in feral cats and house cats.. Behav Processes 2011 Jun;87(2):183-9.
- Taylor AM, Reby D, McComb K. Context-Related Variation in the Vocal Growling Behaviour of the Domestic Dog (Canis familiaris). Ethology 2009;115:905–915.
- Briefer EF, Maigrot AL, Mandel R, Freymond SB, Bachmann I, Hillmann E. Segregation of information about emotional arousal and valence in horse whinnies.. Sci Rep 2015 Apr 21;4:9989.
- Linklater WL. Adaptive explanation in socio-ecology: lessons from the Equidae.. Biol Rev Camb Philos Soc 2000 Feb;75(1):1-20.
- Alberghina D, Caudullo E, Bandi N, Panzera M. A comparative analysis of the acoustic structure of separation calls of Mongolian wild horses (Equus ferus przewalskii) and domestic horses (Equus caballus). J. Vet. Behav. Clin. Appl. Res. 2014;9:254–257.
- Alberghina D, Caudullo E, Chan WY, Bandi N, Panzera M. Acoustic characteristics of courtship and agonistic vocalizations in Przwewalskii’s wild horse and in domestic horse. Appl. Anim. Behav. Sci. 2016;174:70–75.
- Waring GH. Horse Behaviour. (William Andrew publishing, Norwich, NY, USA, 2003).
- Yeon SC. Acoustic communication in the domestic horse (Equus caballus). J. Vet. Behav. Clin. Appl. Res. 2012;7:179–185.
- Soltis J, Blowers TE, Savage A. Measuring positive and negative affect in the voiced sounds of African elephants (Loxodonta africana).. J Acoust Soc Am 2011 Feb;129(2):1059-66.
- Stoeger AS, Charlton BD, Kratochvil H, Fitch WT. Vocal cues indicate level of arousal in infant African elephant roars.. J Acoust Soc Am 2011 Sep;130(3):1700-10.
- Waal FD. The Age of Empathy: Nature’s Lessons for a Kinder Society. (Souvenir Press, 2010).
- Fichtel C, Hammerschmidt K, Jürgens U. On the Vocal Expression of Emotion. A Multi-Parametric Analysis of Different States of Aversion in the Squirrel Monkey. Behaviour 2001;138:97–116.
- Leliveld LM, Düpjan S, Tuchscherer A, Puppe B. Behavioural and physiological measures indicate subtle variations in the emotional valence of young pigs.. Physiol Behav 2016 Apr 1;157:116-24.
- Der Sarkissian C, Ermini L, Schubert M, Yang MA, Librado P, Fumagalli M, Jónsson H, Bar-Gal GK, Albrechtsen A, Vieira FG, Petersen B, Ginolhac A, Seguin-Orlando A, Magnussen K, Fages A, Gamba C, Lorente-Galdos B, Polani S, Steiner C, Neuditschko M, Jagannathan V, Feh C, Greenblatt CL, Ludwig A, Abramson NI, Zimmermann W, Schafberg R, Tikhonov A, Sicheritz-Ponten T, Willerslev E, Marques-Bonet T, Ryder OA, McCue M, Rieder S, Leeb T, Slatkin M, Orlando L. Evolutionary Genomics and Conservation of the Endangered Przewalski's Horse.. Curr Biol 2015 Oct 5;25(19):2577-83.
- Yeon SC. Acoustic communication in the domestic horse (Equus caballus). J. Vet. Behav. Clin. Appl. Res. 2012;7:179–185.
- Linhart P, Ratcliffe VF, Reby D, Špinka M. Expression of Emotional Arousal in Two Different Piglet Call Types.. PLoS One 2015;10(8):e0135414.
- August PV, Anderson JGT. Mammal Sounds and Motivation-Structural Rules: A Test of the Hypothesis. J. Mammal. 1987;68:1–9.
- Peters GP. Purring and similar vocalizations in mammals. Mammal Rev. 2002;32:245–271.
- Briefer Freymond S, Briefer EF, Von Niederhäusern R, Bachmann I. Pattern of social interactions after group integration: a possibility to keep stallions in group.. PLoS One 2013;8(1):e54688.
- Dierendonck MC Van. The importance of social relationships in horses. (Utrecht University, 2006).
- Moe RO. Trace classical conditioning as an approach to the study of reward-related behaviour in laying hens: A methodological study. Appl. Anim. Behav. Sci. 2009;121:171–178.
- Spruijt BM, van den Bos R, Pijlman FT. A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems.. Appl Anim Behav Sci 2001 Apr 26;72(2):145-171.
- Lansade L, Bouissou M-F, Erhard HW. Reactivity to isolation and association with conspecifics: A temperament trait stable across time and situations. Appl. Anim. Behav. Sci. 2008;109:355–373.
- Boersma P, Weenink D. Praat: doing phonetics by computer (Version 5.1. 05)[Computer program]. Retrieved May 1, 2009 (2009).
- Kiley M. The vocalizations of ungulates, their causation and function.. Z Tierpsychol 1972 Aug;31(2):171-222.
- Reby D, McComb K. Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim. Behav. 2003;65:519–530.
- Volodina EV, Volodin IA, Isaeva IV, Unck C. Biphonation May Function to Enhance Individual Recognition in the Dhole, Cuon alpinus. Ethology 2006;112:815–825.
- Sèbe F. Bio-acoustic analyses to assess emotion in animals: Acoustic patterns are linked to behavioural, cardiac and hormonal responses of ewes to the separation from their lambs (abstract). .
- Collins KT, McGreevy PD, Wheatley KE, Harcourt RG. The influence of behavioural context on Weddell seal (Leptonychotes weddellii) airborne mother-pup vocalisation.. Behav Processes 2011 Jul;87(3):286-90.
- Meise K, Keller C, Cowlishaw G, Fischer J. Sources of acoustic variation: implications for production specificity and call categorization in chacma baboon (Papio ursinus) grunts.. J Acoust Soc Am 2011 Mar;129(3):1631-41.
- Charlton BD, Zhihe Z, Snyder RJ. Vocal cues to identity and relatedness in giant pandas (Ailuropoda melanoleuca).. J Acoust Soc Am 2009 Nov;126(5):2721-32.
- Bates D. lme4: Linear Mixed-Effects Models using ‘Eigen’ and S4. (2015).
- Engqvist L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 2005;70:967–971.
- Blois-Heulin C. Animal welfare: Could adult play be a false friend. Anim. Behav. Cogn. 2015;2:156–185.
- Glatthaar A, Wülfert H. Pferde unter sich Verhalten und Verständigung; gezeichnet & erklärt; English, Deutsch, Français. (Wu-Wei-Verl., 2012).
Citations
This article has been cited 12 times.- Greenall JS, Cornu L, Maigrot AL, de la Torre MP, Briefer EF. Age, empathy, familiarity, domestication and call features enhance human perception of animal emotion expressions.. R Soc Open Sci 2022 Dec;9(12):221138.
- Maigrot AL, Hillmann E, Briefer EF. Cross-species discrimination of vocal expression of emotional valence by Equidae and Suidae.. BMC Biol 2022 May 24;20(1):106.
- Briefer EF, Sypherd CC, Linhart P, Leliveld LMC, Padilla de la Torre M, Read ER, Guérin C, Deiss V, Monestier C, Rasmussen JH, Špinka M, Düpjan S, Boissy A, Janczak AM, Hillmann E, Tallet C. Classification of pig calls produced from birth to slaughter according to their emotional valence and context of production.. Sci Rep 2022 Mar 7;12(1):3409.
- Probert R, Bastian A, Elwen SH, James BS, Gridley T. Vocal correlates of arousal in bottlenose dolphins (Tursiops spp.) in human care.. PLoS One 2021;16(9):e0250913.
- Janczarek I, Stachurska A, Wilk I, Wiśniewska A, Różańska-Boczula M, Kaczmarek B, Łuszczyński J, Kędzierski W. Horse Preferences for Insolation, Shade or Mist Curtain in the Paddock under Heat Conditions: Cardiac and Behavioural Response Analysis.. Animals (Basel) 2021 Mar 25;11(4).
- Tuozzi A, Arhant C, Anderle K, Backes J, Cords C, Magierski V, Rault JL, Windschnurer I. Effects of Human Presence and Voice on the Behaviour of Shelter Dogs and Cats: A Preliminary Study.. Animals (Basel) 2021 Feb 5;11(2).
- Nuñez CMV, Rubenstein DI. Communication is key: Mother-offspring signaling can affect behavioral responses and offspring survival in feral horses (Equus caballus).. PLoS One 2020;15(4):e0231343.
- Green A, Clark C, Favaro L, Lomax S, Reby D. Vocal individuality of Holstein-Friesian cattle is maintained across putatively positive and negative farming contexts.. Sci Rep 2019 Dec 5;9(1):18468.
- Safryghin A, Hebesberger DV, Wascher CAF. Testing for Behavioral and Physiological Responses of Domestic Horses (Equus caballus) Across Different Contexts - Consistency Over Time and Effects of Context.. Front Psychol 2019;10:849.
- Friel M, Kunc HP, Griffin K, Asher L, Collins LM. Positive and negative contexts predict duration of pig vocalisations.. Sci Rep 2019 Feb 14;9(1):2062.
- Stomp M, Leroux M, Cellier M, Henry S, Lemasson A, Hausberger M. An unexpected acoustic indicator of positive emotions in horses.. PLoS One 2018;13(7):e0197898.
- Maigrot AL, Hillmann E, Briefer EF. Encoding of Emotional Valence in Wild Boar (Sus scrofa) Calls.. Animals (Basel) 2018 Jun 5;8(6).
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