Abstract
One of the most productive behavioural domains to study visual communication in mammals is social play. The ability to manage play–fighting interactions can favour the development of communicative modules and their correct decoding. Due to their high levels of social cohesion and cooperation, slender-tailed meerkats (Suricata suricatta) are a very good model to test some hypotheses on the role of facial communication in synchronizing playful motor actions. We found that the relaxed open mouth (ROM), a playful facial expression conveying a positive mood in several social mammals, is also present in meerkats. ROM was mainly perceived during dyadic playful sessions compared to polyadic ones. We also found that meerkats mimic in a very rapid and automatic way the ROM emitted by playmates (Rapid Facial Mimicry, RFM). RFM was positively correlated with the relationship quality shared by subjects, thus suggesting that the mimicry phenomenon is socially modulated. Moreover, more than the mere presence of isolated ROMs, the presence of at RFM prolonged the duration of the play session. Through RFM animals can share the emotional mood, they are experiencing and this appears to be particularly adaptive in those species, whose relationships are not inhibited by rank rules and when animals build and maintain their bonds through social affiliation. The meerkat society is cohesive and cooperative. Such features could have, therefore, favoured the evolution of facial mimicry, a phenomenon linked to emotional contagion, one of the most basic forms of empathy.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bales KL, Carter SC (2003) Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44:178–184. https://doi.org/10.1016/S0018-506X(03)00154-5
Bauer EB, Smuts BB (2007) Cooperation and competition during dyadic play in domestic dogs, Canis familiaris. Anim Behav 73:489–499. https://doi.org/10.1016/j.anbehav.2006.09.006
Bekoff M (1974) Social play in coyotes, wolves, and dogs. BioSci 24:225–230. https://doi.org/10.2307/1296803
Bekoff M (2001) Social play behaviour: cooperation, fairness, trust, and the evolution of morality. J Conscious Stud 8:81–90
Bousquet CAH, Sumpter DJT, Manser MB (2011) Moving calls: a vocal mechanism underlying quorum decisions in cohesive groups. Proc R Soc B 278:1482–1488. https://doi.org/10.1098/rspb.2010.1739
Bradbury JK, Vehrencamp SL (1998) Principles of animal comunication. Sunderland, MA
Brotherton P, Clutton-Brock TH, O’Riain JM, Gaynor D, Sharpe L, Kansky R (2001) Offspring food allocation by parents and helpers in a cooperative mammal. Behav Ecol 12:590–599. https://doi.org/10.1093/beheco/12.5.590
Bryant GA, Fessler DMT, Fusaroli R, Clint E, Aarøe L, Apicella CL, Petersen MB, Bickham ST, Bolyanatz A, Chavez B, De Smet D, Díaz C, Fančovičová J, Fux M, Giraldo-Perez P, Hu A, Kamble SV, Kameda T, Li NP, Luberti FR, Prokop P, Quintelier K, Scelza BA, Shin HJ, Soler M, Stieger S, Toyokawa W, van den Hende EA, Viciana-Asensio H, Yildizhan SE, Yong JC, Yuditha T, Zhou Y (2016) Detecting affiliation in colaughter across 24 societies. PNAS 113:4682–4687. https://doi.org/10.1073/pnas.1524993113
Burghardt GM (2005) The genesis of animal play: testing the limits. MIT Press, Cambridge
Burkett JP, Andari E, Johnson ZV, Curry DC, de Waal FB, Young LJ (2016) Oxytocin-dependent consolation behavior in rodents. Science 351:375–378. https://doi.org/10.1126/science.aac4785
Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New York
Byosiere SE, Espinosa J, Smuts B (2016) Investigating the function of play bows in adult pet dogs (Canis lupus familiaris). Behav Processes 125:106–113. https://doi.org/10.1016/j.beproc.2016.02.007
Cafazzo S, Marshall-Pescini S, Essler JL, Virányi Z, Kotrschal K, Range F (2018) In wolves, play behaviour reflects the partners’ affiliative and dominance relationship. Anim Behav 141:137–150. https://doi.org/10.1016/j.anbehav.2018.04.017
Clay Z, Palagi E, de Waal FBM (2018) Ethological approaches to empathy in primates. In: Meyza KZ, Knapska E (eds) Neuronal correlates of empathy. Elsevier Science Publishing Co Inc, San Diego, pp 53–66
Clutton-Brock TH, Manser MB (2016) Meerkats: cooperative breeding in the Kalahari. In: Koenig WD, Dickinson JL (eds) Cooperative breeding in vertebrates: studies of ecology, evolution, and behavior. Cambridge University Press, Cambridge, pp 294–317
Clutton-Brock TH, Gaynor D, Kansky R, MacColl ADC, McIlrath G, Chadwick P, Brotherton PNM, O’Riain JM, Manser M, Skinner JD (1998) Costs of cooperative behaviour in suricates (Suricata suricatta). Proc R Soc B 265:1392. https://doi.org/10.1098/rspb.1998.0281
Clutton-Brock TH, O’Riain MJ, Brotherton PN, Gaynor D, Kansky R, Griffin AS, Manser M (1999) Selfish sentinels in cooperative mammals. Science 284:1640–1644
Clutton-Brock TH, Brotherton PNM, O’riain MJ, Griffin AS, Gaynor D, Kansky R, Sharpe L, McIlrath GM (2001) Contributions to cooperative rearing in meerkats. Anim Behav 61:705–710. https://doi.org/10.1006/anbe.2000.1631
Cordoni G (2009) Social play in captive wolves (Canis lupus): not only an immature affair. Behaviour 146:1363–1385
Cordoni G, Nicotra V, Palagi E (2016) Unveiling the ‘secret’ of dog play success: asymmetry and signals. J Comp Psychol 130:278–287. https://doi.org/10.1037/com0000035
Davila-Ross M, Menzler S, Zimmermann E (2008) Rapid facial mimicry in orangutan play. Biol Lett 4:27–30. https://doi.org/10.1098/rsbl.2007.0535
de Waal FBM, Preston SD (2017) Mammalian empathy: behavioural manifestations and neural basis. Nat Rev Neurosci 18:498–509. https://doi.org/10.1038/nrn.2017.72
Drea CM, Hawk JE, Glickman SE (1996) Aggression decreases as play emerges in infant spotted hyaenas: preparation for joining the clan. Anim Behav 51:1323–1336
Fagen R (1981) Animal play behavior. Oxford University Press, New York
Freeberg TM, Robin I, Dunbar M, Terry JO (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Phil Trans R Soc B 367:1785–1801. https://doi.org/10.1098/rstb.2011.0213
Gall GEC, Strandburg-Peshkin A, Clutton-Brock T, Manser MB (2017) As dusk falls: collective decisions about the return to sleeping sites in meerkats. Anim Behav 132:91–99
Graw B, Manser MB (2007) The function of mobbing in cooperative meerkats. Anim Behav 74:507–517. https://doi.org/10.1016/j.anbehav.2006.11.021.3
Henry JD, Herrero SM (1974) Social play in the American black bear: its similarity to canid social play and an examination of its identifying characteristic. Am Zool 14:371–389
Huber A, Barber AL, Faragό T, Müller CA, Huber L (2017) Investigating emotional contagion in dogs (Canis familiaris) to emotional sounds of humans and conspecifics. Anim Cogn 20:703–715. https://doi.org/10.1007/s10071-017-1092-8
Jolly A (1966) Lemur social behavior and primate intelligence. Science 153:501–506. https://doi.org/10.1126/science.153.3735.501
Kaufman AB, Rosenthal R (2009) Can you believe my eyes? The importance of interobserver reliability statistics in observations of animal behaviour. Anim Behav 78:1487–1491
Korb S, Malsert J, Strathearn L, Vuilleumier P, Niedenthal P (2016) Sniff and mimic—intranasal oxytocin increases facial mimicry in a sample of men. Horm Behav 84:64–74. https://doi.org/10.1016/j.yhbeh.2016.06.003
Llamazares-Martín C, Scopa C, Guillén-Salazar F, Palagi E (2017) Strong competition does not always predict play asymmetry: the case of South American sea lions (Otaria flavescens). Ethology. https://doi.org/10.1111/eth.12594
Madden JR, Clutton-Brock TH (2011) Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal. Proc R Soc B 278:1189–1194. https://doi.org/10.1098/rspb.2010.1675
Mancini G, Ferrari PF, Palagi E (2013) Rapid facial mimicry in geladas. Sci Rep 3:15–27. https://doi.org/10.1038/srep01527
Manser MB, Bell MB (2004) Spatial representation of shelter locations in meerkats, Suricata suricatta. Anim Behav 68:151–157. https://doi.org/10.1016/j.anbehav.2003.10.017
Manser MB, Jansen DAWAM, Graw B, Hollén L, Bousquet C, Furrer R, Le Roux A (2014) Vocal complexity in meerkats and other mongoose species. Adv Study Behav 46:281–310
Markl H (1983) Vibrational communication. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology. Springer, Berlin, pp 332–353
Megan TW, River PR, Muller C, Toni P, Manser MB (2017) Adult meerkats modify close call rate in the presence of pups. Curr Zool 63:349–355
Mendl M, Burman OHP, Paul ES (2010) An integrative and functional framework for the study of animal emotion and mood. Proc Biol Sci 277:2895–2904. https://doi.org/10.1098/rspb.2010.0303
Nakahashi W, Ohtsuki H (2015) When is emotional contagion adaptive? J Theor Biol 380:480–488. https://doi.org/10.1016/j.jtbi.2015.06.014
Palagi E (2006) Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): implications for natural social system and interindividual relationships. Am J of Phys Anthropol 129:418–426
Palagi E (2008) Sharing the motivation to play: the use of signals in adult bonobos. Anim Behav 75:887–896
Palagi E (2009) Adult play fighting and potential role of tail signals in ring-tailed lemurs (Lemur catta). J Comp Phys 123:1–9
Palagi E (2018) Not just for fun! Social play as a springboard for adult social competence in human and non-human primates. Behav Ecol Sociobiol 72:90. https://doi.org/10.1007/s00265-018-2506-6
Palagi E, Cordoni G (2012) The right time to happen: play developmental divergence in the two Pan species. PLoS One 7:e52767. https://doi.org/10.1371/journal.pone.0052767
Palagi E, Mancini G (2011) Playing with the face: playful facial “chattering” and signal, modulation in a monkey species (Theropithecus gelada). J Comp Psychol 125:11–21. https://doi.org/10.1037/a0020869
Palagi E, Scopa C (2017) Integrating Tinbergen’s inquiries: mimicry and play in humans and other social mammals. Learn Behav 45:378–389. https://doi.org/10.3758/s13420-017-0278-x
Palagi E, Norscia I, Spada G (2014) Relaxed open mouth as a playful signal in wild ring-tailed lemurs. Am J Primatol 76:1074–1083. https://doi.org/10.1002/ajp.22294
Palagi E, Nicotra V, Cordoni G (2015) Rapid mimicry and emotional contagion in domestic dogs. R Soc Open Sci 2:150505. https://doi.org/10.1098/rsos.150505
Palagi E, Cordoni G, Demuru E, Bekoff M (2016) Fair play and its connection with social tolerance, reciprocity and the ethology of peace. Behaviour 153:1195–1216. https://doi.org/10.1163/1568539X-0000333
Palagi E, Norscia I, Pressi S, Cordoni G (2018) Facial mimicry and play: a comparative study in chimpanzees and gorillas. Emotion. https://doi.org/10.1037/emo0000476
Panksepp J, Burgdorf J (2003) ‘‘Laughing’’ rats and the evolutionary antecedents of human joy? Phys Behav 79:533–545
Pellis SM (1984) Two aspects of play-fighting in a captive group of oriental small-clawed otters Amblonyx cinerea. Ethology 65:77–83. https://doi.org/10.1111/j.1439-0310.1984.tb00374.x
Pellis SM, Pellis VC (1997) Targets, tactics, and the open mouth face during play fighting in three species of primates. Aggress Behav 23:41–57
Pellis SM, Pellis VC (2007) Rough-and-tumble play and the development of the social brain. Curr Dir Psychol Sci 16:95–98. https://doi.org/10.1111/j.1467-8721.2007.00483.x
Pellis SM, Pellis VC, Bell HC (2010) The function of play in the development of the social brain. Am J Play 2:278–296
Poole TB (1978) An analysis of social play in polecats (Mustelidae) with comments on the form and evolutionary history of the open mouth play face. Anim Behav 26:36–49. https://doi.org/10.1016/0003-3472(78)90006-4
Preuschoft S, van Hooff JARAM (1995) Homologizing primate facial displays: a critical review of methods. Folia Primatol 65:121–137
Prochazkova E, Kret ME (2017) Connecting minds and sharing emotions through mimicry: a neurocognitive model of emotional contagion. Neurosci Biobehav Rev 80:99–114
Reinhart CJ, Pellis VC, Thierry B, Gauthier C, Vanderlaan DP, Vasey PL, Pellis SM (2010) Targets and tactics of play fighting: competitive versus cooperative styles of play in Japanese and Tonkean macaques. Int J Comp Psychol 4:166–200
Russell JA, Fernandez-Dols JM (2017) The science of facial expression. Oxford University Press, Oxford
Schmidt KL, Cohn JF (2001) Human facial expressions as adaptations: evolutionary questions in facial expression research. Yearb Phys Anthropol 44:3–24
Schwing R, Nelson XJ, Wein A, Parsons S (2017) Positive emotional contagion in a New Zealand parrot. Curr Biol 27:213–214. https://doi.org/10.1016/j.cub.2017.02.020
Scopa C, Palagi E (2016) Mimic me while playing! Social tolerance and rapid facial mimicry in macaques (Macaca tonkeana and Macaca fuscata). J Comp Psychol 130:153–161
Sharpe L (2005a) Play fighting does not affect subsequent fighting success in wild meerkats. Anim Behav 69:1023–1029. https://doi.org/10.1016/j.anbehav.2004.07.013
Sharpe L (2005b) Play does not enhance social cohesion in a cooperative mammal. Anim Behav 70:551–558. https://doi.org/10.1016/j.anbehav.2004.08.025
Sharpe L (2005c) Frequency of social play does not affect dispersal partnerships in wild meerkats. Anim Behav 70:559–569. https://doi.org/10.1016/j.anbehav.2004.11.011
Sharpe L, Cherry MI (2003) Social play does not reduce aggression in wild meerkats. Anim Behav 66:989–997. https://doi.org/10.1006/anbe.2003.2275
Sharpe L, Clutton-Brock TH, Brotherton PNM, Cameron EZ, Cherry MI (2002) Experimental provisioning increases play in free-ranging meerkats. Anim Behav 64:113–121. https://doi.org/10.1006/anbe.2002.3031
Somppi S, Törnqvist H, Topál J, Koskela A, Hänninen L, Krause CM, Vainio O (2017) Nasal oxytocin treatment biases dogs’ visual attention and emotional response toward positive human facial expressions. Front Psychol 17:1854. https://doi.org/10.3389/fpsyg.2017.01854
Špinka M, Palečková M, Řeháková M (2016) Metacommunication in social play: the meaning of aggression-like elements is modified by play face in Hanuman langurs (Semnopithecus entellus). Behaviour 153:795–818
Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21. https://doi.org/10.1007/s00265-010-1037-6
Taylor D, Hartmann D, Dezecache G, Wong ST, Davila-Ross M (2019) Facial complexity in sun bears: exact facial mimicry and social sensitivity. Sci Rep 9:4961. https://doi.org/10.1038/s41598-019-39932-6
Thierry B (2000) Covariation of conflict management patterns across macaque species. In: Aureli F, de Waal FBM (eds) Natural conflict resolution. UPC Press, Berkeley, pp 106–128
Thornton A, McAuliffe K (2006) Teaching in wild meerkats. Science 313:227–229. https://doi.org/10.1126/science.1128727
Tinbergen N (1952) “Derived” activities: their causation, biological significance, origin, and emancipation during evolution. Q Rev Biol 72:1–32
van Hooff JA, Preuschoft S (2003) Laughter and smiling: the intertwining of nature and culture. In: de Waal FBM, Tyack PL (eds) Animal social complexity. Cambridge, pp 260–287
Vervaecke H, Stevens JMG, Vandemoortele H, Sigurjόnsdόttir H, de Vries H (2007) Aggression and dominance in matched groups of subadult Icelandic horses (Equus caballus). J Ethol 25:239–248. https://doi.org/10.1007/s10164-006-0019-7
Waller BM, Cherry L (2012) Facilitating play through communication: significance of teeth exposure in the gorilla play face. Am J Primatol 74:157–164. https://doi.org/10.1002/ajp.21018
Ward C, Bauer EB, Smuts BB (2008) Partner preferences and asymmetries in social play among domestic dog, Canis lupus familiaris, littermates. Anim Behav 76:1187–1199
Watanabe S, Kuczaj S (2013) Emotion of animals and humans: comparative perspectives. Springer, Tokyo
Weigel EA, Berman CM (2018) Body signals used during social play in captive immature western lowland gorillas. Primates 59:253–265
Wemmer and Fleming (1974) Ontogeny of playful contact in a social mongoose, the meerkat, Suricata suricatta. Am Zool 14:415–426
Yanagi A, Berman CM (2014) Body signals during social play in free-ranging rhesus macaques (Macaca mulatta): a systematic analysis. Am J Primatol 76:168–179
Acknowledgements
We wish to thank the staff of the Pistoia Zoo for their help and assistance during the data collection; B. Millesimato Caval for the enlightening discussion during the interpretation of the results. We also wish to thank Daniele Santerini for helping with figures.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
As the present study was exclusively observational without any manipulation of animals, all applicable international, national, and/or institutional guidelines for the care and use of animals were followed. In addition, all procedures were in accordance with the ethical standards of the University of Pisa.
Informed consent
No need for an informed consent for this study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Palagi, E., Marchi, E., Cavicchio, P. et al. Sharing playful mood: rapid facial mimicry in Suricata suricatta. Anim Cogn 22, 719–732 (2019). https://doi.org/10.1007/s10071-019-01269-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-019-01269-y