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BMC biology2022; 20(1); 106; doi: 10.1186/s12915-022-01311-5

Cross-species discrimination of vocal expression of emotional valence by Equidae and Suidae.

Abstract: Discrimination and perception of emotion expression regulate interactions between conspecifics and can lead to emotional contagion (state matching between producer and receiver) or to more complex forms of empathy (e.g., sympathetic concern). Empathy processes are enhanced by familiarity and physical similarity between partners. Since heterospecifics can also be familiar with each other to some extent, discrimination/perception of emotions and, as a result, emotional contagion could also occur between species. Here, we investigated if four species belonging to two ungulate Families, Equidae (domestic and Przewalski's horses) and Suidae (pigs and wild boars), can discriminate between vocalizations of opposite emotional valence (positive or negative), produced not only by conspecifics, but also closely related heterospecifics and humans. To this aim, we played back to individuals of these four species, which were all habituated to humans, vocalizations from a unique set of recordings for which the valence associated with vocal production was known. We found that domestic and Przewalski's horses, as well as pigs, but not wild boars, reacted more strongly when the first vocalization played was negative compared to positive, regardless of the species broadcasted. Domestic horses, Przewalski's horses and pigs thus seem to discriminate between positive and negative vocalizations produced not only by conspecifics, but also by heterospecifics, including humans. In addition, we found an absence of difference between the strength of reaction of the four species to the calls of conspecifics and closely related heterospecifics, which could be related to similarities in the general structure of their vocalization. Overall, our results suggest that phylogeny and domestication have played a role in cross-species discrimination/perception of emotions.
Publication Date: 2022-05-24 PubMed ID: 35606806PubMed Central: PMC9128205DOI: 10.1186/s12915-022-01311-5Google Scholar: Lookup
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  • Journal Article

Summary

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This research paper focuses on whether four different types of ungulates – domestic and Przewalski’s horses, pigs, and wild boars – are capable of distinguishing between positive and negative vocalizations, regardless of whether they’re made by their own species, closely related species, or humans. The results suggest that domestication and phylogenetic relations may impact an animal’s ability to recognize emotional expression across species.

Understanding Inter-Species Emotional Recognition

  • The basis of this exploration is the understanding that the ability to discern and respond to emotional expressions regulates interaction within a species and can lead to emotional synchrony (matching emotional states between the emitter and receiver) or more complex forms of empathy. This is heightened by familiarity and physical similarity.
  • It’s recognised that different species can also familiarize with each other to varying degrees. Consequently, the researchers hypothesized that discernment of emotions and subsequently, emotional contagion may occur between different species.

Methodology

  • In this study, the four different species were exposed to vocalizations from a unique collection of recordings. The associated emotional valence (positive or negative) with each vocal production was known.
  • While being accustomed to human presence, the animals were played back these vocalizations to assess their reactions.

Findings

  • The outcome demonstrated that domestic and Przewalski’s horses and pigs, but not wild boars, had a greater reaction when the first vocalization played was negative, regardless of the broadcasting species.
  • This indicates these animals distinguish between positive and negative vocalizations, not only from their own species but also from other species, including humans.
  • Interestingly, there was no noticeable difference in the reaction strength of the four species to the calls of their own species and related species. This is hypothesized to be due to similarities within their vocal structure.

Implications

  • The overall findings suggest that an animal’s evolution and domestication process seems to play a significant role in its capability to detect and respond to emotional expression across species.
  • Further research in this area could help strengthen our understanding of animal cognition, emotions, and inter-species communication, which would have enormous implications for animal welfare, human-animal relationships, and conservation efforts.

Cite This Article

APA
Maigrot AL, Hillmann E, Briefer EF. (2022). Cross-species discrimination of vocal expression of emotional valence by Equidae and Suidae. BMC Biol, 20(1), 106. https://doi.org/10.1186/s12915-022-01311-5

Publication

ISSN: 1741-7007
NlmUniqueID: 101190720
Country: England
Language: English
Volume: 20
Issue: 1
Pages: 106
PII: 106

Researcher Affiliations

Maigrot, Anne-Laure
  • Institute of Agricultural Sciences, ETH Zürich, Universitätsstrasse 2, 8092, Zurich, Switzerland.
  • Division of Animal Welfare, Veterinary Public Health Institute, Vetsuisse Faculty, University of Bern, Länggassstrasse 120, 3012, Bern, Switzerland.
  • Swiss National Stud Farm, Agroscope, Les Longs-Prés, 1580, Avenches, Switzerland.
Hillmann, Edna
  • Institute of Agricultural Sciences, ETH Zürich, Universitätsstrasse 2, 8092, Zurich, Switzerland.
  • Animal Husbandry and Ethology, Albrecht Daniel Thaer-Institut, Faculty of Life Sciences, Humboldt-Universität zu Berlin, Philippstrasse 13, 10115, Berlin, Germany.
Briefer, Elodie F
  • Institute of Agricultural Sciences, ETH Zürich, Universitätsstrasse 2, 8092, Zurich, Switzerland. elodie.briefer@bio.ku.dk.
  • Centre for Proper Housing of Ruminants and Pigs, Federal Food Safety and Veterinary Office, Agroscope, Tänikon, 8356, Ettenhausen, Switzerland. elodie.briefer@bio.ku.dk.
  • Department of Biology, Behavioral Ecology Group, Section for Ecology & Evolution, University of Copenhagen, 2100, Copenhagen Ø, Denmark. elodie.briefer@bio.ku.dk.

MeSH Terms

  • Animals
  • Auditory Perception
  • Behavior, Animal
  • Emotions / physiology
  • Empathy / physiology
  • Equidae / physiology
  • Equidae / psychology
  • Phylogeny
  • Swine / physiology
  • Swine / psychology
  • Vocalization, Animal / physiology

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 53 references
  1. Paul ES, Mendl MT. Animal emotion: Descriptive and prescriptive definitions and their implications for a comparative perspective.. Appl Anim Behav Sci 2018 Aug;205:202-209.
  2. Špinka M. Social dimension of emotions and its implication for animal welfare.. Appl Anim Behav Sci 2012;138:170–181.
  3. Russell J. A circumplex model of affect.. J Pers Soc Psychol 1980;39:1161–1178.
    doi: 10.1037/h0077714google scholar: lookup
  4. Kremer L, Klein Holkenborg SEJ, Reimert I, Bolhuis JE, Webb LE. The nuts and bolts of animal emotion.. Neurosci Biobehav Rev 2020 Jun;113:273-286.
  5. de Waal FB. Putting the altruism back into altruism: the evolution of empathy.. Annu Rev Psychol 2008;59:279-300.
  6. 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.
    doi: 10.1007/s10071-017-1092-8pmc: PMC5486498pubmed: 28432495google scholar: lookup
  7. Palagi E, Norscia I, Demuru E. Yawn contagion in humans and bonobos: emotional affinity matters more than species.. PeerJ 2014;2:e519.
    doi: 10.7717/peerj.519pmc: PMC4137654pubmed: 25165630google scholar: lookup
  8. Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS, Chanda ML, Levitin DJ, Mogil JS. Social modulation of pain as evidence for empathy in mice.. Science 2006 Jun 30;312(5782):1967-70.
    doi: 10.1126/science.1128322pubmed: 16809545google scholar: lookup
  9. Reimert I, Bolhuis JE, Kemp B, Rodenburg TB. Indicators of positive and negative emotions and emotional contagion in pigs.. Physiol Behav 2013 Jan 17;109:42-50.
    pubmed: 23159725doi: 10.1016/j.physbeh.2012.11.002google scholar: lookup
  10. Reimert I, Fong S, Rodenburg TB, Bolhuis JE. Emotional states and emotional contagion in pigs after exposure to a positive and negative treatment.. Appl Anim Behav Sci 2017;193:37–42.
  11. Preston SD, de Waal FB. Empathy: Its ultimate and proximate bases.. Behav Brain Sci 2002 Feb;25(1):1-20; discussion 20-71.
    doi: 10.1017/S0140525X02000018pubmed: 12625087google scholar: lookup
  12. Darwin C. The expression of the emotions in man and animals.. .
  13. Scheumann M, Hasting AS, Kotz SA, Zimmermann E. The voice of emotion across species: how do human listeners recognize animals' affective states?. PLoS One 2014;9(3):e91192.
  14. Geiger M, Sánchez-Villagra MR, Lindholm AK. A longitudinal study of phenotypic changes in early domestication of house mice.. R Soc Open Sci 2018 Mar;5(3):172099.
    doi: 10.1098/rsos.172099pmc: PMC5882729pubmed: 29657805google scholar: lookup
  15. Albuquerque N, Guo K, Wilkinson A, Savalli C, Otta E, Mills D. Dogs recognize dog and human emotions.. Biol Lett 2016 Jan;12(1):20150883.
    doi: 10.1098/rsbl.2015.0883pmc: PMC4785927pubmed: 26763220google scholar: lookup
  16. Proops L, Grounds K, Smith AV, McComb K. Animals Remember Previous Facial Expressions that Specific Humans Have Exhibited.. Curr Biol 2018 May 7;28(9):1428-1432.e4.
    pubmed: 29706519doi: 10.1016/j.cub.2018.03.035google scholar: lookup
  17. Tate AJ, Fischer H, Leigh AE, Kendrick KM. Behavioural and neurophysiological evidence for face identity and face emotion processing in animals.. Philos Trans R Soc Lond B Biol Sci 2006 Dec 29;361(1476):2155-72.
    doi: 10.1098/rstb.2006.1937pmc: PMC1764842pubmed: 17118930google scholar: lookup
  18. 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.
    doi: 10.1098/rsos.180491pmc: PMC6124102pubmed: 30225038google scholar: lookup
  19. 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.
    doi: 10.1038/s41598-017-08789-ypmc: PMC5559457pubmed: 28814756google scholar: lookup
  20. Martin-Malivel J, Okada K. Human and chimpanzee face recognition in chimpanzees (Pan troglodytes): role of exposure and impact on categorical perception.. Behav Neurosci 2007 Dec;121(6):1145-55.
    doi: 10.1037/0735-7044.121.6.1145pubmed: 18085867google scholar: lookup
  21. 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.
    pubmed: 34476652doi: 10.1007/s10071-021-01557-6google scholar: lookup
  22. 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.
    doi: 10.1038/s41598-018-26892-6pmc: PMC6013457pubmed: 29930289google scholar: lookup
  23. 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).
    doi: 10.3390/ani9110862pmc: PMC6912773pubmed: 31653088google scholar: lookup
  24. Quaranta A, d'Ingeo S, Amoruso R, Siniscalchi M. Emotion Recognition in Cats.. Animals (Basel) 2020 Jun 28;10(7).
    doi: 10.3390/ani10071107pmc: PMC7401521pubmed: 32605256google scholar: lookup
  25. Andics A, Gácsi M, Faragó T, Kis A, Miklósi A. Voice-sensitive regions in the dog and human brain are revealed by comparative fMRI.. Curr Biol 2014 Mar 3;24(5):574-8.
    doi: 10.1016/j.cub.2014.01.058pubmed: 24560578google scholar: lookup
  26. Andics A, Gácsi M, Faragó T, Kis A, Miklósi Á. Voice-Sensitive Regions in the Dog and Human Brain Are Revealed by Comparative fMRI.. Curr Biol 2017 Apr 24;27(8):1248-1249.
    pubmed: 28392111doi: 10.1016/j.cub.2017.03.036google scholar: lookup
  27. 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.
    doi: 10.1038/s41598-018-30777-zpmc: PMC6115467pubmed: 30158532google scholar: lookup
  28. Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: A Resource for Timelines, Timetrees, and Divergence Times.. Mol Biol Evol 2017 Jul 1;34(7):1812-1819.
    doi: 10.1093/molbev/msx116pubmed: 28387841google scholar: lookup
  29. Briefer EF, Vizier E, Gygax L, Hillmann E. Expression of emotional valence in pig closed-mouth grunts: Involvement of both source- and filter-related parameters.. J Acoust Soc Am 2019 May;145(5):2895.
    doi: 10.1121/1.5100612pubmed: 31153321google scholar: lookup
  30. 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.
    doi: 10.1038/srep09989pmc: PMC4404681pubmed: 25897781google scholar: lookup
  31. Maigrot AL, Hillmann E, Anne C, Briefer EF. Vocal expression of emotional valence in Przewalski's horses (Equus przewalskii).. Sci Rep 2017 Aug 18;7(1):8779.
    doi: 10.1038/s41598-017-09437-1pmc: PMC5562828pubmed: 28821880google scholar: lookup
  32. Maigrot AL, Hillmann E, Briefer EF. Encoding of Emotional Valence in Wild Boar (Sus scrofa) Calls.. Animals (Basel) 2018 Jun 5;8(6).
    pmc: PMC6025020pubmed: 29874830doi: 10.3390/ani8060085google scholar: lookup
  33. Bänziger T, Mortillaro M, Scherer KR. Introducing the Geneva Multimodal expression corpus for experimental research on emotion perception.. Emotion 2012 Oct;12(5):1161-79.
    doi: 10.1037/a0025827pubmed: 22081890google scholar: lookup
  34. Gaunitz C, Fages A, Hanghøj K, Albrechtsen A, Khan N, Schubert M, Seguin-Orlando A, Owens IJ, Felkel S, Bignon-Lau O, de Barros Damgaard P, Mittnik A, Mohaseb AF, Davoudi H, Alquraishi S, Alfarhan AH, Al-Rasheid KAS, Crubézy E, Benecke N, Olsen S, Brown D, Anthony D, Massy K, Pitulko V, Kasparov A, Brem G, Hofreiter M, Mukhtarova G, Baimukhanov N, Lõugas L, Onar V, Stockhammer PW, Krause J, Boldgiv B, Undrakhbold S, Erdenebaatar D, Lepetz S, Mashkour M, Ludwig A, Wallner B, Merz V, Merz I, Zaibert V, Willerslev E, Librado P, Outram AK, Orlando L. Ancient genomes revisit the ancestry of domestic and Przewalski's horses.. Science 2018 Apr 6;360(6384):111-114.
    doi: 10.1126/science.aao3297pubmed: 29472442google scholar: lookup
  35. Groenen MA. A decade of pig genome sequencing: a window on pig domestication and evolution.. Genet Sel Evol 2016 Mar 29;48:23.
    doi: 10.1186/s12711-016-0204-2pmc: PMC4812630pubmed: 27025270google scholar: lookup
  36. Frantz LAF, Haile J, Lin AT, Scheu A, Geörg C, Benecke N, Alexander M, Linderholm A, Mullin VE, Daly KG, Battista VM, Price M, Gron KJ, Alexandri P, Arbogast RM, Arbuckle B, Bӑlӑşescu A, Barnett R, Bartosiewicz L, Baryshnikov G, Bonsall C, Borić D, Boroneanţ A, Bulatović J, Çakirlar C, Carretero JM, Chapman J, Church M, Crooijmans R, De Cupere B, Detry C, Dimitrijevic V, Dumitraşcu V, du Plessis L, Edwards CJ, Erek CM, Erim-Özdoğan A, Ervynck A, Fulgione D, Gligor M, Götherström A, Gourichon L, Groenen MAM, Helmer D, Hongo H, Horwitz LK, Irving-Pease EK, Lebrasseur O, Lesur J, Malone C, Manaseryan N, Marciniak A, Martlew H, Mashkour M, Matthews R, Matuzeviciute GM, Maziar S, Meijaard E, McGovern T, Megens HJ, Miller R, Mohaseb AF, Orschiedt J, Orton D, Papathanasiou A, Pearson MP, Pinhasi R, Radmanović D, Ricaut FX, Richards M, Sabin R, Sarti L, Schier W, Sheikhi S, Stephan E, Stewart JR, Stoddart S, Tagliacozzo A, Tasić N, Trantalidou K, Tresset A, Valdiosera C, van den Hurk Y, Van Poucke S, Vigne JD, Yanevich A, Zeeb-Lanz A, Triantafyllidis A, Gilbert MTP, Schibler J, Rowley-Conwy P, Zeder M, Peters J, Cucchi T, Bradley DG, Dobney K, Burger J, Evin A, Girdland-Flink L, Larson G. Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe.. Proc Natl Acad Sci U S A 2019 Aug 27;116(35):17231-17238.
    doi: 10.1073/pnas.1901169116pmc: PMC6717267pubmed: 31405970google scholar: lookup
  37. Nicastro N, Owren MJ. Classification of domestic cat (Felis catus) vocalizations by naive and experienced human listeners.. J Comp Psychol 2003 Mar;117(1):44-52.
    doi: 10.1037/0735-7036.117.1.44pubmed: 12735363google scholar: lookup
  38. Tallet C, Linhart P, Policht R, Hammerschmidt K, Šimeček P, Kratinova P, Špinka M. Encoding of situations in the vocal repertoire of piglets (Sus scrofa): a comparison of discrete and graded classifications.. PLoS One 2013;8(8):e71841.
  39. Pongrácz P, Molnár C, Dóka A, Miklósi Á. Do children understand man’s best friend? Classification of dog barks by pre-adolescents and adults.. Appl Anim Behav Sci 2011;135:95–102.
  40. Faragó T, Andics A, Devecseri V, Kis A, Gácsi M, Miklósi A. Humans rely on the same rules to assess emotional valence and intensity in conspecific and dog vocalizations.. Biol Lett 2014 Jan;10(1):20130926.
    doi: 10.1098/rsbl.2013.0926pmc: PMC3917336pubmed: 24402716google scholar: lookup
  41. 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.
    doi: 10.1016/j.cub.2015.08.032pmc: PMC5104162pubmed: 26412128google scholar: lookup
  42. Filippi P, Congdon JV, Hoang J, Bowling DL, Reber SA, Pašukonis A, Hoeschele M, Ocklenburg S, de Boer B, Sturdy CB, Newen A, Güntürkün O. Humans recognize emotional arousal in vocalizations across all classes of terrestrial vertebrates: evidence for acoustic universals.. Proc Biol Sci 2017 Jul 26;284(1859).
    pmc: PMC5543225pubmed: 28747478doi: 10.1098/rspb.2017.0990google scholar: lookup
  43. Goumon S, Špinka M. Emotional contagion of distress in young pigs is potentiated by previous exposure to the same stressor.. Anim Cogn 2016 May;19(3):501-11.
    doi: 10.1007/s10071-015-0950-5pubmed: 26753689google scholar: lookup
  44. Zeder MA. Pathways to animal domestication.. In: Gepts P, Famula TR, Bettinger RL, Brush SB, Damania AB, McGuire PE, et al., editors. Biodiversity in agriculture. Cambridge: Cambridge University Press; 2012. p. 227–259.
  45. Richter SH, Garner JP, Würbel H. Environmental standardization: cure or cause of poor reproducibility in animal experiments?. Nat Methods 2009 Apr;6(4):257-61.
    doi: 10.1038/nmeth.1312pubmed: 19333241google scholar: lookup
  46. Fischer J, Noser R, Hammerschmidt K. Bioacoustic field research: a primer to acoustic analyses and playback experiments with primates.. Am J Primatol 2013 Jul;75(7):643-63.
    doi: 10.1002/ajp.22153pmc: PMC3698702pubmed: 23592340google scholar: lookup
  47. R Development Core Team. R Foundation for Statistical Computing. Vienna, Austria; 2015. http://www.R-project.org.
  48. McGregor PK. Quantifying responses to playback: one, many, or composite multivariate measures? In: Playback and studies of animal communication. Springer; 1992. p. 79–96.
  49. Engqvist L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies.. Anim Behav 2005;70:967–971.
  50. Forstmeier W, Schielzeth H. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse.. Behav Ecol Sociobiol 2011 Jan;65(1):47-55.
    doi: 10.1007/s00265-010-1038-5pmc: PMC3015194pubmed: 21297852google scholar: lookup
  51. Levy R. Using R formulae to test for main effects in the presence of higher-order interactions.. 2014. arXiv preprint arXiv:1405.2094.
  52. Halekoh U, Højsgaard S. A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models: The R package pbkrtest.. J Stat Soft 2014;1:9.
  53. Bates D, Maechler M, Bolker B. lme4: Linear mixed-effects models using S4 classes.. 2011.

Citations

This article has been cited 3 times.
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    doi: 10.1038/s41598-023-37558-3pubmed: 37407601google scholar: lookup
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    doi: 10.1371/journal.pone.0279553pubmed: 36584172google scholar: lookup
  3. Schwartz JW, Gouzoules H. Humans read emotional arousal in monkey vocalizations: evidence for evolutionary continuities in communication.. PeerJ 2022;10:e14471.
    doi: 10.7717/peerj.14471pubmed: 36518288google scholar: lookup